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 1
INTRODUCTION
1.1 Scope o f the book I 1.1.3
1.1.1 Volume 1 / 1.2
1.1.2 Volume 2 3 1.3
1 .1 SCOPE OF THE BOOK
These three volumes contain a survey o f knowledge about
the mechanisms that enable humans and animals to per­
ceive the three-dimensional structure o f the world and
use sensory information to guide their actions in three-
dimensional space. M achine vision and computational
models are mentioned only where they contribute to an
understanding o f the living system.
O u r 1995 book, {Binocular Vision andStereopsis , by I. P.
Howard and B. J. Rogers) dealt only with binocular vision.
In 2 0 0 2 we published Seeing in D epth , which dealt with
all visual cues to depth. The scope o f the present three
volumes has been broadened to include distance perception
by senses ocher than vision. Table 1.1 lists the sources o f
information that animals use to detect the distances o f
objects o r a distance traveled. There are also new chapters
on how humans and animals reach, walk, and navigate in
three-dimensional space.
The topics discussed in Seeingin Depth have been exten­
sively revised and brought up to date with che addition o f
3 ,0 0 0 more references and hundreds o f new figures.
1.1.1 VOLUM E 1
The first volume provides a historical background and deals
with basic coding processes, methods o f investigation, and
basic visual mechanisms.
It starts with a review o f the history o f our knowledge o f
the visual system, from 5 0 0 B C to the early 2 0 th century.
The study o f visual mechanisms of depth perception has a
long history. It began in ancient Greece. The study o f audi­
tory mechanisms of depth perception, including echoloca-
tion, and the lateral-line system, did n ot start until the early
2 0 th century. T he otolith organs o f the vestibular system,
and sense organs responsible for kinesthesia were discov­
ered in the second half o f the 19th century. Electrolocation,
Volume 3 4
Basic terms 6
Indexes and references 7
infrared sense organs, and magnetic sense organs were dis­
covered in the 20th century.
Until the 17th century, the word “optics” meant per­
taining to vision. The study of binocular vision and space
perception in general was fostered by those in the
P erspcctivist tra d itio n , which stressed the geometrical
aspects o f vision. The tradition started with Euclid in the
3rd century B C and progressed through Ptolemy in the 2nd
century A D ; Alhazen in the 10th century; Roger Bacon,
Joh n Peckham, and Vitcllo in the 13th century; and
Aguilonius, Kepler, and Newton in the 17th century. They
all wrote books with titles containing either the word
“optics” or the word “perspective.” The books formed a
continuous tradition.
Som e o f these works have been translated into English
only recently. M ost visual scientists are unaware o f this
ancient Perspcctivist tradition, which culminated in
Keplers discovery o f the laws o f image formation in 1604,
N ew tons book of Optics in 1670 , and projective geometry.
Many o f the early discoveries o f the Perspectivists, having to
do with visual perception, were forgotten after the l 7 th
century and were rediscovered in the 19th and 2 0 th centu­
ries, without reference to earlier sources.
No account o f the history o f sensory science can ignore
the fact that until modern times, medicine, science, and visual
science in particular, were associated with mysticism and reli­
gious dogma. In Europe before the 18th century, light was
identified with divine illumination descending from ethereal
regions down to the earthy sphere of mortal existence.
Perception and thought were identified with the soul, and
philosophers were preoccupied with questions concerning
the nature o f the immortal soul. Science and medicine broke
free from these constraints on rational thought and empirical
investigation in the 18th century, although mystical ideas still
flourish outside the mainstream o f science.
Devices that create imaginary visual worlds have always
fascinated people. The ancients had to rely on masks,
T a b l e 1. /. S O U R C E S O F IN F O R M A T IO N F O R T H F . D E T E C T IO N O F D E P T H
M onocular
Static
Perspective In te rp o s itio n L ig h ting Aerial
Linear Occlusion Shading Optical
Texture Transparency Shadow Mist
Self m ovem ent A u d itio n
Monaural
A ctive Passive Binaural
Kinesthesis Touch
Echo location
Motor efference Otolith organs
Lateral line
puppets, and cheater. Peepshow boxes became popular in
rhc 15th ccncury. In the 16th century, development o f the
camera obscura provided artists with a method for drawing
in perspective. It developed into display systems that pro­
duced panoramic images o f the surroundings. In the 17th
century the shadow theater was imported into F.uropc from
the East and the magic lantern was invented. During the
18th and 19th centuries most cities in F.urope and America
had panoramas, which were huge painted scenes displayed
round the interior o f large arenas. After W heatstone
invented the stereoscope in 1832, domestic stereoscopes
became all the rage. Panoramas and stereoscopes were
eclipsed by the advent o f the cinema. We now have stereo­
scopic movies and virtual reality displays with which the
viewer can interact. These display systems arc reviewed in
Chapter 2.
Perhaps synthetic worlds will become so real and the
real world will become so contrived and managed that the
two will be indistinguishable.
Many psychophysical and analytic procedures have been
used to investigate mechanisms o f depth perception.
Chapter 3 provides a general introduction to these proce­
dures. Key references arc provided to more detailed
treatments.
Perception must start with the detection o f relevant fea­
tures o f the environment. All sensory systems consist o f sen­
sory cells distributed over a membrane. A stereoscopic
movie camera can detect all visible features o f a scene.
Similarly, a microphone can detect all the sounds that a
human ear can detect. In theory, a movie created by infor­
mation picked up by a movie camera and microphone can
be indistinguishable from the real scene. But cameras and
microphones do n ot perceive, they simply detect and recon­
struct stimuli. Perception represents the ability to respond
differentially to stimuli, and to discriminate, identify,
and describe them. These abilities require that stimuli be
V isual in fo rm ation
B inocular
Dynam ic
Focussing Optic flow Vorgencc D isparity
haze Image blur Motion parallax Static Occlusion disparity
Accommodation Accretion/deletion Changing Position disparity
N on-visual inform ation
E lectric fie ld s Heat G eom agnetism O lfaction
Passive electrolocation
Active electrolocation
processed in complex ways, so that they may be acted on
and described, n ot merely detected or reconstructed.
Chapter 4 is an introduction to general principles o f sen­
sory coding, starting with detection and going on to dis­
crimination, identification, and description.
O ver one million axons from each eye feed into the
human visual cortex, more than from all the other sense
organs combined. The processing of these inputs involves
almost every part o f the cerebral cortex, which contains bil­
lions o f neurons. Vision is therefore the main gateway to
understanding the central nervous system. Chapter 5 is a
review o f the general physiology o f the visual system, with
an em phasison those mechanisms related to depth percep­
tion. T he physiology o f other relevant sensory systems is
presented in later chapters.
The human visual system is the most complex system
known. How did such a system evolve? Chapter 6 starts
with a discussion o f how eyes evolved independently in sev­
eral phyla, from simple eyespots to complex lens eyes and
compound eyes.
Chapter 6 continues with an account o f how the visual
system develops. As the sense organs and central nervous
system grow, billions o f cells form appropriate synaptic co n ­
nections, sometimes as many as 2 0 ,0 0 0 on one cell. How do
the multitudes o f growing nerve cells find their proper des­
tinations and form complex functioning networks? Our
understanding o f these processes has progressed rapidly in
the last 5 0 years with the advent o f high-resolution m icro ­
scopes and staining techniques that allow one to observe
living neurons and dendritic processes. This is the m ost rap­
idly developing Held in the whole o f visual science. W ith
these new procedures we can expect m ajor developments in
our understanding of the growth of the visual system. The
complexity o f the visual system and o f the processes respon­
sible for its growth arc overwhelming. Chapter 6 provides
only a general overview o f the subject.
 The study o f the development o f the visu.il system prom ­
ises to be the most fruitful approach to understanding the
development o f the whole central nervous system. This is
because, in the visual system, one can most easily see rela­
tionships between genetic and experiential factors. Even
before the eyes open, activity arising in the eyes affects the
growth o f cell connections in the growing visual cortex. The
study o f the effects o f stimuli arising in the two eyes has
been particularly rewarding in young animals just after their
eyes have opened. In the first place, the routing o f growing
axons at the optic chiasm provides a model system for inves­
tigating mechanisms o f axonal guidance. Secondly, more
than any other branch o f developmental neuroscience, the
study o f the development o f binocular cells in the visual
cortex has revealed how genetic and experiential factors
interact.
Although every cell in the body contains the same ch ro ­
mosomes, different genes are activated in different types o f
cells and at different times during development. The m ech­
anisms that control specific activation o f genes are known .is
epigenesis. It has recently been discovered that visual expe­
rience in early life activates genes that control development
o f the visual system. Sensory experience controls gene
expression even in the adult animal, in the processes respon­
sible for learning.
The study o f the development o f the structure and func­
tion o f the visual system is complemented by behavioral and
psychophysical investigations o f the developing animal.
These investigations are reviewed in Chapter 7, with an
emphasis on che development o f dcpch perception. Some
functions, such as reflex eye movements, develop under the
guidance of genetic factors with little influence from visual
activity. O th er functions, such as stereoscopic vision,
develop only when certain types of visual activity occur in
certain critical time periods. All sensory functions become
finely tuned by experience and complex relationships
between them build over many years and even over the
whole lifetime.
Much can be learned about the visual system by
studying the consequences of early deprivation of sight in
one or both eyes. M onocular deprivation within a critical
period after birrh severely disrupts vision in the deprived
eye— a condition known as amblyopia. It also disrupts
binocular vision and stereopsis. This topic has attracted a
lot o f attention because o f the clinical importance o f
amblyopia. Also, the behavioral and physiological conse­
quences o f experimentally induced monocular deprivation
in animals have revealed much about the way * the visual
system develops and functions. These issues arc reviewed in
Chapter 8.
Chapters 9 and 10 are concerned with oculom otor
mechanisms associated with the perception ofdepth. W hen
we attend to an object, the lenses o f the eyes automatically
accommodate to the correct distance. At the same time, the
eyes converge horizontally, vercically, and by rocacion abouc
che visual axes so as со bring chc two images o f an o b ject o f
interest o n to corresponding positions on the retinas.
1 .1 .2 VOLUM E 2
The second volume is devoted to stereoscopic vision in cats
and primates, including humans. Stereoscopic vision is
defined as the detection o f che 3 -D struccure o f stimuli that
relics on differences between che images in the two eyes.
These differences are detected by specialized disparity
detectors, which occur at various levels of the central
nervous system. The physiology o f disparity detectors is
discussed in Chapter 11.
The fact that inputs from corresponding regions in the
cwo eyes com bine in the visual corcex gives rise со several
interesting problems. Signals from the two eyes that arise
from the same object must be distinguished from signals
that arise from spurious superimposition o f nonmatching
stimuli. M atching signals falling on neighboring points on
the two retinas project to the same region in the visual
cortex and fuse to create the impression of one image.
Nonmatching images falling on the same region in the two
eyes rival for access to the visual system. Chapter 12 deals
with these issues.
Under certain circumstances, a stimulus seen by both
eyes is perceived more readily and appears brighter than
monocular images. Under other circumstances, superim­
posed, neighboring, or successively presented binocular
images engage in mutual suppression. Chapter 13 deals
with these phenomena. It also deals with interocular trans­
fer. A visual phenomenon shows interocular transfer when
an aftereffect generated by presenting a stimulus to one eye
shows when only che ocher eye isopen . 'Hie study o f interne-
ular transfer reveals how inputs from the two eyes arc com ­
bined and, to some extent, where they are combined.
C hapter 14 deals wich che geomecry o f binocular space.
It starts by defining coordinate systems used to specify the
posicions o f images in each eye and che positions of points
in space with respect to borh eyes. In theory, o n e can deter­
mine the locus o f points in space that project images to cor­
responding locations in the two retinas. This locus is known
as the horopter. The horopter can also be derived empiri­
cally by measuring which points appear fused or aligned.
The issues are quite complex.
Similar images in the two eyes that are sufficiently
near each other are combined in the primary visual cortex
and passed on for processing to higher levels. The problem
is to determine the stimulus features used bv the visual
i
system to relate images in one retina with those in a corre­
sponding region o f the other retina. These features could
include proximity, or similarity of contrast, shape, color, or
morion. O n e can also ask whether the visual system per­
forms image matching only locally or both locally and glob­
ally over wide areas. These questions arc discussed in
Chapter 15.
 Images in the cwo eyes may be superimposed or juxta­
posed to product* a perceptual effect n ot evident when
either image is presented alone. Any such effect is known as
a cyclopean effect. Stereoscopic vision is a cyclopean effect
but there arc many others, such as cyclopean figural effects,
cyclopean m otion, and cyclopean acuity. These effects are
discussed in C hapter 16.
A nother issue o f cyclopean vision discussed in
Chapter 16 is how stimuli moving in different directions in
the two eyes are unified into an impression o f coherent
mocion in one direction. A related question is how the
directions o f an o b je ct detected by the two eyes are com ­
bined into one perceived direction. A nother interesting
question is whether we arc aware o f which eye is seeing a
stimulus that is presented to only one eye. This is known as
utrocular discrimination.
Because the eyes are spatially separated, the images in
the two eyes formed by a three-dimensional display differ.
These differences are known as binocular disparities and
form the basis for stereoscopic vision. Binocular disparities
can involve differences in position, orientation, texture,
color, temporal phase, or m otion. Also, part o f an o b ject
seen by one eye may not be visible to the other eye, an effect
known as monocular occlusion. Chapter 17 deals with the
extent to which each o f these differences is used as a basis
for stereopsis. The chapter also asks whether differences in
the positions o f images produced by geometrical illusions
o r chromatic aberration can form the basis for stereopsis.
Discrimination o f differences in depth on the basis o f
binocular disparity is known as stereoacuity. Human stere-
oacuity is truly remarkable. Under the best conditions, an
angular disparity o f only about 2 arcscc can be detected,
which is equivalent to detecting a depth interval o f 4 mm at
a distance o f 5 m. M ethods for measuring stereoacuity and
the factors that influence it arc reviewed in Chapter 18.
Binocular disparities can be considered on a point-for-
point basis and there is evidence that the visual system ini­
tially registers disparities this way. Indeed it is difficult to
see how it could be otherwise. Higher levels the visual
system process patterns of disparities, such as differences in
the orientation, size, and shear o f the images in the two eyes.
The visual system also registers spatial gradients o f disparity,
including linear gradients that specify Hat surfaces inclined
in depth, and higher-order spatial derivatives o f disparity
that specify curvature in depth. The geometry o f patterns o f
disparity is discussed in Chapter 19.
The visual system uses disparities to detect depth steps,
surface slant and curvature, and the shapes ol three-dimen­
sional objects. The eyes are separated horizontally, which
introduces disparities along the horizontal dimension.
Consequently, it had been generally assumed that only hor­
izontal disparities are used to code depth. However, rhe
images from an extended surface also possess vertical dis­
parities. We now know that the visual system uses these ver­
tical disparities in a variety of ways, including the perception
o f absolute distance, depth scaling o f horizontal disparities,
and the perception o f 3 -D shape. These issues are discussed
in Chapter 20.
An object in one location can influence the perceived
spatial disposition o f an o b je ct in a neighboring location or
o f an object seen successively in the same location. These
effects come under the heading o f depth contrast and are
discussed in Chapter 21.
The appearance o f an o b je ct or the way we respond to it
can be influenced by it.s perceived distance with respect to
other objects. For instance, the way an object appears to
move with respect to another o b je ct is influenced by how
the objects are arranged in depth. Also, stimuli that interact
when in the same depth plane may cease to interact when
separated in depth. This is a useful feature o f perception
because it allows us to concentrate our attention on objects
in the plane of interest without being distracted by events
occurring in other depth planes. For example, we can
visually pursue a moving object at one distance while ignor­
ing potentially distracting motion signals arising from
objects at other distances. These issues are discussed in
Chapter 22.
The processing of binocular disparity has temporal as
well as spatial characteristics. The question o f how the visual
system processes signals that arrive both at different times
and in different locations is discussed in Chapter 23 .
Volume 2 ends with an account o f stereoscopic instru­
ments and applications o f stereoscopy.
1 .1 .3 VOLUM E 3
Volume 3 deals with information about depth other than
binocular disparity and with how humans and animals
reach, walk, and navigate in 3 -D space.
Information about depth arising from a specified stimu­
lus feature is known as a depth cue. The first four chapters of
Volume 3 are concerned with visual cues to depth. Som e
information about the distance of an object can be gained
from the state o f accommodation o f the eyes. Also, the angle
o f convergence o f the eyes could specify the distance o f a
fixated object. However, these sources o f information are
useful only for near distances because, beyond about 2 m,
accommodation and vergence change only slightly. Chapter
25 deals with these processes.
The impression o f depth can be very compelling when
only one eye is open. Chapters 2 6 and 2 7 review the static-
monocular cues to depth o f perspective and shading.
Chapter 2 8 deals with the dynamic monocular cue o f
motion parallax produced by motion of an observer with
respect to a 3 -D display. The impression ofd ep th created by
motion parallax has a striking resemblance to that created
by binocular disparity. Fundamentally, the two sources o f
depth information are the same.
The next two chapters deal with how depth cues
interact. Depth constancies are one manifestation of this
interaction. Perceptual constancy refers со the abilicy со
perceive a constant feature o f the world when chc proximal
scimulus is noc conscanc. For example, we can perceive the
size o f an o b ject in spice o f chc facc chac chc size o f ics rccinal
image varies wich chc distance o f chc objccc. Also, wre can
pcrecivc chc shape of an o b ject in spice o f the facc chac chc
recinal image changes when chc o b je cts disposicion in 3-D
space is changed.
Depch cues interact in many ocher ways. Informacion
provided by с wo cues may be added or averaged, or one cue
may resolve chc ambiguicy of another cue. Cue interaccions
are investigaced by introducing conflicts between cues. The
conflicc may be resolved by weighting the cues, or one cue
may be ignored. Chapter 3 0 deals these and other ways in
which depch information is combined.
Ic is imporcanc for any animal со be able со detect the
mocion of objects in depch. Animals must avoid dangerous
approaching objects, navigate around objects, pursue
retreating prey, and catch approaching prey. Dececcion o f
motion in depch is also crucial in games such as crickec,
cennis, and foocball. Pcrccpcion o f mocion in depch has сwo
componencs. The first is dececcion o f how long ic will cake
for an objccc со move from one position со another. This is
especially imporcanc when an objccc is on a collision course
wich chc animal. The second componenc is dececcion o f chc
direction in which an objccc is moving. Perception o f boch
componencs depends on informacion provided by chc
mocion o f che recinal images. Firsc, each image grows in size,
an etfecc known as looming. Second, che images in che cwo
eyes change in binocular disparicy over time. Third, chc two
images differ in che way chey move. The signals used in che
visual perccpcion o f objcccs moving in depch and chc ways
chey are processed in che nervous syscem are discussed in
Chapcer 31.
Much can be learned abouc che visual syscem by scudy-
ing clinical defcccs and abnormalities. Damage со che eyes
or chc visual corcex resulcs in defcccs confined со a particu­
lar region o f visual space. Damage со higher centers can pro­
duce visual neglecc, which is an inabilicy со actend со
particular regions of space. Brain damage or generic defects
such as albinism can also produce defcccs o f depch percep­
tion. These issues arc reviewed in Chapcer 32.
W e are largely ignoranc o f how dcpth-detection syscems
evolved. Buc some insight into chc quescion may be gained
by scudying mechanisms o f depch perception chroughouc
chc animal kingdom, from inscccs со mammals. Mosc o f our
knowledge abouc depch perccpcion has com e from chc
study o f cacs, primaces, and humans. Buc chcre is a bewilder­
ing variecy o f visual mechanisms for dececcion o f depch in
che animal kingdom. Chapcer 3 3 briefly reviews some o f
che highly specialized visual mechanisms chac have evolved
in response со che demands o f particular ecological niches.
Relatively simple changes со an existing sensory system
can render an animal sensitive со new stimuli. For example,
injection o f the gene for the red photopigment into mice,
which do not have color vision, allowed them to discrimi­
nate colors. Binocular cells developed in a goldfish when
inputs from the two eyes were forced to grow into the same
tectum. Tliis indicates how stereoscopic vision could have
evolved from a simple rerouting o f axons in the optic
chiasm. These issues arc also discussed in Chapter 33.
Ultimately animals use information about chc distance
and three-dimensional structure o f objects to guide their
movemcncs and chcir manipulation o f objects. Chapcer 3 4
reviews chese processes.
W h ile mosc animals rely principally on vision со locacc
objcccs, nocturnal animals and animals living in featureless
environments or opaque water must rely on the sound, heat,
or electrical fields generated by objccts or reflected from
objcccs. The final chree chapters review the perception of
distance by nonvisual senses. M any o f these sensory syscems
were discovered onlys reccndy.
/
Chapcer 3 5 reviews chc mechanisms chac allow- animals
and humans со judge che discances o f sound sources. The
chapcer also describes how ccrcain animals, such as whales,
dolphins, and bacs, locacc objeccs by ccholocation.
Chapter 3 6 reviews cwo ocher depch-dececcion mecha­
nisms. The firsc is cleccrolocacion. Som e aquatic animals
dccccc electrical pocencialsemicced by ocher animals. Tins is
known as passive electro location. Certain fish cinic electric
currcncs and chen dececc che discorcions o f che resulting
cleccric field produced by objcccs and ocher fish. This is
known as active cleccrolocacion.
The second mechanism discussed in Chapcer 3 6 is
dececcion o f chc discancc o f a source o f hear. C ertain beetles
dccccc discan с forcsc fires and fly coward chcin. They lay
chcir eggs in chc dead crces. Snakes dccccc che hcac cmicccd
by cheir prey.
Ic is remarkable chac several neural mechanisms involved
in ccholocation and cleccrolocacion resemble chose used in
che visual syscem. For example, all these syscems involve par­
allel processing o f discincc fcacures o f che stimuli, which are
dccccccd by discincc cvpes o f reccpcor. Also, chey all involve
hierarchical processing o f increasingly complex features in
higher neural centers.
Navigation involves detection o f boch chc direction and
discancc o f sites beyond che range o f sensory dcccccors. In
one form o f navigation, foraging animals keep a record o f
che discancc and direction o f cheir movemenc from the
home sicc. This is known as pach incegracion. In crue naviga­
tion, an animal can dccccc chc location of a discan С home
site through information available within a given range. For
example, homing pigeons return to cheir home sice from
locations chey have noc visited previously.
Ic has recently been shown that some animals navigate
by sensing the local direction o f the Earths magnetic field.
It seems chat some animals do cliis by sensing molecular
changes produced in special pigments in chc retina. Chapcer
3 7 provides only a b rief review' o f che vase copic o f naviga­
tion, with an emphasis on detection o f distance.
 Saggital plane
V ertical axis
I
Frontal
plane
N aso-tem poral
A nterior-posterior
axis
Figure I I . Axes o f the vertebrate eye. (A fi«r Howland m S Ho<*4 u id
The basic senses o f vision, audition, couch, smell, and
taste were known in ancient times. The vestibular organs
were discovered in 1875, and the sense organs responsible
for kinesthesia were discovered in die 1880s (see Howard
1982). Infrared sense organs in snakes were discovered in
193 7 (Section 3 6 .2 .2 ). Electrolocation in fish was discov­
ered in 1958 (Section 36.1.2). Sense organs sensitive to the
Earths magnetic field were discovered in the last 2 0 years.
There may be other sensory systems to be discovered.
1 .2 B A S IC T E R M S
Consider an axis system consisting o f three orthogonal axes
contained in three orthogonal planes. An in trinsic refer­
en ce system is one that is anchored to identifiable points in
an object. The planes and axes o f a vertebrate eye arc shown
in Figure 1.1 using a terminology recommended by
1 lowland and 1 lowland ( 2 0 0 8 ). The planes and axes o f the
human body are shown in Figure 1.2. These are both intrin­
sic reference systems. An intrinsic reference system requires
at least three noncollinear and identifiable points. The firsc
step is to define a reference point in the object. For the
human body, this is the center o f gravity. Then one defines
x,y, and z axes through the reference point with reference
to identifiable points in the object. In the human body, we
use the midbodv axis (z axis) and лг and axes orthogonal to
the midbody axis, as shown in the figure. Three orthogonal
planes are then defined, each containing one pair o f axes.
T he mid frontal p lan e contains the у and z axes, the
m idtransverse plane contains the x and у axes, and the
median plane (midsagittal plane) contains t h e * a n d saxes.
A frontal p lan e (sometimes called a frontoparallcl plane) is
any plane parallel to the midfrontal plane. These axes and
planes are intrinsic to the 3 -D object and rotate and move
with the object.
M id-body
‘ or z axis
H orizontal
plane
2008)
An external reference fram e is required to specify the
orientation or location of a 3 -D object relative to other
objects. For the human body, roll is the orientation o f the
median plane, pitch is the orientation o f the frontal plane,
and yaw is the orientation of the median plane with respect
to a specified external reference frame.
The following system is often used in the vision litera­
ture to specify the orientation o f a surface relative to a verti­
cal reference plane. In this system, slant is the dihedral angle
between the surface and the vertical reference plane. T i l t is
the orientation o f the axis of slant relative to horizontal.
T ilt can also be defined as the orientation to vertical o f the
plane within which th e normal to the surface moves as the
surface is slanted. Spin indicates rotation o f the surface
within its own plane. It is the orientation o f a defined line in
the surface, such as an axis o f symmetry, with respect to the
original orientation o f that line. These specifications are
illustrated in Figure 1.3.
In most experiments on the visual perception o f orienta­
tion the stimulus is a line or flat surface that is rotated about
only a single axis: a vertical axis, a horizontal axis, or the
visual axis. For such stimuli, the following simplified terms
will be used. A frontal plane is a vertical plane parallel to the
coronal plane o f the head. S la n t is the angle o f rotation o f a
 Vertical S lanted surface rotated
I in its ow n plane through
an a ng le o f spin

Slant

Inclination

Figure i.J. Illu stration o f tilt, slant, am i sp in . T i lt is th e o rien ta tio n o f the

ax is ab ou t w hich a fron tal surface is slanted . Slan t is the angle through
w hich the surface is rotated ab ou t th e tilt axis. Sp in in the angle through
w hich a surfacc is rotated in its own plane w ith rcsp cct to it» original
o rien tatio n .

line or surface about a vertical axis in a frontal plane, signed

positive in an anticlockwise direction viewed from above.
r»g»r« Ы. D e fin itio n s o f slant, inclination» am i tilt. O th e r co n v en tio n s
Л wall with right side away has positive slant and a wall with
will be defined w hen requ ired.
left side away has negative slant. In clin a tio n is the angle o f
rotation about a horizontal axis in a frontal plane, signed
positive in a top away direction. Л floor surfacc has positive
inclination and a ceiling has negative inclination. S lo p e is
reference are listed in che subject index. A list of portraits is
any slant or inclination o f a surface away from a frontal
provided at the end o f each volume. Also, a list o f journals
plane o f the head. T i l t is che angle o f rotation o f a line from
cited and chcir abbreviacions is provided ac che end of each
the verrical abouc an axis orthogonal со a froncal plane,
volume.
signed positive in an anticlockwise direction. Figure 1.4
Throughouc che book, experimencs are suggested, which
illustrates these definitions.
could perhaps decide theoretical issues. These suggestions
The d istan ce o f an o b ject from an observer is sometimes
are printed in italics.
specified by che discancc between the midfrontal plane o f
There is no ocher book in princ dcvoced со che broad
the head and the froncal plane containing the object. Buc ic
copic of depch percepcion. G ibsons 7be Perception o f the
is more useful со specify che discancc of an object in terms
Visual World ( 1 9 5 0 ) was devoced largely со depch percep-
o f its radial distance from an eye or its radial distance from
cion, and his books on ecological optics are relevant (Gibson
a point midway between the eyes (cyclopean eye).
1961, 1 966). There are chapters on depth perception in
Volume 8 of the H andbook o f Sensory Physiology edited by
Held et al. ( 1 9 7 8 ), the H andbook o f Perception an d
1 .3 IN D E X E S A N D R E F E R E N C E S Performance edited by B o l f et al. ( 1 9 8 6 ) , and the Blackwell
H andbook o f Perception edited by Goldstein ( 2 0 0 1 ).
W h en a key term is first introduced, ic is printed in bold There have been several books on stereopsis and bin oc­
type. In the lisc o f references ac che end o f each volume, ular vision, including O gle ( 1 9 6 4 ), Ogle et al. ( 1967),Julcsz
che section numbers where each reference is mentioned ( 1 9 7 1 ), G ulick and Lawson ( 1 9 7 6 ), Solom ons ( 1 9 7 8 ) ,
are entered in square brackets. This lisc serves as che auchor Reading ( 1 9 8 3 ) Regan (1 9 9 1 a ), Howard and Rogers
index. Names o f people noc associated with a specific ( 19 9 5 ) , and Steinman et al. (2 0 0 0 ).
 Hooks on vergence and binocular vision includc Schor Reviews o f stcrcopsis and binocular vision have
and Ciuffrcda ( 1 9 8 3 ) , Pickwell ( 1 9 8 9 ) , Schciman and been provided in journals by Arditi ( 1 9 8 6 ) , Tvlcr (1 9 8 3 ,
W ick ( 1 9 9 4 ), Goss ( 1 9 9 5 ), and Noorden and C am pos 1 9 9 1 ), and Patterson and Martin (1 9 9 2 ). Reviews on
( 2 0 0 0 ). Books on more specialized topics arc mentioned specific topics arc cited at the ends o f relevant sections in
throughout the text. the book.
 2
HISTORICAL BACKGROUND

2.1 The Greeks 9 2.7 Advent o f precise measurement 41

2.1.1 Ionian period 9 2.7.1 Precision visual instruments И
2.1.2 Classical period in 2.7.2 Psychophysics and experimental psychology 41
2.1.3 Alexandrian period 11 2.8 Lmpiricist-nativist controversy 12
2.1.4 Extromission and intromission theories i? 2.8.1 The protagonists 42
2.2 Science in the post-Greek period IS 2.8.2 The debate about eye movements 45
2.2.1 Ncscorians and Persians IS 2.8.3 The debate about visual direction 45
— tM I X Contacts with China 19 2.8.4 Debate about binocular vision 47
2.2.3 Indian centers of learning 19 2.9 Discovery o f perspective Г
2.2.4 Visual scicncc in the Arabic Empire 20 2.9.1 Perspective in the ancient world 4 7
2.3 Medieval Europe 2 4 2.9.2 Perspective during the 14th century 49
2.3.1 Medicine and science in Medieval Europe 2 4 2.9.3 Perspective in rhe Renaissance 5/
2.3.2 Lenses and spectacles 27 2.9.4 Devices for drawing in perspective 57
2.4 Hie Renaissance 2 7 2.9.5 Trompe loeil and anamorphic art 59
2.4.1 Background 27 2.10 Binocular vision 61
2.4.2 Leonardo da Vinci 2 S 2.10.1 Ptolemv on binocular vision 62
4

2.5 16th-and 17th-century Europe 2 9 2.10.2 Alhazen on binocular vision 66

2.5.1 Giovanni della Porta 29 2.10.3 European studies on binocular vision 6$
2.5.2 Benedetto Castelli 30 2.10.4 History o f the horopter 72
2.5.3 Vesalius and the development o f anatomy 31 2.10.5 Physiology o f stereopsis 73
2.5.4 The development o f visual optics 32 2.11 History o f visual display systems 75
2.5.5 Descartes .>5 2.11.1 Early display systems 75
2.6 Beginnings o f visual neuroscience 36 2.11.2 Advent 0 f t he steгсоscope 77
2.6.1 Detailed structure of the nervous system 36 2.11.3 Ster eop hotograp hy 83
2.6.2 Advances in understanding rhe brain 39 2.11.4 Stereoscopic movies $7

2.1 TH E GREEKS
T he Egyptians anil Babylonians practiced medical ophthal­
mology in the third and second millennia B C (Duke-elder
1 961). T h e fibers Papyrus, which originated in Egypt before
150 0 B C contains an account of ointments used to treat
diseases o f the eyes (Thorwald 1 9 6 3 ). In both Egypt and
Babylon diseases were thought to be due to malevolent
supernatural agents. T he Egyptians had some knowledge o f
practical geometry and astronomy, and we will see that this
knowledge was passed on to the Greeks. However, there do
not seem to be any records about their knowledge of optics
o r vision.
The Greeks laid the foundations o f mathematics, logic,
and political philosophy, ethics, and nacural philosophy in
the Western world. However, it must n ot be forgotten that
developments in all these fields were occurring in India and
C hina at about the same time. Also, C h in a was far ahead in
many technologies (Needham 1962). There was a strong
mystical clement in G reek thought. Myscery religions and
oracles, such as those at Eleusis and Delphi flourished. The
notion o f supernatural agents and the immortal soul per­
meated much o f G reek philosophy and science. However, a
few philosophers, such as Thales and the Epicurians, dis­
carded these notions in their theories o f the natural world.
G reek civilization is divided into three periods: Ionian
(pre-Socratic), Classical, and Alexandrian.
2 .1 .1 IO N IA N P E R IO D
The Ionian period originated in the 6th century B C in
trading cities spread over the Mediterranean coastline,
especially in the region o f Ionia, off* the west coast o f
what is now Turkey. T h ales (c. 6 2 4 - 5 4 7 B C ) is credited
with being the first Greek philosopher and mathematician.
He was born and lived in the city o f Miletus on the coast o f
Asia Minor, which at that time was the center o f a large
trading complex. He visited Egypt and brought back the
study o f practical geometry to the Greeks. None o{ his writ­
ings survive, bur commentaries suggest that he tried to
explain natural phenomena without reference to supernat­
ural agents.
P y th ag oras (c. 5 6 9 - 4 7 5 B C ) was born on the Greek
island o f Samos. He traveled widely in the Mediterranean
with his merchant father. Iamblichus (Clark 1989) wrote a
biography o f Pythagoras. W h en he was about 18 years old,
Pythagoras visited Miletus, where he probably m et the
aging Thales and attended lectures by Anaximander.
According to Iamblichus, he spent several years in Egypt,
where he was accepted into the priesthood o f one o f the
temples. W h en the Persians conquered Egypt in 525 В С
Pythagoras was taken to Babylon, where he became
acquainted with Babylonian mystical rites. In 5 1 8 , o r ear­
lier, he moved from Samos to C roton in southern Italy. 4
There he founded a secret society devoted to discovering
the mathematical-mystical principles underlying reality.
For the Pvthagorians, numbers had mystical significance by
which those with knowledge could achieve spiritual purifi­
cation and union with the divine. M any o f the practices and
beliefs o f the Pythagorians resembled those o f the mystical
practices o f the Egyptian priesthood.
A lcm aeo n (c. 5 4 0 B C ) was born in the G reek city o f
C roto n in southern Italy, probably between 5 4 0 and 5 1 0
B C . H e would have been aware o f che Pythagorians but
most scholars believe that he was noc a m em ber o f chac soci-
ecv. He wroce several medical and philosophical works, buc
only a few fragments have been preserved. Ic has been
claimed chac Alcmaeon was the first to dissecc a human eye,
buc chere is no evidence chat he dissected anything other
chan che eyes o f animals. He described the path o f the optic
nerve and proposed that the brain is the center o f percep­
tion and intelligence. For Alcmaeon, vision occurred when
objects are reflected in the surface o f the eye. He developed
a theory of the immortal soul, which was later adopted and
developed by Plato.
E m p ed o cles (c. 4 9 5 - 4 3 5 BC) was born into a
wealthy family in Acragas (Agrigentum) in souchern Sicily.
He was a flamboyant poet, philosopher, and physician.
He was said со possess magical powers by which he could
cure plagues, raise che dead, and control the weather. He
proposed that all chings consisc o f che four clemencs, earth,
air, fire, and water. He added the two forces o f attraction
and repulsion, which he personified as Love and Strife.
Empedocles was perhaps the first philosopher со produce a
cheorv o f perception. He proposed that objects em it efflu­
ences that vary in shape and size and enter the sensory
organs.
2 . 1 .2 С I. AS S 1С A 1. P E R I О D
The classical period o f G reek civilization extended from
4 8 0 to 3 3 0 B C . It began when the Greeks overcame che
Persians, and Athens became che main center of learning.
This was an unsettled period policically, especially during
che Peloponnesian Wars o f 4 1 4 со 4 0 4 B C . After che wars,
Achens came under the domination o f Sparca for 3 0 years.
Nevertheless, G reek art, drama, philosophy, and science
flourished during this period.
S o cra te s ( 4 6 9 - 3 9 9 B C ) was born in Athens. His father
was a sculptor. He worked as a stonemason before he
devoted him self to discussing philosophical issues with the
aristocratic youth o f Athens. He questioned popular opin­
ions, but offered no clear alternative teaching. It seems that
he produced no written work, and our knowledge o f his
thought is derived from the writings o f his pupil Plato.
P lato (c. 4 2 7 - 3 4 7 B C ) was born in Athens o f wealthy
parents. He was a devoted student o f Socrates. He lied from
Achens after Socraces was executed in 3 9 9 B C and traveled
widely in Greece, Egypt, Italy, and Sicily, where he absorbed
Pythagorean ideas chat com bined mysticism and mathemat­
ics. In 3 8 7 B C , Plato returned to Athens and founded the
Academy in a park just outside the city. The word “acad­
emy” was derived from Academus, the name o f a legendary
Greek who had once owned the park. Although there had
been schools in Greece, Babylonia, Egypt, and C hina well
before this cime, Placos Academy was probably the first pri­
vate school for philosophy. It survived for over 8 0 0 years.
Plato remained head o f the Academy for 4 0 years until his
death in 3 4 7 B C .
Plato’s works consist o f a series o f dialogues between
Socraces and ochers. Like Socraces, Plato was chiefly inter-
esced in moral philosophy and regarded natural philosophy
as an inferior form o f knowledge. In che Tiwacus, Plato
described the cosm os— the macrocosm— as a living entity
with an immortal soul created by a god (see Bury 1946).
Lesser gods created the human body from the four elements
o f earth, water, air, and fire. From Alcmaeon he adopted che
idea o f a divine immortal soul that dwelled in the brain,
which was connected to the sense organs. It was the mission
of the reasoning immortal soul to create an internal copy
(the microcosm) o f the harmony and beauty o f che cosmos
(m acrocosm). A vegetative soul dwelling in the guts was
responsible for bodily functions, lusts, desires, and greed.
A vital soul located in the heart was responsible, along with
the blood, for higher motives, such as courage, and for excit­
ing the body into action.
For Plato, geometry and musical harmonies represented
the divine unchanging truth behind reality. He rejected art
and sensory impressions as imperfect. The Academy there­
fore stressed che teaching o f geometry. However, Placo was
noc a creacive mathematician and certainly/ noc a scientist.
Am ong che pupils o f che Academy were che geomecers
Eudoxus ( 4 0 8 - 3 5 5 B C ) and T lica ctetu s (417-3 69 ),
whose work laid the foundations for Euclid’s Elements o f
Geometry. Eudoxus, like Thales and Pythagoras before him,
spent some time as a guest o f the Egyptian priesthood. He
taught M cn aech m u s ( 3 8 0 - 3 2 0 B C ) , who seems to have
been the first person to describe the conic sections.
A risto tle ( 3 8 4 - 3 2 2 B C ) was born in northern Greece
but grew up in Macedonia bccausc his father was physician
to the King o f M acedonia. At the age o f 17 Aristotle was
sent to study in Plato’s Academy in Athens, where he
remained for 2 0 years. Plato was 44 years older than
Aristotle, and conflicts between the two men soon devel­
oped. Unlike Plato, Aristotle valued the empirical study o f
natural phenomena. In 3 4 3 B C , King Philip o f Macedonia
appointed Aristotle to be tutor to his son Alexander.
Aristotle returned to Athens in 3 3 5 B C , where he founded
the Lyceum. W h en factions opposed to Alexander became
active in Athens in 3 2 3 , Aristotle fled from Athens and died
o f disease in 3 2 2 B C .
Aristotle was an encyclopedist and observer o f natural
phenomena. But, for him, every living thing had a soul that
sought perfection and union with the divine. The human
soul consists o f three faculties— nutritive, sensitive, and an
immaterial rational soul (nous). Nevertheless, Aristotle was
an empiricist in that he believed that all knowledge has its
source in sensation. He distinguished five senses and three
perceptual qualities (sensibles). Proper qualities, such as
color and sound, were peculiar to one sense organ. C om m on
qualities, such as motion or shape, were apprehended by
more than one sense organ. Inferential qualities were those
associated with a familiar o b ject or person. He distin­
guished between immaterial forms received by sense organs
and the material objects from which the forms arise.
However, he had no clear conception o f what he meant by
forms. It is odd that Aristotle placed the seat o f sensation
and reasoning in the heart.
W h en Aristotle left Athens he bequeathed his library
and manuscripts to his student Th eo p h rastu s (c. 3 7 0 - 2 8 6
B C ). Theophrastus became director o f the Lyceum and for
the remainder o f his long life he made Aristotle’s theories
widely known. We are indebted to Theophrastus for most
o f our knowledge ofearly Greek visual science.
D e m o critu s (c. 4 6 0 - 3 7 0 B C ) was born in Abdera in
Thrace into a noble and wealthy family. He visited F.gypt,
Persia, and India. A t some time he was instructed in
Pythagoreanism and became a disciple o f Leucippus, from
whom he acquired the atomic theory. He was interested in
all branches o f science. H e eventually returned to Abdera,
where he gave public lectures.
According to the atomic theory, the world is composed
o f an infinite number o f indivisible atoms in the void o f
space. The atoms differ in shape, arrangement, and magni­
tude. All natural events are due to the endless aggregation
and disaggregation of atoms. There are no gods but the
whole universe is animated by a soul, which is made o f rhe
lightest and most mobile atoms. Dem ocritus expanded
ideas derived from Empedocles. He introduced the idea o f
images (eidola) emitted from objects and received by the
senses, where they give rise to sensation (aesthesis) and
thought (noesis).
Ep icuru s ( 3 4 1 - 2 7 0 B C ) was born on the island o f
Samos. He spent some time in Athens, where he probably
attended Plato’s Academy and the Lyceum. However, he
rejected Plato’s ideal forms and adopted the atomistic
system o f Democritus. In the year 3 0 6 B C , he and a group
o f followers established a school in Athens known as the
G ard en . Unlike the other schools it admitted women and
slaves. M embers pledged themselves to a life o f simple co m ­
munity and the study o f the master’s philosophy.
Epicurus, like Democritus, did n ot believe that super­
natural agents controlled natural processes. He believed
that the soul was corporeal and did not survive after death.
Consequently, Jews, and Christians rejected these beliefs.
Epicurus rejected all forms o f superstition and magic. He
claimed that gods exist in the hearts o f men rather than in
the heavens. The Garden, along with the other Athenian
Schools, was disbanded in A D 5 2 9. There was a revival of
interest in Epicurianism with the publication o f Pierre
Gassendi ’s L ife an d M anners o f Epicurus in 1647. This book
influenced the British philosophers Thomas Hobbes, John
Locke, and John Stuart Mill, as well as Thomas Jefferson.
F.picurus was an empiricist, holding that all knowledge
originates from sensations derived from the five senses.
However, he was primarily a philosopher rather than a sci­
entist. In his theory o f perception he adopted the ideas o f
Democritus. According to these ideas, objects em it thin
replicas (eidola) composed o f atoms that contact sense
organs to producc sensations. W ith the aid o f memory, gen­
eral abstract ideas are developed and used to classify sensa­
tions into recognizable categories. Errors occur only when
the wrong category is applied to a given sensation.
H ip p o cra tcs (c. 4 6 0 - 3 8 0 B C ) was born on the island
o f C o s (K os) o ff the coast o f Asia M inor, where he founded
a medical school. He has been called "the father o f m edi­
cine.” The Hippocratic Corpus consists o f about 6 0 trea­
tises. People other than Hippocrates probably wrote most
and perhaps all o f them. The best-known treatise is the
Hippocratic oath, which was most likely n ot written by
Hippocratcs. Hippocrates and his followers, including
Herophilus, dissected animal and human eyes and described
the main parts o f the cvc.
2 . 1 .3 A L E X A N D R IA N P E R IO D
The Alexandrian period of Greek civilization began in 3 3 0
B C , when rhe center o f learning shifted from Athens to
Alexandria, the Egyptian city founded by Alexander che
Great. Pharaoh Ptolemy Soter (died 2 8 3 B C ) was the first
Greek ruler of F.gypt. Like Alexander, he had been a stu­
dent o f Aristotle. He founded the Museum o f Alexandria,
using state funds to support over 100 scholars. It contained
a huge library, lecture rooms, an observatory, a zoo and
botanical garden, and dissecting and operating rooms.
Several scholars from Aristotle’s Lyceum were brought over
from G reece to help in founding the Museum.
G reek rule over Alexandria ended in 3 0 B C , when
Egypt becam e a Roman province and the last Egyptian pha-
raoh, Q u een Cleopatra, died. Part o f the great library was
destroyed during Caesars siege o f Alexandria. The other
part survived until A D Зб 1. when it was destroyed by a mob
after the Christian emperor Theodosius ordered thedestruc-
tion o f pagan temples. Thus, G reek science survived in
Alexandria for several centuries after the cicv cam c under
Roman rule. Alexandria became a city of schools, many of
which were devoted to mystery religions.
There were four main strands in philosophy and science
in Alexandria. The first was the development o f a medical
school in which dissection o f human bodies was first prac­
ticed. The second was the development o f mathematics and
the application o f geometry to the visual system. The third
was the development o f astronomy. Finally, Alexandria was
a cosmopolitan commercial city, where people o f many
races and from many countries interacted. It became the
center o f diverse syncretic mystical cults that combined ele­
ments from different religions, including Judaism,
Hinduism, Christianity, Gnosticism, and Zoroastrianism.
2 . 1 . 3 a Herop hilus and Erasistratus
Ihere were several physicians in rhe Museum o f Alexandria.
Herophilus ( 3 3 5 - 2 8 0 B C ) and Erasistratus ( 3 0 4 - 2 5 0 B C )
have been described as the fathers o f anatomy. They dis­
sected human cadavers in public and for the first time. It
seems that they alsodissected living criminals (Fraser 1972).
Egypt had an ancient tradition o f dissecting bodies as part
o f the process o f mummification.
The anatomists in the Museum described the nerves
leaving the brain and spinal cord as a network o f fibers dis­
tinct from tendons and blood vessels. They dissected the
human brain, described the convolutions o f the cerebral
cortex, and distinguished between sensory and motor
nerves. They also discovered the brain ventricles, from
which they believed vital spirits flowed to the muscles along
hollow nerve fibers.
Many G reek philosophers, including Alcmaeon,
Anaxagoras ( 5 0 0 - 4 2 8 B C ) , and Hippocrates ( 4 6 0 - 3 7 5
B C ) proposed that the brain was the center o f mental activ­
ity and visual perception. However, Aristotle, Empedocles,
and other G reek philosophers continued to place the
center o f thinking in the heart and relegated the brain to
cooling the blood. O n this question, Aristotle’s disciple,
Theophrastus, disagreed with Aristotle and placed the
center o f sensation in the brain. The anatomists o f in
the Museum o f Alexandria did n ot doubt that the brain
was rhe center for sensation, thinking, and the control
o f action.
2 . 1 .3 b E u clid
Euclid (c. 3 2 3 - 2 8 5 B C ) was born one year before Aristotle
died. It is n ot known where he was born, but he lived in
Alexandria. Euclid was familiar with the geometry o f
Eudoxus and Thcactctus, who worked in Plato’s Academy in
Athens. This suggests that Euclid studied in the Academy.
Euclid’s thirteen books o f the Elements o f Geometry
placed the whole o f geometry known at that time into an
orderly sequence. The Elements were written in G reek but
were later translated into Arabic. They were first translated
into Latin from the Arabic by Adclard of Bath (c. 1 0 8 0 -
1152), tutor to Henry II o f England. The first translation
into English was by Sir I lenry Billingsley in 1570. It was che
primary textbook o f geometry at least until the advent o f
non-Euclidcan geometry in the 19th century. It is one o f
the most published and studied books o f all time.
O th er extant works o f Euclid include two other works
on geometry {D ata and On Divisions), a book on astron­
omy ( Pbaenom ena ), and the Optics.
Euclid’s Optics was written in Alexandria in about 3 0 0
B C . It is the earliest known book on the subject. Burton
( 1 9 4 5 ) produced an English translation. The term “optics"
is derived from the G reek word for vision. Until the 17th
century, optics was mainly che science o f vision. It included
the study o f reflection (catoptrics) and refraction (diop­
trics) because of their effects on vision. The term “optics”
now refers to the physics o f light, whether visible or not.
New terms such as “physiological optics,” “ophthalmology,”
optometry," and “visual science” are used for the study o f
vision and visual perception.
Aristotle and other G reek scholars before Euclid had
applied geometry to vision but Euclid’s Optics was the first
systematic treatment. It laid the foundation for geometrical
optics, leading through Ptolemy and Alhazen to Kepler. In
the G reek period, the mathematical approach to vision
became distinct from the philosophical approach and devel­
oped a distinct terminology. People following the mathe­
matical tradition that was built on the geometry o f light
rays became known as Perspectiviscs. They laid the founda­
tion for the use o f perspective in cartography and painting,
and for projective geometry and visual science. The philo­
sophical tradition continued as metaphysics and cpistcmol-
ogy. The two traditions are still with us,each with its distinct
literature. There is little con tact between them.
Euclid’s Optics begins with seven definitions, or postu­
lates. They declare that light proceeds from the eye in
straight lines in the form o f a cone, or pyramid, with its apex
centered on the eye. O n ly objects on which the cone o f light
fills arc visible. O b jects subtending a larger angle at the eye
appear larger. O b jects intersecting rays higher in the cone
are seen above those intersecting lower rays, and objects
intersecting rays to the left are seen to the left o f those inter­
secting rays to the right. Today we would encompass these
postulates by setting up polar coordinates on the retina.
The seventh postulate states that objects on which more
rays fall are seen more clearly. This postulate arose from
Euclid’s assumption that the visual pyramid contains a fixed
number o f distinct rays. W it h increasing distance, an object
becomes less visible because fewer rays strike it. Eventually
the object becomes invisible because it falls between rays.
The same idea can be expressed in modern radiomctry or in
wave optics (Koenderink 1982). Theoretically, we can now
divide light flux into rays, each containing one photon per
unit time. The amount o f spatial information available to
any optical instrument is the number o f rays tailing on the
instrument per unit area. N o optical instrument can exceed
the limit imposed by the discrete nature o f light quanta and
the wavelength o f light. Additional limitations on the spa­
tial sampling of the image in an optical system are imposed
by the optics o f the system and by the density o f receptors.
Euclid derived 6 5 theorems from his seven postulates.
Nearly all the theorems are concerned with geometrical
relationships between the lengths and directions o f light
rays and the angles subtended at the eye by lines, arcs, and
surfaces. Although Euclid wrote about the appearance o f
objects, most o f his theorems refer only to the geometry o f
what we now call the optic array. A few o f the later th eo ­
rems refer to illusions, or perceptual effects arising from
properties o f the visual system.
Today we would express almost all Euclid’s theorems as
statements linking the geometry o f light rays to the shapes
and positions o f retinal images, without any reference to
appearances. The theorems form part o f whac we call physi­
ological optics. Euclid’s theorems and proofs are still valid,
except for his statements about emission o f light rays from
the eye. But direction of the rays docs n ot affect the geom­
etry. Several o f Euclid’s theorems are listed in Table 2.1 with
corresponding statements in terms o f the geometry of the
retinal image.
T a b le 2 .1 . A S F .I .F .C T I O N O F F .U C L I D ’ S T H E O R E M S W I T H E Q U I V A L E N T S T A T E M E N T S IN M O D E R N T E R M S
E U C L I D 'S T H E O R E M
Fu r л h o riz o n ta l s u r fa c c lo c a te d a b o v e ey e le v e l, th e p a rt* fu rth e r
away a p p e a r low er.
A n a r c o f a c ir c le p laced o n th e sam e p la n e as th e eye a p p e a rs as a
s tra ig h t lin e .
W h e n th e c v c a p p ro a c h e s a sp h ere, th e p a rt seen w ill b e le ss, b u t
w ill seem to b e m o re .
l o r a sp h e re w ith a d ia m e te r sm a lle r th a n th e d is ta n c e b e tw e e n th e
ey e s, m o re th a n th e h e m isp h e re w ill b e se en .
W i e n th e e y e m o v es n e a re r to an o b je c t , th e o b je c t w ill ap p e a r to
g ro w larg er.
W h e n o b je c t s m ove a t e q u a l sp e e d , th o se m o re r e m o te м е с т to
m ove m o re xlowlv.
r
Today we distinguish between the geometry o f retinal
images (physiological optics) and accounts o f visual sensa­
tions (psychophysical functions), because we know that a
given retinal image produces different sensations depending
on the context. Euclid knew nothing about the retinal image.
He did not describe experiments or apparatuses since he was
concerned only with the geometry o f light rays and relied on
mathematical proof. Presumably, he made visual observa­
tions buc he did not mention such things as shape constancy
or aftereffects, which do noc follow from his cheorems.
Euclid described how a near objecc occludes a far objccc
by an extenc that varies with the position o f cheobjeccs with
respect to the horizon and their distances from the eye. He
extended this analysis to explain how an eye can n ot sec the
whole of one half of a sphere. H e then described how two
eyes see more o f a sphere or cylinder than either eye alone
when the object is smaller than the interocular distance. He
was thus aware that the two eyes obtain different views o f a
solid object but did n ot state that this is a cue to depth. We
refer to this type o f difference between the two eyes’ views
as occlusion disparity to distinguish it from disparity in the
positions o f the images o f the same o b ject (Section 17.2).
W e refer to depth impressions caused by occlusion dispari­
ties as da Vinci stereopsis (Section 17.3).
Several o f Euclid’s theorems describe the basic principles
o f linear perspective. They declare that line elements sub­
tend different visual angles to an eye according to their rela­
tive inclinations to the line o f sight and their distances from
che eye. Theorem 6 scates that parallel receding lines on a
horizontal surface appear to converge. Theorem 8 states
chat "Equal and parallel magnitudes unequally discan с from
che eye do noc appear (inversely) proportional to their dis­
tance from che eye.” Euclid’s cheorem is correct for a spheri­
cal image plane like the retina, as shown in Figure 2.1.
Image size is inversely proportional to distance only for a
R E S T A T E M E N T IN T E R M S O F R E T I N A L I M A G E
M o re d is ta n t o b je c t s o n a c e ilin g p la n e p r o je c t o n th e re tin a ab ov e
n e a re r o b je c t s .
A n a rc in a p la n e c o n ta in in g th e n o d a l p o in t
p r o je c ts o n th e re tin a as a s tra ig h t lin e .
W h e n th e eye a p p ro a c h e s a sp h e re , le ss o f its su rfa c c p r o je c ts o n th e
re tin a b u t th e im a g e in c re a s e s in a re a .
F o r a sp h e re w ith d ia m e te r less th a n th e in tc r o c u la r d is ta n c e , th e
c\rc lo p c a n im a g e e x te n d s b e y o n d h alf th e sp h ere.
The mac o f t h e im a g e o f a n o b je c t is i n \ c r * c l y p r o p o r t i o n a l t o th e
d is t a n c e o f t h e o b je c t f r o m t h e e y e .
T h e a n g u la r v e lo city o f an o b je c t m o v in g a t con% tant lin e a r v e lo city is
in v ersely p r o p o r tio n a l to its d is ta n c e .
 А 8
^ - ч ч Im age planes
bi*«rc 2 . 1. It I usem itart o f Euclid'* theorem S. The image produced on a flat
im age plane by vertical line В is tw ice at lo n g as th a t produced by line
A , tw ice as far from th e eve. B u t th e image produced on a spherical
im age plane by line В is less chan tw ice th at p roduced by a line tw ice
as far from th e eve. In deriving theorem 8 Euclid used л diagram that
illu strated p ro jectio n o n a curved surface.
flat retina (Section 26.1.2 ). Several theorems deal with co n ­
ditions under which circles appear as ellipses.
O n e o f his theorems describes how a line element o f a
given length subtends the same angle when its ends touch a
circle passing through che eye. Another describes how a fixed
object subtends the same angle when the eye moves along an
arc o f a circle passing through the ends o f the object. This
theorem is a short step from proving that the horopter is a
circle through the two eyes and the fixated object, but chis
p ro o f had со wait until 1804 (Section 2.10.4).
Seven o f che final theorems deal with visual mocion.
O n e describes how an o b ject moving at the same speed as
che eye seems со scand still, while objects moving at ocher
speeds appear to move. Another states that a stationary
o b ject appears to move in the opposite direction to the
motion o f nearby objects. W e call chis induced motion
(Section 2 2 .7 ). Ocher theorems state thac, as che eye moves
toward an object, the object seems to grow larger, and thac
an object increasing in sire appears to approach che eye.
Finally, Euclid stated that o f objects moving ac equal speed,
chose more remoce seem slower.
O n che face o f it, these seven final theorems seem со
refer со percepcual effects chac Euclid had observed.
However, even these theorems may be restated in terms o f
geomecrical objcccs. For example, che chcorcm on image
size could be restated in the following way. An increase in
che size o f an objccc ac a fixed distance may create the same
change in che bundle o f lighc rays as chac crcaccd by an
approaching o b ject o f fixed size. So, finally, there is some
uncertainty about whether F.uclid was writing only about
geometrical properties o f lighc rays chac he had deduced or
abouc visual phenomena chac he had observed.
2 . 1 . 3 c Apollonius
Apollonius (c. 2 4 0 - 1 9 0 B C ) was born in the Greek city of
Perga on the southern coast o f Asia Minor. He did most o f
his work in Alexandria, where he interacted with men who
had studied with Euclid. He was called “The great geom e­
ter.” He was a contem porary o f Archimedes o f Syracuse
( 2 8 7 - 2 1 2 B C ) , another giant o f mathematics. His main
work was che treatise on conics ( Conica ). It provided a gen­
eral theory ol conic sections, to which he gave che names
ellipse, parabola, and hyperbola. These words com e from
Greek words meaning “to fall shore ofT “to throw as far as,”
and “to chrow lurcher chan,” respectively. Originally, chev
probably referred to throwing rhe javelin. Apollonius was
apparently che firsc person со realize that the curves are sec­
tions o f one circular cone. He generated a circular cone by
anchoring the center o f a line and swinging one end round
che rim o f a circle. This generated cwo cones meeting at a
point. W'hen he cut a section through one cone to produce
a hyperbola a second hyperbola was produced in che ocher
cone. Thus, che cwo branches o f che hyperbola were seen as
a single curve. However, no G reek geomecer fully general­
ized che conic sections to include che plane or line. He came
close со developing che notion o f axes.
G reek geomecrv, like che geomecry o f the ancient
Egyptians, was grounded in the metrical measurement o f
lines, angles, and areas. Abstract notions o f the continuum
o f points on a line, points at infinity, and nonmetric gcom-
etries such as topology were alien to G reek choughc.
O f che ciglu books o f che Conica only che firsc four were
preserved in Greek. However, chree o f che last four books
had been cranslaced by Arabic scholars in Baghdad in che
9th cencury and becam e known in Europe after they
were translaced inco I.acin in 1661. An F.nglish cranslacion
was produced by 'loonier ( 1 9 9 0 ). The writings o f Euclid
and Apollonius dominaced geomecry for cwo chousand
years. The theory o f conic sections developed into the
theory ol perspective and projective geometry (see Sections
2.9 and 3.7.2c).
H eron o f A lexan d ria wroce on optics in abouc che year
A I) 62 . He explained che laws o f reflection by the principle
chac lighc rays travel by che shorcesc pach, and developed a
mechod for solving quadratic equations. He also invenced
che pneumatic device known as Heron s Fountain.
I f any imporcanc advances in vision occurred in che 4 5 0
years becween che 3rd century B C and Ptolemy in che 2nd
cencury A D all records o f chem have been lose (Hahm
1978).
2 . 1 .3 d Ptolemyф
Claudius Ptolemaeus, or P tolem y (c. A D 1 0 0 - 1 7 5 ) , was a
Greek-speaking astronomer, optician, and geographer living
in Alexandria during che reigns o f rhe R om an emperors
Hadrian and Marcus Aurelius. Although past its heyday,
Alexandria was still a greac center o f learning.
Ptolemy is besc known for his work on planetary orbics,
which h esero u c in che M athcrnatikesyntaxis. Arabic schol­
ars called ic A / tnaghesti, meaning "che greatest book.”
In F.uropc ic became known a s the Almagest. Ptolemy’s
Geographia contains procedures for making maps and co n ­
tains 2 7 maps (sec Section 2.9.1). He also wrote Tetrabiblos,
a book on astrology in which he speculated about the influ­
ence o f planetary configurations on human affairs.
Som e time later, Ptolemy• wrote a five-volume work in
Greek, entitled Optics. It received little attention in
Ptolemy’s time. However, after its translation into Arabic,
probably in the 9th century, it became known to Arabic
scholars and formed one o f the foundations for Alhazens
Rook o f Optics in the 11th century. The first book o f
Ptolemy’s Optics and parts o f rhe fifth book were lost before
Alhazens time. The other parts survive in a Latin transla­
tion o f the Arabic version made during the latter h alf o f the
12th century by Emir (Admiral) Eugene o f Sicily.
A t that time Sicily was flourishing under Norman rule
and was a meeting place for Arabic, Byzantine, and Greek
scholars and for scholars from Western F.uropc. Latin ver­
sions o f Ptolemy’s Optics from the I 4 t h century still survive
in Berlin, Paris,and the Bodleian Library,Oxford. Alhazens
Rook o f Optics was translated into Latin with the title De
aspectibus at about the same time. Alhazens book eclipsed
Ptolemy’s Optics, which became almost forgotten until very
recently. Govi published a Latin version in 1885. Lcjcunc
(1 9 5 6 ) produced a greatly improved annotated version of
the Latin text and a translation into French (Lcjcu nc 1989).
Smith ( 1 9 9 6 ) produced an English translation. The brack­
eted numbers in the following refer to volume and para­
graph numbers in Sm ith’s translation.
Historians of science have concentrated on the sections
o f Ptolemy’s Optics that deal with what we now call physical
optics, but Ptolemy’s real interest was in vision and visual
perception. He adopted Euclid’s geometrical analysis o f
visual ravs, but his investigations extended into visual per­
ception and, particularly, visual illusions. Ptolemy described
light as a form of energy, and realized that objects are not
visible unless illuminated. He nevertheless retained the
notion that light is emitted from the eye in the visual
pyramid— a cone-shaped bundle o f rays that produce
sensations when they strike an object. He placed the apex of
the pyramid at the center o f curvature o f the cornea. He
insisted that light rays form a continuous bundle rather
than a set o f discrete rays separated by spaces, as Euclid had
postulated. He pointed out that if light rays were discrete,
objects would appear discontinuous and a small o b jcct that
fell between rays would become visible again if the eye
moved. The rays arc what wc now call visual lines, and the
central ray, or “proper axis,” is the visual axis. He argued that
only the central ray, which is normal to the corneal surface,
forms a clear sensation. O th er rays fall on the cornea
obliquely and produce blurred impressions in the visual
periphery. He had no clear idea o f image formation and
made no mention o f the optic nerves or brain.
Book 1 is lost but a summary in Book II indicates that
Book I dealt with the relationship between light and the eye.
In Book II, Ptolemy discussed light and color and various
classes o f stimuli, such as objects, sky, and shadows. He
divided vision into three stages. The first involved the initial
contact between the eye and rays extending to external
objects. The second stage involved the immediate registra­
tion o f simple visual properties such as color, size, and dis­
tance. The third stage involved perceptual judgments
derived by inference from the simple properties.
According to Ptolemy, visual Hux leaves the eyes at great
speed to strike external objects and feel them. The further
the flux extends from the eye the weaker its capacity to sense
what it touches. The direction o f an o b ject is detected by
the angle the ray makes with the visual axis (II, 2 6 ). T he size
o f an o b jcct is provided by the angle formed at the eye by
the ravs from the extremities o f the object. The distance and
slant o f a near o b jcct are apprehended by the lengths o f the
rays that strike its surface. The distance o f a far object is
apprehended by the dimm ing o f the image with increasing
distance.
He described how an o b je c ts perceived size depends on
its angular subtense, its distance, and its inclination to the
frontal plane (II, 5 2 - 6 2 ) . He noted that a change in the
perceived distance of an object allects its perceived size.
These ideas form the basis o f what wc call size constancy
and shape constancy. H e discussed lateral motion in terms
o f the changing visual rays intersecting an objcct, and
motion-in-depth in terms o f shortening or lengthening o f
rays (II, 7 6 - 8 1 ) . He described how shading creates an
impression o f 3-D in an otherwise flat surface (II, 128).
Ptolemy described several visual illusions. For example,
he described how a person on a stationary boat on a swiftly
flowing river perceives the boat as moving. We refer to this
phenomenon as visually induced self-motion, or vection.
W h en the person looks at the shore the river appears to
move and the b o at is seen to be stationary (II, 131).
He also described how the portrait of a face appears to
follow a moving observer. He explained how the gaze o f
the painted face remains aligned with the visual axis of the
viewer as it would if the face were real and moved with the
viewer (II, 133).
Books II and HI also contain an account o f the geom e­
try o f binocular vision. This account is described in detail in
Section 2.10.1 o f this chapter.
Books III and IV deal with reflection (catoptrics),
including reflection from convex, concave, and polygonal
mirrors.
Book V deals with refraction. Phenomena due to refrac­
tion, such as the apparent bending o f a half-submerged
o b jcct and the magnification o f objects seen through a
bottle o f water, were well known to the Greeks and Romans,
but Ptolemy seems to have been che first to investigate
refraction quantitatively. He measured angles o f incidence
and refraction by h a lf submerging a protractor in water
and aligning a point seen in rhe water with a point above
the water (Delam brc 1912). He did this for various
com binations o f transparent media, and set out the results
in a table. He concluded that the ratio o f these two angles is
constant for a given pair o f media. This is approximately
true for small angles. The correct rule is that the ratio o f the
sines o f the angles is constant.
Several other Greek geometers flourished in Alexandria
after Ptolemy. These included D io p h a n tu s (c. A D 2 0 0 -
284) and Pappus (c. A D 2 9 0 - 3 5 0 ) . Pappus wrote
M athem atical Collections, which is a commentarys on all
G reek mathematics known in his time. It deals with rhc
geometry of spirals, conic sections, and other curved sur­
faces. Tw o well-known theorems bear his name. O n e of’
them concerns the generation o f a solid by revolution of a
plane and the other is a generalization o f the theorem of
Pythagoras, which is now part o f projective geometry.
Pappus was the first to announce the invariance o f cross-
ratios o f four collinear points in polar projection (Section
3.7.2c). There was little advance in geometry between the
3rd and 17th centuries.
The surviving part o f the great library in Alexandria was
destroyed by a mob in A D 361 after the Christian emperor
Theodosius ordered the destruction o f pagan temples.
To understand this period o f history, and subsequent
developments in European thought, we must take a look at
the conglomeration o f intellectual and mystical ideas in
Alexandria at that time.
2 . 1 .3 e A le x a n d ria as a C e n c c r o f M y stery R e lig io n s
During the early centuries A D Alexandria was a melting
por o f mystical ideas deriving from Egyptian mystery cults,
Hinduism, Persian Zoroastranism, Judaism, Christianity,
and Greek mysticism.
In the 2nd century A D the Christians set up a school
next to the Museum to counter what they regarded as heret­
ical teaching. O n e of its students, A m m o n iu s Saccas,
turned against an exclusively Christian dogma and founded
the Eclectic school, in which he advocated the idea o f a
universal brotherhood based on a mix o f several mystery
religions.
P lotin u s (A D 2 0 4 - 2 7 0 ) studied at the Eclectic
school for many years. He was born in Egypt but traveled in
Persia and studied Indian philosophy before going to live in
Rome, Plotinus was the founder o f what came to be
known as Neoplatonism. Neoplatonism epitomizes the
syncretic fusion o f mystical thought from many cultures
that occurred in Alexandria at that time. The writings o f
Plotinus and those o f his student Porphyry exerted an
influence on the G nostic cults that arose in Alexandria.
These ideas became fashionable again in Renaissance Italy.
An Islamic Neoplatonism is evident in contemporary
Sufi theology.
Tlieon (c. A D 3 3 5 - 4 0 5 ) taught mathematics and
astronomy in Alexandria and was one o f the last members o f
the Museum before it was destroyed. His daughter Hypatia
(c. A D 3 7 0 - 4 1 5 ) taught mathematics and philosophy in
the Neoplatonist school in Alexandria. She became head o f
this school in about A D 4 0 0 . For Christians, the teaching
o f the school was heresy, and Hypatia was murdered by a
Christian m ob in the year 4 15 . It is ironic that the teachings
o f Plotinus and the occult Ncoplatonic 2nd-century litera­
ture from Alexandria became the focus o f interest in
Christian Renaissance Italv.
2 .1 .3 Г G a le n
Galen (c. A D 1 2 9 - 2 0 1 ) was born in Pergamon, Asia Minor,
which was part o f the Roman Empire. He was the son o f an
architect and was educated in Pergamon, Smyrna, and
Alexandria. He practiced medicine in Pergamon, and was
involved in healing gladiators in the amphitheater. At age
3 2 he went to Rome, where he became a friend o f Emperor
Marcus Aurelius and physician (medicus) to three succeed­
ing emperors. M uch o f his extensive writing perished in a
fire in A D 191. His book l)e иfa parti ton corporis hum ani
(O n the uses o f parts o f the human body), which he c o m ­
pleted in A D 175, is available in English translation
(May 1 9 6 8 ). It consists o f 17 books, with Book 10 devoted
to the eyes.
Galen dissected pigs, oxen, goats, and tailless apes, but
n ot humans. He also experimented on living animals. For
example, he cut nerves and the spinal cord to reveal what
functions they served. Sometimes he erroneously general­
ized his findings to humans. He based his anatomy o f the
eye on Herophilus of Alexandria, who described the eyeball
and optic nerve in about 3 0 0 B C . The optic chiasm was first
described by Rufus o f Ephesus (c. A D 5 0 ) working in
Alexandria. A spherical lens at the center o f the eye was
thought to be the recipient organ and an extension of the
brain. Galen regarded the retina as an organ that nourishes
the lens. It has been suggested that the lens was placed at the
center o f the eye because it tends to migrate there in the
dead eye. Galen also proposed that each optic nerve is a
hollow tube, which projects from the rear surfacc o f the lens
to the lateral cerebral ventricle on its own side o f the brain.
He referred to these ventricles as the thalami, meaning
“inner chambers,” but overlooked the organ that we now
call the thalamus.
According to Galen, “visual spirit,” or pneuma, is co n ­
veyed from the brain to the eye along the hollow optic
nerve. Pneuma leaves the eye and interacts with the air to
form a sentient medium, which extends to distant objects.
This is essentially the same cxtromission theory developed
by the Stoics and Platonists 6 0 0 years earlier (Section 2.1.4).
He argued that visual spirit conveys sensations from the
lens along the optic nerve to the cerebral ventricles, where it
mixes with “animal spirit.” Animal spirit is generated in the
base of the brain from “vital spirit” arriving from the heart.
The animal spirit is stored in the cerebral ventricles and
circulates through nerves to different parts of the body.
Galen discovered the ventricles by dissecting a sheeps brain.
The notion that circulating fluids carry sensory information
and signals to muscles was consistent with the prevailing
theory o f four vital fluids, or humors. Л hydraulic theory o f
brain function survived into the 17th century and was
adopted by Descartes. Galen rejected Artistotle's notion
that the seat o f sensation is in the heart. He concluded from
observing effects o f head injuries that the brain is the seat o f
“reason,” or 'mind,” rather than an organ tor cooling the
blood, as Aristotle had proposed.
Galen stated that th co p tic nervescombine in die chiasm
to unite impressions from the two eyes into a single image
and direct the flow o f visual spirit into one eye when the
other eye is closed. This idea gave rise to the idea o f a cyclo-
pean eye located at the chiasm. W e shall see that this idea
was not overthrown until the 17th century. We now use the
term “cyclopean eye” to refer to the fact that we judge direc­
tions o f objects as if we sec from a single eye midway between
the eyes {Section 16.7). Galen described the six extraocular
muscles, although n ot accurately.
Galen adopted Euclid’s optics. He described binocular
parallax and how each eye sees distinct parts o f an object,
such as a cylinder, which are com bined into a unified visual
impression. However, he did n ot relate this to the percep­
tion o f distance or solidity. He suggested that binocular
vision is advantageous because it extends the field o f view.
Book 10 contains a condescending explanation of why he
docs not describe the geometry o f light rays and binocular
vision. He stated that his readers would nor understand
geometry and would hate him tor explaining it. The little
geometry he did provide is inaccurate and vague. Perhaps it
was Galen who did not understand geometry. Until at least
the 13th century, Galen’s writings were treated as dogma,
which inhibited experimentation. Siegel ( 1 9 7 0 ) reviewed
Galen’s theories o f perception.
Like Hippocrates and Aristotle, Galen believed that
four humors— black bile, yellow bile, blood, and phlegm,
circulated in the bodv. Diseases caused bv fluid imbalance
i •
were “cured” by bleeding, purging, or the application o f
herbs. Many procedures carried out today under the name
o f alternative medicine are no better.
The Romans developed land surveying, architecture,
and engineering but added little to mathematics or science.
Marcus Vitruvius Pollio, known as Vitruvius, produced his
great work on architecture in about the year 2 0 B C . He
included some discussion o f optics. Gaius Plinius Sccundus,
known as Pliny ( A D 2 3 - 7 9 ) , wrote the 3 7 books o f his
N atural History , which contain some mathematics.
2 .1 .4 E X T R O M IS S IO N AND
IN T R O M IS S IO N T H E O R IE S
The Greeks were apparently the first to inquire into the
nature o f vision. O ver time, two theories emerged— rhe
extromission theory, also known as the emanation and
emission theory, and the intromission theory. Each o f them
occurred in various forms.
The extrom ission th eo ry is o f uncertain origin but it
has been identified with the Stoic philosopher Heraclitus
(c. 5 3 5 - 4 7 5 B C ) and with Empedocles (c. 4 9 5 - 4 3 5 B C ).
The theory was adopted by Alcmaeon, who was associated
with the Pythagorean school (early 5th century B C ) . Plato
(c. 4 2 7 - 3 4 7 B C ) , and Hipparchus ( 1 6 0 - 1 2 5 B C ) . Galen
adopted essentially the same theory in the 2nd century A D
(Cherniss 1933).
In the Timaeus Plato proposed a variant of the extromis-
sion theory. A stream o f light corpuscles from the eye
coalesces with external light rays to create a sensory ray
within a cone-shaped volume o f air reaching out from the
eye. Each ray in the cone o f air becomes an active sensory
medium throughout its length. But this happens only after
the fusion o f external light and rays from the eye somehow
transform the air. The sensory rays feel the forms and
sizes o f the objects on which they impinge, like the fingers
o f the hand. The information is simultaneously conveyed to
the eve.
The Stoic philosophers and Plato’s disciples in the
Academy adopted similar extromission theories o f vision.
However, during the 3rd and 2nd centuries B C , these
two groups disagreed about the reliability of sensory infor­
mation and its relationship to knowledge (von Standcn
1978).
Several theorists regarded the image that can be seen
reflected in a persons cornea as crucial to the visual process,
believing that it represented the seen image seen by the
person. Aristotle refuted this idea and explained that the
image in the cornea is formed by reflection.
The extromission theory was designed to solve the prob­
lem o f how the visual world is externalized and seen in its
proper size. In touch, the problems o f external reference
and proper size were regarded as solved because the fingers
touch an external o b ject and the impression formed on the
skin has the same location and size as the object. So, in
vision, something had to leave the eyes to touch an o b je ct so
as to detect its shape and size. But they realized that seeing
also requires external light, since one ca n n o t see in the dark.
Thus, they concluded that the two forms o f light must
somehow interact. Thedistance o f an o b ject was thought to
be sensed by the length o f the light ray in the same way that
the distance o f a touched o b ject is sensed by the degree to
which the arm is extended.
The idea that the eye emits light may have been inspired
by the flash seen when a finger is pressed against the eye in
the dark— the pressure phosphene. This observation was
credited to Alcmaeon o f C roton in the 6th centuryШ B C .
The extromission theory also provided an account of how
the visual world is actively explored by eye movements and
by focused attention. It was not a logically impossible
theory. Bats and dolphins explore their surroundings wirh
emitted sounds (see Chapter 35).
 Euclid, about 3 0 0 B C , adopted a simplified version o f
the extromission theory. He postulated that light rays leave
the eye in straight lines and that all objects on which they
fall are seen. Ptolemy, in the 2nd century A D , adopted the
same theory. Neither o f them made any attempt to define
the nature o f the rays. Nor did they explain how the rays
detect objects and convey information back to the eye.
Rather, they used the idea o f rays as a mathematical tool to
analyze the geometry of vision. Their analysis would have
been the same i f they had postulated that light rays enter
the eye rather than leave it.
The in trom ission th eo ry was developed by Epicurus
( 3 4 1 - 2 7 0 B C ) , a follower o f the atomise school, founded
by Leucippus (c. 4 3 0 B C ) and his pupil D em ocritus (c. 4 6 0
B C ). He proposed that objects continuously em it 3-D
images o f themselves, known as eidoLt or simulacra. The
images maintain the shape of the o b ject and move in straight
lines into the eye through the intermediate translucent
medium. Epicurus realized that images must shrink as they
enter the eye. The atomists were then left with the problem
o f how the image o f a given object shrinks by the correct
amount for observers at different distances. The substance
o f the images was variously described as atoms, corpuscles,
or an ephemeral substance that peeled o ff a seen object, like
the skin of an onion.
Aristotle ( 3 8 4 - 3 2 2 B C ) , in his D e anim a (Aristotle
1 9 91 ) and De sensи >rejected the extromission theory. He
argued that, according to this theory, we should be able to
see in the dark. He also rejected rhe idea o f a substance
emitted by the object. Instead, he stated that images travel
to the eye as a disturbance o f the transparent medium o f rhe
air, which he called the diaphanous medium. For Aristotle,
light could n ot travel in a vacuum. The disturbance was
thought to impresses itself on the eye like a seal expresses its
form on wax without anv transfer o f material from seal to
wax. However, Aristotle occasionally expressed things in
terms o f the extromission theory. For example, in his
Meteorologicay he accounted for the rainbow in terms o f
visual lines leaving the eye. Alexander o f Aphrodisias in
about A D 2 0 0 suggested that Aristotle used the extromis­
sion theory in this context for mathematical convenience
(see Frangenbcrg 1991).
Aristotle did n ot mention light rays but he had the idea
o f rectilinear propagation, since he realized that one sees
double when a given point in space does n ot fall on corre­
sponding places in the two eyes. He described how an object
on which the gaze is fixed appears double when the eyes are
caused to misconverge by pressing against one eye with the
finger (see Bcare 1906, 1931). This is perhaps the earliest
known reference to binocular disparity. He did not discuss
how the sizes and shapes of objects appear different when
rhe objects are viewed from different distances o r angles.
George Stratton ( 1 9 1 7 ) translated Aristotle’s De sensu
(O n rhe senses) into English. See Lindberg (1 9 7 8 ) for
details on the intromission-extromission controversy.
See Siegel ( 1 9 7 0 ) and Hahm ( 1 9 7 8 ) for accounts o f Greek
theories o f vision.
After the Roman conquest o f Greece, G reek learning
continued with declining vitality in Greece, Rome,
Alexandria, and in the Eastern Roman Empire o f Byzantium.
The three great centers o f learning in Athens: the
N coplatonist Academy, the Lyceum, and the Garden were
disbanded in A D 5 2 9 by order o f Justinian, the Christian
emperor o f Byzantium. Many o f the Greek-speaking schol­
ars migrated to Syria and Persia, taking their Greek manu­
scripts with them.
2.2 S C I E N C E IN T H E P O S T - G R E E K
P E R IO D
2 .2 .1 N E S T O R IA N S A N D P E R S IA N S
In the middle o f the 2nd century A D the small kingdom o f
Osrhoene became the first Mesopotamian kingdom to be
Christianized (see W hipple 1 936). Christian scholars in
F.dcssa, the capital o f Osrhoene, translated the Old
Testament into Syriac. At about the same time, Jewish
scholars in Alexandria had produced the G reek version o f
the O ld Testament, the Septuagint. The scholars o f Edessa
learned G reek so that they could compare the two versions.
As a consequence, they became familiar with Greek m edi­
cine and philosophy. In about A D 3 6 4 they established che
theological and medical school o f Edessa.
In A D 4 2 8 , a priest named Ncstorios became patriarch
o f Constantinople. Three years later he was deposed by the
orthodox Catholic C hurch at the C ouncil o f Ephesus
because o f a dispute about when chc soul enters the body.
He and his followers were excommunicated, whereupon
they formed rhe Nestorian Church and moved to Edessa.
The school o f Edessa became the center o f Nestorian teach­
ing and the center o f learning in the Middle East. The
Christian emperor Z eno had che school abolished in 4 8 9 .
The Nestorians fled to Persia, India, Turkestan, and China.
Nestorian communities still exist in southern India.
Remains o f Nestorian churches have been unearthed in
China.
King Kobad, o f the Sassanid dynasty, ruled Persia from
4 8 8 to 5 31 . He welcomed the Nestorians to Persia, where
they established a school o f medicine in the city o f G ondi-
Shapur (Gundishapur) in southwest Persia. Here they
brought their translations o f Hippocrates, Galen, and
Aristotle. King K obads successor. K ing Nushirwan sup­
ported the school during his long reign ( 5 3 1 - 5 7 8 ) .
Justinian, the Christian emperor o f Byzantium, dis­
banded che Ncoplatonist Academy in Athens in A D 529.
King Nushirwan welcomed the exiled G reek scholars to the
university of Gondi-Shapur, which became the world s lead­
ing center o f learning during rhe king’s reign. The school
had a facultv o f astronomv wich an obscrvacorv. W ith in che
Ф в 4
city, G reek J e w i s h , Nestorian, Persian, and Hindu scholars
exchanged ideas. The principal language was Syriac. The
great teaching hospital, the Bimaristan, was built near the
medical school. This was the first hospital defined as a place
for healing. The scholars at G ondi-Shapur reestablished the
method o f learning developed by the Greeks in the
Alexandrian School. They met every day to read and discuss
ancient texts. The medical school became the model for all
subsequent medical schools in the Middle F.ast.
The Mohammedans captured Gondi-Shapur in 6 3 8 ,
but the school continued until the 10th century. The
Abbasid caliph, al-Mansur, employed 1 0 0 ,0 0 0 workers to
build Baghdad between 7 6 2 and 7 6 6 . He founded a medi­
cal school and the world s firsr free public hospital. Baghdad
was the intellectual capital o f the world until the Mongols
sacked it in 1258. Many scholars moved from G ondi-
Shapur to the new school. Nestorians and the school o f
Gondi-Shapur thus formed a vital link that preserved G reek
learning and transmitted it to the Arabs when scholarship
was at a low ebb in Europe.
2 . 2 .2 C O N T A C T S W IT H C H IN A
During the late Roman and medieval periods, there was a
to-and-fro (low o f goods and ideas between C hina and the
Middle East over the 7,400-kilom eter Silk Road through
Turkestan to Persia, Syria, and Constantinople. Also, in the
medieval period, huge Chinese boats (junks), which were
able to carry 1,000 men,sailed between Gungzhou in C hina
to India, Arabia, and Alexandria. To the East went glass
manufacture, irrigation techniques, grapes, carrots, and
Buddhism. To the West came gunpowder, the compass, the
stirrup, silk, jade, porcelain, paper, chickens, peaches, and
tea. A Nestorian priest is said to have brought the first silk
worm eggs back to the West hidden in a bamboo staff
(Carter 1955).
Paper was perhaps the most im portant item to be
imported from C hina. It laid the foundation tor the devel­
opm ent o f printing and the subsequent explosive develop­
ment o f learning and science in the West. The invention o f
paper is credited to Tsai Lun in A l ) 104. Paper reached
Samarkand between the 4th and the 6th centuries. In the
8th century, the Persians learned how to manufacture paper,
and it began to replace parchment. The 5th and most
famous Abbasid caliph, Harun-al-Rashid ( 7 6 4 - 8 0 9 ) , o f
Arabian Nights fame, ruled the Muslim empire at the peak
o f it power. H e imported Chinese papermakers and
established a paper factory in Baghdad in 7 9 4 . A factory
established in Damascus became the main source o f
paper in Europe. The technique o f papermaldng entered
Europe through Spain. The first paper mill in Christian
Europe was founded in 1157 on the French side o f the
Pyrenees. In Germany, paper was first made in Nuremberg
in 1 3 9 0 at about the time that block printing developed in
that citv.
i before being passed to the Arabs, and then to Europe.
Block printing and movable type printing were first
developed in C h in a in the T in g dynasty (A D 6 1 8 - 9 0 6 ) .
But most o f the Buddhist temples that contained printed
material were destroyed in the civil wars that brought the
Tang dynasty to an end. The oldest known printed book
comes from C h in a and is dated 8 6 8 . Islamic law forbade the
Koran to be printed. Since the Koran was thought to be the
only book worth reading, very few books were printed in
the Islamic world until 1825, when the first press was estab­
lished in Cairo.
See Needham ( 1 9 6 2 ) for a detailed treatment o f early
Chinese science.
2 . 2 .3 IN D IA N C E N T E R S O F L E A R N IN G
Various land and sea trading routes had intermittently co n ­
nected India with the Middle East since the 14th centuryJ
B C ( O ’Leary 1964). A bout 6 0 0 B C , a comprehensive trea­
tise on anatomy, medicine, and surgery, known as the
Sushruta sarnheta was written in the classical language o f
Sanskrit. It is attributed to Sushruta, who has been called
the “father o f surgery," but there were probably several
authors spread over a period o f time. It contains an account
o f eye diseases, such as glaucoma. Sushruta may have been
the first person to perform operations for cataracts.
Pythagoras and Dem ocritus visited India at about that time
and it has been suggested that many o f the ideas in the
Sushruta saw heta were brought back to Greece (Bidyadhar
1941). The text was translated into Arabic in the 8th
century A D .
Alexander the Great conquered parts o f northern India
in the 3rd century B C , but his stay there was short-lived. In
A D 3 2 0 the G upta dynasty was founded in northwest
India. The G upta kings founded a center o f scientific stud­
ies in the city o f Pataliputra. Also, an observatory was built
in the city o f U jjain, which had been a center o f trade with
the G reco-R om an world since the 2nd centurv A D . The
mathematicians and astronomers in Ujjain had access to
G reek writings, including those o f Euclid and Ptolemy.
They developed the study o f mathematics by using Hindu
numbers, a decimal system, and algebraic symbols. In the
7th century the astronomer Brahmagupta wrote an astro­
nomical manual known as the B rah n a Siddhanta
(Knowledge o f the sun).
In the year A D 8 1 0 , Mohammed ibn Musa al-
K hw arizm i (died 8 4 7 ) introduced the Brahm a Siddhanta
into the Middle East, where it became known as the
Sindhind. It introduced Hindu numbers into the Arabian
empire. Two hundred years later, these same astronomical
tables introduced the Hindu number system, now referred
to as Arabic numbers, into Europe. AI-Khwarizmi was the
founder o f systematic algebra (al-jabr). The term “algorithm”
is derived from his name. Thus, India formed a second co n ­
duit by which G reek learning was preserved and extended
 2.2.4 V I S U A L S C I E N C E IN T H E
A R A B IC E M P IR E
The Prophet Mohammed was bom in M ecca in A D 571.
T he Muslim Empire eventually stretched from Samarkand
to Spain. It lasted until the Tartars overran the city o f
Baghdad in the 13th century. The Moslem Empire toler­
ated other religions and races. Scholars working in the
empire included Arabs, Persians, Jews, and Christians.
Harun al-Rashid,becam e the Abbasid caliph in 7 8 6 . He
and his son, al-Ma’mun who reigned from 8 1 3 to 8 33 ,
founded the House o f W isd om {B ait al-H ikm a) in their
capital city o f Baghdad. Many o f the most learned Muslim
scholars worked in this research and educational institute.
The Abbasids followed the injunction in the Koran that
“the ink o f a scholar is more holy than the blood o f a martyr."
During this period Baghdad was the intellectual center for
science, philosophy, medicine, and education. The library
became the center lor translation o f G reek works into
Arabic. During the reign o f al-Ma’mun, emissaries were sent
to the Byzantine Empire to collect Greek manuscripts,
which were then translated into Arabic.
Egypt came under the control o l the Fatimid dynasty in
9 69 , after the fall o f the Abbasid Caliphate. The Fatimids
claimed descent Irom Fatima, the daughter o f the Prophet
M oham m ed. At its greatest extent, their empire stretched
along the southern Mediterranean coast Irom Syria to
Algeria and included Sicily. They traded with India via the
Red Sea.
2 . 2 . 4 a J o h a n n itiu s
Hunayn ibn Ishaq ( A D 8 0 8 - 8 7 3 ) , known in the West as
Johannitius, was a Nestorian Christian born in the town ol
Hira and educated in the medical school in Gondi-Shapur.
At an early age he began translating Greek texts into Syriac,
his m other tongue. Later he worked in Baghdad under rhe
patronage o f the Abbasid caliphs. He was the most prolific
and precise translator o f Greek medical, scientific, and phil­
osophical works. H e translated Euclid, Aristotle, Plato, and
almost all the works o f Galen. He also improved transla­
tions produced by earlier Nestorians. He traveled to Syria,
Palestine, and F.gypt in search o f ancient manuscripts. For
Nestorian Iriends and pupils he translated Greek texts into
Syriac, a language that disappeared from literature in the
14th century. For Arabic patrons he translated into Arabic.
It was these translations that were later translated into Latin
in Europe. In addition, he wrote more than 100 books o f
his own in Arabic. These included Ten Treatises on the Eye
and the Book o f the Questions on the Eye. These works were
very influential in Islam. The Ten Treatises were translated
into Latin in rhe 11th century. This translation contains
the earliest known diagram of an eye and was the principal
source o f information for Western scholars about
Galen’s theory (F.astwood 1982). Johannitius adopted the
G alenic-Stoic theory o f vision in which rays from the eye
interact with light rays to form a sensory medium in the air
that reaches o u t to sense objects. His translations were so
valued that he is said to have received their weight in gold in
payment. Many leading scientists in the next generation
were his pupils. For an account o f his life and times see
M eyerhof (1 9 2 6 ).
2 . 2 . 4 b A1 K in d i
The first great Islamic scholar was Abu Yusuf Ya’q uib ibn
Ishaq al-Kindi, a person o f royal descent born in the late 8th
century in the city o f Al-Kufa, which is now in central Iraq.
I le worked in Baghdad under the patronage o f the Abbasid
caliphs and died in about 8 73 . He was an optician, musical
theorist, pharmacist, mathematician, and philosopher. I le
wrote about 2 6 0 books, but most have n ot survived. He
devoted him self to the teaching o f Aristotle. His most
important extant work on vision was based on Euclid and
Ptolemy. It survives in a Latin translation made in the 12th
century by Gerard o f C rem ona; entitled l)c aspectibus. It
became a popular textbook, and its influence lasted lor
hundreds o f years.
In line with his holistic and magical view ol the universe,
al-Kindi believed that everything in the world produces
rays in all directions, like a star, and that this radiation binds
the world into a network in which everything acts on every­
thing else to create natural and magical effects. Al-Kindi
adopted Euclid’s geometrical approach to vision, although
he criticized several o f Euclid’s ideas. For example, he argued
that the visual rays emanating from the eyes arc continuous
rather than discrete (Lindberg 1971). He conducted exper­
iments with shadows to establish the rectilinear propaga­
tion o f light. He described how a clear view o f an object is
built up by scanning the object with the ray o f clearest
vision— the visual axis. In spite o f this theoretical approach,
and in spite o f his experiments, he clung to the emanation
theory o f vision. He argued that the 3 -D eidola o f the atom-
ists could not account lor effects o f perspective, such as the
elliptical appearance o f a circular object viewed at an angle.
I le falsely reasoned that only an emanation theory could
account for perspective. Like his contemporary, Hunayn
ibn Ishaq, al-Kindi adopted the Galenic-Stoic theory o f
vision. He did not realize that his theory o f light rays radiat­
ing in all directions provided a basis lor a more satisfactory
theory (see Lindberg 1978).
2 . 2 . 4 c Avicenna
Attacks on the extromission theory appeared in the writ­
ings o f the Islamic physician Abu Bakr Muhammad ibn
Zakariya al-Razi ( A D 8 6 0 - 9 3 2 ) , known as R hazes because
he was born in Rai in Persia. These attacks continued in the
works o f his younger contemporary al-Farabi (Alpharabius)
(d. 9 5 0 ) and Abu Ali al-Husain ibn Abdullah ibn Sina (A D
9 8 0 - 1 0 3 7 ) , known in the West as Avicenna.
Avicenna was bom in Bokhara and became physician
and vizier to the emir in Hamadan and later worked under
the patronage o f the sultan o f Isfahan in Persia. His great
book Qaniin (C an on ) reviewed ancient and contemporary
medical knowledge and was used in Arabic lands and in
Europe for six hundred years. His writing was clearer and
more systematic than was Galen’s. He discussed vision in the
Canon and in several other books, including De anim a sen
sextus de naturalibus, which still exist. He refuted the emana­
tion theory o f vision in all its forms. He adopted Aristotle’s
theory ot visual optics and Galens ideas on visual anatomy.
In his Book o f Directives an d Remarks he described the
cosmos as a series o f symbols through which one could seek
knowledge o f the Divine (gnosis). See Lind berg( 1976) for a
discussion o f al-Kindi, Avicenna, and other Islamic scholars.
2 .2 .4 d A lh a z e n
O f the Islamic scholars, Alhazen (Abu Ali al-Hasan ibn al-
Hazan ibn al-Haytham) made the most significant contri­
butions to optics and vision (see Bauer 1912; W in ter 1 9 5 4 ;
ten Doesschate 1 9 6 2 ; C rom bie 1967). He was born in
about A D 965 in Basra in what is now southern Iraq. He
moved to Cairo, where he spent the rest o f his life teaching
and writing in che Azhar mosque and university under the
patronage o t the Fatimid caliph Al-Hakim.
Alhazen died in about 1040. In his autobiography he
tells very little about himself, but provides a list o f ninety-
two o f his works, more than sixty o f which have survived.
He made significant contributions со physics, astromomy,
mathematics, optics, and vision.
Alhazen was a devouc Muslim and wrote books on phi­
losophy and theology. He stated that his empirical investi­
gation o f the world was based on the teaching o f the Quran.
He argued that only God is perfect so that to discover truth
about nature one must not trust the sayings ot others but
only knowledge gained by empirical observation. Human
error can be eliminated only by letting nature speak tor
itself. Articles o f faith should not be applied to mathemat­
ics or to the examination o f nature. Investigators should
approach a problem from every side and critically examine
their own conclusions to avoid error and prejudice (Qadir
C A 1990; Sabra and Hogcndiijk 2 0 0 3 ) . This description o f
the scientific m ethod probably inspired Adelard, Magnus,
Bacon, and others to express similar ideas in Europe two
hundred years later (Section 2.3.1).
In the seven books o f his great synthetic work, the Rook
o f Optics (Kitdb aU wandzir), he systematically summarized
whac was known about vision. He also used geomecrv and
experimental observation to explore new phenomena and
develop new theories.
Alhazen was familiar with the writings o f Aristotle,
Galen, and Ptolemy and with the Conics o f Apollonius,
although he did not make explicit reference to them.
He used the same division ol the subject into vision troin
rectilinear rays, vision by reflection, and vision by refrac­
tion, as in Ptolemy’s Optics. He also used a similar tripartite
division o f vision into image formation, immediate percep­
tion, and inferential perception. Alhazens work was not
well known in the Middle F.ast for 2 5 0 years after his death,
but became generally known after Kamal al-Din Abdu’I-
Hasan al-Farisi (died c. 1 3 2 0 ) produced his Tanqih al-
m andzir (Revision o f the Optics) in about the year 1300 in
Iran. This book reviewed all the subjects discussed by
Alhazen and was supplemented by criticisms and new ideas
(Sabra 1987a).
In the 12th century, an unknown person translated
Book o f Optics into Latin with the title Perspectiva.
Fourteen medieval manuscripts produced between the 13th
and 15th centuries survive. In Basel, in 1572, Risner pro­
duced the Opticae thesaurus, A lhazeni arabis libri septum,
which contains the first printed version o f Alhazens book
with added titles and annotations. It also contains V itellos
book Perspectiva, a 13th-century work based largely on
Alhazen. The Opticae thesaurus became the principal source
for optics in Europe until the 17th century. The original
Arabic version o f Alhazens Book o f Optics produced by
Alhazens son-in-law in 1083 was unknown to Western
scholars until 1913, when Rescher made a brief announce­
ment o f its existence, but it remained unnoticed until che
investigations o f Krause in 193 6 (see Polyak 1 941). In 1989,
A. I. Sabra o f the Department o f the History o f Science at
Harvard University produced an English translation o f the
first three books o f the Book o f Optics from the original
Arabic version in Istanbul. In the following summary che
numbers in brackets refer to pages in Sabras translation.
Book I o f the Book o f Optics is devoted mainly to visual
optics and the structure o f the eye. Alhazen firmly rejected
the emanation theory ot vision and described how rays ot
light enter the eye from sources o f light such as the sun and
from objects that reflect and refract light. In the Greek
intromission theory, a visible object issues a copy o f itself to
the eye. This raised the problem o f how multiple copies can
be sent to a multitude o f eyes over an extended period, and
the problem ot how a copy o f a large object can enter che
pupil. In solving these problems, Alhazen adopted al-Kindis
idea that light radiates in all directions from each point o f
an object. Instead o f an o b ject issuing copies o f itself, each
point on an object emits or reflects light rays in all direc­
tions and those rays that enter the eye produce an image.
This geometrical analysis o f visual rays solved the problems
raised by the older intromission theory and laid the founda­
tions of modern geometrical optics, although Alhazen
regarded light rays as geometrical conveniences rather than
as real.
Alhazen experimented with a “dark cham ber” into
which lightencered through a small hole ro form an inverted
image. This was what we now call the pinhole camera,
or cam era obscura (sec Section 2.9.4). Al Kindi had also
described such an instrument (W erner 1910). Also, a
camera obscura was described in the M o Ching, a Chinese
work from the 4th century B C , and was used back then to
prove that light travels in straight lines (R on an 1978). The
invention o f the camera obscura is often credited to Roger
Bacon or Leonardo da Vinci.
The pinhole camera works because the aperture is so
small that only a narrow beam ot light passes from each
object poinr to a each image point. Alhazen understood
that the image is sharp only when the hole is small. He
described how an eclipse o f the sun could be safely observed
by looking at the image produced by a hole in the wall ot a
dark chamber. He used the image produced by a pinhole to
prove that light rays travel in straight lines and pass through
a small aperture without interacting. The camera obscura is
discussed in Section 2.11.1 b.
Since the Muslim religion forbade dissection, Alhazen
based his ideas ot the anatomy ot the eye on Galen. Figure
2.2 shows a diagram o f the eyes and visual pathways from
the earliest known copy ot Alhazens book. This diagram
O p tic nerve
C ornea
Figure 2 .2. . M iattrit d iag ram o f th e visual system. D iagram from the B o o k o f
O ptics (K icab al-m an azir) by A lh azen , copied bv his son-in-law in 1 0 8 3
from an earlier version {M S 3 2 1 2 , Faith L ib rary in Istan b u l). T h e lower
figure is a key to che parts.
and a diagram in Book 111 arc the only figures in the original
text. O th er diagrams were added later in Latin translations
(Bauer 1912).
Alhazen realized that the pupil is too large to allow the
eye to work as a pinhole camera. Although he did not
understand image lormation by a lens he realized that, lor
clear vision, each point on the recipient surface in the eve
must receive light from only one o b ject point. He was thus
confronted with the problem o t how light from each object
forms a disrinct image on the surface o f the lens without
being diluted by rays from other objects.
The solution Alhazen adopted was that the surface o f
the cornea and the front surface o f the lens are concentric,
so that those ravs striking the two surfaces at right angles
pass unrefracted through the com m on center. He proposed
that only rays striking each point on the surface o f the eye at
right angles are allowed to pass into the sentient interior ot
the lens. He realized that other rays arc refracted, and
assumed that, because o f this, they are weakened (p. 124).
W e now know that most rays falling on a given point on the
cornea reach the retina, but that each ray is refracted to a
point on the retina appropriate to its point o f origin in the
part o f the visual scene on which the lens is accommodated.
There is nevertheless some truth to Alhazen s idea o f
the predominance o f orthogonal rays. Light rays normal to
the retinal surface are more likely to enter the elongated
visual receptors than are rays at any other angle. This is the
Stiles-Crawford effect (Section 5.1.2a). Also, the c o m ­
pound eyes o f insects work in the way suggested by Alhazen,
since each ommatidium accepts light from only a narrow
visual angle.
In B ook V, Alhazen questioned his own theory and
admitted that refracted rays as well as normal rays are
detected. He thus grappled with the problem o f how the
cornea and lens form a clear image by refraction, but he
failed to find a solution (Sabra, p. 116; Lindberg 1976,
p. 7 6 ). A solution was n ot forthcom ing until Kepler devel­
oped a theory ot image formation in his A d Vitellionetn
Pandipomcna in 1 6 0 4 , which was published in his Dioptrice
in 1611.
Alhazen stated that the initial process o f sentience,
which we now call visual processing, occurs along radial
lines in the interior o f the lens. In his account, the lens senses
the images (forms) o f objects defined by the cone o f light
rays that com e from the surface o f the object. The rays enter
the lens after striking the cornea and lens at right angles.
Each object produces a distinct cone o f rays, so that objects
are seen distinct from each other. He argued that the image
must be sensed before the rays converge to a point. In the
first place, sensation can n ot occur at the point where the
rays converge because images ot distinct objects would all
be fused together. In the second place, sensation cannot
occur after that point because the image would be inverted.
He believed that the rear surface o f the lens is mounted on
the optic nerve. Like Galen, he believed that the form
(image) is conveyed along a sec o f hollow cubes in each optic
nerve to the optic chiasm where the images from the two
eyes fuse into the sensus comunus. He realized chat the recti­
linear propagation o f light determines the spatial integrity
o f the initial image. He also realized that once the “form” is
conveyed into the curved optic nerve its spatial integrity
depends on retention o f the relative order o f parts within
the optic nerve, rather than on rectilinear propagation. We
make a similar distinction between the retinal image formed
by rectilinear propagation o f light rays and topographic
projection along the axons ot the optic nerve.
Alhazens description o f image formation and his c o n ­
cept o f an image were very hazy (Eastwood 1986). Sabra
( 1 9 8 9 ) describes the uses that Alhazen made o f chc Arabic
word tor “torm” or ' image." Alhazen s ideas on basic visual
processes, erroneous though they were in many ways, set the
stage tor subsequent developments in physiological optics
and, ultimately, for Kepler’s account o f image formacion.
In addition to the discussion o f optics and the structure
o f the eye, Book I contains descriptions o f several percep­
tual phenomena including visual masking, dark adaptation,
afterimages, chc dependence o f acuicy and color perccpcion
on luminance (pp. 5 1 - 5 4 ) , and color mixing (p. 97 ). Book
I also contains a description o f corresponding retinal points
(p. 8 7 ), diplopia o f images tailing on noncorresponding
points, and fusion o f those falling on corresponding points
(see Section 2 .1 0 .2 ). Alhazen argued that the eye is round
so that it may be moved quickly to bring the images o t dif­
ferent objects o n to the region o f clearest vision— the region
wc call the fovea (p. 104). He explained that clear vision is
built up from che separate impressions obtained as the gaze
moves over che scene.
Book II contains some discussion o f image formation in
the eye but is concerned mainly with visual perception.
Although Alhazen referred to the lens as chc sentient struc-
cure he also stated that no sensation is accomplished until
the image arrives in che brain (p. 8 9 ). This seeming
contradiction is resolved when we read that only the two
primary sensory features o f light and color are sensed at the
recipient surface. The rest o f the 2 2 visual features that
Alhazen listed, such as direction, distance, size, shape, c o n ­
tinuity, m otion, and transparency, arc derived trom patterns
o flig h t and color at a higher level by recognition, inference,
and memory.
Today we say chac the first stages of’ visual processing
occur in the retina to be followed by further stages in the
brain, involving complex interactions and memory. Wc also
distinguish, as did Alhazen, between the initial, preatten-
tive, impression o f a visual stimulus and impressions gained
after higher levels o f processing (p. 2 0 9 ). Alhazens views on
the role o f inference and experience at an unconscious level
(p. 136) are very similar to H elm holtzs theory o f uncon­
scious inference (see Sabra 1 978). Alhazen also described a
level o f perception involving conscious knowledge (see
Q .W a n g e t a l . 1994).
Book II also contains descriptions o f basic visual fea­
tures such as direction, distance, size, shape, continuity,
m otion, and transparency. The phenomena include color
constancy (p. 141), additive color mixing on a spinning top
(p. 145), the role o f texture gradients and the ground plane
in the perception o f distance (pp. 152, 179), size constancy
(p. 177), and the contribution o f eye movements to the
perception o f motion (p. 193).
Book III is concerned with errors and illusions in visual
perception. There are descriptions o f the equal motion o f the
eyes (p. 2 2 9 ), induced visual motion (p. 2 6 1 ), and many other
visual phenomena. The book also contains Alhazens ideas on
binocular vision, which are reviewed in Section 2.10.2.
Books I V to V II are devoted со reflection and refrac­
tion. Alhazen made paraboloid mirrors, probably on a lathe,
and explained how parallel rays arc brought со a single focal
point by such a mirror, although D io d es had proved this in
chc 2nd cencury B C . Alhazen rcpcaccd Ptolemy’s measure­
ments o f refraction, but failed to find the sine law, even
though he knew Hindu trigonometry. He discusscd magni­
fication by a plano-convex lens.
Alhazen described the apparent enlargement o f the
m oon near the horizon, an effect known as the m oon illu­
sion (sec Section 29.3 .5). In the Almagest, Ptolemy explained
the m oon illusion in terms o f refraction o flig h t through the
atmosphere. However, in chc Optics he explained ic in terms
ot an illusory size change induced by differences in apparent
distance. Cleomedes, who probably lived in the first cen ­
tury A D , had offered a similar explanation (Ross 2 0 0 0 ) . In
C h in a, Shu Hsi proposed a perceptual explanation o f the
moon illusion in che 3rd or 4ch century A D (see Needham
1962, vol. 3, p. 2 2 6 ) . Alhazen, also, proposed an explana­
tion o f the moon illusion in terms o f che relationship
between apparent size and apparent distance (see Ross and
Ross 1 9 7 6 ; Sabra 1987b; Plug and Ross 1994). However, in
a collection ot writings on the moon illusion, Alhazen did
not rule out a possible contribution from refraction (Sabra
1996). Books IV to V II o f Alhazens Book o f Optics have not
been translated into English.
Although Alhazens Book o f Optics inspired many co m ­
mentaries and derivatives, it was noc superseded until the
early 17th century. Alhazens discoveries in optics and phys­
iological optics contained in Book I have been extensively
reviewed. His discoveries in visual perception, described in
Books II and III, were mentioned by Priestley ( 1 7 7 2 ) and
reviewed by Bauer ( 1 9 1 2 ) . However, they have been almost
totally ignored by visual scientists, and many o f the phe­
nomena discussed by Alhazen are described as having been
discovered only in the last two hundred years (Howard
1996).
It has been claimed that Alhazen founded psychophys­
ics (Khaleefa 1 999). However, his methods were almost
wholly descriptive. There is no evidence that he developed
general methods for quantifying visual phenomena
(Aaen-Stockdale 2 0 0 8 ).
 2 . 1 .4 c Islamic C e n t e r s o f L e arn in g in Spain
In the 8th century, Islamic civilization spread westward
from its ccntcrs in Egypt, Damascus, and Baghdad. In the
10th century, the Umayyad caliph, uUHakam IIestablished
Arabic and Jewish ccntcrs o f learning as far west as Sicily
and C ord oba in Spain. His court in C ordoba contained an
enormous librarv and attracted the foremost scholars. It
outstripped any other center o f learn ingin Europe. Maslama
al-Majriti (d. 1 0 07 } founded a school o f mathematical and
astronomical studies in C ordoba. The Hindu astronomical
tables that al-Khwarizmi had introduced into Baghdad in
A D 8 1 0 were brought to C ordoba. Maslama al-Majriti
revised them to fit the meridian o f C ordoba and added
tables for astrological calculations. These tables involved
calculations using Hindu numbers— the numbers we now
use. Maslama al-Majriti also edited Arabic translations ot
Ptolemy’s geometrical constructions that defined the opera­
tion o f the astrolabe.
Averroes ( 1 1 2 6 - 1 1 9 8 ) was an important Islamic
scholar working in Cordoba. The Jewish scholar Moses ben
M aim on, or M a im o n id e s ( 1 1 3 5 - 1 2 0 4 ) , was born in
C ordoba but moved to Cairo, where he became physician
to the great Saracen leader Saladin. He wrote a well-used
synopsis o f Galen’s works.
Moslem religious zealots from north Africa subse­
quently burned most o f the books in the library at Cordoba.
C ordoba fell to Spanish Christian forces in 1236. Granada
resisted for 2 0 0 years longer. The M ongols sacked Baghdad
in 1258. By the 13th century, Arabic science had declined,
but interest in science began to develop in Europe.
2 .3 M E D IE V A L E U R O P E
2. 3. 1 M E D I C I N E A N D S C I E N C E IN
MEDIEVAL EUROPE
T he empire o f Charlemagne ( 7 4 2 - 8 1 4 ) extended over
much ol what is now France and Germany. Charlemagne
exhorted every cathedral and monastery in his empire to
establish schools and imported scholars Irom Ireland and
Italy. These schools formed the basis o f European universi­
ties. M on ks working in the scriptoria o l the monasteries
produced magnificent illustrated manuscripts. But these
were produced as luxury items for show rather then for
scholarship. The empire broke up after che death o l
Charlemagne. O n e kingdom, known as L o th arin g ia, cov­
ered a wide strip ol land irom the North Sea to Italy. This
kingdom was later restricted to present-day Netherlands,
Belgium, Luxembourg, Germany west o f the Rhine, the
French provinces o f Alsace and Lorraine, and Switzerland.
It existed until the middle o f che 12th century.
/ sacked Constantinople in 1204.
Greek and Arabic learning entered Christian Europe
mainly irom the Arabic center ot learning in Cordoba.
This influx o f knowledge caused a profound change in phil­
osophical and theological thinking. By the late 10th cen ­
tury, knowledge o f astronomical tables, Hindu-Arabic
numbers, and the astrolabe had spread from C ord oba into
Christian Catalonia. The cables were used tor ascronomy,
astrology, and calculation o f church calendars. O th er texts
from C ordoba concerned the theory and practice o f mea­
suring heights and distances. These cexcs fostered the devel­
opment o f surveying. O th er texts sec ouc che principles o f
ascrology.
This influx o f knowledge led to the development ot the
curricula known as the crivium and quadrivium . 'flic criv-
ium consisced ot grammar, rhetoric, and logic. The quadriv­
ium consisted o f arithmetic, geomecry, music, and
astronomy. They were developed in the cathedral schools o f
Orleans and Chartres, and in the city o f Liege in
Lotharingia. Liege was known as the Athens ot Lotharingia.
In the 12ch cencury, Bernard o f Charcres and Thierry, who
were chancellors o f the school ot Chartres, and the Chartres
scholar, W illiam o f Conches, were Platonists. They argued
that the world is governed by geometrical order, which can
be comprehended through inquiry. G od set the world in
motion but, once started, it was governed by lawful m echa­
nisms. There was opposition from theologians w ho stressed
the power o f G o d to work miracles and who objected to
any atcempc со rationally explain scripcurc.
Even before the Norman conquest o f England in 1066,
Lotharingian scholars had been brought into che cachedral
cities o f England. The influx o f scholars into England
increased after the conquest.
Because books and writing material were scarce, the
abacus was used tor teaching arithmetic, the celestial
spheres for geomecry and ascronomy, and che m onochord
for music. The m onochord was a single scring on a resonanc
box. The idea was to use instrumencs со represenc che
number, measure, and proporcion o f che celestial spheres
created bv God.
Also, because o f the scarcity o f books, there was an
emphasis on learning by mem ory (Yates 1966). In ancient
Greece and Rome, public speakers used the m nemonic
method known as the art o f memory. The speaker learned
to walk past a sequence ot “places” in a large imaginary
building. Each “topic” o f the speech was represented by a
vivid “image” and placed in order on one ot che places.
D uring che delivery o f che speech che speaker mencally
walked around the building by a particular route and picked
up each topic in turn. 1c is a very powerful method, scill used
by stage mnemonists.
During the 1 1th and 12th cencuries.ecclesiascical schol­
ars working in Constantinople translated Greek and Arabic
works inco Latin. But that activity/ ended when Chriscians
o f che 4th crusade with rhe connivance o f the doge o f Venice
The firsc organized medical school in Europe was
founded 109 6 in the health resort ot Salerno, which is near
the monastery o f M onte Cassino just south o f Naples. The
allied armies bom bed the monastery to dust in 1944, but it
has been restored. C o n sta n tin iu s A frican u s ( 1 0 1 0 - 1 0 8 7 )
worked in the medical school and in the neighboring m on­
astery in the 1 1th ccnturv. He translated into Latin many
books that had been translated from Greek into Arabic, or
had been written by Arabic scholars.
G erard o f C rem o n a , an Italian who worked in loledo,
was an important translator ot Arabic books in the 12th
century. The efforts o f these and other translators produced
a revival of learning in Europe in the 13th century, and laid
the foundation for the Renaissance and the growth o f
science (Sharif 1966).
In the 12th and 13th centuries, medical schools founded
in Montpellier, Bologna, Padua, O xford, and Paris over­
shadowed the school at Salerno (Guthrie 1945). Universities
in these cities developed a common curriculum and taught
in the com m on language o f Latin (sec Lc G o f f 1993).
In any age, the progress ot scholarship and science
depends on the prosperity o f the culturc. The prosperity o f
Ancient Greece and Rome depended on conquest, trade,
and slave labor. The wealthy few who could engage in
learned pursuits had little contact with artisans and there­
fore had no incentive to develop new technologies or engage
in empirical science. During the so-called Dark Ages, after
the collapse o f the Roman Empire, Roman technology,
architecture, and roads tell into decay.
By the 9th century, new technologies began to emerge
in Europe. Agriculture was improved by the development
o f the heavy Saxon plough coupled with crop rotation and
new methods o f harnessing horses. The invention o f rhe
horseshoe allowed horses to pull heavy loads. New sources
o f power were developed. The 13th century saw the intro­
duction of the overshot water wheel and windmills. They
were used to power Hour mills, forging hammers, sawing
mills, and hoists and pumps in mines. Although gears
existed in antiquity, they were developed in the medieval
period for amplification and transmission o f power. Cams
and cranks were invented for conversion o f rotary motion
into linear motion. Improvements in metallurgy led to the
refinement o f existing precision instruments such as the
astrolabe and compass. New instruments were invented,
such as the mechanical clock, precision balance and, in the
14th century, the printing press with movable type. The
12th century saw the invention o f stained glass windows,
spectacles, and basic tools such as the lathe and brace-
and-bit. The wool industry developed, which eventually
produced great wealth in England, Holland, and Florence.
Many o f these developments occurred in, or were
encouraged by, the monasteries. In ancient Rome and
Greece, manual labor was performed by slaves. The monas­
tic tradition emphasized the virtue o f manual labor.
Benedictine and Cistercian m onks were required to both
pray and engage in manual labor. The monasteries owned
many o f the water mills that were the chief source o f power
for grinding flower, tanning, and metallurgy. The wealth
these mills generated helped to build the monasteries,
cathedrals, and universities.
W e will now sec that these events encouraged ecclesias­
tical scholars in 12th-century Europe to take an interest in
technology and, ultimately, in empirical science. The roots
o f technology and scicncc in Europe were laid in the m o n ­
asteries, cathedrals, and universities of the medieval period,
well before the Renaissance.
The growing interest in logic, stemming from the writ­
ings o f Aristotle, led some churchmen to question inconsis­
tencies in the Hiblc. For example, the French scholastic
philosopher and logician, Peter Abelard ( 1 0 7 9 - 1 1 4 2 )
taught in the cathedral school o f Notre Dam e in Paris. He
stressed the logic and spirit ot inquiry o f Aristotle rather
than the idealism o f Plato. In his Sic et non he wrote, “We
seek through doubt, and by seeking we perceive the truth.’’
Adelard o f Bath (c. 1 0 8 0 - 1 1 5 2 ) played a major role in
translating Arabic texts into Latin. He was probably aided
by Arabic-speaking Jews (Bu rnett 1997, 1998). Bath is a
beautiful city in the southwest o f England. Adelard s father
had probably com e to England from Lotharingia, as had the
Bishop o f Bath. Adelard was educated in the French towns
o f I.aon and Tours. Like several other scholars o f that time,
he visited the medical school in Salerno. He spent some
years learning Arabic in Antioch, in the wake o f the cru­
sades. Later, he became tutor to King Henrv II o f England.
He produced the first full translation o f Euclids
Elements o f Geometry from Arabic into Latin. He distin­
guished between empirical inquiry, which seeks to discover
how things work, and theology, which is concerned with
why things are as they are. He took an active interest in
practical science. He translated a Latin text on practical
chemistry and the astronomical tables ot al-Khwarizmi. He
wrote treatises on the abacus ( ReguLie abaci) and the astro­
labe. He also performed experiments. For example, he
showed that water does n ot How from a hole in the bottom
ot a closed vessel until a hole is made in the top to let air in.
This contradicted Aristotle’s theory o f natural place.
R o b e r t G ro sseteste (b. с. 1 1 70 ) was the leading scholar
in early 13th century England. He was bom in Sussex o f
humble parents and was educated in Lincoln, O xford, and
probably also in Paris. He taught theology in Oxford and
later became chancellor o f the university. In 1235 he left
в
Oxford to become Bishop o f Lincoln. He translated texts
trom G reek into Latin and wrote influential commentaries
on Aristotle’s Posterior Analytics and Physics. He wrote trea­
tises on astronomy, the reform o f the calendar, sound, heat,
and optics. He adopted Aristotle’s ideas about scientific
inquiry. Inquiry begins with experienced facts (scientia
quia) and progresses to an analysis o f complex phenomena
into principles. Deduction o f hypotheses derived from
abstract mathematical principles leads to the discovery o f
reasons for the fact (scientia propter quid). These ideas,
and similar ideas o f scholars like Albertus Magnus in Paris,
represented chc beginnings o f empirical science in F.uropc
(C rom bie 1961).
At chac cime, chere was no defined boundary between
science and occult mysticism. The 13th and 14th centuries
saw chc beginnings o f an influx o f Greek occult wricings
into Europe. This literature constitutes the G nostic tradi­
tion ot thought, which is conccrned with occult knowledge
and magical personal redemption— not science. The
G nostic tradition incorporates a mixture o f ideas trom
Persian Zoroastrianism, from the Neoplatoniscs o f Greece
and Alexandria, and from the 2nd century Hermetic
liceracure o f Egypt (Yates 1964).
O ptics was the most important science in 13th century
Europe. l ight was primary because o f its association with
spiritual light in Christian theology and with the idea o f
divine illumination chac leads со ccrcain knowledge o f
abstract Platonic forms. Light reaches the Earthly sphere o f
mortal existence, where ic unices wich chc soul in chc human
body (the microcosm). The highest part o f the soul is the
intelligence chac receives the divine light. Hut, che morcal
body is weighed down and alienated by its Earthy existence.
Mortals aspire to escape che bounds o f Earthy existence and
reunite with the divine essence both over cons ot historical
time and over a lifetime. The process involves progression
through stages represented by the steps o f a pyramid (Ja co b s
ladder). Ic is possible for pure incellecc со gain knowledge o f
the universal and o f the immutable principles underlying all
creation and chereby glimpse che supreme cruch present in
God. But this knowledge most often consisted o f knowing
the ethereal inhabitants ot the celestial spheres and magic
spells. Musical harmony was identified with che harmonic
structure o f the planetary spheres. These ideas hark back to
Plotinus, Plato, and G reek mystical cults. They are still with
us in the teachings of mystical cults.
Grosseteste was seeped in the G nostic tradition (Lynch
1941). He wrote scriptural commentaries, and translated
chc Greek occult liceracure o f Pseudo-Dionysius. The anal­
ogy between light and divine illumination led Grosseteste
to believe chac gcomecry provides che key to knowledge. In
his D e luce and his De m otи corporali et luce he described
illumination, or lux, as chc divine essence that pen с traces
the nine planetary spheres (the macrocosm) through the
mediation o f angels.
A lb crtu s M agnus (c. 1 1 9 7 - 1 2 8 0 ) , known as Albert
the Grcac, was one o f the leading scholars o f this period. He
was born near U lm on the Danube, the son ot a lesser noble­
man. His actual name was Albert von Bollscadc. He studied
liberal arts at the University ot Padova before joining the
Dom inican order in 1223. He lectured and traveled in
Germany and Paris and sec him self the task o f translating
the entire works o f Aristotle into Latin. Thomas Aquinas
was his pupil. Boch men cried со reconcile Aristotelian
teachings with Christian theology and were attacked by
conservative theologians, who clung to Platonic and Neo-
platonic beliefs. In 1931, Albcrtus Magnus was canonized,
and chc Roman Catholic Church declared him the pacron
o f the natural sciences.
Albcrtus Magnus wrote an encyclopedia that concaincd
accurate technical information about such things as astron­
omy, chemistry, and agriculture. In Swnma de creaturis he
discussed the senses and perception. H e expressed the belief
that all knowledge is founded on percepcual experience and,
like Adclard o f Bath, separated empirical knowledge about
how things work from theological questions o f “why” His
writings on the sense organs and the brain followed Galen,
Avicenna, and Alhazen. In D ean im a he argued that the eye
operates like a convex mirror and concluded chat “che righc
side ot an o b je ct is located in the left part ot the eye and vice
versa.” He described how a soldier injured in chc left cemple
lost his vision in the right eye. He concluded that each optic
nerve crosses со che opposite side o f che brain (sec Thciss
and Grusscr 1994). This is the earliest known reference to
the decussation o f the visual pathways.
R o g er Bacon (c. 1 2 1 4 - 1 2 9 4 ) , the “d octor admirabilis,”
was a Franciscan m onk who studied in Oxford under
Robert Grosseteste and in Paris. He acknowledged the co n ­
tributions o f Adclard o f Bath and used his translation o f
Euclid’s Elements o f Geometry. He lectured on the
Aristotelian corpus in Paris, where he met Albcrtus Magnus,
with whom he shared an interest in empirical science.
Nevertheless, both men believed in astrology and mysti­
cism. Bacon was familiar with the works ot Aristotle, Galen,
and Alhazen. In his Opus majus o f 1268 (Edited by J. H.
Bridges, Oxford, 1 8 97 ) he mentions that people with weak
eyes can use a lens for reading. His work, and especially his
Scientia perspectiva, was based on the geometrical optics ol
Alhazen, as were works on optics by other 13th-century
scholars.
Roger Bacon has been eulogized as the founder o f
English empirical science and described as an experimental
scientist, unique in his time. Buc a more sober assessment
shows chac B acon s ideas on empirical science differed liccle
from those o f Grosseteste, Albcrtus Magnus, and others
(Thorndike 1958, vol. 3, p. 6 5 0 ) or from those o f Alhazen
(Section 2.2.4d ). However, Bacon had access to a wider
range o f ancient texts than had those who preceded him.
V itcllo ( 1 2 3 0 - 1 2 7 0 ) lived in Poland and wrote
Perspectiva. This was based on Alhazen and was the first
European treatise on optics (1 2 7 0 ).
Jo h n Peckham (1 2 4 0-12 91 ), Archbishop of
Canterbury, wrote the book Perspectiva communis, which
was also based on Alhazen. The frontispiece is shown in
Figure 2.3 (ten Doesschatc 1962; Lindberg 1983).
The word “perspective” was synonymous with the word
"optics.” The tradition of geometrical optics starting with
Euclid and continuing through Ptolemy, Alhazen, Bacon,
Vitello, and Peckham was known as the perspectivist tradi­
tion, and che practitioners were known as the Perspectivists.
The tradition culminated in Keplers discovery o f rhe basic
laws o f optics.

Figure 2. v F ron tisp iecefiv »i P crsp tctiva com m u n is (1 5 0 4 ). The au thor,
Jo h n P cck ham ( 1 2 4 0 - 1 2 9 1 ) * was A rch b ish o p o f C anterbu ry.
T h e b ook sum m arizes the w ritings o f iiu clid , al-K in d i, A lhazen,
G rosseteste» and B aco n .
In che early 14th century, the disastrous plague, the
Black Death, spread over Europe and brought most scien­
tific inquiry to a halt. Scholastic implications o f classical
learning for Christian doctrine and che exercise ot dialecti­
cal skills dominated learning in Europe. The Black Death
produced a shortage o f labor, which improved che living
standards o f those who survived. Also, it loosened the grip
o l the medieval svstem
/ ot sert labor and ot the church and
produced a redistribution o f wealth and political power.
This opened up new opportunities tor enterprising people.
2.3.2 LENSES AND SPECTACLES
The oldest known lenses were made in Egypt between 2 6 0 0
and 2 4 0 0 B C . They were plano-convex lenses o f high qual­
ity made from rock crystal, a form ot quart/. They formed
part o f artificial eyes placed in funerary statues during the
4th and 5 th dynasties o f the O ld Kingdom. These statues,
with their eyes, can be seen in che Louvre and che Egypcian
Museum in Cairo. The lenses create the impression that the
eyes follow an observer walking past the statue. Enoch and
Lakshminarayanan ( 2 0 0 0 ) have built a replica o f one o f
these eyes.
Lenses from Greek and Roman times have been exca­
vated. Aristophanes (c. 2 5 7 - 1 8 0 B C ) mentioned cheir use
in focusing che suns rays со make fire, and Pliny (A D 2 3 - 7 9 )
mencions cheir use in cauterizing. Seneca (c. 4 B C - A D 65)
described how a glass ball filled with water magnifies letters
(Polyak 1957).
The Chinese appear to have made lenses from rock crys­
tal or glass to focus the sun’s rays as early .is the 3rd century
(see Needham 1962, p.l 18). Magnifying lenses were used
in C h in a in the 12ch cencury for reading illegible docu­
ments and possibly for fine engraving, but do n ot seem to
have been used as spectacles until the early M in g dynasty in
che 15ch cencury (Needham 1962, p. 119).
The study o f refraction, or d io p trics, was begun in
Greek and Roman times. Alhazen mentioned the magnify­
ing propercies o f plano-convex lenses in che 11 ch cencury.
Kepler, in 1604, gave che first account ot image tormation
by a lens.
Spectacles seem со have been firsc made in abouc che
year 128 7 by an unknown person, probably a worker in
glass in Pisa, Italy. The principal evidence for this date is
contained in notes for a sermon delivered by the Dominican
friar Giordano da Rivalto, in che church o f Santa Maria
Novella in Florence on Wednesday, February 23, 1306. He
wrote, "It is not yet twency years since chere was found the
arc o f making eyeglasses.” This is the earliest known wriccen
reference со spectacles (Rosen 1956, p. 28).
Speccacle making was in che hands o f illiterate crafts­
men and there was litcle wriccen about lenses until the 16th
century. R on ch i ( 1 9 7 8 , p. 6 7 ) could find no mention o f
concave lenses tor the correction o f myopia earlier chan a
passing reference со cheir use in L a practica della perspettiva
by Daniele Barbaro, published in Venice in 1568.
The earliest known work o f art depicting spectacles is a
porcraic ac Treviso o f Hugh Sc. Cher, painted by Tommaso
da Modena in 1352. Since Hugh St. C h er died well before
the painter was born and more than 2 0 years before specta­
cles were invented, the spectacles in che porcraic arc an
anachronism. Rosen (1 9 5 6 ) provides an amusing account
ot spurious claims chac speccacles were invented in Venice,
in England by Roger Bacon, in Belgium by Bacon trans­
formed inco a Walloon, and in Germany.
2 .4 T H E R E N A IS S A N C E
2 .4 .1 BACKGROUND
The Renaissance was criggered by the growth o f wealthy
centers ot trade in the cities o f northern Italy coupled with
an influx o f ancient Greek and Arabic texts inco Europe. 1c
was dominated by a revival ot inceresc in ancient mystical
ccxcs racher chan by an inceresc in science.
In 1438 Joh n Bessarion, Archbishop o f Nicea in
Byzantium, came to Italy wich 6 0 0 G reek manuscripts. He
left Byzantium because he ancicipaced its overthrow by the
Turks. The Turks did overthrow che Byzantine Empire in
1453. These texts formed the nucleus o f the Marciana
library* in Venice. They
J
were studied bv *
scholars in
rhe University o f Padua, which became a major center for
learning.
 In the 15th century, C o sim o de Medici founded the
Florentine Academy. The leading members were Marsilio
Ficino ( 1 4 3 3 - 1 4 9 9 ) and Giovanni Pico della Mirandola.
Their main activity was translation into Latin o f the works
o f Plotinus and the G nostic occult literature known as the
Corpus Hermeticum from 2nd-century Alexandria (King
1973; Dorcsse 1970). Alexandria had been a melting pot
o f mystical ideas from Persian Zoroastrianism, and Greek,
Egyptian, Jewish, Indian, and Christian sources.
The C ath olic C hurch persecuted heretical cults, such as
the Manichaeans, Albigcnsians, Cathars, and Beguins
because they threatened the monopoly o f the church (see
L c ff 1967). Nevertheless, several popes were fascinated by
Gnostic beliefs, which permeated European thought during
the Renaissance (Thorndike 1958, vols. 7 and 8; Westfall
1970; Thomas 1971; Shumaker 1972; C rom bie 1 996). It
has been argued that, during the Renaissance, mystical ideas
o f natural magic and numerology spurred the emergence o f
empirical and theoretical science (Yates 1967). It was not
until the 18th century that the two ways o f thinking parted
company.
Gnostic beliefs thrive among literate and educated
people, unlike witchcraft, which thrives am ong illiterate
people. Gnostic beliefs still exist in the Jewish Cabala,
astrology, Jungian psychology, Scientology, Rosierucianism
(Howe 1 9 7 2 ), and New Age cults (W eb b 1 976). They were
evident in the ideology o f the Nazis and are evident in
American biblical prophesy and in the pyramid on the
American dollar bill. There is no limit to the idiocy o f such
beliefs, the gullibility of believers, or willingness o f che mass
media to propagate them (M acDougall 1983).
Pope Gregory I X established the Office of the
Inquisition in 1233. It was used initially to repress the
Cathars in southern France but became an instrument for
the general suppression o f heresy in Europe. In the 16th and
17th centuries, the Inquisition and the protestant churches
were guilty o f the horrific persecution o f witches. However,
astrology and alchemy were widely practiced and rarely
prosecuted. Also, the Inquisition was rarely used to sup­
press scientific inquiry or technology.
During the Renaissance, the art o f m em ory became
increasingly associated with cosmic mysticism stemming
from translations o f Hermetic literature and the Jewish
Cabala. The aim o f the mystical scholar, or magus, was to
learn the whole o f G o d s creation. This consisted o f the
planetary spheres and the multitude o f angels. Then, by
using magic rites, a person could ascend through the spheres
to unite with G od. This tradition is typified in the writings
o f G iordano Bruno ( 1 5 4 8 - 1 6 0 0 ) (Yates 1 964), who was
burned at the stake for heresy.
W ith the advent of printed books and humanism in the
16th century, printed charts replaced the ancient art o f
memory. Knowledge was classified into treelike structures.
General headings representing general principles were suc­
cessively subdivided into subheadings. The method was
pioneered by Peter Ramus ( 1 5 1 5 - 1 5 7 2 ) at the university o f
Paris (O n g 1 974). Peter Ramus was born Pierre de la Ramee
in the village o f C u ts in France, where a plaque in his
memory can be seen on the town hall. It is odd that the
Latinized version o f his name is the Latin word for branch.
W h a t came to be known as Ram ism is essentially the draw­
ing up o f branching structures to represent knowledge. The
m ethod was mainly pedagogical and was applied to logic,
grammar, medicine, and other areas o f knowledge. Ramus
was murdered in the horrific massacre of over 3 ,0 0 0
Protestants in Paris on St. Bartholom ew s day, August 24,
1572. Catherine de M edici, the Catholic Queen o f France,
condoned the massacre.
2 .4 .2 L E O N A R D O DA V I N C I
Leonardo da Vinci ( 1 4 5 2 - 1 5 1 9 ) was born in Vinci near
Florence, the son o f a notary and a peasant woman. He
studied painting in the studio of Verrocchio in Florence
and worked in the service o f Ludovico il M oro in M ilan.
Later he worked in Rome, Bologna, and Venice. In his last
years he lived in France in a house provided by King Francis
I. See ( ’ alder ( 1 9 7 0 ) and Kem p ( 2 0 0 4 ) for accounts o f his
life and works. See M acCurdy ( 1 9 5 4 ) for a collection o f
Leonardos notebooks and Todd ( 1 9 9 1 ) for a collection o f
Leonardos anatomical drawings.
The following passage from Leonardo da V in ci has been
viewed as the first suggestion that light travels as waves
rather than corpuscles, as earlier writers believed. He
wrote,
Just as the stone thrown into water becomes the
center and cause o f various circles, and sound made
in the air spreads out in circles, so every body placed
within the luminous air spreads itself out in circles
and fills the surrounding parts with an infinite
number o f images o f itself, and appears all in all and
all in each part.
( f i v w л L E O N A R D O m .u iu w n p tD ell А паимтш Fogli»
if/ t b t In stitute d e Fram e. C ited in I:u$fiJ> in K cd t 19$$,
In Lindbergs ( 1 9 7 6 ) opinion, this was an analogy
describing the propagation o f images and indicted nothing
about how light is propagated. Be that as it may, the quota­
tion essentially reaffirms al-Kindi’s principle o f universal
radiation o f light rays. Leonardos knowledge o f optics was
based on Alhazen cither directly, or through Bacon,
Peckham, or Vitello. Like Alhazen, Leonardo proved that
light from many objects passes through each point o f space
by showing that many objects produce distinct images
through the same hole in a pinhole camera. He then proved
that light from any one o b ject is in each location o f space by
showing that several images o f the same o b ject are produced
by several pinholes. He regarded the eye as a miracle o f
Nature and was amazed by the fact that all light rays
entering rhe eye pass through one narrow opening without the optic pathways end in the posterior ventricles, rather
interference. He wrote. than in the anterior ventricles as generally believed at that
time (sec Kcclc 1955).
This it is that guides human discourse to consider Leonardos writings on vision had no effect because they
divine things; here the figures, here the colours, here were in private hands until 1636. They were not studied
all the images ot every part of the universe are co n ­ until the end o f the 18th century. His detailed drawings o f
tracted to a point. О what point is so marvellous. human anatomy remained hidden in a c h c s t in Kensington
(From L E O N A R D O ’ S Codex AtUnrtcuf. Palace, London, until the end o f the 18th century (Calder
C ited In Eng!id/ In K eelс 1955» (>390) 1970; Todd 1991).
Leonardos contribution to drawing in perspective is
He observed the colors ot the spectrum formed by light described in Section 2.9.3 and his ideas on binocular vision
passing through a glass o f water. In his Six Books on Light are discussed in Section 2.10.3a.
an d Shade (Richter 1970, pp. 6 7 - 1 2 8 ) , Leonardo distin­
guished between attached shadows and cast shadows (see
2 .5 1 6 T H - A N D 1 7 T H - C E N T U R Y E U R O P E
Section 27.3.1). He noted the persistence ot vision by
observing how a swinging torch produces a circle o flig h t.
Leonardo boiled an eye in egg white and then sectioned 2 .5 .1 G IO V A N N I D E L L A PO RTA
it. Til is is one o f rhe first uses o f tissue embedding. His
Giovanni Battista della Porta (c. 1 5 3 5 - 1 6 1 5 ) (Portrait
drawings show a spherical lens, probably because a dead
Figure 2.4) was a flamboyant collector and investigator o f
lens becomes spherical. He compared the eye with a camera
obscura. He believed that an inverted image is produced in
the ccntcr o f the eye, but that rays cross again to form an
erect image on the head o f the optic nerve. He described
how a needle held in front o f a hole in a card elose to the eye
appears inverted. By moving the needle to diiterent parts ot
the pupil he showed that an image is formed by light enter­
ing any part ot the pupil (see Ferrero 1952).
W h ile believing that vision depends on light entering
the eye, it seems he believed chat vision had special powers
over things seen. He wrote:

. . . the wolt has power by its look to cause men to

have hoarse voices.” “T he ostrich and the spider are
said to hatch their eggs by lookingat them.” “Maidens
are said to have the power in their eyes to attract to MAGIC К
themselves the love ot men. in x x -B o o k o
fy
(C ited in M A t : с: и К 1) Y 1954./Л23Л)
0 1 IN .B A P T I S T P O R T
, a N c c p o lit u iie :
This last statement has some basis in fact. In his later
writings he was less inclined to speculate about mystical
powers. 11ГС
Leonardo noted that the pupils ot animals, such as the
owl, increase in the dark. In early writings, he had the erro­
neous idea that objects appear larger when the pupil
enlarges. This idea may have arisen from his observation
that a dark object on a bright ground appears smaller than a
bright o b ject on a dark ground (Strong 1979, p. xxxii). After
1513 he referred to vision being intensified when the pupil
dilates (Lindbcrg 1983). He did n ot observe pupil changes
related to changes in accommodation. These changes were
VE'atrr
described by Schciner in 1631. Leonardo made an accurate
drawing o f the optic chiasma and concluded that it was
FijL«r< 2 -*. G iovan n i B u titsu dclLx P e r u (с. I S 3 5 1615). H e is show n here
responsible for the coordinated movements ot the eyes.
o n the fron tisp iece o f a 1 6 5 8 English tran slatio n o t his b o o k M a g id c
Leonardo injected wax into the cerebral ventricles to N a tu ra lis { 1 5 5 8 ) . I Ic was a c o lle cto r and investigator o f natu ral
obtain an accurate idea ot their shape, and concluded that w onders, living in N aples.
natural wonders, a playwright, and translator o f Greek texts.
His fathers house in Naples was a center for philosophers,
musicians, and poets. Giovanni founded a group calling
themselves Oliosi (M en o f leisure). Each member was
required to have made a new discovery in natural magic.
"This was the first scientific society o f modern times although
magic, superstition, and empirical enquiry were inextrica­
bly mixed. At age 2 3 he wrote M agiae Naturalis ( 1 5 5 8 ) , a
collection o f wonders, medical remedies, and recipes tor a
great variety o f things including transmutation o f gold,
hunting, and beautifying women. It was one o f the most
popular books o f its time. It was translated into English in
1658. Dover published a facsimile edition in 1957.
Many popular books on “natural magic” were published
during the 17th century. Gradually, empirical science
became divorced from superstition and the occult.
In his major work on optics, De Refraction e Optices Parte
L ibri Novem (1 5 9 3 ) Porta dealt with refraction and
expounded Alhazens view that an image is formed on the
lens by perpendicular rays in the manner o f a pinhole
camera. He added his own view that this happened only
after a second inversion o f the image by reflection from the
back o f the eye, which acted as a concave mirror. The eye o f
the scallop works this way (sec Section 6.1.3).
He was apparently the first to give an account o f binocular
rivalry between differently shaped images in the two eyes. He
also described two tests o f eye dominance, one based on bin­
ocular rivalry and the other based on binocular parallax occur­
ring when one or the other eye is closed (see Wade 1998b).
He knew that a lens in the aperture o f a camera obscura
improves rhe image and he obtained an erect image with a
concave mirror. He knew that increasing aperture size
increased illumination o f rhe image. However, he con tin ­
ued to believe that the image in the eye is tormed on the
lens. He was perhaps che first to use che camera obscura for
drawing, simply by tracing round the image.
2.5.2 BENEDETTO CASTELLI
Benedetto Castelli ( 1 5 5 7 - 1 6 4 3 ) was born in northern Italy.
He was a priest and lecturer in mathematics in Pisa and then
in Rome. H e was the first and closest disciple o f Galileo and
die only member o f the Galilean school to write about vision.
Ariotti ( 1 9 7 3 ) points out that Castelli has been totally
ignored outside Italy. He is not mentioned in the histories o f
visual science by Priestley (1 7 7 2 ) or Boring (1 9 4 2 ).
Castelli s Discorso sopra la vista was written in 1 6 3 9 and
printed in Bologna in 1669. It is in the form o f a long letter
to Giovanni Ciam poli, a prelate of the Roman Curia. The
quotations in rhe following are from an English translation
by Ariotti (1 9 7 3 ). The page numbers refer to the pages in
rhe original Italian text.
Castelli described several well-known and some novel
visual phenomena. Like della Porta, he describes a camera
obscura with a lens and added some ot his own novel
observations. He described the effects o f using lenses o f dif­
ferent focal length and noted the range o f distance o f the
projected image over which it remained in focus. He co m ­
pared the camera obscura with the eye. He wrote:
W e found by experiment that when the hole was
made notably larger, there also followed confusion
and fogging up o f the images and when it was made
very narrow the image appeared very dimmed (p. 7).
H e described how the afterimage ot an illuminated
window frame appears large when projected o n to a far
surface and small when projected o n to a near surface.
He explained chis as follows:
once the image is impressed on che retina it occupies
a determinate area ot this tunica. W h en we turn the
eye to an object like a white wall placed ten or thirty
times farther away than the first [object], the already
impressed area o f the retina will be covered with an
image o f as large a portion ot the wall as greater is the
distance between the eye and the wall to the distance
between the eye and the original object, (p. 26).
This clear statement o f E m m erts law was written 2 4 2
years before Em m ert announced his law (see Section
2 9 .3 .4 ). Castelli applied the same explanation to the moon
illusion (Section 29.3.5 ). He described a size-distance illu­
sion that occurs in drawings.
were a painter со draw . . . two equal figures o f
men . . . against a background in such a way that one
appeared in a place far away from our eye and the
other one nearer, we would then judge that the one
that is represented as much farther away as, so to
speak, a giant even though the two figures are ot
equal height, (p. 3 2 )
Most textbooks on perception contain such a picture
(see Figure 2 9 .4 ), although nobody has cited Castelli. Also,
this is a clear statement o f the size-distance invariance
hypothesis (see Section 29.3 .2).
Castelli had a dig at classical scholarship. He declared
that nature itself is “the original book o f every true knowl­
edge o f ours.”
1 care not the least a b o u t. . . those who do nothing
other than collate diverse opinions from different vol­
umes and . . . give birth to most extraordinary m on­
sters and to mosc futile chimerae o f new views. . . that
have no odier reality than in the fantasies and in those
sheets o f paper that rhey keep filling up (p. 20).
C ould rhe same ching be said abouc some present day
branches o f “scholarship”?
2 . 5 . 3 V F. S Л I. IU S A N D T H I D E V E L O P M F. N T O P
ANATOMY

Prohibition o f dissection ot the human bodv/ was lilted in

the 14th century. Anatomists in Italy directed assistants to
perform dissections in front o f a large audience. Leonardo
da Vinci made the first detailed drawings o f human anat­
om y based on his own dissections in the hospital o f Santa
Maria Nuova, Florence. But his drawings and notes on
anatomy/ were not studied until the end o f the 18th century.
*
They can be seen in Todd (1 9 9 1 ).
Andreas Vesalius initiated the modern study o f human
anatomy (Portrait Figure 2.5). Me was born in Brussels in
151 4 and studied medicine in Paris, Louvain, and Padua,
where, che day after his graduation ac the age o f 25 , he was
appointed to the chair ofanatom y and surgery (see O ’Malley
1964). He became physician to Charles V in 1544. Charles
was Holy Roman Emperor, ruling Spain, parts o f Italy, and
the Netherlands. This position prevented Vesalius from
engaging in further research. After the abdication ofC harles
in 1559, Vesalius hoped to rccurn ro his chair in Padua, bur
was forbidden to leave Madrid by the new emperor, Philip
II. In 156 4 Vesalius made a pilgrimage to Jerusalem. O n the
return journey, stormy weather forced him to land on the
island ot Zantc, where he became sick and died.
The great work De Corporis Hurnani Fabrica (Or/ the
Structure o f the I luma?) Body) was published in 1543, when
Vesalius was 29 years old (Figure 2.6). It contains many fine
anatomical drawings, including drawings o f the eye, based
Ftferc 2 .6 . T itle p ag efrom th e D c C orp oris Н и т л т F a b rica . T in s b o o k , by
A ndreas Vesalius, was published in 1 5 4 3 . It laid the fou n d ation o t
m odern anatom v.
*

on his own dissections. They are woodcuts made in Venice

Figure 2.s . if/d rat* Vesalius ( I 5 H - A n d r e a s Vesalius was b o m in
Brussels in 1 5 1 4 and studied m ed icin e in Paris, Lou vain , and Padua.
H e was protcssor o f an atom y and surgery in Padua and physician to the
I lolv R om an Em perors C h arles V a n d P hilip II. (Гг.жс.%Рicce, Л. P/aqyjwtvf,
E tttd ii M A \ Aj <! I r & u V . C /.iA V , I H i 1 У
by a master engraver in T itia n s workshop and assembled
into a book in Switzerland. Saunders and O ’Malley ( 1 9 5 0 )
reprinted the book from the same blocks.
Vesalius could not confirm that the optic nerve was
hollow, as required by G alens theory that it transported
visual spirits. In spite o f this, and his critical attitude to clas­
sical anatomy, Vesalius did not question the doctrine o f
animal spirits, which persisted inco the 17th century. He
also retained a spherical lens in the center o f the eye and
placed the optic nerve on the optic axis. Like Galen, Vesalius
believed that the optic pathways project to the lining o f the
most anterior o f the three cerebral ventricles.
It has been claimed that in the 12th century the Spanish
Arab Averroes ( 1 1 2 6 1198) described the retina as the site
ofimage formation. O thers havedeniedthisclaim (Lindberg
1983). Abn Rushd, another Spanish Arab scholar certainly
expressed the idea in the 13th century (Polyak 1957). In
1543, Vesalius suggested that the retina is the sensitive
organ o f sight but produced no evidence.
Eustachio ( 1 5 2 0 - 1 5 7 4 ) , in his Tabulae Anatomicae,
was the first person to recognize that the optic pathways do
not project directly со the brain bur first pass to the poste­
rior part of the thalamus (che lateral geniculate nuclei),
although his discovery was ignored for more than 150 years.
In 1854 Louis-Pierre G ra tio le t ( 1 8 1 5 - 1 8 6 5 ) discovered
the optic radiations projecting from the thalamus to the
occipital cortex.
2 . 5 .4 T H E D E V E L O P M E N T OF
V ISU A L O P T IC S
Felix P latter ( 1 5 3 6 - 1614), professor of medicine at Basel,
was the first person со dissect che human body in a German-
speaking country. He was also the firsc со scace clearly chac
che recina is the recipient surface o f the eye, and produced
supporting anatomical evidence in his D e Corporis H um ani
Structura ci Usu o f 1583. He clearly described rhe recina
and ciliary muscles supporting the lens (Figure 2.7).
However, his accounc lacked a clear stacemcnc o f che diop-
cric principles ot image formacion.
Jo h a n n e s K epler ( 1 5 7 1 - 1 6 3 0 ) (Porcraic Figure 2.8)
was born of Lutheran parents in Weil near Stuccgarc. He
studied ac che Univcrsicy o f Tubingen, inccnding со become
a Lucheran clergyman. Inscead, he taught mathemacics ac
che Proccscanc seminary in Graz. In 1600 lie became che
assiscant to che astronomer Tycho Brahe ac che court ot
Rudolph II in Prague. W h en Brahe died a year later, Kepler
became court mathematician and astrologer. From the exact
astronomical measuremencs gachered by Brahe. Kepler
derived his three laws o f planetary m otion. After che abdi-
cacion ot Rudolph II, Kepler became a machemacician in
Linz. He died in Regensburg in 1630.
Fij,urc 2.". F ir s t d ea r diagram o f t h e e v e . From Лг ГГ»г/>пЬH u m a n i
p u liln lic d b r Felix I 'L l ter l a И 5 ) .
Fl&ucc 2 .K. Jo h a n n es K ep ler ( /57/ 1630). Jo h a n n e s K epler was b o rn in
W eil, G erm any. H e studied ac the U niversity o fT u b in g e n and taught
m athem atics at the P ro testan t sem inary in G raz. In 1 6 0 0 he becam e
the assistant to th e astro n o m er T y ch o B rah e a t th e c o u rt o f Rudolph
II in Prague. W h e n B rah e d ied, K epler becam e co u rt m athem atician
and astrologer. H e was later a m athem atician in L in z, and finally in
R o sto ck . (FfcmMidi 1929)
Kepler lived ac the height o f the witch-burning craze.
His own mother would have been burned if he had not
intervened. The horrific Thirty Years’ War raged in Germany
during the last 15 years of his life. This war is vividly
described in the book I he 'thirty Years War by Wedgwood
( 1 9 9 5 ) . See Koestlcr ( I 9 6 0 ) for a biography ot Kepler.
In the 17th century, chemistry, ascronomy, and mathe­
macics were emerging from che myscical, hermccic cradicion
of choughc with which they had been inextricably co n ­
nected (Thorndike 1 958). Kepler’s attitude to astrology
was ambivalent. He cast horoscopes for the emperor bur
once remarked that the “wayward daughter, astrology,” had
to support the “honcsc dame ascronomy.” Ncvcrchclcss, he
believed in a world soul (anim a tnuneii) chat propagates
from the center (the sun) by rays o f light. H e also believed
that the stars and planets affect human affairs and that
com ets were portents o f the future.
Like Marin Mersenne in France, Kepler was among the
first to scace clearly
i che distinction between ccstablc scicn-
tific hypotheses and mystical speculation, and between che
use o f mathematics со describe natural phenomena and its
use in myscical numerology. This is clear in his famous dis­
pute with Robert Fludd, an English physician and devotee
o f che medical alchemical theories o f Paracelsus. The
alchemical tradition had its roots in Greece and C hina. It
permeated the G nostic, hermetic (G nostic) literature o f
rt t-iii 2nd century Alexandria. This liceracure was broughc
into Europe through the translations by the Renaissance
philosophers Marsilio Ficino and Giovanni Pico della
M irandola (Yates 19 6 4 ; Bonelli and Shea 1 975). Those
wholly in chc occult tradition relied 011 ancient authority,
symbols, images, and analogies.
In his Mysterium C.osmographicion o f 1597 Kepler stated
that the planetary orbits conform to the diameters ol the
five nested Platonic solids {cube, tetrahedron, dodecahe­
dron, icosahedron, octahedron). Ibis theory was inspired
by concepts derived from the mystical Pythagorean tradi­
tion and from Plato’s occult ideas about rhe five regular
polyhcdra. W h en Brahe’s measurements did n ot fit this
theory, Kepler relinquished it in favor o f his theory o fellip -
tical orbits, as set out in his Harmonice M undi. Thus,
Kepler s respcct for evidence allowed him to break free from
the suffocating influence o f occult beliefs. Kepler s work on
planetary orbits laid the foundation for N ew tons theory o f
gravity.
W h ile in Prague, Kepler discovered chc geometrical
principles of image formation on the retina, which were set
out in A d Vitellionem Paralipomena, quibus Astronomiae
pars Optica Traditur ( 'things appended to Vitello, in which
the optica! part o f astronomy is treated). M ost o f this work
was written in 1603 and it was presented to Emperor
Rudolph II, on New Years Day, 1604. The book is now
available in English translation (Kepler 1604). His theories
were also presented in his book Dioptrics ( 1 6 1 1 ). Since
V itellos book o f optics was little more than a commentary
on Alhazens book o f optics, one can say that Alhazen p ro­
vided rhe foundation for Keplers work. Kepler established
the modern principles o f dioptrics and put physiological
optics on a firm foundation.
In Chapters I and II o f A d Vitellionem Kepler discussed
rhe nature o flig h t, which he described as consisting o f rays
o f constant intensity traveling from a source in all direc­
tions at great speed. H e explained how, for a uniform source,
intensity per unit area on a spherical surface decreased in
proportion to the square o f the distance from the source.
He applied these ideas to the operation o f the pinhole
camera. In Chapter III he discusscd reflection and in
Chapter IV he presented measurements o f refraction.
However, like Ptolemy, he used only small angles and co n ­
cluded that the angle of refraction was proportional to the
angle o f incidence. T he correct rule is that the ratio o f the
sines o f the angles is constant for a given pair o f media.
T h om as H arrio t, scientific advisor to Sir Walter
Raleigh, had stated the correct rule of refraction in unpub­
lished notes in about 1601 (M cLean 1 972). W illeb ro rd
Snell, professor o f mathematics at Leiden, published the
correct rule in 1621 (German spelling Snel, Latin Snellius).
However, he did n ot use the sine terminology (Vollgraff
1936).
Keplers analysis o f vision is contained in Chapter V,
entitled "D e m odo Visionis,” of A d VitelI ion on . He was
prompted to investigate image formation because o f diffi­
culties that Tvcho Brahe had been having in measuring the
sizes o f the sun and m oon from images produced in a camera
obscura. His exploration o f the effects o f changing the size
o f the aperture and its distance from the image plane led
him to consider the image formed in the eye.
Kepler derived his ideas o f the anatomy o f the eye and
the idea that the retina is the site o f image formation from
Felix Platter s De Corporis HttmaniStructura et Usu o f 1583.
He also relied on the most accurate available drawings of
the eye in A natom ia Pragensis written in 1601 by Johannes
Jessenius, professor o f medicine at W ittenberg.
As his starting point Kepler considered the problem
raised by Alhazen— chat clear vision requires that each
poinc in the image plane receives light from only one point
in an object plane. Kepler rejected Alhazens solution o f
allowing only normal rays to enter che eye, on the grounds
chat there would be no way со distinguish between normal
rays and slightly refracted rays. By analyzing the paths o f
light rays through a lens, he arrived at the corrcct solution,
which he then applied to the eye. The following quotations
arc from an English translation o f Kepler s A d Vitellionem
by D onahue (2 0 0 0 )
Since any point you please radiates in an orb, it will
therefore also radiate to the parts o f the orb, with
the result that it will radiate to the whole o f the
small portion o f the little sphere o f the cornea, and
will illuminate the iris and its black center, or the
opening o f the uvea. And sincc the cornea and the
aqueous humor that is beneath it, are a medium
denser than air, th e rays sent down to the inclined
surface o f rhe little sphere are accordingly refracted
towards the perpendicular. Thus those rays which
previously were spreading out in their progress
through the air, are gathered together now that they
have entered the cornea.
( K E P L E R 1604, p. 1 7 1 ).
Light radiating ouc from any point in an object plane is
refracted by the lens со form a cone o f light, which co n ­
verges on a point in the image plane. Eight radiating from
any other poinc in the o b je ct plane converges in another
point in the image plane. There is thus a one-to-one m ap­
ping o f o b ject points o n to image points, and therefore
refracted light rays do not dilute the image.
Although convex and concave lenses had been used to
improve vision long before Kepler s time, he was the first to
explain their function. He wrote:
Therefore, chose endowed with a point o f distincc
vision that is rather distant, when they use convex
glasses, they alter the cone of radiations of the same
nearby point, so as to appear to arise as if from a dis­
tance, and to enter the e y e .. . . O n the other hand,
those endowed by nature with a point or distance o f
distinct vision that is short and close, by using
 concave glasses, alter the cone o f radiations coming
from the same distant point, so that it may seem as it
ic originates and enters che eye from nearby.
( K E P L E R 1604,[>.20!)
Like Alhazen, Kepler realized that optical principles
could not apply beyond che retina, because che opcic nerve
is nor straight and contains opacities. He clung to Galen’s
notion ot visual spirics, buc admicced chac he knew nothing
abouc visual processes beyond che recina. He wrote,
I say chac vision occurs when an image (idolum) o f
the whole hemisphere of die world chat is betore the
eve, and a little more, is set up at the white wall, tinged
with red, ot the concave surface o f the retina. How
this image o f picture is join ed together with the visual
spirits that reside in the retina and in the n erv e,. . . I
leave to che natural philosophers [Physici]
( K E P L E R !6 0 4 ,f.t6 S ).
Kepler concluded that an inverted and left-right reversed
picture o f che visual scene is projected on the retina. He
wrote:
Thus vision is brought about by a picture o f the
thing seen being formed on the concave surface o f
the retina. That which is to the right outside is
depicted on the left in the retina, that to the left on
che right, that above below, and that below above.
Further, green things are depicted in che color green,
and in general any object whatever is pictured in its
own color. So, it ic were possible tor cliis picture on
che retina to persist when the retina was revealed by
removing the anterior parts ot the eye which form it,
someone with sufficiently sharp sight would recog­
nize the exact shape o f the hemisphere compressed
inco che confined space o f the retina.
( K E P L E R 1604,p. 170)
At first, Kepler was disposed to accept Alhazens solu­
tion со che problem o f che inverccd image by posicing a
second inversion, buc he soon abandoned this idea. He co n ­
cluded that a mental process was responsible for seeing the
image in its correcc oricncation, which is tantamount to
saying that he left the problem unsolved.
C h risto p h S c h c in c r ( 1 5 7 3 - 1 6 5 0 ) was born near
Mindelheim, Germany. He was a Jesuit priest and became
professor o f mathematics in Ingolstadt and advisor to
Archduke Maximilian. Between 1624 and 1633 he lived in
Rome. He built telescopes and observed the sunspots,
which involved him in a priority dispute with Galileo.
Decails about his life and work have been provided by
Daxccker ( 1 9 9 2 , 1994).
In the book Oculus, published in 1619, Scheiner
described the anatomy ot che eye. He produced che firsc
E ,
Figure i.9. S c h c in c r s draw ing o f the eye. Fi\*in bit О.мЛг ni 1619.
accurate drawing o f an eye, showing che correct curvacure of
the cornea and lens and the correct position o f the optic
nerve, as shown in Figure 2.9. He proved experimentally
that a miniature inverted image is formed on the retina
(Scheiner 1 6 1 9 ,1 6 3 0 ) . He did this by making a model o f an
eye. He also observed the image directly by cutting away the
back ot a bull’s eyeball.
Knowledge abouc che structure o f che retina had to wait
until the microscope was developed in the 17th century. In
the book Rosa Urstna Siva So/, published in 1630, Schcincr
compared the optics o f the eye with the optics o f a tele­
scope. I Ic correctly placed the nodal point o f the eye near
the center o f the eye and suggested that accommodation
involves both the forward and backward movement and
flattening o f the lens.
I Ic observed that an inverted image ot a small object
held near the pupil appears in each o f several small holes in
a card held beyond the object. Porterfield developed this
effect into the first optom eter (Section 9.2.4).
W illia m M olyneux. a Dublin lawyer and scientist, pub­
lished his Treatise o f Dioptricks in 1692. Ic seems to have
been the firsc book on optics printed in English. O n page-
105 he proposed the correct answer to the inversion prob­
lem. The perceptual system docs not have access to the abso­
lute orientation o f the retinal image bur only to its
oriencacion wich respect to that indicated by other sensory
modalities. Molyneux was prompted to approach the pro b­
lem in this way by reading Joh n Locke’s Essay Concerning
Human Understanding ( 1 6 1 9 ). Molyneux also posed the
question about what a blind person would see i f sight were
suddenly restored (see Section 8.1.3).
G e o rg e Berkeley ( 1 7 0 9 ), fellow o f Trinity College
Dublin and later Bishop o f Cloync, also scaced che correct
solution со the problem o f the inverted image (Portrait
Figure 2 .1 0 ). See 1 Ioward ( 1 9 8 2 ) for an account o f investi­
gations o f the effects o f inverting the retinal image.
Any useful opcical system must change ics focal length
when the distance o f the o b ject changes. Kepler speculated

L J
Figure2. 10 . G eorge B erkeley (1 6 8 $ I753X H e was born in D v sert, Ireland.
H e b eca m e a fellow o f T rin ity C o lleg e D u b lin in 1 7 0 7 . B etw een 1 7 1 3
and 1721 he traveled in England and Italy. H e th en held offices in
the U n iv ersity
4
o f D u blin and was dean o f D err фv. H e visited A m erica
b etw een 1 7 2 8 and 1 7 3 2 . In 1 7 3 4 he becam e Bishop o f C lo y n c in
Ireland. (O il p ain tin g by J . Ssm b ert, 1 7 2 5 . N ation al P ortrait G allery,
London)
chat accommodation is achieved bv back and forth movc-
m e n c s o f the lens. In 1 6 7 1 , Jacqu es Rohaulc ( 1 6 1 8 - 1 6 7 2 )
constructed an artificial eye in which focus was changed by
moving the image surface. John Theophilus Dcsaguliers
(1 7 1 9 ) proposed that changing pressure in the fluids o f the
eye caused the cornea to change its curvature. Scheiner
( 1 6 3 0 ) had speculated that the eye could accommodate by
changing the shape o f the lens. Descartes ( 1 6 6 4 ) and
N icholas M alebranche ( 1 6 7 4 ), adopted the same theory.
In 1738, Wi l l i am Porterfield (c. 1 6 9 7 - 1771), a physician
in Edinburgh, introduced the term “accommodation” to
describe a change in the focal length o f the lens. After
observing a person lacking lenses he concluded that accom­
modation involves changes in lens curvature. He invented
the optom eter for measuring the near and far points o f
accommodation (Section 9.2.4). P ro o f chat the lens changes
its shape had со wait for experiments conducted by Joseph
Pricsdcy ( 1 7 7 2 ) and Thomas Young (1 8 0 1 ).
Helm holtz (1 8 5 5 ) developed Youngs cheory o fa c c o m -
modacion inco che generally acccpccd cheory. As che lens
accommodates for a near object, che ciliary muscles reduce
tension in the fibers supporting the lens, which allows the
lens to relax into a more spherical shape (see Section 9.2.1).
Descartes (1 6 3 7 ) speculated that presbyopia is due to
the lensbecomingflatterw ich advancing age. The Dutchm an
Frans Cornelius D onders ( 1 8 1 8 - 1 8 8 9 ) produced a fuller
account o f dcfcccs in accommodacion (D onders 1864).
Isaac N ewton ( 1 6 7 0 ) shone a beam o f sunlight ch rough
a prism and observed the resulting spectrum. In this way he
was the firsc со demonstrate chac white light contains all the
colors o l the spectrum. He concluded in his Opticks ( 1 7 04,
p. 26) chac “ The lighc o f che sun consists o f rays differently
refrangible.”
Newton observed phosphcncs produced by pressing a
blunt probe against on his eyeball. He also described a
simple dcmonstracion ofchrom acic aberration in the human
eye. He held a hole in a card close to one edge o f the pupil
so chac lighc rays scriking che cornea obliquely were scrongly
refracced со form an image on che fovea wich visible chro-
macic fringes. This procedure is still used (see Seccion
9.1.3).
Franciscus G rim aldi ( 1 6 1 3 - 1 6 6 3 ) discovered che phe­
nomenon ofditfraccion, which led him со suggest thac lighc
cravels in waves, like waves on che surface of a liquid. The
Ducch scientist Chriscian Huygens ( 1 6 2 9 - 1 6 9 5 ) devel­
oped che wave cheory of lighc (Huygens 1690). This theory,
as modified by Augustin Fresnel ( 1 7 8 8 - 1 8 2 7 ) , accounts
for a wide range o f optical phenomena. The wave theory
was contrasted wich N ew tons corpuscular cheory until che
theories were combined in modern optical cheory.
In 1873 Ja m e s Clerk Maxwell ( 1 8 3 1 - 1 8 7 9 ) published
his four field equations that established the unity o f lighc
and clcccromagnccism. G u sto ff K irch o ff ( 1 8 2 4 - 1 8 8 7 )
showed thac the Huygens-Fresnel wave theory can be
deduced from Maxwells equations. These equations paved
the way for Einstein’s theory o f relativity.
Jean Mery ( 1 7 0 4 ) observed the blood vessels in che cats
recina by shining candlelight through che pupil. In 1823,
Purkinjc used che same mechod со observe che blood vessels
in che human recina (see Weale 1 994). In 1850 Helm holtz
invented the ophthalmoscope, which overcame che prob­
lem o f the observer’s head getting in the way o f the retinal
image (H elm holtz 1851).
2 .5 .5 DESCA RTES
Rene Descartes ( 1 5 9 6 - 1 6 5 0 ) (Porcraic Figure 2 .1 1 ) was
born o f Jewish parents in La Have near Tours in France. He
was educated at ajesu ic school in La Fleche, France, where
he formed a lifelong friendship wich his fellow scudenc
Mersenne. After studying law in Poitiers he lived aimlessly
in Paris on his private income. He made a sudden decision
со cravel and joined the D utch Protestant army of Prince
Maurice of Nassau as a gentleman volunteer in che Ducch
city o f Breda. The Ducch were fighcing for independence
from Spain wich che help of Cacholic France. During a long
lull in the fighcing Descartes m et a soldier scientist named
Isaac Bccckm an, with whom he studied mathematics. Then,
after wandering through Europe for some time, he joined
the Cacholic army of che Duke ot Bavaria. He seems со
have had an easy life as a gentleman soldier during che hor­
rific Thircv Years’ War of 1618 со 1648. This war, wich ics

Figure 2 . 11. Rent-D escartes (1 $ 9 6 -1 6 5 0 ). Rene D escartes w as born near
lo u rs in F ran cc and ed u cated a t a Je su it sch ool in La Fleche, France
A fter studying law in P oitiers he jo in ed the D u tch P rotestan t arm y o f
Prince M aurice o f Nassau a n d . later, th e C a th o lic arm y o f th e D uke
o t Bavaria. H e then settled in H o lla n d , where he devoted him selt to
m ath em atics and philosophy. In 1 6 4 9 he m oved to S to ck h o lm to
teach philosophy to Q u een C h ristin a . H e died o f p n eu m on ia during
his first w in ter there. (E n g rav in g by VC'. H o ll from a p ain tin g by Frans
H als in the Louvre» Paris. C o u rtesy C rerar Library* D r. So n n en sch ein
C o lle c tio n , C h ic a g o )
associated famine and disease, killed about one quarter
o f the population o f Germany and left most o f the country
in ruins.
Descartes moved from Paris to Holland in 162 8 to
devote him self to mathematics and philosophy. W hile there
he developed Cartesian geometry. In Holland, he was safe
from the clutches o f the Inquisition. This was the time when
Galileo was brought before the Holy Office. Heretics and
those accused o f witchcraft were burned at the stake by both
the Catholic and Protestant churches. Even in Holland, he
was cautious about what he published. In 1649 he was
reluctantly persuaded to move to Stockholm to teach phi­
losophy to 23-year-old Queen Christina. He died o f pneu­
monia during the first winter, aged 54. See Watson (2 0 0 2 )
for a biography of Descartes.
Descartes published his account o f vision in L a diop-
triqu e in 1637 and in TraitideI'hom m tne [Treatiseon M an)
in 1664 (English translation by Hall 1972). He set out to
reconcile the scholastic Aristotelian account o f perception
with his mechanistic theory and his mind/body dualism.
Descartes adopted K eplers ideas of image formation but
retained Galen’s animal spirits. He believed these spirits
were formed in the pineal gland and thac fine filaments in
the optic nerves opened valves in the walls o f the ventricles
and pineal gland and allowed animal spirits to flow to mus­
cles. These mechanical ideas were inspired by his interest in
clocks, animated statues, and toys. Descartes saw the human
body as an automaton controlled by chc mind and soul
operating through the pineal gland. The consequences of
this misguided duality— the unfortunate division between
the material and mental— are still with us.
Dcscartes believed that cach optic nerve projects to its
own side o f the brain. He thus moved the site where visual
inputs com bine from the chiasm into the brain. He p ro­
posed that each fiber in the optic nerve projects to a specific
location on the lining o f the ipsilatcral ccrcbral vcncriclc.
From chere, inputs from che eyes com bine in che pineal
gland. He selected this gland because he saw it as the only
unpaired scruccurc in che brain thac could account for sin­
gleness o l vision. It is unlikely that Descartes had a clear
idea that corresponding points from the two eyes project to
the same location in the brain. Figure 2.12a seems to have
been added to the Traite de I'hommme after Descartes death
(see Wade 1998a).
The French physicist, Ja c q u e s R oh au lt ( 1 6 7 1 ), sug­
gested that ipsilaterally projecting corresponding
fibers from the two eyes converge somewhere in the brain
(Figure 2.12 b ). Descartes’s ideas of brain structure and
function were largely speculative.
Descartes accepted the psychophysical postulate, which
states that every percept is represented by a distinct scacc o f
the brain. He also stated that the memory o f an object
involves the same brain scacc as that creatcd bv the actual
object.
In his L a dioptrique ( 1 6 3 7 ) Dcscartes described the eyes
as "feeling o u t” a distance by the convergence o f the visual
axes, as a blind man might feel out a discancc with a stave in
each hand (Section 25.2).
2 .6 B E G IN N IN G S O F V IS U A L
N E U R O S C IE N C E
2 .6 .1 D F.ТА 11. F. D S T R U С T U R F. О F T H F.
NERVOUS SYSTEM
It is not clear who first made a microscope. T he Jesuit priest
A thanasius K irch er ( 1 6 0 2 - 1 6 8 0 ) , inventor o f the magic
lantern, was perhaps the first microscopist. His Ars Magna
et Umbrae contains observations on light and lenses and a
description of his microscope. M arcello M alpighi ( 1 6 2 8 —
1 6 94 ) was professor o f anatomy at Bologna, Pisa, and
Messina. He was the greatest 17th-century microscopist
and the founder of histology. During the last three years of
his life he was physician to Pope Innocent X II. His PuHi in
ovo o f 1673 describes the neural groove, and the cerebral
and optic vesicles.The Ducchman A n to n Van Leeuw enhoek
( 1 6 3 2 - 1 7 2 4 ) made his first microscope in Delft in 1671. It
is in a museum in Ucrechc. He made microscopes o f increas­
ing quality (Leeuwenhoek 1675). He studied bacteria and
animal tissue, including nerve tissue. In 1674 he sent a
communication to the Royal Society of London, which
 (a) D escartes (1664) used K epler's theory o f im age form ation.
E ach optic nerve projects to the lining o f the ipsilateral ccrcbral
ventricle, an idea taken from G alen. Pairs o f corresponding points
m ap onto the pineal gland to form a unified im age.
(b) Rohault (1671) adopted ipsilateral projection and com bined
corresponding fibres in the brain.
(c) B rig gs (1676) adopted ipsilateral projection and described the
optical projection o f corresponding im ages.
Figure 2. 11. F.arly draw ings o f the visual pathways.
stated that he could n o t find canals in the optic nerve,
as claimed by Galen. Harris ( 1 9 9 9 ) described the work ot
early microscopists.
T h om as Young ( 1 7 7 3 - 1 8 2 9 ) was a physician in Sc
G eo rg es Hospital in London, and foreign secretary o f che
Royal Sociccv (Figure 2 .1 3 ). He was a distinguished lin-
guisc, Egyptologist, physicist, and physiologist and made
several significant contributions со visual science. He was
che firsc со demonstrate che wave nature o f light by observ­
ing interference fringes produced by passing light through
an aperture. He was also che firsc со explain che mechanism
o f lens accommodacion and astigmatism (Section 9.2.2),
and was che firsc со propose che trichromacic cheory o f color
vision. See Robinson ( 2 0 0 6 ) for a biography.
R o b e r t H o o k e ( 1 6 3 5 - 1 7 0 3 ) , professor of mechanics
to che Royal Society, constructed che first compound m icro­
scope and published drawings o f che microscopic scructurc
o f com m on materials in his Micrograph ia o f 1665. He firsc
(d) N ew ton , in about 1706, w as the first to suggest hem idec-
u ssation o f the pathw ays. H e erroneously fused corresponding
fibres in the chiasm a. (U npublished m anuscript, see C ron e 1992)
(c) T ay lor (1738) corrected N ew ton 's erroneous idea o f fu sion of
fibres in the chiasm a
(f) Porterfield (1759) rejected N ew to n 's hem idecussation. Like,
Rohault, he show ed how im ages p roject to corresponding points.
used che cerm “cell” to describe structures in sections o f a
cork. H ooke made some observations on the limits o f visual
resolution and, like Descartes, he was inceresced in the rela-
cion becween resolucion and che diamcccr o f sensoryt end-
ings in che eye. See Wade ( 2 0 0 4 ) for an accounc o f early
cxperimcncs on visual acuity.
Early microscopes had poor resolution, and images were
discorced by lens aberracions. Ic was noc uncil che incroduc-
cion o f achromatic lenses in the 1820s that details o f cellular
structures could be observed. J a n P u rk in jc ( 1 7 8 7 - 1 8 6 9 ) ,
in Breslau, and Jo h a n n e s M u ller ( 1 8 0 1 - 1 8 5 8 ) , in Berlin,
helped to lay che foundations o f histology. T h e o d o r
Schw ann , 1 8 1 0 - 1 8 8 2 ) described clearly che cell doccrinc
o f anatomy (Schwann 1839).
In 1830, Purkinjc dcmonscratcd chac shadows o f retinal
capillaries are visible when one looks through a pinhole.
H ein rich M u ller ( 1 8 5 4 ), professor o f anatomy at Wurzburg
in Bavaria, measured the parallactic displacement o f the

Figure 2.i>. Tlx/niAs Youtig (1 7 7 3 IS 2 9 ). T h o m as Young w as born in
So m erset, E n glan d , and stu died in L o n d o n , E d in b u rg h ,a n d G erm any.
U c was a physician a t S t. G e o rg e s I Josp ital in L o n d o n , and foreign
secretary o f th e Royal Society. H e was a d istinguished lin guist,
E gy p tologist, physicist, and physiologist and m ade several significant
co n trib u tio n s to visual science.
shadows o f capillaries for a given morion o f a lighc source.
From chis, he compuccd chc discancc between the vessels
and the layer o f receptors behind them. The distance was
chc same as che anatomically determined distance becwcen
chc blood vessels and chc layer containing the rods and
cones. Muller deduced chac photorecepcion occurs in the
outer scgmcncs o f chc rods and cones. Miillcr also described
che principle layers o f che recina.
M ax Schultzc (1 8 6 6 ) showed chac chc fovea contains only
cones. Knowing thac the fovea and color vision do noc func­
tion in dim light, he dcduccd that concs arc responsible for
photopic color vision and that rods are responsible for sco-
topic achromatic vision. Franz Boll (1 8 7 7 ) showed chac chc
recina changes color when exposed со lighc. This led со che dis­
covery o f rhodopsin by Willy Kiihnc and Carl F.wald (1877).
In 1873 C a m illo G o lg i ( 1 8 4 3 - 1 9 2 6 ) discovered chac
silver nicracc scains many
*
nerve cells со reveal cheir fine
structure. However, he failed to observe synapses. Like
R udolf von Kollikcr ( 1 8 1 7 - 1905) and others, Golgi
believed chac nerve cells form a continuous network, or
reticulum, throughout the body. Ironically, the develop­
ment o f G o l g i s histological procedure soon allowed others,
such as W ilhelm Hiss ( 1 8 3 1 - 1 9 0 4) and Ramon v Cajal to
propose the neuron th eory, in which neurons are indepen­
dent cells linked by synapses. See Shepherd ( 1 9 9 1 ) for a
detailed hiscory o f che neuron theory.
S an tiag o R am o n у C ajal ( 1 8 5 2 - 1 9 3 4 ) (Figure 2.14)
was the founder o f modern neuroscience. He was born in
f 2.14. San tiago R am on у C a ja l ( I $ $ 2 1934). H e was born in the
village o l P c tilla d c A ragon in n o rth east Spain and studied m ed icin e in
Z aragoza. A fter som e years as an arm y physician in C u b a he ob tain ed
his P h .D . in M adrid w ith M acstrc de San Ju a n . H e held academ ic
ap p o in tm en ts in Z aragoza, V alencia, B arcelo n a, and finally M adrid.
H e was 5 5 in th is p h otog rap h . (From \U* >♦. 1907}
the village o f Pecilla de Aragon in northeast Spain, the son
of a doctor. A s a young man his passion was arc buc, because
o f his fathers opposition, he agreed to study medicine in
Zaragoza. After some years as an army physician in C u ba he
obtained his Ph.D. in Madrid with Maestre de San Juan.
He held academic appointments in Zaragoza, Valencia,
Barcelona, and finally Madrid (see Ramon у Cajal 1937).
In 1887, while professor of histology in Barcelona, he
visiced Madrid, where Luis Simarro incroduced him со
che Golgi scaining procedure.
Ramon v Cajal developed and popularized che Golgi
staining procedure and used it to reveal the cellular organi­
zation ot the spinal cord, recina, cerebellum, and cerebral
cortex in great detail (Section 5.4.1 a). He proposed the idea
thac informacion is received bvj dendrices and transmicced
to other nerve cells bv
*
the axon. He remained unsure about
how information was passed from one cell со anocher, buc
rejecced the idea chat nerves form a continuous network.
He discovered dendritic spines and growth cones and for­
mulated the theory o f neurotropism in the development o f
the nervous system (see Section 6.3.3).
In h isC ro o n ia n Leccure, delivered in London in 1894,
C ajal spcculaccd chac use and disuse ot neural circuics p ro­
duces a remodeling o f dendritic fields as a basis for memory
and learning (see Section 6.5).
Ramon v Cajal wrote papers only in Spanish, which he
published in his own journal— Rivista frbnestralde histolo-
gia norm al у patoldgica. His three-volume work Textura
del sistew a nervioso del hom bre у de los vertebrados was
published between 1899 and 1904. This work became gen­
erally known only after it was translated into German by
Albrecht von Kolliker and into French by Ramon у Cajals
friend Leon Azoulay as Histologie du systbne nerveux de
I’hom m e et des venebres (1 9 1 1 ).
Stephen Polyak visited RamOn у C ajal in 1924. He was
inspired to apply C ajals methods to the primate retina,
including the human retina. Polyaks book 'the Retina
appeared in 1941. In 1 9 0 6 , Cajal and Golgi shared the
Nobel Prize in Physiology. In 1 9 0 1 , Cajal published a paper
on stercopsis and binocular vision in a journal o f photogra­
phy in Madrid, in which he described a form o fran d o m -d o t
stereogram, which is described in Section 24 .1 .5 (Bergua
and Skrandies 2 0 0 0 ).
In Bologna, at the end ot the 18th century, Luigi
Galvani showed that electrical discharges produce muscle
contractions. W ith this discovery, the fluid theory o f nerve
conduction was replaced by th e idea o f electrical conduc­
tion. In Berlin, in the 1840s, Emil Du Bois-R eym ond
measured resting potentials in nerve and muscle, and
H elm holtz measured the speed o f nerve conduction. In
1877, Richard C aton used a galvanometer to detect electric
currents in the brains o f rabbits and monkeys (see O chs
2 0 0 4 ).
Discovery o f the mechanism o f nerve conduction had
to wait until the 2 0th century. К . C . C o le, H . J . Curtis, and
A . L . H odgkin, working in W oods Hole, Massachusetts,
discovered that the action potential in the giant axon ot the
squid (diameter up to 1 m m ) is associated with a change in
impedance between electrodes placed on opposite sides o f
the axon (C ole and Curtis 19 3 9 ; C ole and Hodgkin 1939).
A. L. Hodgkin and A . F. Huxley ( 1 9 3 9 ) , in Plymouth,
England, made the first intracellular recording o f an action
potential by inserting a electrode into the giant axon. They
later developed a set o f equations that describe the ionic
currents that determine the properties o f the action poten­
tial (Hodgkin and Huxley 1952). These H odgkin-H uxley
equations provided the foundation tor computational neu­
roscience. This work was done at Cambridge University.
Until the middle o f the 2 0 th century there was a lively
debate about whether synaptic transmission was electrical
o r chemical. We now know that both types occur. In 1933
Wi l l i am Fcldberg ( 1 9 0 0 - 1 9 9 3 ) , in Berlin, identified ace­
tylcholine associated with the stimulation o f muscle tissue.
After the Nazis forced him to leave Germany he worked
with H enry D ale ( 1 8 7 5 - 1 9 6 8 ) in Cambridge, England.
They proved that acetylcholine is released at motor syn­
apses. Many investigators, such as Jo h n Ecclcs, continued to
believe that all synapses in the C N S were electrical. In the
1950s, at University College, London, Bernard K atz and
his associates elucidated the basic mechanism o f synaptic
transmission (see Heuser 2 0 0 3 ) . In the 1950s several inves­
tigators identified glutamate as the main neurotransmitter
in the brain (see Section 5.5.2). See Robinson ( 2 0 0 1 ) for a
detailed history ot investigations o f synaptic mechanisms.
2 .6 .2 A D VAN С E S I N U N D E R S ТА N D I N G
T H E B R A IN
The earliest written reference to the brain is contained in an
Egyptian papyrus dating from abouc 1700 B C , which was a
copy o f a document from the O ld Kingdom, 1,000 years
earlier. Sec Breasted (1 9 3 0 ) for an English translation. It
describes the brain protruding from a skull fracture, along
with the meninges, and the cerebrospinal fluid. The
Egyptians believed that the heart was the seat o f the mind,
which explains why, during the process of mummification,
they preserved the heart buc scooped ouc the brain and
discarded it.
Aristotle’s ( 3 8 4 - 3 2 2 B C ) De an bn a and Parva natura-
lia contain discussions ot the five senses of seeing, hearing,
smell, taste, and touch and a vague discussion o f cognitive
functions. However, he placed the center for perception
and cognition in the heart. In Alexandria, Hcrophilus
( 3 3 5 - 2 8 0 B C ) and Erasiscracus ( 3 0 4 - 2 5 0 B C ) placed che
cencer for perception and cognition in the brain. They
described the nerves leaving the human brain and spinal
cord as a network o f fibers distinct from tendons and blood
vessels. Thev described the convolutions o f the cerebral
cortex, and distinguished between sensory and motor
nerves.
Galen in the 2nd century A D placed higher mental
functions in the three ventricles o f the brain. Arabic schol­
ars elaborated these ideas in a variety o f ways. Avicenna (A D
9 8 0 - 1 0 3 7 ) , in De anitna , developed a five-fold classifica­
tion ot mental functions that were called internal senses.
Albertus Magnus adopted this scheme in his D e anitna,
written in about 125 6 (see Steneck 1 974). The lowest level
contains the function called com m on sense, which is what
we call apprehension or perception. This level receives
information from the five sense organs and extracts, relates,
and compares the perceived properties ot objects. This is
followed by the imagination, which retains sensory infor­
mation when sensory objects are n ot present. These two
functions were placed in the anterior ventricles. Next comes
estimation, which is concerned with interring che incen-
cions o f persons and animals со carry ouc cercain actions.
This was placed in che middle ventricle along with fantasy,
which allows a person to conjure up images o f objects that
do n ot exist, such as mythical monsters. Finally, memory
was placed in the posterior ventricle. Animal spirit circulat­
ing in the ventricles activated each o f the five internal
senses.
The ideas o f medieval and Renaissance physicians on
the nervous system were based on a mixture o f G reek phi­
losophy and Christian theology. Following Plato, they
believed that desires and appetites were centered in the veg­
etative soul in the liver, passions and action were centered in
the vital soul in the heart, and the cognitive functions o f
apprehension, reasoning, and mem ory were centered in che
immorral soul in che hollow ventricles ot che brain.
 Ideas abouc chc anacomy and functions o f chc body
began со change during the 17th century. In 163 6 dissec­
tion became part o f medical training at Oxford. Medical
students were allowed to dissect the bodv» o f anyone
в who
had been cxccutcd near Oxford. The new generation o f
anatomists began to question the dogmas o f Galen and
Aristotle. The discovery/ o f the circulation o f the blood by
/ phology, or “bumps on chc head” that particular functions
William Harvey ( 1 5 7 8 - 1 6 5 7 ) , physician to Jam es I and
Charles I, set the stage for empirical investigations ot the
nervous system.
A t Oxford University, a remarkable group o f Harveys
disciples sec out со map chc nervous syscem and brain (Frank
1980; Zim m er 2 0 0 4 ) . This group included T h om as W illis
( 1 6 2 1 - 1 6 7 5 ) , R o b e r t Boyle, C h risto p h e r W ren, Jo h n
W ilk in s, and W illia m Petty.
Thomas W illis had been a Catholic royalist during the
civil war. W h en the monarchy was restored in 166 0 he was
rewarded with the professorship o f natural philosophy at
Oxford. The house in which he lived can still be seen in
Merton Street. In 1655, Robert Boyle, another disciple o f
Harvey, join ed the group at Oxford. W illis and Boyle both
wanted to explain the workings o f the body “without
recourse to occult qualities, sympathy, or other refuges o f
ignorance”
W illis obtained the body o f a serving woman, Anne
Greene, who had been hanged for killing her stillborn baby.
Just as he was about to perform a public dissection she
began to breathe and W illis was able to revive her. She
recovered, married, and had three children. This incident
enhanced his reputation as a clinician, and his income.
W illis and his assistants dissected animal and human
brains. In 1664, W illis recorded chis work in Cerebri
Anatome: Cui Accessit Nervorum Descriptio et Usus. Tit is was
che first book on che brain. The original I.acin has been
translated into English (Feindel 1965). W illis saw che brain
as the scat of mental functions, with different functions
localized in different regions. However, he speculated about
invisible circulating vital spirits. He coined the term "neu­
rology” and named many parts o f the brain, including the
anterior commissure, claustrum, internal capsule, corpus
striatum, and optic thalamus (see Hughes 1 991). He estab­
lished that the optic nerves project to the thalamus. He
described the circle o f arteries round the base o f the brain,
which is known as the circle o f W illis. Christopher Wren
helped with the dissections and drew illuscracions o f the
brain. O n ly later did he become the architect who designed
S t Pauls Cathedral in London.
O n a November afternoon in 1660 twelve scientists,
including W illis, W ren, W ilkins, and Petty, met at Gresham
College, London, where they decided to found a scientific
society. Forcunacely, the restored king Charles II was inter­
ested in science and granted che new society a royal charter.
It became the Roval Societv o f London.
/ i
Many physicians in the 18th century believed chac ali
parts o f the brain functioned in the same way. The idea was
championed by A lb re ch t H aller ( 1 7 0 8 - 1 7 7 7 ) , professor
o f anatomy in G ottingen and leading physiologist o f his
time. It fitted in with chc nocion o f an indivisible “soul.”
Franz Jo s e p h G a ll ( 1 7 5 8 - 1 8 2 8 ) and J o h a n n G aspard
Spu rzheim ( 1 7 7 6 - 1 8 3 2 ) challenged chis omnipotcncial
idea. They argued from spurious evidence of cranial m or­
are localized in particular areas. This gave rise to the popu­
lar fad o f phrenology, which is still with us.
C h a rles Bell in England in 1811 and Francois
M agend ie in France in 1822 discovered the m otor and sen­
sory roots o f the spinal cord. Bell, also, challenged the
omnipotential idea. Real evidence for functional localiza­
tion in the brain was provided in 1861, when Paul Broca
( 1 8 2 4 - 1 8 8 0 ) established a relationship between speech
defects and chc left frontal lobe. In 1870, G . Fritsch and
Eduard H itz ig ( 1 8 3 8 - 1 9 0 7 ) showed that stimulation o f
the motor cortex produced movements o f specific pares on
the contralateral side o f the body. For English translations
o f these papers see Von Bonin (1 9 6 0 ).
In 1855, B a r to lo m e o Panizza ( 1 7 8 5 - 1 8 6 7 ) , professor
o f anatomy at Pavia in Italy, reported that damage to an eye
in various animals caused degeneration in part of the thala­
mus and the contralateral posterior cortex. He also showed
that lesions in the posterior cortex caused contralateral
blindness. This was the first report o f the location o f the
visual cortex. The work was written in a local Italian journal
and is largely unknown, although Polyak ( 1 9 5 7 , p. 147)
gives credit to Panizza. See C o lo m b o et al. ( 2 0 0 2 ) for an
English translation o f Panizzas paper.
H erm an n M unk ( 1 8 3 9 - 1 9 1 2 ) , professor o f physiology
in Berlin, is usually credited with establishing the site o f the
primary visual cortex, although he erred in placing it on che
lateral surface o f the occipital lobe rather than at its poste­
rior pole (M unk 1879).
By studying effects o f brain lesions, S a lo m o n H enschcn
( 1 8 4 7 - 1 9 3 0 ) , in Stockholm , showed that the visual cortex
lies around the calcarine fissure. He was uncertain about
the representation o f the fovea. H . W ilb ra n d (1 8 9 0 ),
in Hamburg, observed the effects of central scotomas.
He dcduccd that each location in the visual cortex receives
inputs from a pair o f corresponding locations in the
two eyes.
Anatomists known as the decentralists, including D.
Fcrricr, C . von Monakow, and F.. Hitzig, objected to the
idea o f a precise cortical mapping o f visual space, mainly
because they had observed visual defects from damage to
many parts o f the brain. We now know that visual defects
arise from cortical areas other chan che primary visual area.
The firsc maps showing the recinocopic organization o f
the visual cortex were obtained by recording visual defects
in soldiers with gunshot wounds to the head. The first stud­
ies were conducted by T . Inouye ( 1 9 0 9 ) in Japan after the
Russian-Japanese war. G o rd o n H olm es ( 1 9 1 8 ) performed
similar studies in England during the 1 9 1 4 - 1 9 1 8 period.
 Ramon v Cajal suggested chat crossed and uncrossed
axons from che two eyes remain distinct in the visual path­
way. In 1913, M ieczyslaw M inkow ski, director o f the
Brain Research Institute in Zurich, was the first to establish
that they terminate in distinct layers o f the 1 G N. M inkowski
also helped to establish that the visual cortex is the main
recipient o f visual inputs and that the visual field is mapped
in a precise and stable manner. In 1905 A lfred W . C am p b ell
( 1 8 6 8 - 1 9 3 7 ) o f Sydney published his Histological Studies
on the Localization o f the Cerebral Function. Sec Polyak
( 1 9 5 7 ) lor a review o f early studies on the visual pathways
and cortex.
Clare and Bishop (1 9 5 4 ) discovered a visual area out­
side the primary visual corcex. This was the suprasylvian
cortex o f the cat, also known as the Clare-Bishop area. In
the 1970s, Zeki revealed a series o f visual areas in the
monkey (see Section 5.8).
A lively historical account o f the cerebral cortex has
been provided by Finger (2 0 0 0 ).
2 .7 A D V E N T O F P R E C IS E
M EA SU REM EN T
2 .7 .1 P R E C IS IO N V ISU A L IN S T R U M E N T S
Before the advent o f psychophysics in the 19th century,
investigations o f sensory systems were almost entirely quali­
tative and descriptive. In his Critique o f Pure Reason o f 1781
Immanuel Kant declared that the perception o f space and
time is beyond the scope o f experimental science. He was
soon to be proved wrong.
The precise determination o f visual detection and dis­
crimination thresholds had to wait for the invention o f reli­
able light sources and photometers in che early 20ch century.
Early examples are che measurement o f the contrast sensi­
tivity function by Schade ( 1 9 5 6 ) and o f the quantal effi­
ciency o f the eye by H ccht, Schlaer, and Pirennc (1 9 4 2 ).
T he second h a lf o f the 2 0 th century saw the arrival o f the
oscilloscope and computers for vision research.
D etection o f a simple stimulus such as a single light
source would seem to be immune to ambiguities. However,
with che development o f signal detection procedures in the
mid 20th century, it was realized that even a simple detec­
tion task is influenced bv the observers criterion, as well as
by the sensitivity of the sensory system (see Section
ЗЛ.К1).
Tlie precise measurement o f visual acuity, including ste-
reoacuitv, began in the second h a lf ot the 19th century. The
vernier scale is the most precise visual measuring instru­
ment. It was invented by Pierre Vernier ( 1 5 8 4 1 638), an
engineer who worked for the Hapsburgs. It formed part o f
his vernier calliper, which he described in 1631 in L a con­
struction, / ’usage, et les proprieties du quadrant nouveau de
tnathematiques. The user detects the offset o f two lines on a
secondary scale that slides parallel to the main scale. We
now use the term vernier acu ity со describe che offset o f
two lines thac can just be detected. It provides the most sen­
sitive measure o f visual acuity.
The study o f spatial aspects o f vision was triggered by
W h ea tsto n es invention o f the stereoscope in 1836. The
second h a lf o f the 19th century was marked by the measure­
ment ot visual illusions ot all kinds. The realization that
something as subjective as a visual illusion could be mea­
sured had a profound impact. However, a typical illusion,
such as the Muller-Lyer illusion, is noc due со a single visual
process, and measurements are notoriously difficult to
interpret. Great ingenuity is required to design stimuli and
procedures that tap specified processes.
During the 19th century, specialized instruments were
invented that allowed precise measurement ot temporal
aspects o f vision such as visual persistence, and reaction
times. In 1833 Plateau described an instrument for produc­
ing an impression o f continuous m otion from a sequence o f
images, which was based on Michael Faradays description
o f the process o f persistence o f vision. This eventually led со
the development o f cine photography (Section 2 .1 1 .3 ). In
1845, W heatstone built a chronoscope for measuring short
time intervals. In 1859 Volkmann constructed a tachisto-
scope for controlling the duration o f stimulus presentation.
For an account o f these developments see Wade and Heller
(1 9 9 7 ).
2 . 7 .2 P S Y C H O P H Y S IC S AND
E X P E R IM E N T A L P SY C H O L O G Y
The development o f instruments in the 19th century led to
the need tor precise quantitative psychophysical proce­
dures. The
publication o f Fechner’s Elem ente der
Psychophysik in 1860 filled this need.
G ustav T h e o d o r F ech n er ( 1 8 0 1 - 1 8 8 7 ) was born in a
village in southeastern Germany (Portrait Figure 2 .1 5 ). His
father was the village pastor. In 1822 he graduated in medi­
cine at the university o f Leipzig. His interests then turned
to mathematics and physics. In 18 3 3 , he was appointed p ro­
fessor o f physics at Leipzig, where he stayed for the rest o f
his life. In 1840 he wrote a paper on afterimages produced
by lookingat the sun through colored glasses. Unfortunately
he burned his retina while doing these experiments. During
the three years it to ok for his sight to recover, he developed
an interest in religion and problems o f the soul and co n ­
sciousness. Like Kepler, he developed a belief in a world
soul. I Ic believed that the universe, including animals,
planes, and the Earth, was alive and conscious. He saw psy­
chophysics as a way to measure the relation between body
energy and mental energy.
E rn st H einrich W eb er ( 1 7 9 5 - 1 8 7 8 ) was also in Leipzig
at that time. In his Tastsinn und Geweingefuhl (Touch and
 2 .8 E iM Р I R I С I S T - N A T I V 1 S T
CONTROVERSY

2 .S .1 T H E P R O T A G O N IS T S

The empiricist-nativist controversy that flourished in

Germany in the 19th century had its origins in the F.nglish
empiricists such as Hume, in K an ts concept o f the a priori
status of the percept and concept o f space, and the local sign
theory o f Hermann Locze. Helmholtz and Hcring were the
most vigorous opponents in the controversy. The battle
between these giants has been described by Turner ( 1 9 9 3 ,
1994).
Herm ann von H elm holtz was born in the Prussian city
of Potsdam in 1821 and died in 1894 (Portrait Figure 2. 16).
His father was a master at the Potsdam Gymnasium. His
mother was a descendant ot W illiam Penn. He did his d o c­
toral work with Johannes Muller in Berlin (Portrait Figure
2 .1 7 ). W h ile serving as a military physician, he was able to
conduct experiments in the Potsdam barracks. His first
fig u re 2. IS - G u s t a v Ц ) O u tО Г F c c h n e r ( I S O I f S S 7 ). (C o w m y Iiutitu rion experiments in physiology showed that energy is conserved
b b fiU K f. VC'nbiAiioe, D C >
in metabolic processes, leaving no room for che vital force
proposed by German idealist philosophers. He shared his
antivicalisc views wich his friend, Emil du Hois-Rcymond
general feeling) o f 1846 he seated chac che racio o f che jusc ( 1 8 1 8 - 1 8 9 6 ) , physiologist, founder o f electrophysiology,
noticeable difference in the intensity of a stimulus to the and essayist.
*
initial intensity is a constant. Fechner later expressed this
relationship in mathematical form, and called it W e b e r s
law. In about 1853 Fechner began to perform psychophysi­
cal experiments with the help o f his brother-in-law A. W.
Volkmann. Little was published until 1860, when the
Elementc der Psychophysik appeared. ’The b o ok immediately
attracted the attention o f H elm holtz, Hcring, and Wundt.
It laid the foundations o f experimental psychology, c o lo ­
rimetry, audiology, and optometry. Fechner s interests then
turned со experimental aesthetics.
Since then, psychophysics has become more and more
refined and sophisticated (see Chapter 3).
W ilh e lm M ax W u n d t ( 1 8 3 2 - 1920) in 1875 went to
Leipzig, where he founded the first laboratory of
experimental psychology in 1879. In spite of being recog­
nized as the founder o f experimental psychology, W undt
distinguished between physical and psychic causality. For
Wundt, psychic causality is based on immediate experience,
which can n ot be derived from physical causality (W undt
1894a).
In 1893, O sw ald Kiilpe, W u n d ts assistant, wrote
Grundriss der Psychologic, in which he argued that
Figure i.i6. H erm ann I. ltd wig von H elm holtz. B o rn in P otsdam , G erm any
psychology should be based on the idea of a biological
in 1 8 2 1 . H e studied m ed icin e at the R oyal M ilita ry In stitu te in Berlin.
organism rather than a psychic entity. This approach was W h ile a surgeon in the Prussian arm y from 1 8 4 3 to 18-*8 he worked on
based on the writings o f the philosophers Avenarius and problem s in physics. H e was professor o t physiology at th e U niversity
F.rnst Mach. Kiilpe moved to Wurzburg in 1994 to found o t K on igsberg ( 1 8 4 9 - 1 8 5 5 ) , the U n iv ersity o f B o n n ( 1 8 5 5 - 1 8 5 S ),
and th e U n iv ersity o f H eid elberg { 1 8 5 8 - 1 8 7 1 ). From 1871 to 1 8 8 8
what became known as the Wurzburg school. These ideas
he was professor o f physics at Berlin U niversity. H e was awarded the
gave rise to logical positivism and behaviorism (sec Danziger G ra cfc M edal in 18 S 0 and m any o th e r h on ors. I Ic lectu red at the Royal
1979). S o ciety o f L o n d o n in 1 8 8 1 . H e died in 1 8 9 4 . Ko^n-ibc^o i9o:l

Figure 2.17 Johan n es M u Her ( ISO / IS S S ). Professor o t anacom y and
physiology in B o n n and B erlin . (From Pc*r*k 1957).
In 1850 H elm holtz was appointed professor o f anatomy
and physiology at the University o f Konigsbcrg, where he
measured the speed o f nerve conduction and invented the
ophthalmoscope. He visited England in 1853 and tried
without success to meet W heatstone. In 1855 he became
professor o f anatomy in Bonn and, in 1858, professor ot
physiology in Heidelberg. In chc 1850s his interests
shifted from nerve and muscle physiology to sensory
physiology. His Handbuch der Physiologischen Optik ,
appeared in full in 1867. This has been the most influential
book in visual science. In 187 0 he became professor o f
physics at the University o f Berlin. By 1875 lie had aban­
doned sensory physiology for physics. He died o f a stroke in
1894. Koenigsberger ( 1 9 0 2 ) produced a biography o f
Hclmholcz.
For H elm holtz, sensations were “signs o f external
objects” learned by “practice and experience.” He argued
that sensations do not resemble the objects they symbolize,
any more than letters o f chc alphabet resemble the sounds
they represent. He revolted against German idealist m eta­
physical philosophy, as expounded by such figures as Hegel.
For Helm holtz, metaphysical hypotheses were worthless if
not accompanied by critical empirical invcstigacion.
H elm holtz ( 1 9 0 9 , vol. 3, p. 5 3 3 ) stated:
The fundamental thesis o f the empirical cheory is:
The sensations ot che senses are tokens for conscious­
ness, ic being left со our incclligencc со learn how со
comprehend cheir meaning. . . . The only psychic
accivicy required for chis purpose is chc regularly
rccurrenc associacion becween cwo ideas which have
often been connccccd before.
Hclmholcz ( 1 9 0 9 , vol. 3, p. 2) also wrocc,
wc always believe chac wc sec such objeccs as would,
under condicions o f normal vision, produce the reti­
nal image o f which wc arc actually conscious.
In attacking H cring’s nativisc theory o f visual dircccion,
he scaced ( 1 9 0 9 , p. 5 3 5 ),
I am inclined to think thac ic is even probable chac
chc growch o f chc muscles, perhaps coo even chc
efficiency o f nervous cransmission, is so adapced со
chc demands made upon ic during chc life ot che
individual, and perhaps by inheritance during the
life ot che species, chac the requisite movements
that are the most suitable becom e also che easiest со
execuce.
He weakened his case for empiricism by adm itting thac
natural selection may also play a role. The nativist also takes
this view. But Helm holtz qualified this by adding the scace-
ment, “In any event, even if chis anacomicai mechanism
exists ic is merely conducive, and noc obligacory
In pare 3 o f his H andbook o f Physiological Optics,
Hclmholcz defined and defended empiricism, buc Hering,
chc nacivisc, was his real cargcc. O thers who supported chc
empirical approach included W ilhelm von Bezold ( 1 8 3 7 —
1 9 0 7 ), Sigmund F.xncr ( 1 8 4 6 - 1 9 2 6 ) , Alfred von Gracfc
( 1 8 3 0 - 1 8 9 9 ) , Johannes von Kries ( 1 8 5 3 - 1 9 2 8 ) , and
Willibald Nagel ( 1 8 4 8 - 1 9 1 7 ) .
Ewald H ering ( 1 8 3 4 - 1 9 1 8 ) (Porcraic Figure 2 .1 8 ) was
born in Saxony. His father was a Lutheran pascor. He stud­
ied medicine in Leipzig. There is no biography o f Hering.
Although not a scudent ot Johannes Muller, ic is ironic chac,
like Helmholtz, he was very much influenced by Muller.
Hering practiced as a private physician between I 8 6 0 and
1865, during which time he published his firsc papers on
binocular vision and wrocc chc five-volume work Beitrage
ztir Physiology. In 1865 he was appoinced professor o f phys­
iology in che Milicary Medical Academy in V ienna, where
he worked on respiracion and binocular vision. His 'Theory
o f Binocular Vision appeared in 1868, a year after Helmholczs
Physiological Optics. In 1870 he succeeded Jan Purkinje as
professor ot physiology ac che Universicy o f Prague where
he wrocc chc book Spatial Sense an d Movements o f the Eye.
In 1895 he succeeded Karl Ludwig ac che Universicy o f
Leipzig. His final book, Outlines o f a Theory o f Light Sense,
appeared in 1920, cwo years after his deach. All chese books
are available in English cranslacion.
Hering acknowledged chc role o f learning in perception
and rcsenccd being idencificd as a nacivisc. However, he
insisced that basic sensory and perceptual mechanisms are a
product of a long evolutionary process and occur mainly in
or near che sense organs racher chan ac the level o f cogni­
tion. He vigorously opposed wliac he considered со be

Figure M i- F.watd H ering. B o m in A ltgersd orf, G erm any, in 1 8 3 4 . H e
o b ta in ed an M .D . from th e U niversity o f L eipzig in 1 8 5 8 . Betw een
1 8 6 2 and 1 S 7 0 he worked in th e P hysiological R esearch U n it ac the
U niversity o f L eipzig and th e Josep h s-A kad cm ie. In 1 8 7 0 he was
appointed professor o f physiology at the U niversity o t Prague. From
1 8 9 5 u ntil his d eath in 1 9 1 8 he was professor o f physiology at the
U niversity o f Leipzig. H e was aw arded th e G ra cfc M edal o t the G erm an
O p h th a lm o lo g ica l S o ciety in 1 9 0 6 . 1930
H elm holtzs undue emphasis on learning and experience.
His students and those devoted to his approach included
Alfred Bielchowsky ( 1 8 7 1 - 1 9 4 0 ) , Carl von Hess ( 1 8 6 3 —
1 923), Franz Hillebrand (1 8 6 3-19 26 ), and Armin
Tschermak-Seysenegg ( 1 8 7 0 - 1 9 5 2 ) . H erings views were
also supported by F.rnst M ach ( 1 8 3 8 1 916), his colleague
in Prague (Portrait Figure 2 .19 ). For an account o f Mach s
contributions to visual science see Ratcliff ( 1 9 6 5 ) and
Banks (2 0 0 1 ).
Hcring was 13 years younger than Helm holtz. He was
sometimes deferential but usually attacked in a sarcastic and
vitriolic style. A sample ot that style can be found in the
foreword to his book On the theory o f the Light Sense o f
1874. Hering wrote,
that modern tendency in sensory physiology, which
has found its most acute expression in the
Physiological O ptics o f H elm holtz, is n ot leading us
to the truth, and whoever wishes to open up new
avenues o f research in this area, must first free him­
self from the theories which now prevail.
He argued that, just as earlier physiologists had
explained troublesome phenomena in terms o f vital forces,
so today, in treatises on physiological optics one secs invoca­
tions o f the “psyche” or “inference.” For Hering, this was
rijtuM м у . Ernst M ach ( /S 3 8 -1 916). Born in Furas, M oravia. H e studied
in V ie n n a and b ccam c professor o f m ath em atics in G raz to r 3 years* in
Prague tor 2 8 years, and finally, professor o t physics in V ien n a.
J < r O f l c i r t i i i i K h c n Naft*>atk»blioiKek)
tantamount to the “spiritualism” and idealism that
H elm holtz abhorred. Hering looked forward to the day
when physiological psychology, including the physiology o f
consciousness, would replace the descriptive tradition ot
“philosophical psychology,” which investigated sensory
phenomena without regard for their organic basis.
In his Founders Day lecture at Berlin University in
1878 H elm holtz declared,
First o f all, nacivistic hypotheses about knowledge
o f the visual world explain nothing at all, but only
assume that the fact to be explained exists, while at
the same time rejecting the possibility ot tracing
this knowledge back to reliably established mental
processes.
Helm holtz was irritated and frustrated by H erings
attacks but tried to maintain his composure. For instance,
he wrote ( 1 9 0 9 , vol. 3, p. 5 5 7 ),
I have been obliged to make this criticism ot Mr.
Herings views o f the facts o f the case, but I trust it
will n o t be regarded as an expression ot personal irri­
tation on account o f the attacks which he has made
on my latest articles.
There was a strange futility about the battle between
Helm holtz and Hcring, as there is about the whole nativist-
empirieist controversy. It was fueled as much by personal
animosity as by scientific issues. W e will see in the following
sections that, in spite o f the animosity between the two
men, H elm holtz came to agree wich m a n y o f H erings views,
and Hering came to agree with many o f Helmholczs views.
The disagreement stemmed largely from H erings vitriolic
attacks and from H elm holtzs reluctance to consider low-
level physiological mechanisms for such phenomena as see-
rcopsis, color contrast, and coordinated eye movements.
The nativisc-empiricist debate about color vision has been
reviewed by Kingdom ( 1 9 9 7 ). ’Ihc following three sections
describe the debaces between Hering and Helmholtz about
three aspects o f spatial vision, namely eye movements, visual
direction, and binocular vision.
2 . 8 .2 D E B A T E A B O U T EYE M O V E M E N T S
Helm holtz argued that the eyes are separate organs, which,
in principle, may be moved wholly independently. He
claimed that D o n d ers and Listings laws (Section 10.1.2d)
are habits acquired to facilitate clear and easy visual orienta­
tion. O n c e acquired and ingrained, however, the facility
can n ot be overridden by acts o f will. But movements other
than habitual ones are anatomically possible. He argued
that by using prism glasses, which produce abnormal
separation o f the visual axes, we can induce the eyes to per­
form vertical or absolute divergences. He observed
thac, when sleepy, he saw double images o f objeccs chat dif­
fered in a way chat indicated that the eyes had diverged ver­
tically o r cyclorotated. W h en fully awake, he could not
perform these eye movements voluntarily (Hclmholcz
1910, vol. 3, p. 59 ).
Hering held chac che coordinated movements of the
eyes arc innate. He responded sarcastically to H elm holtzs
observation,
It is likely that the great H elm holtz in his dozing
state, had simply failed to notice chac he had allowed
his head to nod со one side. This would produce che
same rcsulc.
( H E R I N G 1864. p. 2 74 ).
Hclmholcz recorted,
I did n ot make che miscake which he (H ering) accri-
buces со me, and o f which even a person wich licde
training in observing double images could scarcely
beguilcy; namely, che miscake o f supposing chac che
images were on dilferenc levels when chcy were really
side by side, simply because my head happened со be
tilted!
( H E L M H O L T Z , 1909. v o t X fo x n o u . f . 5 9 ).
In his Theory o f Binocular Vision Hering insisted that
there are no cyclovergence eye movements bur, in his later
book on Tlx Spatial Sense an d Movements of the Eyes, he
agreed with H elm holtz that these movements exist, as
indeed they do (Section 10.7)
Helm holtz believed that the motion aftereffect is
due to eye movements. Ic seems that he was reluctant to
allow thac there are dedicated motion detectors at an early
stage o f visual processing. Dvorak ( 1 8 7 0 ) , working under
Ernst Mach, pointed out that the eye-movement theory
cannot account for the spiral aftereffect in which motion
in several directions occurs at the same time (see Broerse
et al. 1994).
2 . 8 .3 D E B A T E A B O U T V ISU A L D IR E C T IO N
Steinbuch ( 1 8 1 1 ) was the first to propose a theory o f how-
visual directions are calibrated. He suggested that the spa­
tial value o f each locacion is provided by che m otor response
required to move the eyes to that location. In concrasc,
Tourcual ( 1 8 2 7 ) proposed that che spacial senses are innacely
calibrated (see Rose 1999). Lorze ( 1 8 5 2 ) coined the term
“local sign” and also proposed a m otor theory o f spatial
calibration.
According to Hering ( 1 8 6 4 ) , each point in each recina
has a local sign composed o f chree space values: ics eleva-
cion, azimuth, and depth value. He named che p o in to f fixa­
tion the core point ( Kernpunkt) and che vertical plane
containi ng the horizon cal horopccr he n amed che A'crnftachc.
He stated that objects lying in this plane appeared to lie on
a frontal surface. In H erings terminology, elevation and
azimuth signify the direction o f the point, and the poin ts
depth value is its signed lateral posicion relative со che fovea.
Points on rhe nasal retina have positive depth values and
those on the temporal retina have negative depth values
(Figure 2 .2 0 Л ). Images w ith positive depth values appear
beyond the convergence plane, even when only one eye is
open. Images with negative depth values appear nearer than
the convergence plane. The depth values o f images falling
on corresponding points in the two retinas are equal anil
opposite, and the object lies in the horizontal horopcer. He
speculaced chac all points on che horizontal horopcer appear
on a froncal surface. H e conceded thac che perception of the
absoluce discancc o f an objecc depends on learned cues
rather than on innate mechanisms.
Hering claimed to demonscrace his cheory o f depch
values by fixating a point in the midline and observing
che double images o f a vertical wire nearer and со the left
(Figure 2 .2 0 B ). He claimed that the image o f the wire on
the nasal h a lf o f che left eye appears more discant than the
fixation plane and thac che image on the temporal half o f
che righc eve appears nearer chan che fixation plane (Hering
1865).
After crying со observe the effect, Hclmholcz wrote,
I have gazed at the pin so long and so fixedly thac
everything was extinguished by rhe negative after­
images___ I have never been able to persuade myself
that chis phenom enon occurred in rhe main as ic
ought to occur according to che Hering cheory; and

в Helmholtz, supported his empiricism by the fact that
Fiftwc 2 .20 . H cring i theory o f d ep th ы !ы ек (A ) A cco rd in g to H crin g , im ages
o n ca ch nasal retin a have positive depth values, and th o se on each
tem p oral retin a have negative depth values, as show n in the upper
figure. ( B ; H e claim ed th a t a near wire on the left o f fixation produces
an image w ith positive depth value in th e left eye and therefore appears
beyond the fixation plane. Its rig h t-cy c im age has negative d ep th value
an d appears nearer than the fixation plane. H elm h o ltz could n ot
co n firm th e effect.
I never should have ventured to lav the foundation
o f a new theory o f vision on an observation made
with images that are half-extinguished in this fash­
ion. However, 1 admit that 1 may have been unskill­
ful. Only, Mr. Hcring will have to forgive me for not
being able to say that 1 have been convinced by this
“overwhelming p r o o f ” o f the correctness ot his
theory, as he put it.
( H E L M H O L T Z S<S09, Г»1. i, />.55-/)
depth values
Fipwc i n . H d n J/o ltz >
’ refu tation o f H cring i theory. I Ich n h o ltz argued that,
accord m y to H c rin g s th e o ry o f rc tiru l d ep th values, a wall seen 01» the
right hv on ly th e leti eve and on the left by on ly th e right eye should
appear to slant in op p osite d ire ctio n s a b o u t th e m id iin c.
H elm holtz ( 1 9 0 9 ) argued that, according to Hering, a
wall should appear inclined in opposite directions when
one eye sees only the nasal half and the other eye only the
temporal halt (Figure 2 .2 1 ). But this does n ot happen.
Hcring abandoned his theory o f retinal depth values after
this attack and agreed with H elm holtzs that stcreopsis is
based on binocular disparity. However, there is some truth
in H crin g s theory, as we shall see in Section 17.2.
persons with restored sight do not recognize simple objects
(Section 8.3.3). However, he admitted that they rapidly
learn to distinguish between objects in different positions.
He concluded that, prior to all experience, adjacent points
are seen as adjacent (H elm holtz 1910, vol. 3, p. 2 2 7 ). This
was close to Hering s view.
Helm holtz asked, i f perceptions are shaped by learning
to conform to the objects o f the world, why do we suffer
from illusions? He described two classes o f illusions. Those
o f the first class arise because identical impressions on a
sense organ can be produced by distinct distal stimuli. For
example, the illusion that a stereogram viewed in a stereo­
scope is three-dimensional arises because it produces rhe
same proximal stimulus as a real scene. Illusions o f che
second class arise when a sense organ is used in an unusual
way o r is exposed to an unusual stimulus configuration.
H crings experiments on binocular visual direction per­
suaded Helm holtz that directions arc referred to a point
midway between the eyes— the egocenter. Hue, for
H elm holtz, this relation between images and direction was
learned. It is odd that neither Hcring nor H elm holtz cited
Ptolemy, Alhazen, Briggs, or Wells on this question (see
Section 16.7).
2 . 8 .4 D E B A T E A B O U T
B IN O C U L A R V ISIO N
T he first encounter between Helm holtz and Hering
occurred in 1864, when Hering was an unknown lecturer in
Leipzig. The two men had independently produced a gen­
eral solution ot the horopter. There was some dispute over
priority (see Helmholtz 1909, vol. 3, p. 4 8 4 , footn ote 4)
but the main dispute concerned the inclination o t the verti­
cal horopter. Helm holtz believed it was shaped by experi­
ence to lie along the ground. Hering described the
inclination o f the vertical horopter as varying at random.
In general, Hering believed that binocular correspon­
dence is innate. Helm holtz held an empirical view o f bin ­
ocular correspondence, as described in Section 2 .10.5. He
stated that,
any theory that assumes that fibres proceeding from
corresponding places on the two retinas are united
in a single fibre that transmits the impressions in the
two eyes unseparated to the brain, is inadmissible
and incompatible with the facts.
(1909, e d . 3, f>. 539)
He reluctantly considered the possibility that corre­
sponding fibers split into two branches, two o f which unite
and two o f which remain distinct. See Section 1 1.9 for a
discussion o f this issue.
The debate about whether binocular correspondence is
innate o r learned was centered on reports that people who
squint develop an anomalous pattern o f binocular corre­
spondence. Followers o f the nativist school allowed that
anomalous correspondence can develop but argued that
this does not prove that the normal pattern is learned
(Section 14.4.1). Another long debate about the shape o f
the horizontal horopter is described in Section 14.6.2.
Helm holtz came to accept that the pattern o f retinal
correspondence responsible for the form o f the horopter
has an innate com ponent. In spite o f these concessions to
Hering, H elm holtz persisted in believing that experience
shapes the development o f spatial perception.
I he nativist views o f Hering and the empiricist views o f
H elm holtz arose because each antagonist selected evidence
to suit his theory and each looked at different aspects o f the
visual process. For example, H elm holtzs trichromatic
theory o f color vision and the apparently conflicting
opponcncy theory o t Hering are now understood as differ­
en t stages in a complex process. Both men became em otion ­
ally involved. Hering used ridicule and bombast. Helm holtz
was more restrained and conceded several points to Hering
but he occasionally resorted to sarcasm. H elm holtz became
very frustrated by his encounters with Hering, as revealed
in one o f his letters to his friend, du Bois-Reymond, dated
February 1865 (Kirsten 1986).
Mr. Hering has annoyed me considerably with his
impertinent ways o f judging other peoples work
which, in part, he has not taken the trouble to under­
stand properly. However, I do n ot want to treat him
in a nasty way since he is an intelligent man in his
own way. liven though, at the moment, his views
conflict with mine, he is working out his own view­
point in a consistent manner. He has been, as I have
heard, mentally ill and this has until now held me
back from bringing him down, which he has at times
deserved.
It may have been frustration with Hering that caused
Helm holtz to return to physics in 1875.
W e will see in Chapters 6 and 7 that the interplay
between genetic factors and experiential factors that gov­
erns the development o f the nervous system and visual
mechanisms is much more complex than either Helmholtz
or Hering imagined.
2 .9 D IS C O V E R Y O F P E R S P E C T IV E
2 .9 .1 P E R S P E C T I V E IN T H E
A N C IE N T W O R LD
In paintings from ancient F.gypt, Babylonia, and Assyria,
depth is represented by overlapping images, but there is no
hint o f any type o f perspective. O b jects at different dis­
tances were drawn in the same size. Human figures were
drawn in front view or profile o r in a com bination o f front
view and profile. Chariots were drawn in side view with one
circular wheel. G reek paintings before about 5 0 0 BC. were
limited in a similar way. By about 5 0 0 B C , human figures
began to be drawn at an oblique angle and wheels
and shields seen at an angle were drawn as ellipses, as in
Figure 2 .2 2 (K n o rr 1992).
In about the year 2 4 A D the Roman architect, Vitruvius,
wrote Dc A rchitecture known in English as The ten books on
architecture He stated that Agatharcus o f Samos ( 5 2 5 - 4 5 6
B C ) had invented a method for painting scenes for the the­
ater o f Dionysus in Athens so that they appeared in depth.
Such procedures were known assccnography ( skenographia ).
Vitruvius wrote,
For in the beginning in Athens, when Aeschylus was
presenting a tragedy, Agatharcus set the stage, and
left a commentary upon the matter. Instructed by
this, Dem ocritus and Anaxagoras wrote about the
same thing, how it is necessary that, a fixed center
f igure 2 .2 L P a in t i n g 0 П a (trccic VOSe (k a n ti)a r o s ). Frc-m the «rc o n d halt ot rh r $ t b t t n t iir v

B C (R r it iib M ntcism )

rijtuf* 1.23* G re e k p a r a lle lp n 'fp c s tu 'c . Гго-л» an A pulia n с л К я к г л к г . i r h c<nmr>- B C

being established, the lines correspond by natural
(W t r c b u r j;)
law to the sight o f the eves and the extension o f the
rays, so that from an uncertain object certain images
may render the appcarance o f buildings in the paint­ lower one tor a seated observer. N ot all receding lines co n ­
ing of the stages, and tilings which are drawn upon verge to one or other o f these vanishing points, suggesting
vertical ad plane surfaces may seem in one case to be that artists used an intuitive procedure rather than vanish­
receding, and in another to be projecting (Vitruvius, ing points. Several murals in perspective have also been
Book 7 , Chapter 2, p. 2. In an English translation by unearthed near Rome. Textual evidence reveals that the
Granger 1931). Romans, like the Greeks, painted stage sets in perspective
(R ich ter 1970; Little 1971).
O pinions differ about whether the word “center” refers The practice o f mapmaking influenced the development
to a vanishing point in the picture or in the center of the of painting in perspective. In 13th- and 14th-century Italy,
eye. Although this passage describes rhe general principle o f maps o f the Mediterranean were made for navigation. These
linear perspective it does not provide an exact geometrical so-called portolan maps consisted o f stretches ot coastline
procedure for drawing in perspective. with place names and a superimposed lattice o f radiating
Anaxagoras ( 5 0 0 - 4 2 8 B C ) is credited with writing a direction lines. In 1395 some prominent citizens ot Florence
book on scenography. Plutarch describes how rhe aristocrat formed a study group to learn classical Greek. In 1400, two
Alcibiades kidnapped a scene painter and forced him to members ot the group, Manuel Chrysoloras and Jacopo
decorate the walls o f his mansion (Little 1971). The prac­ d’Angiolo, journeyed to C onstantinople in search o f early
tice of painting the interiors of mansions with frescoes in G reek texts and returned to Florence with Ptolemy’s
perspective continued into Roman times. By about 425 Geographia, which was unknown in Western Europe at
B C , foreshortening began to show in G reek vase paintings. that time.
Half-open doors were represented foreshortened with This 2nd-ccntury work contained eight books and 27
inclined top and bottom edges, but the receding edges were maps, one o f which was o f the whole known world from
parallel rather than converged. Foreshortening and oblique Sweden and Russia in the North to the Nile in the South,
parallel lines were also used in drawings of buildings, as and from Gibraltar in the West to India in the East. 'Ihe
shown in Figure 2.23. About 3 0 0 B C , F.uclid provided work was translated into Latin in 15th-century Florence.
some geometrical analysis o f perspective in his Optics M ost importantly, the work provided three procedures
(Section 2.1.3b). tor mapping lines of longitude and latitude on the curved
Frescoes discovered in Pompeii have convergent per­ surface o f the earth o n to a flat surface (Edgerton 1975). In
spective, as shown in Figure 2.24. These date from before one procedure the eye was placed in the plane ot a defined
A D 7 9 , the year that Pompeii was engulfed by the eruption line o f latitude, which was drawn as a straight horizontal
o f M ount Vesuvius. The added construction lines show that line on the map. The central line ot longitude was then
the artist used two vanishing points in rhe midline. Perhaps drawn as a vertical line. W ith the eye as the center o f projec­
the upper one was designed tor a standing observer and the tion, other lines ot latitude and longitude were projected
Figure 2. 24 . D raw ing m ad e fr o m л m ural in Pom peii. Added bold lines approxim ately converge on tw o vanish in g p o in ts. A dded fine lines converge on
o th e r p oin ts usually, b u t n o t always, in th e m id lin c. (AH»f«dfrnm Lmle 1971)
inco che picture plane as curved lines. Ptolemy increased che
spacing ot lines o f lacicudc as chcy approached chc Norch
Pole со avoid che crowding chac scricc projeccion creaces.
Unlike chc dircccion lines ot chc earlier porcolan maps, chc
lines o f lacicude and longicude precisely indexed locacions
on chc map.
The eye is geometrically equivalenc со che projeccion
ccnccr, and chc ccncral line o f lacicude is equivalenc со che
horizon line o f a pcrspcccivc transformation. Thus, Pcolcmy
had developed che basic principles o f drawing in perspec­
tive in chc 2nd ccncury, alchough he applied chcm only со
cartography. The arrival o f che Gcographia in Florence in
140 0 was one o f chc faccors chac led со chc devclopmcnc ot
perspeecive in art in that city. It was also a major factor that
inspired Columbus to sail across chc Atlantic.
M. Friendly has produced an illustrated history o f map-
making and other graphic procedures ( http://www.mach.
yorku.ca/SCS/Gallery/milescone/).
The Lacin word “perspecciva” refers со che cradicion ot
applying geomecry to vision, developed by Euclid, Ptolemy,
Alhazen, and the Perspcccivists ot medieval Europe. This
tradition culminated in Keplers discovery o f the optical
principles ot image tormacion. As we shall sec, practicing
artists developed methods o f drawing in perspective w ith­
out reference to chc Pcrspeccivises, buc chc firsc formal
description o f perspective and che subsequent development
ot projeccivc geomecry owed something со che perspecciviscs.
2 .9 .2 P E R S P E C T IV E D U R IN G T H E
14TH C E N T U R Y
The arrises ot ancicnc C h in a and medieval Europe used
overlap, height in the field, foreshortening, and oblique
lines to represenc depch. There was no accempc со rcprcsenc
parallel lines converging inco che distance. In fact, parallel
lines were often drawn diverging racher chan converging
wich discance, as in che examples shown in Figure 2.25. This
may be because lines drawn in parallel perspective appear to
diverge, as shown in Figure 2 .2 5 Л . An artisan copying a
sketch drawn in parallel perspective o n to a fresco would
draw rhe illusion. This could then serve as a model for ocher
arcisans and che ettecc would gee larger as successive genera-
cions o f pupils copied from cheir masters.
W hatever che Romans had learned abouc convergent
perspective was lost after che fall o f che Rom an Empire.
Convergenc perspeecive did noc emerge again until the early
I4ch cencury {Bunim 1940). During chc 14ch cencury,
Gioeeo and his pupils, che Lorcnzeeci brochers, and Duccio
began со use converging lines со dcpict riles on ceilings and
floors, as shown in Figure 2.26. Avanzano and Giusco used
chc same procedures in Padua during che lasc quarcer o f che
I4ch cencury. However, while lines depiccing parallel
receding edges somcrimes converged со a poinc, che same-
vanishing poinc was noc used consiscencly for differenc parts
ot ehe paincing. These arrises followed cercain basic rules
 В D

i.*m c 2 .2 *. lu irly divergen t perspective. (A ) Illu so ry d ivergence o t parallel lines o n the apparently reced in g sides o f the draw ing o t an o b je ct.
(B ) A m osaic in P om peii (pkou^a^by John Н ш т) ( С ) A fresco in th e m on astery o f D e ca n i in Yugoslavia painted in the 13th or early 14t h century.
N o te the divergence o t the sides o t the c a rt and the haphazard perspective o n the tow ers. (Fk*«. 19ьб) ( D ) A fresco from the g ro tto o f T ou cn
H o u an g . C h in a , from the T a n g d yn asty ( 6 1 8 - 9 0 6 ) . N o te th e divergence o t the sides o t the table, (fro*» FoukjJ c I9&)

that had been described b v C en n in o C en n in i before G iotto.
Cennini wrote,
The mouldings which you make at the top o f build­
ings should slant downwards from the edge next to
the rooi; the mouldings half way up the face must be
quite level and even, the mouldings at the base o f
the building must slant upwards in the opposite
direction to the upper mouldings.
U r K E M P I97S}
In drawing tiled floors or ceilings in perspective, artists
o f the 14th century seem to have used one or two distance
points (see Section 26.1 .2 ). Distance points are points on
the horizon to which lines at 4 5 ’ converge. For example,
the fresco in the Lower C hurch at Assisi has a tiled ceiling
drawn in accurate perspective, even though the painting as
a whole is not in accurate perspective (Klein 1961). O n e
can still sec brackets at the location o f the two distance
points o f the diagonals in the painting. It was apparently a
com m on practice in early 14th century Tuscan workshops
to draw diagonals on receding surfaces by rotating a piece o f
string attached to nails (Panofsky 1927). Thus, artisans of
the 14th ccnturv were using distance points before the use
o f the principal vanishing point and well before Viator gave
the first written account o f distance points in his De
A rtificiali Perspectiva o f 1505. These artisan traditions pro b­
ably originated in ancient Rome. The development o f per­
spective must have been delayed by the advent o f the Black
Death in 1346.

Figure 2. 1 *. Perspective in H lh-cen tu ry Italy, (A ) Tit с lu is t S u p p er by D u ccio
S ien a , M ils, d e ir O p e ra tlcl D u o m o . ( B ) Je s u s b e fo r e th e C a if, by G io tto
( 13 0 5 } . T h e c eilin g rafters show con v ergen t perspective, but the
in co n sisten t vanishing p o in t is above th e h orizon . Edges o f the dais
have parallel perspective.
2 . 9 .3 P E R S P E C T I V E IN T H E R E N A I S S A N C E
A precise procedure for drawing in linear perspective was
discovered by Filippo Brunelleschi ( 1 3 7 7 - 1 4 4 6 ) , the archi­
tect who designed the cathedral in Florence. In about 1420
he painted the baptistery as seen from a distance o f about
3 5 m, which is inside the door o f the cathcdral, approxi­
mately as seen in Figure 2 .27 (Dam isch 1994). The painting
has not survived. According to Brunelleschi’s biographer,
A ntonio di Tuccio M anctti ( 1 4 2 3 - 1 4 9 1 ) , people stood in
the cathedral doorway and, while facing the back o f the
painting, looked through a small hole in itsccntcr, as shown
in Figure 2.28. The hole was as small as a “lentil” on the
painted side and widened to the size o f a “ducet” on the
m
Идо* 2 .27. Ih c baptistery o f San G iovanni, Florence. View from th e d o o r o f
the cath cd ral. (РЯо|.'^ripfe bv Brunn#r in P a m iw h 1 99 4 )
Projected
Figvrc 2 .2s. Uhtstoation ofB rtin cU esebi) v iew in gdevke. I he observer stood
behind the p ictu re and looked throu gh a hole a t a reflection o i the
p ictu re in a m irror.
viewing side. A suspended mirror produced a reflection o f
the painting, which filled the same visual angle as the bap­
tistery. Brunelleschi did not paint rhe sky. Instead, bur­
nished silver on the picture surface reflected the real sky and
drifting clouds. People were fooled into believing that they
were looking at the actual building. The hole forced viewers
to look with only one eye, thus removing binocular cues to
depth.
Brunelleschis second painting in perspective was o f
the Palazzo della Signoria in the Palazzo Vccchio. It was
apparently larger than the earlier painting and was viewed chc scenc. Lynes suggests chat Brunelleschi overcame chis
directly in the location where it was painted. The parts cor­ problem by scanding back from che mirror and, with che
responding to sky were cut away so that when viewed from head in diffcrenc positions, marking che mirror with each
the correct position, the skyline in the painting coincided point of the scene as it aligned with the reflection of the end
with the skyline o f the real buildings in the Palazzo. This o f a rod inserted into a hole in the mirror. This could have
painting has also not survived. been the same hole that supported the gnom on. Lynes also
There are three theories about how Brunelleschi pro­ suggests chat Brunelleschi painted his second picture, that
duced his paintings. The first theory is that he used the o f the Palazzo della Signoria, by tracing ic on che window o f
measuring instruments and geometrical constructions avail­ chc church. In chis ease, no mirror was required, cither for
able to architects at chat time. These instruments included producing the paincing or for viewing ic.
rods, squares, quadrants, and mirrors. Geometrical co n ­ Neicher ot che above cwo mechods involves che explicit
structions consisted o f plans and elevations o f buildings. In use o f a vanishing poinc, alchough che paintings would c o n ­
his L ife ofBrunelleschi ( 1 5 5 0 ), Vasari stated that Brunelleschi tain a unified vanishing point. The third theory about
drew lines from a plan and an elevation o f the building he Brunelleschi s method is chac he used geomecrical principles
was painting to intersect planes according to what is now ot perspective. We have seen chac che basic ideas underlying
known as orthographic projection (see Hyman 1974). perspective were expressed in Euclid’s Optics, and Roman
Carter 1970) suggested that Brunelleschi used the co n ­ and 14th-century painters came very close со che corrccc
struction depicted in Figure 2.29. This resulted in the paint­ solution.
ing being a mirror image o f the scene, which would explain A few years after Brunelleschi painted the baptistery,
why Brunelleschi used a mirror to exhibit the painting. some painters in Florence began со use a unified vanishing
The second theorv is that Brunelleschi traced the poinc. For example, Masaccio, a friend ot Brunelleschi,
reflected image o f the baptistery on the surface o f a mirror painccd chc Trinity fresco in chc church o f Sanca Maria
(Krautheimer and Krautheimer-Hess 1982). Lynes ( 1 9 8 0 ) Novella in 1425 (Figure 2.30). Measuremenrs have revealed
concluded that Brunelleschi used a polished metal sundial.
The mirror inversion of the picture would not be apparent
in chc painting o f a symmetrical building seen through an
arch. But Brunelleschi muse have realized lacer that the
mirror image would be corrected when the picture was
viewed by reflection through a hole in the picture. He need
not have drilled a hole because a sundial would have had a
hole to support the gnom on. Sundials contained a series o f
etched lines converging on the gnom on, which may have
prompted the idea o f perspective. W h ere there was sky,
Brunelleschi could have simply left the polished surface o f
the mirror chac reflecced che real sky. Brunelleschi was a
friend o f che machcmatician Toscanclli, who used a large
sundial on checachedral in Florence со measure che alcicude
o f che sun ac noon. O n e problem wich paincing a piccure on
a mirror is chac che head o f chc paincer obscruccs che view o f

Plan P rojection plane

2 .30 . M asaccio's T rin ity fresco. T h is fresco was painted in the church
o t San ta M aria N ovella* F lo ren ce, in 14 2 5 . It is the oldest know n
Figure 2.29. Pcrspcccivc m eth od possibly used by B ru n d lc sc h i. (ЛЛлргсс! from p aintin g w ith a unified vanishing p o in t. (iW>:Gabnnctto Foto*r*£c<»<WL
Сдпсг 1970) SofMintcAilnwAxi Bciti Avthtici с Slonci, Kkucmc)
that ic has a unified vanishing point at eye level (Field et al.
1 9 8 9 ). It is believed to be the oldest known painting with a
perfect vanishing point. It has been suggested that
Brunelleschi drew the sketch for this painting, but the evi­
dence is not conclusive (ten Doesschatc 1964).
In 1 4 2 0 , G hiberti used inconsistent vanishing points
when constructing his first baptistery door. Two o f the
panels o f the Gates o f Paradise, made in the 1420s and
1430s, embody a central vanishing point (Parronchi 1964).
Strangely, the distance point o f one picture was the princi­
pal vanishing point of the other picture. The distance points
and vanishing points arc nor on the same horizon, as they
should be. O th er artists continued to use inconsistent van­
ish ingpoints well after 1420 ( К rauthcimcr and К rautheimer-
H ess 1982).
In 1435 L e o n B attista A lberti ( 1 4 0 4 - 1 4 7 2 ) wrote
D ellapittura . It was available only in manuscript form until
it was published in Basel in 1540. The book was the first
account ot the geometry o f drawing in perspective using a
single vanishing point. A lbertis father, Lorenzo, was a
banker who had been banished from Florence by a rival
banking family. Leon grew up in G enoa and Padua and in
1431 became architect to Pope Eugene IV. Between 1431
and 1434 he was in Rome, where he surveyed buildings and
composed Latin letters for the pope. There is no indication
that he saw ancient Roman murals drawn in perspective.
He traveled with the pope to northern Europe and in 1434
arrived in Florence just .us Brunelleschi was completing the
dom e o f the cathedral, Donatello was completing the sculp­
tured facade, and G h ib ertis doors were newly installed on
the baptistery. This so impressed Alberti that he devoted
himself to making the art ot Florence understandable to a
wide audience.
Betore the Renaissance, artists were tradesmen orga­
nized into guilds. Painting and sculpting were not part o f
the liberal arts, which included philosophy, grammar, dia­
lectic, mathematics, and astronomy. N or were they part o f
mechanical arts, which included architecture, navigation,
and medicine. This attitude toward artists probably origi­
nated in Rome, where artists were usually slaves. Also, Plato
had condemned painting because he argued that visual per­
ception is subject to errors, which are compounded in
painting. Plato respected only knowledge based on mathe­
matical certainty. Alberti and Renaissance artists saw per­
spective as a way to ground painting in mathematics and
thus elevate it to the level o f geometry and astronomy.
Paolo T oscan elli ( 1 3 7 9 - 1 4 8 2 ) was a physician and
leading mathematician. Architects and artists such as
Alberti, Brunelleschi, Donatello, Uccello and, later,
Verrocchio and his apprentice Leonardo da Vinci, gathered
at Toscanelli s home of on the banks o f the Arno. Leonardo
learned mathematics and many other things from him.
Brunelleschi and Leonardo da V in ci were also close triends
o f the Franciscan monk Luca P acioli ( 1 4 4 6 - 1 4 1 7 ) . He
too was a leading mathematician who taught Leonardo
da Vinci. He wrote the first treatise on double-entry
bookkeeping.
Like other humanists o f the Renaissance, Alberti was
fascinated with antiquity and read Greek and Roman
authors, including Galen, Euclid, Ptolemy, and Vitruvius.
He was aware o f the contributions o f Alhazen through the
writings o f Roger Bacon, Joh n Peckham, and Vitcllo. He
adopted the concept ol the visual pyramid and centric ray
from Galen and relied on Euclid’s theorem 21 to establish
that the size o f an image in the picture plane is inversely
proportional to the distance o f the object. He became inter­
ested in cartography and applied ideas from Ptolemy’s
Geographia to construct a map ot Rome. He used a grid
based on polar coordinates with th co rig in o n thcCapitoline
hill (Edgerton 1975).
Pre-Renaissance drawings in partial perspective did not
rely on the scholarly perspcctivist tradition ot geometrical
optics that included the works o f Euclid, Apollonius,
Ptolemy, Pappus, and Alhazen. Artists were probably illiter­
ate and, in any case, would n ot have had access to ancient
texts. Alberti did consult ancient texts, and his method
derives mainly from perspcctivist geometry rather than
from practical methods used by artisans. The geometrical
theory o f visual optics became known as perspectiva natu-
ralis because it dealt with the formation o f the natural
image in the eye. The geometry o f perspective drawing
became known as perspectiva artificial is. or perspectiva
practica.
The retina is spherical, but pictures are painted on flat
surfaces. This has led to the mistaken notion that a drawing
in accurate perspective does not produce the same image on
the eye as the 3 -D scene. Panotskv ( 1 9 4 0 ) wrote, “ Perspective
construction as practised in the Renaissance is, in fact, not
correct from a physiological or psychological point ot view.”
Bur in polar projection, the scene, the drawing, and the
retinal image o f the scene are projectivclv equivalent when
the picture is viewed from the same location as che eye o f
the painter. A picture drawn on a flat surface is not isomor­
phic with the image on the curved retina. However, a pic­
ture is n ot designed to be a copy ot the retinal image but
rather to send to the eye the same optical array as that cre­
ated by the scene (Pirenne 1952). The retinal image pro­
duced by a correctly drawn and viewed picture is isomorphic
with the image produced by the scene.
A picture in perfect perspective may appear distorted
relative to the original scene (Section 26.3 .4). But this is not
due to incorrect perspective but to other visual cues indicat­
ing that the picture is flat. W h en these cues are removed,
the distortions are no longer present.
In constructing drawings in perspective, Alberti proba­
bly used a small box with a peephole in the front surface.
The floor o f the box (the ground plane) was marked out as a
square grid. The tar end ot the box was the picture plane and
its base was the ground line. The groundline was marked o ff
into equal divisions, corresponding to where the grid lines
on the floor plane intersected the groundline. A vanishing
point, P, was placed at eye level on the midline o f the pic­
ture plane (Figure 2.31 A). Diverging lines were drawn from
the vanishing point to the points marked of! on the ground-
line. These lines indicated the images o f receding parallel
lines on the ground plane. The picture plane was then drawn
in side elevation as a vertical line. The eye (station point)
was drawn at the level o f che vanishing point ac a designaced
distance irom the picture plane (Figure 2 .3 1 B ). Visual lines
were drawn from rhe station poinc to each o f the equally
spaced cransverse lines on che ground plane. Horizontal
lines w'ere drawn on che piccure plane chrough che points
where the visual lines intersected the picture plane, as shown
in Figure 2 .3 1 C . The accuracy o f these transversals was
checked by drawing diagonal lines across the picture plane.
Each diagonal should incersecc opposite corners o f all the
squares chac ic craverses. Opposice diagonals incersecc che
horizon line in cwo discancc poincs. The distance between a
Eye point
Figure 2 .31. A lberti's (on slru ziotieleg iftim a. (A ) V an ish in g p o in t, P. is placed
o n the p ictu rc at cvc level. D iverging lin es, rep resenting the im ages ot
reced in g parallel lines, arc drawn to th e base o f th e pictu re.
(B ) In tersectio n s o f visual lines to equally spaced transversals o n the
grou nd plane arc p lo tted on the side o f the pictu rc plane.
( C ) T h e spacing o f the im ages o f transversals is ch ecked by draw ing a
d iag onal across the p ictu rc plane.
distance point and chc central vanishing point equals chc
discance becween che painter’s eye and the picture (see
Section 26.1.2 ). However, Alberti made no reference to dis­
cance points and was thus ignorant o f or discarded the
methods used by 14th-century painters. Alberti’s method
was known as the co n stru z io n e legittima.
Alberti also described drawing in perspective using a
glass plate or a lattice o f orthogonal threads suspended on a
vertical frame, a method that became known as Leonardos
window (see Section 2.9.4). In general, Alberti represented
a picture as a section ot the cone ot vision.
The notion o f a divine basis for geometry echoed down
the centuries and inspired Luca Pacioli to write his D ivina
proportione in 1509. In chis book he applied geomecry со
archiceccurc, che arcs, che divine proportions ot che Placonic
solids, and chc human body. The Placonic solids are che tct-
rahedron, cube, occahcdron, dodecahedron, and icosahe­
dron. They are che only regular polyhedra. Placo had
identified che regular solids wich che tour elemencs and che
universe. After Placo, Pacioli identified che five regular
solids wich che four elemencs o f carch, wacer, air, and fire,
plus chc cosmos. He also praised linear perspective.
Leonardo da V inci drew che diagrams for che book, one ot
which is shown in Figure 2.32.
Paolo U ccello ( 1 3 9 6 - 1 4 7 5 ) was an enchusiascic expo-
ncnc o f perspective. Piero della Francesca ( 1 4 1 4 - 1 4 9 2 )
wroce De Prospective Pingendi, which circulated only in
manuscript form during che Renaissance (sec Field 1986).
Daniele Barbaro ( 1 5 1 3 - 1 5 7 0 ) , chronicler ot the Venetian
Republic, included large parts ot Pieros treatise in his L a
practica della perspettiva o f 1569.
In 1509 Jean Pclcrin (pseudonym V iator) (с. 1 4 4 5 —
1 5 24 ) wrote D e Artificial! Perspectiva. V iator was not an
Figure 2 .32. D raw ing in perspective by L eon ard o d a 17nei. Thi s draw ing o f
a cruncatcd d od ccah cd ro n was produced fo r Luca P acio lis D iv in a
P ro p o rtio n ? o t 1 5 0 9 .
 Лиса pinM sM ft
r«gufc2.J3. D iagraw illustrating distan ce points. L im a te r r e a is the ground
Iinc,//>/*v* ftin im id tilis is the horizon lin e. T h e diagonals (Лил*
d y a m c tr a lis) end in the d istan ce p oin ts o n th e h orizon lin e. (Fr**» Vi*.**
/><AfdJidjIi of 1W)
artist but secretary to I.ouis X I o f France and, later, a canon
4
ot the Benedictine abbey at Toul. His was the first book on
perspective in northern F.uropc and the first anywhere to
contain illustrations ot scenes in perspective. It contained
the first account o f distance points (see Figure 2.33).
However, we saw in the last section that distance points
were used by painters in the 14th century. V ia to rs book is
reproduced in Ivins (1 9 7 3 ).
L e o n a rd o da V inci used the construzione legittim a until
about 1500. He then becamc dissatisfied with it because it
took no account o f the curvature o f the eye or o f move­
ments o f objects and o f the eye. He was frustrated by the
fact that a flat picturc never looks as solid as the real object,
unless one views the o b ject with one eye. He explained that
the impression o f depth with two eyes arises bccausc each
eye seesdillerent parts ot a surface placed beyond an object
(see Strong 1979, p. 3 8 5 ) . He was thus aware that what wc
now call monocular occlusion can create an impression o f
depth (see Section 17.3). He did n ot describe any other
kind o f binocular disparity.
He was frustrated by his inability to represent in a draw­
ing the full effect o f depth that is achieved by binocular
vision (Wade e t al. 2 0 0 1 ) . In his later drawings da Vinci
con fined himself to portraying objects in isolation rather
than in architectural settings. He represented motion in the
form o f waves, whirlpools, birds in flight, the human figure
in action, and the effects o f eye movements on the appear­
ance o f things (Strong 1979, p. 3 9 2 ) . He would have been
delighted to sec a stereogram or stereoscopic movie.
A lb rech t D iirer ( 1 4 7 1 - 1 5 7 8 ) o f Nuremberg learned
about perspective during a visit to Bologna in 1506, proba­
bly from Luca Pacioli, a mathematician and associate o f
Alberti. After the meeting he became enthralled by geome­
try and bought a copy o f Euclid’s Elements. He had access to
the manuscript o f De Prospective Pingendi by Piero della
Francesca, and to the manuscript version o f Alberti’s Della
pittura. But V ia to rs D e A rtificiali Perspectiva had the great­
est ctfcct; soon after it appeared, the perspective in Diirer s
drawings and prints became more precise. Also, some o f
D iirer’s drawings resemble those in the first edition o f
Viator. In the second edition o f his book, Viator
reciprocated by using some ot Diirer s drawings (Strauss
1977).
In 1525 Diirer published Unterxveisung der Messung
{Instruction o f M easurement), which remained the standard
German work on perspective for some time. It is divided
into four books. The first deals with lines, curves, and spi­
rals. He described a procedure for obtaining conic sections,
based on Apollonius’s treatise. However, he mistakenly
drew the elliptical conic section as an egg shape. The second
book deals with polygons and the third with solid pyramids,
cylinders,architectural structures, and astronomical instru­
ments. The final book deals with polyhedra and the analysis
o f perspective. His interest in polyhedra no doubt derived
from his reading ot Paciolis Divina proportione with its
illustrations by Leonardo da Vinci. Diirer developed his
own method ot perspective, which he called naberer Weg
{Shorter way). This was A lberti’s construzione legittim a but
with the station point moved to the projection plane. This
change revealed that Diirer had an imperfect understand­
ing ot the geometry and it introduced distortions into
D iirers paintings (see Carter 1970; Ivins 1973). Panofsky
(1 9 7 1 ) has written a biography o f Diirer.
During the 16th century aseriesof authors in Nuremberg
produced books on perspective. The best known is Wenzel
Jam nitzer’s Perspectiva C.orporium Regularium o f 1567,
which contains perspective drawings o f polyhedra but with
no instructions about how to produce them.
Ja n Vredeman d e Vries ( 1 5 2 7 - 1 6 0 4 ) was a D u tch
architect and painter who worked in Antwerp, Danzig, and
at the court o f Rudolph II in Prague. He wrote illustrated
pattern books for apprentice architects and engravers. In
1604 he published Perspective, which became the leading
book on perspective in Holland. The book was reprinted by
Dover in 1968. It contains only illustrations, one o f which
is shown in Figure 2.34. In 1616, the D utch mathematician,
Marolois, produced a book that contained a geometrical
analysis o f perspective. This became the standard text on
perspective for Dutch artists.
G u id o b a ld o del M on te, (15 4 5 -1 6 0 7 ) published
Perspectivae L ibri Sex in Pcsaro, Italy, in 1600. This was one
o f the leading texts o f the time. He pointed out that per­
spective is not affected by rotation o f theeye (see Frangenbcrg
1986). A ndrea Pozzo ( 1 6 4 2 - 1 7 0 9 ) , clergyman, painter,
and architect, wrote Perspectiva Pictorwn et Architectorum
in 1693. An English translation appeared in 1707, which
was reproduced by Dover in 1971. The English mathemati­
cian Brooke Taylor ( 1 6 8 5 - 1 7 3 1 ) , wrote New Principles o f
L in ear Perspective in 1715. This was the first geometrical
analysis o f perspective written in English.
In o n c -p o in t perspective, all receding lines in the scene
(lines not parallel to the picture plane) are parallel to each
other and therefore project to the same vanishing point, as
shown in Figure 2 .3 5 A . In a one-point perspective paint­
ing, objects arc usually rectilinear and orthogonal to the
Figure 2 . v»- .In error in th e u se o f ‘t hree-poin t perspective. 71i с box m arked “ Г ’ is in clin ed to the h o rizo n tal. V anishing p o in t P 1 should th erefo re b e above
the h orizon line. V anishing p o in t P 2 is c o rre ct sin ce the co rresp on d in g sides o f o b je c t 2 arc b oth h o rizo n tal.
frontal plane. In tw o -p o in t perspective, all receding lines
in the scene lie in parallel planes but are not all parallel to
each other within those planes. The vanishing points for
different sets o f parallel lines lie on the same horizon line. In
a typical tw o-point perspective painting, all objects sit on
horizontal or vertical surfaces but some are slanted about a
vertical axis, as in Figure 2 .3 5 B . In th re e -p o in t p ersp ec­
tive, not all receding lines in the scene lie in parallel planes.
The vanishing points for different sets of parallel lines do
not lie on a single horizon line. Som e objects are both
slanted and inclined, as in Figure 2 .3 5 C . The vanishing
points of inclined objects lie above or below the horizon
(Section 2 6 .3 .2 ). Brunelleschi s first painting involved two-
point perspective because the baptistery sits on a horizontal
surface but is not rectangular.
In his book on perspective, Viator drew objects at vari­
ous angles but always on horizontal surfaces. H e therefore
used only one- and tw o-point perspective.
De Vries drew a few inclined objects in his textbook but
incorrectly placed the vanishing points on the principal
horizon line. For example, in Figure 2 .3 4 , the box marked 1
is clearly not horizontal, but one o f its vanishing points is
incorrectly placed on the horizon. The vanishing point
would be correct only if the box were tapered in the direc­
tion o f inclination. But de Vries probably did n ot intend to
draw a tapered block, since all the other objects in the pic­
ture are rectangular. It is evident that Viator did not under­
stand three-point perspective. There is a passage in Piero
della Francesca’s D e Prospectiva Pingendi describing three-
point perspective in the drawing o f a cube placed on one o f
its corners (Elkins 1988). M ost painters during and after
{F ro m . I c V n . , ! « > ♦ )
the Renaissance avoided problems o f three-point perspec­
tive by n ot drawing inclined objects.
In the 15 ch century, manuals o f perspective drawings o f
architecture and machinery began to circulate in Italy
(Ferguson 1977; Edgcrton 1991, Chapter 4 ). O n e o f the
most influential was an unpublished but widely circulated
illustrated manual Trattato d i arcbitettura written about
1475 by Francescodi G iorgio M artini. O n e o f the surviving
copies contains margin notes by Leonardo da Vinci. Thus,
the tradition o f recording and transmitting technical infor­
mation by perspective drawings was well established by the
15th century, when Leonardo da Vinci began filling his
notebooks with technical drawings.
In the 16th century, technical manuals o f industrial and
military machines drawn in perspective appeared through­
out Europe. In 1556 Georgius Agricola published De Re
Metallica> the classic record of mining machinery (F.nglish
translation,Dover 1950). In 157 8 Jacques Besson published
Theatre des instruments w atbew atiques et mtfebaniques in
Lyon. In 1588 Agostino Ramelli published L e diverse et
artifieiose m achine in Paris. It contains hundreds of techni­
cal drawings, many o f novel machines. Figure 2 .3 6 shows
one o f Ramelli s drawings. O th er drawings from this period
arc reproduced in F.dgerton (1 9 9 1 ).
D enis Diderot, one o f the Encyclopedists o f 18th-cen­
tury France, produced hundreds o f drawings in perspective
in his Pictorial Encyclopedia o f Trades an d Industry (English
translation, Dover 1987).
The mathematics o f perspective had its origins in
Mcnacchmus, Euclid, and Apollonius in the 3rd and 4th
centuries B C and in Pappus o f Alexandria in the 3rd
 А В
Figure 2. >5. Oner-, tw o-, a n d three-poin t perspective. C u b e on a h orizon tal surface w ith a face parallel to th e p ictu rc plane has a single v an ish in g p o in t, P I .
C u b e on a surface a t an angle to picture plane has tw o vanishing p oin ts. P2 and P 3 . on the h o rizo n . C u b e n o t lying o n a h orizon tal surface has three
vanish in g p oin ts, P 4 , P 5 , P 6 , n o n e o f w h ich arc on the h orizon .
Figure 2 . ve. A n early m ech an ical draw ing in perspective. Frumname*•!№*»</
uro fi.Jbit ГЛati'Jnc o f I SH8.
ccncury A D . These early approaches to perspective centered
on the conic sections— the projections o f a circle o n to a
plane (Section 3.7.2c). Further developments in the math­
ematics o f linear pcrspcctivc had to wait 1,400 years.
Modern projective geometry was developed by the French
' . ‘С
• 11
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»I»
■|»
v
«и
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mathematicians Girard Desargues ( 1 5 9 3 - 1 6 6 2 ) , Blaise
Pascal ( 1 6 2 3 - 1 6 6 2 ) , and J. V. Poncelet ( 1 7 8 8 - 1 8 6 7 ) . In
che 19ch cencurvФ came che German mathematicians Von
Staudt and Felix Klein (see Coolidge 1968).
For accounts o f the development o f perspective in arc
see W hice ( 1 9 6 7 ), Pirenne ( 1 9 7 0 ), Edgercon (1 9 7 5 ),
Descargues ( 1 9 7 7 ), Bartschi ( 1 9 8 1 ), W right ( 1 9 8 3 ),
Kubovy ( 1 9 8 6 ) , and Kemp ( 1 9 9 0 ). Perspective is discussed
more cxcensivcly in Chapccr 26.
2 .9 .4 D E V I C E S F O R D R A W I N G IN
P E R S P E C T IV E
Many artists used projection devices racher chan geometri­
cal constructions со draw in perspective. Albcrci described a
picture as a “window through which we look out inco a sec­
tion o f chc visible world.” In his Treatise on Painting
Leonardo da V inci described in detail a device for painting
in pcrspcctivc, which became known as Leonardo’s window.
The drawing was first made from a fixed vantage poinc on a
vertical plate o l glass and later transferred со canvas. The
device is illustrated in one o f D u rers woodcuts shown in
Figure 2 .3 7 A . Leonardo wrote,
Perspective is nothing but seeing an object behind a
sheec o f sm ooth transparent glass, on che surface o f
which everything behind the glass may be drawn;
these things approach the point o f chc eye in pyra­
mids; and chese pyramids cut che said glass.
(see К E EL E W 5 A
In a variant o f Leonardos window che arcist viewed chc
scene chrough a grid o f chreads and transferred what was
 А
Fifwc2.3,7. T w o types o t L eon ard o S window , bom Abiccfct Direr. Untt,w«inmEJet Мсшш,(Nurembiig, 11 W)
seen in each square to a corresponding square drawn on the
canvas, as shown in Figure 2 .3 7 B . In the 17th century,
Andrea Pozzo drew structures and figures in perspective on
the curved ceiling o f the church o f St. Ignazio in Rome. He
placed a horizontal grid below the ceiling, which corre­
sponded to a grid on a small version o f the painting.
He then stretched a tight thread from a fixed point on the
ground through each corner o f the grid to a point on the
curved ceiling (see Pirenne 1970).
Before the invention o f photography many artists used a
camera obscura, in which the scene to be painted is pro­
jected o n to the canvas through a lens. Giovanni della Porta
(Section 2.5.1) seems to have been the first to describe the
camera obscura for drawing. He wrote in his Nattiriae
N aturalis (1 5 5 8 ),
If you cannot paint, you can by this arrangement
draw with a pencil. This is done by reflecting the
image downward o n to a drawing board with paper.
For a person who is skilful, this is a very easy
matter.
Artists tended to be secretive about their use o f artificial
devices, presumably because they wished it to be thought
that they painted by pure skill. For example, Bernardo
Bellotto ( 1 7 2 1 - 1 7 9 0 ) , known as C analetto, concealed his
use o f the camera obscura. Philip Steadman ( 2 0 0 1 ) has
demonstrated that Jan Vermeer o f Delft ( 1 6 3 2 - 1 6 7 2 ) may
have used a camera obscura to paint his photograph-like
D u tch interiors. Hockney ( 2 0 0 6 ) has claimed that many
artists after the 15th century used optical instruments, but
some art historians reject his arguments. Som e early instru­
ments are shown in Figure 2.38. In about 1567 Robert
Hoyle made a camera obscura with a lens on an extending
hood and an opening in the top for drawing landscapes, like
that shown in Figure 2 .3 8 B . In the instrument depicted in
Figure 2 .3 8 C , the artist sits in a cabinet and traces the image
o f the scene reflected by a mirror on top o f the cabinet.
Pictures drawn with these instruments were limited by the
size o f the drawing surface and by the angle o f view o f the
lens (W right 1983). See Ham m ond ( 1 9 8 1 ) lor a history ot
the camera obscura.
In 1806, the English scientist W illiam Wollaston
( 1 7 6 6 - 1 8 2 8 ) patented thccameralucida. In a “sec through”
camera lucida the artist sees the scene through two reflect­
ing mirrors that produce an erect image. O n e o f the mirrors
is semitransparent so that the artist can see the scene super­
imposed on the drawing paper. In the “split pupil” camera
lucida the artist uses part o f the field o f view to see the scene
through mirrors or prisms and the other part to see the
drawing paper. A camera lucida is more com pact than a
camera obscura. Versions ot the camera lucida tor use on

А sented in the device used by Brunelleschi to display his first
f.riiic 2 .м . E xam ples o f th e cam era obscura. (A ) C am era ob scu ra m ade by
Jo h a n n Z a h n in 1 6 8 5 - T b e im age reflects o n to th in paper placed on
a plate o f glass. ( B ) A n 1 8 th -cen tu ry cam era ob scu ra. ( C ) A n 18th-
cen tu ry French cam era obscu ra. A rotatable m irro r on to p reflected the
im age throu gh a lens o n to the draw ing surface at D . A lig h t trap under
the sca t provided v en tilatio n . The apparatus could be carried on poles
like a sedan chair. (FromWight iss*)
microscopes still appear in the catalogs o f optical instru­
ment makers. Sec Hammond ( 1 9 8 7 ) for a history o f the
camera lucida.
W ith the invention o f photographic film, the camera
obscura developed into the camera. Artists could then paint
from a photograph, which is an image in a camera obscura
captured on film.
2 . 9 .5 T R O M P U L 'O E IL AN D
A N A M O R P H IC ART
Renaissance artists were preoccupied with representing 3-D
scenes on a Bat surface. In the tradition ot painting known
as tro m p c I’o cil (tool the eye), the artist paints in perspec­
tive with the aim o f convincing viewers that they are look­
ing at a real 3 -D o b jcct or scene. The tradition goes back to
Roman times, when wall frescoes were designed to create
the impression o f a large room or garden. It is also repre­
painting in perspective. Renaissance artists painted objects
in perspective on walls, ceilings, and doors in great detail
and the same size as the real objects. They placed them
where one would expect to see real objects, such as cabinets
lull ot curiosities or rare books, and windows with outside
views. An example, executed in marquetry, is shown in
Figure 2.39.
Artists usually draw on a surface in a frontal plane.
A drawing in perspective creates the correct image in the
eye only when the eye is at the correct vantage point and the
picture is orthogonal to the line o f sight to the principal
vanishing point. A picture drawn on a canvas slanted about
a vertical axis produces the correct image only when viewed
with the picture at the same angle to the principal line o f
sight. Viewed frontally, the picture may appear a jumble ot
lines. This simple principle gave rise to the tradition o fa n a -
m orp hic a r t, which flourished in the 16th and 17th centu­
ries. Figure 2 .4 0 shows one o f the earliest anamorphic
pictures, entitled Vexicrbild (puzzle picture). It is a wood
engraving produced in about 1 5 3 2 by Erhard Schon, a pupil
o f Diirer. An anamorphic portrait o f Edward V I, painted in
1546, hangs in the National Portrait Gallery in London.
Hans H olbein s IheA m bassadors ,painted in 1 5 3 3 ,contains
an anamorphic skull. The scene was drawn on a frontal
canvas and then transferred point-by-point o n to a canvas at
a steep angle to the picturc.
In cylindrical anamorphic art, the picture is drawn so
that it appears in its true form only when viewed through a
vertical cylindrical mirror placed on the center o f the pic­
ture, as shown in Figure 2.41. Many ot these pictures
depicted erotic scenes.
A nother type ot anamorphic art involved painting the
interior surfaces o f a box with tapering sides. W h en viewed
through a peephole the interior ot the box appears as a rect­
angular furnished room. The first box o f this kind seems to
have been built by one o f Rem brandts pupils, Carel
Fabritius o f Del ft ( l 6 2 2 - 1 6 5 4 ) . O n e o f his boxes is in the
National Museum in Copenhagen (Hulten 1952). The box
is triangular but appears as a rectangular furnished room
when viewed through a peephole.
Figure 2 .4 2 shows the plan o f a viewing box constructed
by another pupil o f Rembrandt, Samuel van Hoogstraten
( 1 6 2 7 - 1 6 7 8 ) (van de G eer and de Natris 1962). The
four surfaces fold to form a triangular room, which appears
F«*mc2.3*. 7rom p el'otik A n exam ple o f crom pc lo e il a r t by D o m e n ic o R osselli in the study o f che D u cal Palace o f U rb in o , 1 4 7 6 . T h e cab in ets and
cheir co n ten ts arc p ainted . (РЬоеодоЬ Ь>Alm*t GiruuU,» 1>ш.neb,IS9t)

Figure 2.40. .In am orpbtc art. P o rtra its o f C h arles V, Ferdinand I. Pope Paul 111, and Francis I em erge when the picture is viewed obliqu ely from the
Side, {lijdfrli&iby bkaiJ Sckun,«. 15 !2)

Figure 2. 11. A n am orphic m irror art. P o rtra it o f C h arles 1» с. 16 4 9 . In
G rip sh o lm C a stle, Sw eden.
Figure 2.42. 17th-<entury d istorted room . T h e tour panels fold in to a
triangu lar b o x . W h e n viewed from the co rre ct p oin t o n the op en side,
th e room appears rectan gu lar and in c o rre ct perspective. The box was
painted by Sam u el van H o o g straatcn ( 1 6 2 7 - 1 6 7 S ). (In th e M u n icip al
M useum o f ’I he H ague)
rectangular when viewed from the correct point.
Hoogstraten traveled to Rome and Vienna, where he was
patronized by the emperor. He visited London in 1 6 6 6 , the
year o f the G reat Fire, and finally settled in his native town
o f Dordrecht. An elegant viewing box that he constructed
at about that time is in the National Gallery in London.
This box portrays a series ot connected rooms and has two
viewing holes through which two interior scenes can be
seen. Another box, probably by Hoogstraten, is in the
Detroit Institute o f Arts (Hulten 1952). In his manual on
the art o f painting entitled Inleyding tot de Hooge Schoole
der Schilderkom r Hoogstraten wrote,
B u t I say that a painter whose work it is to fool the
sense o f sight, also must have so much understand-
in g o t the nature o f things that he thoroughly under­
stands by what means the eyes are tooled, (p. 24).
The Ames distorted room described in Section 26.2.2 is
an anamorphic structure built for scientific purposes in
1935.
In 17th-century Italy, the principle o f anamorphic art
was developed on an architectural scale. For example, the
famous ceiling in the church o fS t. Ignazio in Rome, painted
by Andrea Pozzo, creates a compelling impression ot 3-D
columns with a multitude of human figures when the viewer
looks up while standing on a spot marked on the lloor
below. The painting is actually on the curved surface o t the
ceiling. The Palazzo Spada in Rome contains a real arcade
with misleading perspective, which looks elongated when
viewed from one end and shortened when viewed from the
other end. The Piazza del Campidoglio in Rome was co n ­
structed to enhance the sense o f distance and size. The
ancient Greeks evidently used the same principles to design
stage sets (Section 2.9.1). Stage designers and artists still use
these principles (see Wade and Hughes 1999).
The history o f anamorphic art is discussed and exten­
sively illustrated in books by Pirenne ( 1 9 7 0 ) , Mastai (1 9 7 6 ),
Baltrusaitis ( 1 9 7 7 ) , Lecman ( 1 9 7 6 ) , and Kemp (1 9 9 0 ).
2 .1 0 B IN O C U L A R V IS IO N
Since ancient times, artists have struggled with the problem
o f how to represent 3-D space in a picture. This preoccupa­
tion with 2-D pictorial space led to an emphasis on m o n ­
ocular cues to distance and away from binocular cues. Euclid
knew that the two eyes have different views o f 3 - D objects,
and Aristotle noted that one sees double images when a
finger presses against one eye (Section 2.1.2). But the prob­
lem raised in peoples’ minds was how we torm an impres­
sion o f a single visual world, despite these differences
between the two images. The binocular disparities and
double images were regarded as something to be overcome
rather than made use of.
 Ic is amazing that the simple facts about binocular ste­
reoscopic vision were n ot appreciated until about 170 years
ago. O n e reason for this ignorance is that, even with one eye
closed, a rich variety o f monocular information is available
for coding depth. Thus, the importance o f binocular stere-
opsis is not apparent with casual observation o f everyday
scenes.
2 .1 0 .1 P T O L E M Y ON B IN O C U L A R V ISIO N
In the 2nd century A D Ptolemy wrote a five-volume work
in G reek, entitled Optics. Parts o f Books 11 and 111 deal with
binocular vision. The following quotations are from an
English translation o f these parts prepared by Dr. Fiona
Somerset o f O xford University. The full translation is in
Howard and Wade ( 1 9 9 6 ). These sections are quoted at
some length, since this is the earliest known account o t the
basic geometry o f binocular vision. Apart from a brief
review by C ron e ( 1 9 9 2 ) , it does not seem to have been cited
in the vision literature. The section and figure numbers
correspond to those in Lejcunes French translation (1 9 5 6 ).
The first sections com e from Book II.
27] An o b ject appears in one location when seen
with only one eye, but when seen with both eyes an
o b ject is seen in one location only i f it falls on con-
similar radii, namely those that have corresponding
positions with respect to the visual axes. And that
comes about when the visual axes converge on the
object to be seen, which happens when we see things
with a simple gaze and in the way which is natural
when we inspect an objcct.
C'onsimilar radii are now known as corresponding
visual lines. The modern term will be used in the remaining
quotations.
28] It seems too that nature sets up double vision so
that we will look more and so that our viewing will
be ordered and brought to a definite position. It is
natural for us to turn our gaze toward diverse loca­
tions, our gaze shifts without our conscious etfort
with a marvellous and diligent turning m otion, until
both visual axes intersect on the center o f the object
wc wish to see, and other pairs o f corresponding
visual lines within the two visual pyramids are also
brought into coincidence.
Here Ptolemy suggests that we have two eyes and double-
vision so that we will actively bring the visual axes o n to rhe
object ot interest. There is no suggestion that binocular
vision has anything to do with depth perception.
33) L et A be the left eye and В the right eye
[Figure 2.43a]. Place two rods G and D on the
perpendicular to A B. Extend to them from each eye
the visual lines GA, g b, da, d b. Let the eyes be co n ­
verged on the nearest rod G.
34] A G and B G fall on the visual axes. O f the
remaining two visual lines, A D is to the left o f
the visual axis o f the left eye and В D is to the right o f
the visual axis o f the right eye. Thus G is seen in one
location, because the two visual axes are correspond­
ing visual lines; but D appears double sincc visual
line A D is ro the left o f the visual axis o f the left eye,
but visual line B D is to the right o f the visual axis o f
the right eye. Therefore when we cover the left eye,
the left image will n ot be seen; and when we cover
the right eye, the right image will nor be seen.
35] If the eyes converge on D, it will com e about
in the opposite way. Because A D and B D are on the
visual axes D will be seen as one. G will appear
double because AG is to the right o f the visual axis
o f the left eye, and B G is to the left o f the visual axis
o f the right eye. I f we cover the left eye, the image
which appears on the right on visual line A G will
not be seen, and i f we cover the right eye, the image
which appears on the left on visual line B G will not
be seen.
These sections describe the essentials o f binocular dis­
parity and the ditfcrence between what we now refer to as
crossed images produced by objects nearer than the conver­
gence point and uncrossed images produced by objects
beyond that point.
36] If the visual axes are parallel so that they do not
converge on either rod [F ig u re2.43b] both rods will
be seen double according to the principles we have
presented.
37] To demonstrate this clearly the near rod at L
should be painted white and the far rod at M black.
Therefore objects at I. and M will both be seen in
two positions to the sides o f their actual positions.
Therefore if we cover the left eye, the images which
are on the right side will not be seen; but if we cover
the right eye, the images on the left side will n ot be
seen. Visual line A L will be more toward the right
than line A M , and line BI. more toward the left than
line B M . In this way the images on the right will be
seen through the left eye, and those on the left by the
right eye.
38] Again place the visual axes parallel and place
the white rod on the visual axis o f the left eve and4
the black rod on the visual axis o f the right eye
[Figure 2.43c]. The distance between the rods is the
same as that between the eyes. The two rods will be
seen as three.
39] Through the corresponding visual lines, each
rod will be seen as one, although neither ot them
 E D Z

A В
(a) Eyes a t A and В converge on G , then on D. O bjects at G and D.

(f) E yes conve rg e on D. O bjects placed at H. Т. К

А В
(b) V isu al a xes parallel. O bjects L and M a re on the m idline.

(g) E yes conve rg e on D. O bjects placed at H,T. К

A В

(с) O bjects L and M are o n the parallel visual axes.

A G В

(h) E yes conve rg e on D. O bjects К and H a pp e ar a t M and S.

(d) O bjects L and M are outside the parallel visual axes.

(e) O bjects L and M are inside the parallel visual axes. (i) Eyes converge on E. Lines a lo ng GD. A Z. BH. and TK.

ttgurc 2 . i.v D iagram s fro m P toU m /s O ptics. In ca ch figure the eyes arc a t p o in ts A and B. Bold lines in dicate the visual axes, and bold letters in dicate the
physical lo cation s o f vertical rods or sm all o b jects.
 falls on both visu.il axes because chc rods arc placed
side by side. But through the noncorresponding
visual lines Л М and B L , che child, middle image will
be seen, composed ot an image ol the white rod trom
chc right eye and an image o f chc black rod from chc
left eye. I f we cover the right eye, the image o f
the black rod to the righc side ot che middle and the
whice image o f che middle composice image will noc
be seen. It wc cover che left eye, che image o f the
whice rod on che left and che black image o f che
composice middle image will n ot be seen.
40] For when we have joined chc noncorrespond-
ing visual lines A M and BL , boch rods will be seen in
one posicion, namely chac on which chc cwo colors
com e cogcchcr; buc as concerns che remaining cwo
visual lines falling on Г. and M , chrough che righc o f
chem will be seen che black rod, and chrough che
left che whice. Therefore when wc cover che righc
eye, che black rod on che righc and che whice pare o f
che central composice image will noc be seen; and
when we cover chc left eye, che whice rod on che left
and chc black pare o f chc cencral composice image
are not seen. And this is demonstrated by the figure
Figure 2.43c].
Ptolemy was confused here, alchough chc confusion
may have been introduced in che translation from the Greek
o r from the Arabic. Ic is chc images projccccd by che corrc-
sponding visual axes (.-//. and BM) chac fuse inco a com pos­
ice image on che cyclopean axis. Peolcmy incorreccly formed
rhe midline composite image from che images projected by
visual lines A M and BL. Ic is clear from Scccions 2 8 and 35
o f Book 111 chac he was well aware chat objects anywhere on
the visual axes are seen as one in the midline. The image ot
the black rod projected by AM is seen well со chc right
and the image o f the whice rod projccccd by B L is seen well
со che left. He may have been misled by his diagram in which
visual lines A M and BL incersecc. His dcscripcion o f which
images disappear w'hen one eye is closed is also in error. The
images would have disappeared in chc way he described it he
had inadverccndy converged racher diverged.
41 ] W h e n chc discance bee ween chc rods is noc equal
со chat bccween che eyes, cwo rods will be seen in
four locarions.
42] I f chc discance bccween I. and M is grcaccr
chan chac bccwccn chc eyes [Figure 2.43d] and chc
rods arc outside che visual axes, chc black rod will be
seen in cwo posicions on che righc, since A M and
BM are both to rhe right o f rhe visual axes, and the
white rod will be seen in cwo posicions on chc left,
since A L and BL are со che left o f the visual axes.
Thcretorc when wc cover chc left eye, che image o f
che black rod on visual line AM and the image
o f chc whice rod on visual line A L will noc be seen.
W h en wc cover chc righc eye, chc image o f chc whice
rod on visual line BL. and the image o f the black rod
on visual line B M will noc be seen.
4 3 ] I f che discance between L and M is less than
chac bccwccn chc eyes [Figure 2 .4 3 c], chc visual axes
arc со chc sides o f L and M.
4 5 ] These phenomena occur only by vircuc o f chc
horizontal separation o f the eyes since the height
and depth o f chc eyes are che same. Boch visual axes
curn unci! chev converge on chc chingto be seen. The
eves can converge horizontally со ditfcrcnc posi­
cions; buc they do n ot change their vertical angle o f
vcrgence, since one ot the eyes is not placed higher
chan chc other.
Ptolemy goes on to discuss si/.c constancy, and returns
со binocular vision in Book III.
26] Lee us speak firsc abouc chac construction in
which chc heads o f chc cwo visual pyramids (che
eyes) arc poincs A and В join ed by line A B and
divided ac chc middle ac poinc G [Figure 2 .4 3 f ] .
Produce trom this middle point a pcrpcndicular
G D and let the visual axes A D and B D converge on
an object ac poinc D. Under these conditions object
D is seen as one and in icscorrecr locacion.
27] I f through poinc D wc draw a line E D Z ac
righc angles со G D , anyching posicioned on chac
line, since ic is ac chc head o f (in the same frontal
plane as) point I) , will appear as one and in its
correct location.
Ptolemy claims incorreccly chac the locus ofsingle vision,
what wc now call chc horopcer, is rhe froncal plane chrough
chc fixacion point. Theoretically, it is a circle chrough the
eyes and chc fixacion point. However, as Tyler ( 1 9 9 7 )
pointed out, the difference between these loci is small
tor small angles ot eccentricity and, in any case, the
empirical horopccr is flaccer chan chc cheorecical horopcer
(Seccion 14.6).
28] W h e n che line Н Т К is produced parallel to
E D Z , and che eyes are converged on poinc D , an
objecc ac poinc T will be seen in two locations H and
K. Moreover, cwo objects positioned in H and К
will be seen in three locations,T, L ,a n d M. They will
both appear superimposed at poinc T as if chcy were
one thing. In addition, they will appear separately,
H at point L and К at point M . Any object on LT
and T M will be seen in the same manner on H K.
Here Ptolcmv asserts that an object on the midline
nearer than the fixation point appears diplopic, with a sepa­
ration equal to the disrance between the visual axes. O bjects
on the two visual axes, with symmetrical convergence, arc
seen as a fused pair in the midline and as monocular images
separated by twice the distance between the visual axes.
These ideas express the fundamental principles ofcyclopean
visual direction, which arc usually credited to Hcring
( 1 8 6 5 ) or Wells ( 1 7 9 2 ) (Section 16.7).
29] If we converge on point T we will see D at points
E and Z.
3 0 This may be confirmed by someone using a
board on which two rods are placed. W hoever wants
truly to recognize their locations may discern them
by placing a finger on the thing to be seen. For his
finger will land upon the object when it appears in
its correct location. W h e n the o b ject does not
appear in its correct location, his finger will not land
upon i t ___
3 1 . Those objects seen by corresponding visual
lines, even if there arc two o f them, arc seen as if in
one position; but it n o t by corresponding visual
lines, even if there is only one it will be seen as if it
were in two locations.
3 2 I f we join lines л е , a z , z b , е в , t a , t b , b h , a k
[Figure 2.43g] any o f E , D. and Z will appear in one
location, since A D and HD arc the visual axes, and
the visual lines which converge on E and Z are cor­
responding visual lines because AF. corresponds to
B E and A Z corresponds to B Z . But H and К will
appear in one location T , since A H and В К are visual
axes. Because BH and A К are noncorresponding
visual lines, H and К will appear at points I. and M.
Because visual lines AT and В Т are noncorrespond­
ing, point T will appear in locations H and K.
Here, Ptolemy restates that objects tailing on corre­
sponding visual lines arc seen as one. However, he is nor
correct in stating that points E and Z fail on corresponding
visual lines. To do so, they would have to fall on the locus o f
equal binocular subtense, which is a circle (the Victh-Mtiller
circle) passing through the eyes.
3 4 ] If the line Н Т К (Figure 2.43h ] is not parallel to
line A B but instead A H is greater than B K ; and the
visual axes converge on point D , things placed on
points К and H will appear on line G D , on either
side o f point T. Hut К will appear nearer than H
because the line H K is inclined to the plane AB on
which the eyes are positioned. Then H will be seen
at M , and К at S. Points H and К are such that per­
pendiculars from line G D from points M and S fall
on points H and K.
This rule about perpendiculars is somewhat arbitrary.
M ore accurately, an object on a visual axis and its apparent
location on the cyciopean axis lie on an arc centered on the
poinc o f convergence.
351 It is fitting that nature should equalize the dis­
tance between the two visual axes, and gather them
in accordance with the position o f the thing to be
seen. Therefore the visual axes are seen as tailing on
the line through the midpoint between them and
the point where the axes converge. This line is equi­
distant from the two visual axes and the two visual
axes appear to coincide with it. O b jects on the two
visual axes arc in different directions since the visual
axes are inclined to each other. The only way they
can be seen as one is it they are both seen as lying on
an axis midway between them. And that middle axis
should rightfully be called the com m on axis.
Here Ptolemy explains the need to com bine the distinct
m onocular headcentric visual directions into one. Ptolemy
called the axis on which objects on the two visual axes
appear to lie the com m on axis. It is now known as the cycio­
pean axis.
37] Let the lines A D and B D be the visual axes
[Figure 2 .4 3 f ]. O b je cts on line F.DZ appear in their
actual positions; but objects on line Н Т К appear
displaced from their true positions.
38] It is clear that points E, D, and Z will appear
in their true positions, because each o f them falls on
the perpendicular to the com m on axis at the point
where the visual axes intersect and where the dis­
tance from the visual axes to the com m on axis is
zero. Since the visual axes converge on the com m on
axis, so points E, D, and Z appear in their true posi­
tions. Therefore, each ot these objects will be seen in
its true position.
Tli is is a spurious proof o f the incorrect conclusion chat
the horopter is the frontal plane through the fixation point.
Ptolemy realized that an o b je ct appears single and in its true
position when it falls at the intersection o f two correspond­
ing visual lines, but he failed to realize that this does not
generate a planar horopter. We will see that, in the 11 th cen­
tury, Alhazen deduced that an o b ject appears single when it
subtends the same angle to the two eyes as that subtended
by the visual axes. From this, Alhazen proved that the
horopter is not a plane. However, description of the true
horopter had to wait for Pierre Prcvost in 1804. It is ironic
that the theorem o f Euclid that Prcvost used for this proof
was well known to both Ptolemy and Alhazen.
4 3 ] W e can sec this more clearly i f we take a black
rectangular board [Figure 2 .4 3i] and mark o f f on its
shorter side two points A and В separated by the dis­
tance between the eyes, and extend from the mid­
point G a perpendicular G D , and draw lines A E Z ,
B E H , and Т Е К , with Т Е К parallel to AB. C o lor
G D white, Т Е К green, A E Z red, and B E H yellow.
 Place the eyes .it points A and В and converge on a
small o b ject placed at point E.
44] Lines A Z and В H fall on the visual axes, and
the green line Т Е К will appear as one line, since it
intersects the point o f convergence. Red line AF.Z
and yellow line Б Е Н will appear superimposed on
G D ; but each o f them will also appear in another
position, A E Z on L E M , and B E H on N E S. The
white line G E D , will appear on lines A Z and B H .
4 5 1 W h en we cover eye B, green line Т Е К is still
seen. But the white line on A Z , the vellow line on
G l ) , and the red on LM will be hidden. The other
lines will keep the positions they had when both
eyes were open. All this is consistent with what has
already been determined.
Ptolemy completed his treatment ot binocular vision
with a discussion o f th e binocular appearance o f oblique
lines and curves in the plane o f regard.
Ernst Mach ( 1 9 2 9 ) gave an account o f Ptolemy’s work
on binocular single vision and reproduced two diagrams
similar to Figures 2.41 a and 2.4 l c , but there seems to be no
other reference to Ptolemy’s work on binocular vision in the
visual science literature. M ost visual scientists do n ot know
that Ptolemy/ wrote a book on vision.
2 .1 0 .2 A LH A ZEN ON B IN O C U L A R V ISIO N
In his Rook o f Optics, written in rhe 1 1th century, Alhazen
followed Galen in explaining that wc have two eyes so that,
when one is harmed, rhe other remains intact. He added
that two eyes beautify the face (Sabra 1989, p. 102). Like
Aristotle and Galen, he mentioned that an o b ject appears
double when a finger pushes one eye. Also, like Galen, he
pointed out that, when converged on a point, the visual axes
lie in o ne plane, which we now call the plane o f regard. He
stated that the two eyes always move together and by an
equal amount, so that the visual axes converge on the object
o f interest. As Heller (1 9 8 8 ) pointed out, this idea lay dor­
mant until the 19th century when Hering, without any ref­
erence to Alhazen, described the principle o f equal
innervation (Section 10.8.1).
In Chapter 6 o f Book I and Chapter 2 o f Book III,
Alhazen described corresponding points in the image planes
o f the eyes. He explained that visual lines from an o b ject
near the intersection ot the visual axes project to corre­
sponding points in the eyes and appear single. Images fall-
ingon noncorresponding points are seen asdouble. Alhazen
therefore extended Ptolemy’s conccpt o f corresponding
visual lines to that o f corresponding points in the eye,
although he had no clear idea o f the image in the eye.
Like Ptolemy, Alhazen believed that signals evoked by
objects on the two visual axes travel along the optic nerves
to converge in a point he referred ro as “the center.” This
point fits with what we now call the chiasm. W e use the
term “cgocentcr” or “cyclopean eye” to refer to the point
from which visual directions are judged. We do not place it
in the chiasm or think o f it as where images fuse. Like
Ptolemy, Alhazen called the axis extending from the center
to the fixation point the “com m on axis.”
Alhazen stated that an object above or below a fixation
point in the midline (the sagittal plane o f the head) is not
seen double because its distance from the two eyes is the
same and it therefore projects equal angles to the two eyes.
This idea anticipated the modern concept o f rhe vertical
horopter (Section 14.7). He then discussed double
images produced by an o b je ct nearer o r further away than
the fixation point, with both the object and the fixation
point in the median plane. He invited rhe reader to view
lines on a board extending horizontally trom the bridge ot
the nose, as shown in Figure 2.44. This resembles the
figure used by Ptolemy. H e described the following visual
impressions.
An object at point 1 docs n ot appear double if it is not
too far from the frontal plane through TKH , in which the
eyes are converged. But an object at O, well away from the
plane o f convergence, appears double. He thus realized that
small differences in visual angle arc tolerated without diplo­
pia. W e now refer to this tolerated disparity as Panums
fusional area (Section 12.1). W e should call it Alhazens
eye eye
Figure 1A4. A lhazen'sgeom ctoy o f bin ocu lar vision. T h e b o лid is held
h orizon tally fro id th e bridge o f th e nose and fixation o n K . Sm all
o b je c ts arc placcd at K , 1%L , I. and Q . Line L Z appears as a cross
th ro u g h K . Lines B G an d A D appear a* four lines w ith the tw o cen ter
lines superim posed on the m id lin c. O b je c ts Г and L produce double
im ages, straddling th e m id lin e. O b je c t Q produces double im ages,
o n o n e side o t th e m id lin c. O b je c t I produces double im ages to o near
to g eth er to be seen as tw o . O b je c ts at T and H appear single, but
o b je cts m ore e cc e n tric o n the sam e fro n ta l plane appear dou ble. (Fro*
Alh/u<n4 J
g 1
tu n » . S.tbt. , 1 9 9 9 , |». 2M t)
fusion a I area! O b jects closer со or far chc r chan chc
fixacion poinc (poines L and F) appear double and on oppo-
sicc sides o f chc fixated objccc when chey arc bccwccn chc
visual axes. They appear on che same side o f chc fixated
o b je ct when chcv arc oucsidc chc region lying bccwccn chc
visual axes (poinc 0 ). Here he follows Pcolemy in describing
che basic faecs abouc diplopic images and cheir relative
order.
Small objeecs, T and H , in che same froncal plane as che
fixacion poinc appear single when noc coo far from chc fixa­
cion poinc, buc double when well со che side. Alhazen
proved chis by showing chac che angle bccwccn an eccencric
o bjccc and che median plane was noc che same tor chc cwo
eyes. He chus proved chac che locus o f fused images for a
given viewing discance docs noc lie in a troncal line or plane,
as Pcolemy had believed. Ic is a picv chac he did noc go one
seep turchcr and apply Euclid’s geomecry, which was well
known со him, со show chac che locus o f fused images (che
horopcer) is a circle passing chrough che fixacion poinc and
chc cw'o eyes.
He followed Pcolemy in describing how chc cencral line,
EZ, appears as cwo lines inccrscccing in chc fixacion poinc,
K. Finally, cwo lines, A D and BG , excending diagonally
from each eye and inccrscccing in chc fixacion poinc appear
as tour lines, wich chc middle cwo appearing close cogeeher
along chc median plane o f che head. He wrocc,
These ideas o f Pcolemy and Alhazen have been almosc
coeallv ignored. Figure 2 .1 2c is from Opbtbabnographia wric-
ccn by William Briggs ( 1 6 5 0 - 1 7 0 4 ) in 1676. Ic illuscraces
che facc chac objeecs on che visual axes appear in che mid-
line. W illiam C . Wells ( 1 7 5 7 - 1 8 1 7 ) gave an accounc o f
cyclopean visual direction in his Essay upon Single Vision
with Two Eyes, wriccen in 1792, 8 7 years before Hering
wrocc his accounc in 1879. None o f chese auchors acknowl­
edged chc concribucions o f Pcolcmy o r Alhazen.
Kamal al-Din Abdu’l-Hasan al-Farisi (died c. 1320)
reviewed A lhazcns wricings in his Tanqih al-m anazir
[Revision o f the Optics) in abouc che year 130 0 in Iran. A
diagram ot che binocular system trom one ot al-Farisi’s man-
uscripcs is shown in Figure 2.45. Ic shows how rays from a
fixaccd objccc tall on corresponding points and how rays
from nearer or more discanc poincs fall on noncorrespond-
ing poincs on che assumed reccpcive surface on che lens.
W hile che works o f Alhazen and ocher Arabic scholars
became known in Europe in che 12eh cencury, cherc were no
dcvclopmencs in chc underscanding o f binocular vision
uneil chc Renaissance.

The reason why cwo ot che tour appear closer

cogecher is chis: when che cwo visual axes meec ac che
middle objccc, chen each o f che cwo diamcccrs will
be perceived by che eye nexc со ic chrough rays chac
arc very close со che visual axis; chus cheir forms
(images) will be very close со che cencer wichin che
com m on nerve (che chiasma) and cheir poinc ot
incerseccion will be ac che cencer itself, and chus che
diamcccrs will appear very close со che middle (chc
median plane), (p. 2 4 2 )

Noce chac Alhazen scaced chac lines falling “close со che

visual axes” appear close со che midline. His cheory predicts
chac lines on che visual axes appear as o n e on chc cyclopean
axis. Som e cimc after his Book o f Optics, Alhazen wrocc a
shore nocc enciclcd Doubts about Ptolemy. He claimed chac
Pcolemy was wrong, boch cxperimencally and in cheory, in
claiming chac visual lines meeting in the poinc o f conver­
gence appear со lie on chc com m on axis. Alhazen argued
chac chcv approach each ocher, buc do noc mccc (sec Sabra
1966). Buc Pcolemy was correcc— when lines are drawn
from chc cenccrs o f che pupils chey do indeed appear со
coincide in che cyclopean axis. Perhaps Alhazen did noc
have his lines lined up wich che ccncers ot chc pupils. Ic is
noc clear whv* Alhazen claimed chac Pcolemy 4 was cheoreci-
cally incorrcce when his own cheory prediccs chc cffccc chac
»:i*«c 2 .*> D iagram o f the b in o cu lar system by a l-l:arisi. From * l ab ccmury
Pcolemy reporced. This w'ork by Alhazen proves chac he had A ra b ic r a ji t u t i n p c w it h лп F .n g lith т г л я Л л п с о c i i W o f R t j S t .b k K j j n f t s .ViJrdt/ c f O ft r . . in t h e A v-ivo ly*

read Pcolemy s Optics. L i b r a r | ,h c in b u l .

 2 .1 0 .3 E U R O P E A N S T U D IE S ON
B IN O C U L A R V ISIO N

2 . 1 0 . 3 a L e o n a r d o D a V in c i
o n B in o c u la r V is io n

Leonardo da V inci ( 1 4 5 2 - 1 5 1 9 ) , in Trattato della pitttira

(Treatise on Painting , wrote,

A painting, though conducted with the greatest art

and finished to the last perfection, both with regard
to its contours, its lights, its shadows and its colors,
can never show a relievo equal to that o f the natural
objects, unless these be viewed at a distance and with
a single eye.
( F rom л T ran si.(lio n o f L E O N A R D O ' S FRANCkSCI
Treatise by SieM ahon, /9 5 6 . p. /7 7 )
AGVI LON 11
E S O C IE T A T E IE S V
He described how an o b ject obscures from cach eye a
different part of the distant scene (see Figure 17.18). This is
OPTI CORVM
occlusion disparity that had been described by Euclid and
Galen. However, they confined their attention to the fact LIBRI SEX
that one eye secs more o f one side o f a sphere than docs the tffiLplbu iuxtu acMatnmuUiris
other eye. Da V in ci also considered how regions ot a tex-
ew i
turcd background beyond an object arc seen only by one
eve
* and described monocular occlusion as a source ot in tor-
mation about depth (sec Keelc 1955; Strong 1 979). He
observed that objects seen with both eyes appear rounder W A X TV ER P1/C , N
Л ОГТП1ХЛ rtA V T IS lA K A
than when seen with only one eye. This topic is discussed in A n Rfc* MorelI
M tX. XIII.
Section 17.2.4.

2 . 1 0 . 3 b A guilonius on B in o c u l a r V is ion

Franciscus Aguilonius (Francois d’Aguillon) was born in

Brussels in 1546, the son of the secretary to King Philip II.
He becam e a Jesuit priest in 1586 and died in Antwerp in
1617. He taught logic, syntax, and theology and was
charged with organizing the teaching o f science in Belgium.
In 1613 he published part one o f a three-part work on
optics designed to synthesize the work o f Euclid, Alhazen,
Vitello, Roger Bacon, and others. He died before com plet­
ing the book . The published work consists o f six books with
the title Opticorum L ibri Sex. The frontispiece is shown in
Figure 2.46, and tw o o f several illustrations by Rubens are
shown in Figure 2.47.
In his treatment o f visual optics and perception he fol­
lowed the order o f topics in Alhazens book, but he did not
refer to Alhazen. Opticorum Libri Sex appeared 2 years
afier Keplers Dioptrice, but Aguilonius did not refer to
Keplers work on the formation ot the retinal image. Like
Alhazen, he realized that clear vision occurs only if each
object point is represented by one image point in the eye.
Aguilonius followed Alhazen in believing that the image is
formed in the lens. He adopted Alhazens theory that only
light rays orrhogonal to the cornea and lens surface are clearly
registered.
2,i(\ Frontispiece fr o m O ptu oru m L ib r i S ex. W ritten by Francois
D ’A gu illon (A g u ilo n iu s) in 161 3-
His ideas on binocular vision arc in Book 2. He was
aware that binocular vision improves the sense o f depth but
did not relate this to binocular disparity. He adopted Galen’s
idea ot the cyclopean eye located in the chiasm. O n e ot the
illustrations by Rubens shows putti dissecting the eye taken
from a cyclops. In theorems 144 to 146 he clearly described
how an o b je ct o f appropriate size and at an appropriate dis­
tance occludes a far surface so that halt the far surface is seen
by one eye and half by the other eye. He also described how
a larger o b ject creates a region of the far surface invisible to
either eye and a smaller o b ject creates monocular zones
separating a binocular zone (see Section 17.2.1). However,
lie did not relate these facts to depth perception.
Aguilonius used the term “horopter” to describe the
locus in space within which fused and diplopic images appear
to lie. The word is derived from the Greek words “boros”
meaning “boundary,” and “opter" meaning “observer.”

А
к. *uгс 2 . *7. Etchings by R ubensfrom A guilonius (1 6 1 3 ). (A ) A m an. blind in
on e cv c, is show n having d ifficu lty reach in g fo r an o b je ct.
(B ) Ih e eves converged on a sm all sphere on a stem and the p osition s
o f its tw o disparate im ages w ere p rojected o n the far plane, w hich
A g u ilo n iu s defined as th e horopter. (FW. o/n Mr/Sex.
ISi'illo hi Librjry.OfcfurJ)
Aguilonius presented the diagram shown in Figure 2.48Л
and wrote,
L et the centers ot sight be at A and В which the
straight line A В connects. The optic axes A C and
B C com e together at C , and through C , parallel со
A li runs a straight line, D E.
He called this line chc horopcer and the vercical plane
containing ic che horopcer plane. He continued,
The appearance o f all those objects placed in the
plane (ot regard) assume places for themselves. For
example, F is a visible object, the optic radii AF and
B F jo in at F, buc chey carry beyond the image o f the
o bject, until chey site ic in che horopcer as in a
com m on terminus and station, where the twin sites
o f H and G are placed. For an o b ject ас I, che images
appear at К and L. In this way, che horopcer is the
с
A
H&wc 2 .*s. D iagram s fro m A guilonius (16 1 y). (A ) A gu iloniu s defined the
h o ro p te r as th e plane in w h ich double im ages appear to lie. 'Hie eyes
a t A and В converge o n p o in t С on a fron tal plane, D E . Im ages o f an
o b je c t a t 1: p ro je ct o n to the plane a t G and H . T h o se o t an o b jc c t at 1
p ro ject to К and L. ( B ) L ocu s o t equ al subtense o f visual lines. Points
С and D on a circle throu gh the eyes a t A and В p ro je c t equal angles to
the eves.
terminus o f all things which exist beyond and on
chis side o f chc junccion o f chc optic radii.
( /613, Definition I0yp. I J J) .
Tlius, for Aguilonius, chc horopcer was noc based on the
concept o f corresponding points, which he does not discuss
in his book. However, in theorem 148 on page 52 he
Stated,
The object on chc point on chc horopcer where the
opcic axes meet is seen mosc clearly. In che second
place, objcccs lying on chc rest o f rhe horopter are
seen less clearly. In the chird place, most imperfectly
o f all arc seen those things which lie outside the
horopter, which are seen as double.
Aguilonius went on to describe how only objects on che
horopter are seen in their crue location and he buile an
instrument со measure the spacing o f double images in che
horopter as he defined it. Rubens provided rhe fanciful
illuscration o f chis instrument shown in Figure 2 .4 7 B . In
the actual in stru m en t chc vertical plane could be moved to
different distances from the observer.
Ic is clear trom Rubcnss illustration, trom Figure 2.47B,
and from Aguiloniuss account that he used his instrumenc
со ploc projecCcd positions ot disparace images racher chan
che locus o f fused images. Aguilonius maincained chat the
horopter, defined this way was a troncal plane passing
chrough che poinc o f convergence. He probably believed
chis because he visually projected the double images ot
objeccs thac were well oucside rhe plane o f binocular fixa-
cion onco che froncal plane. We will see in Chapcer 14
chat chc horopcer, defined as che locus o f fused images, 2 . 1 0 . 3 c K e p le r o n D e p t h P ercep tio n
is approximacely a circle passing chrough chc poinc o f co n ­
In his Dioptricc o f 1611, Kepler explained depth perception
vergence and chc cwo eyes— che Viech-Miiller circle.
in terms ot the feeling o f rotation o f the eyes as they co n ­
Alhazen had already proved in chc 1 lch cencury chac the
verge o n an object. He probably derived chis m otor cheory
locus o f fused images is noc chc fronc.il plane, alchough he
o f depth perception from Alhazen. Rene Dcscartcs also
did noc establish its shape. Aguilonius had read Alhazen
adopted che m otor cheory in his L a dioptriqtie o f 1637,
and cited him four times. However, he did not refer to
which contains a picture o f a blind man using two sticks to
Alhazens proof. Nor did he refer со Alhazens concepc o f
triangulate distance, which Dcscartcs described as analo­
corresponding poincs or со his demonstrations on cyclo-
gous to the use o f convergence by sighted persons. The
pean vision and chc limits o f fusion.
m otor theory o f depth perception and o f vision in general
Wc now define che horopcer as che locus in space in
was further elaborated by George Berkeley in his Essay
which an objccc muse lie со appear single, a definicion chac
Towards a New Theory o f Vision (1 7 0 9 ).
Aguilonius only hinced ac. O n page 156 o f his book
The cheory stemmed from che general belief chac depth
Aguilonius produced che drawing shown in Figure 2 .4 8 B
could not be detected by vision alone, since the image is
and the following statement:
two-dimensional. The deeper philosophical position under­
lying these views is that vision is mediated by images that
If objects fall upon different rays it can happen that
replicate the seen o b je ct— by pictures in che m ind— and
things ac different discanccs can be seen ac equal
chac chcsc pictures arc interpreted in terms o f motor actions.
angles. I f point С be directly opposite the eyes,
The modern view is that vision, like ocher sensory processes,
A and 11, with a circle drawn chrough che chree
is mediated by coding mechanisms that process informa­
poincs, A , B, and C . By cheorem 21 o f Euclid’s Third
tion about the perceived o bject, but not in an isometric
book, any ocher poinc 1) on ics circumference which
form or even, necessarily, in a copographic form. The coding
lies closer со the observer chan C , will subcend an
o f depth by binocular disparity is a good example o f non-
angle A D B which will equal angle A C B . Therefore,
topographic coding o f a spatial feature. The persistence o f
objeccs ас С and ac D are judged equally far from the
che old view caused che long delay in che discovery o f purely
eye. Buc chis is false, because poinc С is farcher away
visual mechanisms devoccd со che perception o f depth. The
chan D. Therefore a judgment o f distance is false
old idea o f pictures in che mind scill lingers on when people
when based on the angles between converged axes,
wonder why we do noc see upside down when che retinal
quod erac probandum.
image is reversed or when chey speculacc that the geomccri-
cal transformation o f patterns o f neural activity on che sur­
Ac firsc glance, ic looks as chough Aguilonius discovered
face o f the visual cortex has something to do with shape
che gcomecrical horopcer more chan 2 0 0 years before
recognition (Section 5.5.4d).
Prcvost and Viech and Muller. However, it is clear from chis
The set o f possible matches between che images o f an
quocacion that he was concerned to prove that objects equi­
array o f objects is known as the Kcplerian projection, which
distant from an observer do noc subcend equal angles to che
is described in Section 14.2.2. 1 have not been able to trace
two eyes. He thoughc o f his circle as che locus o f equal
che source o f chis idea in Keplers writings.
angles o f binocular subtense o f visual lines, racher chan as
che locus of zero disparity. Euclid him self had used the same
theorem со prove thac an objccc subtends che same visual
2 . 1 0 . 3 d N e w t o n o n B in o c u l a r V is io n
angle when an eye moves round che circumference ot the
circle passing chrough chc ends o f che o b ject and chc cencer Isaac N ew ton ( 1 6 4 2 - 1727) (Portrait Figure 2 .4 9 ) was che
o f che eye (see Burcon 1945, p. 3 6 7 ). Ic would have been an leading scientist o f his time. He made fundamencal discov­
easy seep со prove chat che locus o f equal binocular subcense eries in machcmatics, ascronomy, and optics. But he also had
and che locus o f fused images are cheorecically the same. a strong mystical streak and devoted much time to alchemi­
Aguilonius did noc cake chac seep, probably because, like cal experiments and mystical speculation.
Euclid, he did nor have a clear conccpeion o f how lighc rays W c now know thac, in humans, the inputs from only the
arc projccccd onto che retinas. temporal h a lf o f each recina projecc ipsilaterally. Inputs
The idea o f a froncal-plane horopcer persisted until the from the nasal h a lf o f each retina cross over, o r decussate, in
early 19th century, when Pierre Prcvost established thac the optic chiasm and project to the concralaceral half o f che
the locus o f fused images is a circle passing chrough che cen- brain. Isaac Ncwcon in his Optieks ( 1 7 0 4 ) was the first to
cers o f chc eves. Prevost used the same theorems thac propose chat visual inpucs segregace in chis way. He wroce,
Euclid and Aguilonius had used со establish che locus o f
equal angles ot binocular subcense. He was apparendy Are not che species o f objeccs seen wich boch eyes
unaware o f che Aguilonius contribution and did nor refer uniccd where chc opcick nerves mccc before chey
to Alhazen. come inco che brain, che fibres on che righc side o f

F.fiuc2.'»$. Isaac N ewton. B orn in W o o lsth o rp c, England, in 1 6 4 2 . He
attend ed T rin ity C o lle g e o f C am brid g e U n iv ersity in 1661 and becam e
Lucasian P rofessor o f M ath em atics in 1 6 6 9 . In 1 6 8 9 he was elected to
Parliam ent and becam e m aster o f the M in t in 1 6 9 7 . H e was presiden t of
the Royal S o ciety from 1 7 0 3 u ntil he died in 1 7 2 7 . IГто. 195"*
both nerves uniting there, and after union going
chcncc into the brain in the nerve which is on the
right side o f the head, and the fibres on the left side o f
both nerves uniting in the same place, and after union
going into the brain in the nerve which is on the left
side ol the head, and these two nerves meeting in the
brain in such a manner that their fibres make but one
entire species or picture, h a lf o f which on the right
side o f the sensorium comes from the right side o f
both eyes through the right side o f both optic nerves
to the placc where the nerves meet, and from thcncc
on the right side o f the head into the brain, and the
other h a lf on the left side o f the sensorium comes in
like manner from the left side o f both eyes. (p. 3 46 )
He went on to explain that this is true only o f animals
with frontal vision. He conccivcd o f each optic nerve as a
multitude o f “solid, pellucid, and uniform capillamenta,”
which transmitted vibrations causcd by light to “the placc
o f sensation” in the brain. Newton believed that corre­
sponding fibers fused just after the chiasma, so that
the brain received only one nerve from each pair o f
corresponding retinal points, as shown in Figure 2.12d from
one o f his manuscripts {see C ron e 1 992). He thus returned
to Galen’s concept o f the cyclopean eye. Newton stated that
similar images fuse to give the impression o f a single o bjcct
when they fall on corresponding points and are seen as
double when they fall on noncorrcsponding points. He also
realized that dissimilar stimuli falling on corresponding
points rival rather than fuse.
2 . 1 0 . 3 c O t h e r s in th e 1 7 th and 18 t h C e n tu r ie s
Several writers in the 17th and 18th centuries, including
the French physicist Ja c q u e s R oh au lt ( 1 6 7 1 ) , N icholas
M a leb ra n ch e ( 1 6 7 4 ), and R o b e rt B o y le ( 1 6 8 8 ) , stated
clearly that binocular vision contributes to the impression
o f visual depth. Like Aguilonius, they noted thac it is more
difficult to reach accurately for an object with one open eye
than with two open eyes. Rohault noted that, after losing
one eye, people recover the ability to judge the distances o f
objects. He suggested that they use parallax generated by
moving the head from side to side. Perhaps he was aware o f
the use o f binocular parallax by people with two eyes.
S ebastien Le C le rc ( 1 6 7 9 ), an authority on perspec­
tive, described clearly the differences between the images o f
a solid object in the two eyes, but did not relate these differ­
ences to the perception o f depth.
R o b e rt Sm ith ( 1 6 8 9 - 1 7 6 8 ) was master o f Trinity
College, Cambridge. In his Compleat System o f Opticks o f
1738, he described how he sighted a distant object between
the points o f a vertical pair of dividers about 6 cm apart.
W h en the dividers were placed at the correct distance, the
inner pair of diplopic images fused to appear as a rod extend­
ing down the midline from the hand to the distant object.
This is essentially
*
the same effect that Ptolcmvi and Alhazen
had observed when looking at the fused image o f lines
extending out from the two eyes.
W illia m Porterfield (c. 1 6 9 6 - 1 7 7 1 ) , a physician in
Edinburgh, produced drawings o f an object as seen by each
eye (Figure 2 .1 2 f ) . He cited anatomical authorities in
rejecting N ew tons idea o f hemidecussation o f the visual
pathways (Porterfield 1759). Like Rohault ( 1 6 7 1 ) , he sug­
gested that corresponding visual fibers com bine in the
brain. After having had one leg amputated, Porterfield was
able to give a firsthand account o f his phantom leg sensa­
tions in his Treatise on the Eye, the M anner an d Phaenomena
o f Vision o f 1759. He used these sensations to support the
general idea that visual sensations arc projected into space.
Jo h n Taylor ( 1 7 0 3 - 1 7 7 2 ) styled him self “O phthal-
miatcr, Pontifical, Imperial, and Royal.” Fie traveled F.uropc
performing eye operations on wealthy patrons. His opera­
tions for cataract on the composers J. S. Bach and G. F.
Handel resulted in their blindness. He claimed to have per­
formed the first operation for correction o f squint but, in
fact, Johann Dietfenbach ( 1 7 9 2 - 1 8 4 7 ) performed the first
successful operation (sec Wade 2 0 0 8 ).
In 1738, Taylor adopted N ew tons idea o f hemidecussa­
tion. He was the first person to correct the erroneous notion
that the optic fibers from corresponding retinal regions fuse
in the optic chiasm (Figure 2 . 12c). However, we shall see in
the next section that conclusive anatomical cvidcncc on
this question was not available until 1870.
Je a n T h eo p h ilc D csagu licrs ( 1 6 8 3 - 1 7 4 4 ) was an
ardent disciple o f Newton (Wade 2 0 0 0 ) . He was born in
France o f Huguenot parents. W h en he was 2 years old, his
father, fleeing religious persecution, brought him со
England. He studied and taught at O xford and in 1714
became demonstrator and curator o f the Royal Society. He
investigated corresponding points and color rivalry by plac­
ing a candle on the visual axis o f each eye and viewing the
candles through an aperture. In support o f N ew tons notion
that corresponding nerves from the eyes fuse in the optic
chiasm, Desaguliers claimed that different colors presented
to corresponding regions in the two eyes rival rather than
fuse. He argued that this supported New tons idea that
inputs from the two eyes rival for access to the com m on
nerve in the chiasm. O th er early studies o f color rivalry are
described in S ection 12.2.1.
Desaguliers ( 1 7 3 6 ) also conducted experiments to show
that the apparent size ot an object depends on its apparent
distance. W ith the visual surroundings in view, two candles
o t the same size appeared equal in size when one was twice
the distance as the other. This is size constancy. W ith the
surroundings eliminated by viewing through an aperture,
naive observers continued to see two candles the same size
and at different distances when, in fact, they were the same
distance but one was half as high as the other. He related his
findings to the theory that the m oon illusion is due to the
greater perceived distance o f the horizon moon relative to
the zenith moon (Section 29.3.5).
Jo s e p h H arris, master o f the M in t in London, who died
in 1764, made drawings ot crossed and uncrossed dispari­
ties arising from objects nearer and further than the point
o f fixation, as had Alhazen and others. He realized, as had
da V inci, that m onocular occlusions contribute to the
impression o f depth, not only within a single o bject, but
also between an o b ject and its background, as revealed in
the following passage from his Treatise o f Optics, published
in 1 7 7 5 ,1 1 years after his death.
And by the parallax, on account o t the distance
betwixt our eyes, we can distinguish besides the
front, part o f the tw o sides o f a near object not
thicker (wider) than the said distance and this gives
a visible relievo to such objects, which helps greatly
to raise or detach them from the plane, on which
they lie. Thus, the nose on a face is the more remark­
ably raised by seeing each side o f it at once. These
observations, I say, are o t use to us in distinguishing
the figures o f small and near objects; and when the
breaks, prominences and projections are more c o n ­
siderable, we do n ot want them. The distances
betwixt the legs o f a chair are visible many yards olf,
and the projection o f a building is visible still far­
ther. But as the distance is increased, different
degrees of eminences, cavities, et cetera, disappear
one after another, (p. 171)
It is clear from this passage that Harris realized that
occlusion disparity is scaled by absolute distance. He seems
to have been the first to realize this. He was aware o f che
position disparity in the images o f an o b ject out o f the plane
o f convergence, but did n ot relate this type o f disparity to
the perception o f depth. He used the term “horopter” in its
m o d em sense as the locus o f objects producing single
images. However, he believed the horopter to be a frontal
surface. He also wrote,
An o b ject that is a little out o f the plane ( o f the
horopter), may yet appear single . . . it will also shift
its place by winking either eye, and looking at it with
both eyes. (p. 113)
Tli is description o f Pan urns fusional area was written
7 0 0 years after Alhazen had made the same point and 8 0
years before the account provided by Peter Ludvig Panum,
professor o f physiology at Kiel University. The quotation
also states the principle o f parallactic motion, although
Galen had made a similar observation.
2 .1 0 .4 H IS T O R Y О F T H E H О R O P T E R
For Ptolemy in the 2nd century, the locus o f objects
producing single images was the frontal plane through the
fixation point (see Section 2.10 .1 ). Alhazen, in the 11th
century, proved that the locus is n ot a frontal plane. He also
defined a locus o f fused images forming a vertical line
through the fixation point in the median plane o f the head.
Aguilonius introduced the term “horopter” but defined it
as the frontal plane in which fused and diplopic images
appear to lie. Pierre Prcvost ( 1 7 5 1 - 1 8 3 9 ) was the first
person to describe the horopter as a circle through the cen ­
ters o f the eyes and the fixation point. In his Essais de phi­
losophic on etude de I’esprit hum ain , published in Geneva in
1804, he wrote,
It follows from the stated law that, in the plane o f
the optic axes, the position o f those points seen
single with the two eyes is a circumference o f a circle
which passes through the two centers o f the eyes
and the intersection o f their axes. I refrain here from
demonstrating this proposition which is easy to
deduce.
( P R £ V O S T I $04, p. 173. T ransU uJinto Vntftsh by
S bipky< in d Rdto'tings 1970)
Presumably, Prcvost s deduction o f the circular horizon­
tal horopter relied on theorem 21 from Iiook III o f F.uclids
Elements, which states that angles subtended by the cord o f
a circle on the circumference are equal. Prcvost incorrectly
described the vertical horopter as formed by rotating the
intersection o f the visual axes about the interocular axis.
Vieth ( 1 8 1 8 ) was the first person to specify clearly
the geometry o f the horizontal horopter, which he

fr.fturc 2 .vo. D ra w in g itia lb y I u'tb ( IS IS ). V ic th used a draw ing like this
to prove chac the h oro p ter is a circlc passing through the o p tica l ccn tcr
o f each eve (O and U ) an d fixation p o in t P. P oin ts A and В represent
the foveas and arc therefore co rresp on d in g p o in ts. P oin ts M and К
rep resent the im ages o f p o in t X and fall o n corresp on d in g p oin ts w hen
M is as far Irom A a s К is trom B . '[h is is true w hen angles о and u
a rc equal. B u t angles о and u arc equ al w hen angles x and p arc equal.
A ngles x and p arc equal w hen they fall o n th e circu m fcrcn cc o f a
circlc passing through О and U , since angles subtended on a circlc by
co m m o n chord arc equal. L in e S T is the fron tal plane.
defined as th e locus o f objccts producing fused images. I Ic
wrote,
Firstly ic is correct and established from com m on
experience, thac poinc P in Fig. 2 [Figure 2.50]
cowards which boch eyes are direcced, or ac which
boch visual axes incersecc is seen singly.
W h eth er che so-called corresponding poincs M
and N, or more specifically, whether chesc images o f
a poinc X are equidiscanc or ac unequal discanccs
from A and B, che images o f poinc P, chac depends
on whether che angles о and u ac che pupil are equal
or unequal. However, о — v - x and u = v - p.
T h erefore,. . . if x is equal со p, chen о is equal со u.
Thus, in chac condition, where che angles p and x
arc equal, che images M and N arc cquidiscant from
A and B, and chis case occurs when X lies on che cir­
cum fcrcncc o f a circlc, which passes chrough О and
U and P, because all angles on chis circumference are
subtended by chc same chord О U.
Thus, Victh established that the locus o f single vision —the
horopcer— is a circle chrough che fixacion poinc and the
cencer o f each eye. The theorem o f F.uclid that he used was
the same as chac used by Aguilonius со escablish che locus o f
equal angles o f binocular subtense. Victh continued,
Thus, if by chc expression corresponding points
one understands such poincs which lie in chc same
direction in boch eyes, and are equidiscanc from A
and В which seems со me che correcc meaning, and
one asscrcs one sees chac ching singly whose images
fall on such corresponding poincs, chen, according
со chis rule, one sees chac ching singly which is situ-
aced wichin che boundary o f a sphere which passes
chrough O , U, P, hence, n ot what lies in che plane S
T , which one has called che horopcer.
{ V I E T H IS IS , p. 2 3 4 , Iin g liJ; tTiirnLufon b y A. Ilo u w d )
Here V icth incorrectly generalized his principle o f cor­
responding points in claiming chac che horopcer is a sphere
rather chan a circle. N o t all angles subtended by a chord
o n to the surface o f a sphere arc equal. We will see in Chapter
14 that che chcorctical horopter for parallel visual axes is an
infinite coroid formed by sweeping che horopcer circle
abouc che incerocular axis. Alexander Prevost (1 8 4 3 ) first
pointed o u t chac, when chc visual axes are converged, the
horopter is n ot a surface but a horizontal circle and a verti­
cal line in the median plane (Section 14.6).
Victh went on to state, as had Ptolemy and Alhazen,
chac an objccc positioned bccween che visual axes projects
images on opposice sides o f che image o f the fixation point,
whereas an objccc со eicher side o f chc cwo visual axes pro­
duces images chac fall on the same side o f the image o f the
fixacion poinc. Like others before him, he stated that images
ol an object nearer than the fixation point are crossed wich
respecc со che fixacion poinc, and chose ot an objccc beyond
che fixacion poinc are uncrossed. These ideas are explained
more fully/ in Section 14.2.
Jo h a n n e s M iiller ( 1 8 2 6 ) produced a similar and inde-
pendenc analysis, buc became aware ot Viechs work, which
he acknowledged in his paper. Miiller ( 1 8 0 1 - 1 8 5 8 ) was
protessor o f physiology and anacomy in Berlin. He caughc
Hclmholcz and was one o f che founders o f experimencal
physiology. The chcorctical horizontal horopcer is now
known as the V ieth -M u ller circlc. Muller had che horopcer
passing chrough the ccncers o f che cwo lenses. He discussed
binocular disparicy in che conccxc o f fusion and rivalry o f
binocular images and concluded chac che ditierences
bccween che images in chc cwo eyes were coo small со be
decected.
In 1843, five years after W heatscone reported that dis-
pa race images produce a sensation ot depth, Miiller agreed
chac disparicy is involved in che perception o f depch.
Volkmann ( 1 8 3 6 ) firsc specified che geometrical assump­
tions underlying che chcorctical horopcer. Hclmholcz
(1 8 6 4 ) generalized rhe geomecry o f che horopcer over che
visual field. For more dccails on che hiscory o f che horopcer,
see Shipley and Rawlings (1 9 7 0 ).
2 . 1 0 .5 P H Y S IO L O G Y OF S T E R E O P S IS
Before che 19ch cencury, cherc was a general consensus chac
each opcic nerve projcccs to its own side o f the brain.
Newton (1 7 1 7 ) had proposed that the nasal half o f each
optic nerve crosses over to the opposite side o f the brain
(Section 2.10.3d ). W illiam Wollaston ( 1 7 6 6 - 1 8 2 8 ) cited
anatomical evidence that the optic nerves o f fish hilly decus­
sate. He inferred corrcctlv that this is bccausc their eves arc
4 4
placed laterally so that they have no need for corresponding
points in the two retinas. He suffered from recurrent
hemianopia, in which he was blind for objects to rhe right
o f the midline. He inferred, correctly, that this was due to
injury to the left thalamus, which receives uncrossed inputs
from the left half o f the left eye and crossed inputs from the
left h a lf o f the right eye. He concluded that the right thala­
mus receives inputs from the right half o f each eye. These
observations provided the first empirical evidence in sup­
port of New tons idea o f hem idee ussation (Wollaston
1824).
In 1870, Bernhard von Gudden produced conclusive
anatomical evidence that the human visual pathways
hem idee ussate. Von Gudden was an eminent neuroanato­
mist and professor o f psychiatry in Zurich and Munich
(von Gudden 1870). King Ludwig II o f Bavaria was one o f
his patients. The politicians were annoyed with King
Ludwigs use o f state funds in building the fantastic
Ncuschwanstcin castle. They asked von Gudden to ccrtify
the king insane and have him incarcerated in Schloss Berg.
O n the second day o f incarceration, in June 1886, the king
asked von Gudden to walk with him by Lake Starnberg.
Both men were later found drowned in shallow water. It is
generally believed that rhe king killed von Gudden and then
drowned himself, but this has not been proved (Blunt
1970).
Before the 1960s, many visual scientists believed that
binocular stereopsis arose from high-level cognitive pro­
cesses rather than from the conjunction o f visual inputs at
an early stage o f visual processing. This idea was motivated
by the belief that only higher mammals have stereoscopic
vision and by the observation that the 3 -D appearance o f
the world does not change appreciably when one eye is
closed. H elm holtz ( 1 8 9 3 , p. 2 6 2 ) wrote,
Wc therefore learn that two distinct sensations arc
transmitted from the eyes, and reach consciousness
at the same time and without coalcscing; that
accordingly the combination o f these two sensations
into a single perceptual picture o f the external world
is n ot produced by any anatomical mechanism o f
sensation, but by a mental act.
He realized that stereopsis depends on the registration
o f disparities but argued that,
the coincidence o f localization o f the corresponding
pictures received from the two eyes depends upon
the power o f measuring distances o f sight which we
gain by experience.
Tliis view stemmed from his empirical theory o f vision
and the associated theory of unconscious inference (Section
2.8). W undt (1 8 9 4 b , p. 2 0 9 ) , who had been H elm holtzs
assistant in Heidelberg, expressed the same opinion.
Sherrington ( 1 9 0 4 ), also, concludcd from his work on bin ­
ocular flicker that monocular images are processed inde­
pendently, and that the final synthesis is “mental."
R am on у Cajal ( 1 9 1 1 ) proposed that inputs from cor­
responding regions o f the two retinas converge on what he
called “isodynamic cells,” and that this mechanism forms
the basis of unified binocular vision. This idea received
experimental verification when Hubei and W iesel (1 9 5 9 ,
1 9 62 ) reported that pairs o f afferent fibers originating in
corresponding locations in the retinas o f the cat converge
on binocular cells in the visual cortex. They also reported
that the monocular receptive fields o f cells that feed into
each binocular cell occupy corresponding positions in the
two eyes and arc similarly tuned to orientation. If the m o n ­
ocular receptive fields feeding into each binocular cell had
identical structures and were identically positioned in each
eve, then all binocular cells would respond optimally to
stimuli with zero binocular disparity. Depth could not be
recovered from binocular information in such a system.
This was the gist o f H elm holtzs argument against the idea
of convergence ot visual inputs in the visual cortex.
The problem would be solved i f there were cells specifi­
cally tuned to similar images in slightly dilferent positions
in the two eyes. Different cells would be optimally tuned to
dillercnt disparities. Simple as this idea is, it was not p ro­
posed until 1965. This is probably because the idea o f any
cortical cell being tuned to a specific stimulus feature was
not in vogue until 1959, when Hubei and Wiesel discov­
ered cortical cells tuned to stimulus orientation and move­
ment. Hubei and W iesel tailed to find disparity-sensitive
cells. However, they did not have close control over the
positions o f the eyes, and it is n ot clear trom their report
whether they had thought o f binocular cells devoted to the
detection o f disparity.
Jack Pettigrew produced the first evidence o f disparity
detectors that occur at an early stage ot visual processing.
He did this work for his undergraduate thesis in the
University o f Sydney in 1965. He got the idea while inspect-
in g a ju lesz ran d o m -d o t stereogram and mentioned it to his
supervisor, Peter Bishop, who was working on binocular
cells in the cat visual cortex, but not with this particular
idea in mind. Bishop suggested to Pettigrew that he repeat
the experiments o f Hubcl and Wiesel on the visual cortex o f
the cat using a Risley prism to control the disparity o f the
images from a single display rather than using separate stim ­
uli for each eve.
i
The search for binocular cells selectively tuned to differ­
ent disparities was beset with the problem o f ensuring that
the images in the two eyes were in binocular register.
Pettigrew solved this problem by paralyzing the extraocular
eye muscles with gallamine and curare.
 Bishop cook Pettigrews thesis со a conference in
California in 1966 and showed ic со Horace Barlow, who
had j'usc set his graduate studenc, C olin Blakemorc, the cask
o f looking for disparity deceecors. Barlow invited Peccigrew
to work with him and Blakemorc at Berkeley. The three o f
them confirmed the presence o f disparity-sensitive cells in
the visual cortex ot the cat and reported their findings
in 196 7 (Barlow et al. 1967). They found that certain
binocular cells in the visual cortex ot the cat respond selec­
tively to line and bar stimuli having a particular binocular
disparity.
Similar findings, based on work done between 1965
and 1967, were reported about the same time from the
University o f Sydney, Australia, by Pettigrew, Nikara, and
Bishop (1 9 6 8 ). The history ot these discoveries is described
by Bishop and Pettigrew ( 1 9 8 6 ). In 1977, G ian Poggio and
his coworkers at Jo h n s Hopkins University in Baltimore
first reported disparity detectors in the primary visual Figure 2 .51 - Л shadow tb cattr in P aris in th e 1S90*. T h e show was designed
by M . C aran d/\che and often depicted b attle scenes. S o m e parts o f the
cortex ot the monkey. Later developments are described in
silh o u ettes con sisted o f colored paper. A ssistants m oved them a e r o » the
Chapter 11. screen. The au dience viewed them from the o th er side w hile the band
For a detailed history o f ophthalmology see Hirschberg p la y e d m u s ic . <Fr..mHoPkm« IS^R)

( 1 9 8 2 ). For more details on the history o f visual optics

and binocular vision see Lindberg ( 1 9 7 6 ), Polyak ( 1 9 5 7 ),
and G ulick and Lawson ( 1 9 7 6 ). Wade ( 1 9 8 7 ) has provided
an interesting account ot the discovery ot stereoscopic
vision.
2 .1 1 H IS T O R Y O F V IS U A L
D IS P L A Y S Y S T E M S
2 .1 1 .1 EA R L Y D IS P L A Y S Y S T E M S
2 . 1 1 . 1 a S h a d o w g ra p h s
More than a thousand years ago, starting with the Tang
dynasty, showmen traveled all over C h in a with shadow
plays. Shadows o f hand-operated flat puppets were cast
onto a screen ot fine paper or cloth to the accompaniment
o f music. The puppets often consisted o f thin colored paper
so that the projected images were also colored. The audi­
ence sat in a darkened room. Shadow plays spread to all
parts ot the Far East and can still be seen in Java. In Java and
India the shadow theater sometimes tormed part ot reli­
gious ceremonies or funerals (H erbert 2 0 0 0 , vol. 3).
In the 17th century, shadow plays reached Europe
through Turkey. They were displayed in palaces and at street
corners. In the 18th century there were at least four
large shadow theaters in London, one with a screen 14 feet
high. By the 19th century, wooden, hand-operated puppets
were replaced by mechanically operated metal puppets
(see Figure 2 .5 1 ). People could buy puppet kits to create
shadow plays in their own homes (Thurman and David
1978).
2 .1 1 .1 b C a m e r a O b s c u r a an d M a g ic L a n te r n
In the camera obscura an image ot a scene is projected
through a small hole or through a lens onto the wall o f a
darkened chamber. The camera obscura had its origin in the
pinhole camera that was known from ancient times. During
the 16th century, several people added a biconvex lens,
which allowed more light to enter the dark chamber. These
included Girolamo Cardano, protessor ot mathematics in
M ilan, and Daniele Barbaro, a Venetian architect, inventor
ot the variable diaphragm and author ot L a practica della
perspettiva ( 1 5 6 8 ). The instrument was used tor observing
solar eclipses and for popular amusement (see Hammond
1981). Della Porta (c. 1 5 3 5 - 1 6 1 5 ) was probably the firsc
person со use the instrument for drawing (Section 2.5.1).
Its use in drawing in perspective is described in Section
2.9.4. Kepler coined the name “ca m era o b scu ra ”
A panoramic camera obscura produces an image ot the
surroundings on a horizontal surface in the center o f a large
room. An operator rotates a mirror and lens mounted in a
cylinder on the ro o f tobringd ifferent parts o f the surround­
ing scenery into view. Panoramic instruments exist in
Edinburgh, Bristol, the Isle o f Man, and in the C liff House
in San Francisco. The one in the museum in Dumfries,
Scotland, was built in 1836. The oldest instrument in
Europe was built by the Viennese astronomer Miksa Hell
( 1 7 2 0 - 1 7 9 2 ) in the Lyceum in Eger, Hungary. Its cross sec­
tion is illustrated in Figure 2.52.
In the 17th century, these basic optical elements were
rearranged to produce the first projector— the magic lan­
tern. It seems that the first magic lantern was built by
Athanasius Kirchcr ( 1 6 0 1 - 1 6 8 0 ) , a Catholic priest. He was
 Rotatable cylinder 2 .1 1 .1 c P eep sh ow s

During the 18th and 19th centuries, viewing boxes became

a popular form o f entertainment throughout Europe, Japan,
and C hina. They became known as peepshows. Most
people, and especially children, have an almost irresistible
urge to see what is hidden inside a box. Showmen carried
peepshow boxes from town to town either on their backs or
on a cart. Balzcr ( 1 9 9 8 ) has published a fascinating collec­
tion o f paintings and prints o f peepshows, one o f which is
shown in Figure 2.53. Showmen attracted a crowd by ring­
ing a bell or blowing a trumpet and extolled the wonders o f
the views displayed in their peepshow. In the 17th and early
18th centuries most people did n ot move far from the vil­
lage in which they were born. M ost people were illiterate,
and in any case there were no public libraries or magazines.
Peepshow boxes usually contained several scenes o f exotic
foreign places or battles illuminated by light entering
Fif*r« M i. P an o ram ic cam era obscu ra in Eger, H ungary.
through chc back or top o f the box or by candles inside it.
The showman changed scenes by pulling on strings
protruding from rhe side o f the box or by turning a crank.
born in Germany and worked in Rome, where he published
Som e showmen enhanced their show with a live monkey, a
Ars M agna Liu is et Umbrae ( 7 be Great Art o f Light and
music box, o r puppets. Som e peepshows became known as
Shadows) in 1648. Painted transparent slides were rear-
Raree Shows because chey showed rare objects or scenes.
projected o n to a taffeta screen by a lens attached to a lan­
The boxes contained several viewing apertures so that
tern containing a candle. He placed several slides on the rim
several people could look ac che same cime. A person bend­
o f a disc. He was a showman and made the pictures grow,
ing over со view a peepshow prcscnccd a good cargcc
shrink, and dissolve and rccurn transformed into other
forms. The Dutch scientist Christiaan Huygens also co n ­
structed an early magic lantern.
Alter the discovery o f limelight at the end o f the 18th
century, magic lantern shows became a popular form of
public entertainment. Limelight was a brilliant flame pro­
duced by igniting jets o f oxygen and hydrogen on lime.
Before the advent o f photography, colored pictures were
painted on glass slides. After about 1850, black and white
photographic slides were hand painted with translucent
pigments. The superimposition of pictures from two pro­
jectors allowed one picture to be dissolved into another. A
rear-projected picture could be made to move or loom.
Mechanical slide holders allowed one part o f the picture to
move with respect to a fixed background (see C o e 1981;
H erb ert2 0 0 0 , vol. 2). In 1798 a show called Phantasmagoria
opened in a reputedly haunted chapel in Paris. Pictures o f
skeletons were projected onto billowing smoke to create an
impression o f solid writhing forms emerging from the
tombs o f the chapel. W illiam Nicholson ( 1 8 0 2 ) described a
Phantasmagoria presented by a Mr. Philipsthal at the
London Lyceum in 1802. Similar methods were used to
create ghosts on the theater stage (H opkins 1898).
Stories were created with sets o f slides accompanied by
spoken words. They often contained a moral message
(Household and Smith 1997). The magic lantern became
the modern projector. Operating in reverse with the addi­
tion o f light-sensitive film, it became the camera (Gcrnshcim I i*u « 1 .5 3 . A 1 9 tb * x'CJiturypccpfbow box. (Гохп $*rg<onc Bril and H i*fC jr«e Show, by

1969). Cruikth*ril;*.1>ininp4oft. W illiM ftt.published b j Т Ь л т м T<>$. Loudon IH ?J)

for pickpockets. The artist, Thomas Gainsborough, made a
peepshow box in about 1781 for which he painted pictures
on glass plates.
Viewing boxes with slides or short movie sequences
remained popular at seaside resorts until well into the 2 0th
century. M any o f them titillated viewers with naughty
sccnes, with names such as “W h a t the butler saw.” Today
they arc represented by the cinema, video games in amuse­
ment arcades, and television.
2 .1 1 .Id P a n o r a m a s an d D io r a m a s
Л panoramic display is one that is projected onto a large
cylinder that encircles the viewer. In 1787, Robert Barker
patented the idea of a panoramic display. The word “pan­
orama” came into the language in the 1890s, although it is
not known who first used it. Robert Baker built the first
panoramic display for large audiences in Edinburgh and
London in 1797. Viewers stood at the center of a cylinder,
13 meters in diameter, which was painted with a view o f
Edinburgh or London as seen from a tall building.
Panoramas were built in many European and American
cities during the 19th century. Examples are shown in
Figure 2.54. T he audience entered a central observation
platform from below, as shown in Figure 2.55. The
cylindrical canvas was illuminated by light from a window
round the r o o f o f the building o r from lamps suspended in
the building. Panoramas still exist in many parts of
the world.
Panoramas were designed to reproduce a scene so accu­
rately that viewers could believe they were looking at the
real thing. They were an extension o f the trompe loeil tech­
nique to fill the whole field o f view. The floor surrounding
the audience contained a display o f real objects that blended
into the 2 - D scene painted on the cylindrical canvas, as
shown in Figure 2.56. Artists painted the scene on a scries
o f flat canvases, which were then joined and formed into a
cylinder. This introduced some distortion o f perspective,
which could be avoided by use o f a camera lucida with a
curved ruler, a device invented by a Frenchman called
Gavard in 1830. A t a later time the panoramic scene was
made from a series o f photographs. Teams o f artists stand­
ing on a movable scaffold, as shown in Figure 2.56, trans­
ferred the preliminary paintings or photographs piece by
piece o n to the full-size canvas, which was typically 3 0 0 feet
long and 4 0 feet high. This was done by drawing square
grids on the painting and on the large canvas. A long
drawing instrument was used to transfer the image piece­
meal. Photographs could be converted into slides and pro­
jected o n to the large canvas. D ifferent artists specialized in
painting people, buildings, and landscape. The whole p ro­
cess took at least a year to complete. For a history o f the
panorama see Bapst ( 1 8 9 1 ) and the lovely book by
O etterm ann ( 1 9 9 7 ).
A diorama is a large display that typically fills much o f
the visual field but does not extend through 3 6 0 * . Louis
Daguerre, before he turned to photography, built the
Diorama in Paris in 1822. He and Charles Bouton painted
enormous pictures, 7 2 feet wide and 4 6 feet high, with
translucent and opaque paints with subjects such as The
Tomb o f Napoleon, Tl)e Beginning o f the Deluge, and Vje
Grand Cana! o f Venice. These were exhibited in a large room
with a mixture o f reflected and transmitted light controlled
by mirrors and shutters. In 18 2 3 , Jo h n Nash had a similar
structure built in Park Square, London. In both structures
up to 2 0 0 people sat on a circular platform, which rotated
periodically to reveal a different scene. The building still
exists, but nor the machinery. Dioramas created such real­
ism that audiences were convinced that they were observing
a 3-D scene.
Painted dioramas that fill the field o f view for viewers in
a given position are still used as backdrops to exhibits in
manv/ museums, such as the Natural HistoryU Museum o f
New York. In recent times, realistic 3 -D moving displays
have been created in wide-angle cinemas such as those
developed by the Imax Company.
The three-volume book A History o f Pre-Cinem a by
Herbert ( 2 0 0 0 ) contains a large collection o f original pub­
lications from magazines and journals that describe visual
display systems before the advent o f the cinema.
2 .1 1 .2 A D V EN T OF T H E S T E R E O S C O P E
2 . 1 1 .2 a E a rly D e v ic e s fo r D i c h o p t i c V ie w in g
It was explained earlier in this chapter how Ptolemy and
Alhazen com bined the images o f distinct objects by co n ­
verging on an object in another depth plane. In the 18th
century, Desaguliers ( 1 7 1 6 ) added the refinement o f view­
ing objects on the two visual axes through an aperture. This
removes the unwanted monocular images. Durour ( 1 7 6 0 )
removed unwanted monocular images by placing a board
between the eyes as they converged on two side-by-side dis­
plays. Reid ( 1 7 6 4 ) viewed distinct objects through two
tubes aligned with the two visual axes. They all used these
devices to study corresponding points, binocular disparity,
and binocular rivalry, but n o n e o f them realized that dis­
parities could create impressions o f depth.
The first binocular optical instrument was a twin tele­
scope built in Middleburg, Holland, by the optician Hans
Lippershcv in 1608. A Capuchin friar, Antonius Maria
Schyrleus de Rheita, was familiar with Lippersheys work
and built a binocular telescope in 1645. which he described
in his book Oculus Enoch a t Eliae, published in Antwerp in
1645.
'I he Capuchin m onk, Pere Cherubin d’Orleans, made a
binocular microscope in 1677 and presented it to the dau­
phin o f France. Chcrubin d’Orleans ( 1 6 7 1 ) also made a
binocular telescope in 1671. However, the images in these
 в
Fijmc2& . P anoram as. (A ) T h e first Parisian p an oram a b u ilt on the Boulevard M o n tm artre in 1 8 0 2 . {bum R»P*t ik h. in Oeiicmunn m ? )
(B ) P anoram a M arignv b u ilt on the C ham p s-E lv sees in Paris in 1 8 8 6 . It exh ib ited th e Battle o t Buzenval and later a D ioram a o f Paris. In ab ou t 1 8 9 3
it was con v erted in to the Th eatre M arignv, w h ich still exists. <Ff<un Oeitai.um. l99?)<Fr«m IHH6. inOctuimmn
f.5iiic2 .sv Cross section o f a p an oram a. People en tered «it A and passed through passage В up to the observ ation platform C . T h ey viewed the cylin drical
display, t , w ith a visual angle ind icated by D . T h e flo o r consisted o f a m o ck terrain th at blended in to the p an oram ic display. (F«.mОкшш»» IW )
F>*uic2 .*6 . P ain tin g.г pan oram a. The scene d ep icts the B a ttle o f
G etty sb u rg . It was ex h ib ited in N ew York at the end o f the 19th
century. (Fii'in I lop*.*, 1*98)
instruments were inverted, which reversed the sign o f dis­
parity and created a pseudostereoscopic effect. Riddell
( 1 8 5 3 ) added erecting eyepieces to a binocular microscope
to produce a true stereoscopic effect (see Wade 1981).
These instruments were not stereoscopes because the
stimuli were 3 -D objects. They were equivalent со looking
at the world through two tubes.
2 .1 1 .2 b W h e a tsto n e
The invention o f che scereoscope must be crediced со Sir
Charles W heacstone (Figure 2.57). He was born in 1 8 0 2 in
n t «rc S ir C harles W heatstone. (E n grav in g from a p hotograp h in the
U lu str.tted L o n d o n N ew s, 1 8 6 8 ,5 2 , p. 14 5 . R ep rod u ced by perm ission
o f the Illustrated L on d on N ew s P icture L ib rary)
che village ot Barnwood, near Gloucester, England. His
father, W illiam , was a shoemaker who owned a shop in
Gloucester, which is still there. W h en Charles was four
vears old the family moved to London, where his father
made musical instruments and gave lessons on the flute. His
pupils included Princcss Charlotte, the only daughter o f the
future King George IV. She would have succeeded to che
throne if she had n ot died in childbirth at an early age.
As a young man, Charles made and sold musical instru­
ments. He invented several musical instruments, including
the concertina. In 1823, Charles and his brother inherited
their uncles music business in the Strand, London. In the
same year, Charles began to write scientific papers on
acoustics. He became a triend ot Michael Faraday, who gave
lectures to the Roval
j Institution on W heatstones discover-
ies in acoustics. Wheatstone was shy and reluctant to give
lectures.
W heatstone later contributed to many fields, including
electricity, chronometry, optics, cryptography, and telegra­
phy, and invented many useful devices. In 184 3 he published
a description ot the W heatstone bridge tor measuring elec­
trical resistance, although he acknowledged that the bridge
had been devised by S. H. Christie. W heatston es inventions
are described and illustrated in Bowers ( 2 0 0 1 ). Many o f
them may be seen in the South Kensington Science Museum,
in London. In 1834 W h eatston e became professor o f exper­
imental physics at K in gs College, London. He retained this
position for 41 years. He died in Paris in 1875.
Toward the end o f 1832, W h eatston e had two stereo­
scopes made by Murray and Heath, opticians in London.
O n e was a mirror stereoscope, the other a prism stereoscope
(see Gernsheim 1969). M irror stereoscopes are still called
W heatstone stereoscopes. He then became involved with
the electric telegraph and waited until 1838 before report­
ing his mirror stereoscope and his experiments with
the instrument to the British Association in Ncwcastle-on-
Tyne in northeast England (W h eatsto n e 1838). However,
his colleague Herbert Mayo, professor o f anatomy and
physiology at King’s College, London, gave an account ot
W h ea tsto n es stereoscope in his Outlines o f Human
Physiology, which appeared in 1833.
W h eatston e called his new instruments stereoscopes.
Aguilonius had used the word “stereoscopique” in 1613 to
denote binocular vision, and J. G. A. Chevallicr had used
the word “stereoscope” to describe an instrument that
created an impression ot solid objects trom a variety ot
к$и>с2 .«&. W h e a t s to n e s first m ir r o r ste re o s c o p e . <F..mi w h e t* one 18 *S)
m onocular cues (sec Helm holtz, 1909, vol. 3, p. 3 6 3 ).
W h eatston e stated the principle o f the stereoscope thus.
It being thus established that the mind perceives an
object o f three dimensions by means o f the two dis­
similar pictures projected by it on the two retinas,
the following question occurs. W h a t would be the
visual effect o f simultaneously presenting to each
eye, instead ot the o b ject itself, its projection on a
plane surface as it appears to that eye? To pursue this
inquiry it is necessary that means should be
contrived to make the two pictures, which must
necessarily occupy different places, fall on similar
parts o f both eyes.
{ W H E A T S T O N E , 1838, p.
His mirror stereoscope consisted o f two mirrors at right
angles and two vertical picture holders (Figure 2 .5 8). In a
later version each half o f the instrument could be rotated
about a vertical axis centered under the eye. This changed
the angle o f convergence in the way still used in amblyo-
scopes. He described twenty pairs o f pictures, or stereo­
grams, that appeared three-dimensional when viewed in his
stereoscope. These included a scries o f points stepped in
depth, a cube, a cone, and a pyramid, as shown in Figure
2.59. He observed that all these shapes appeared flat when
the pictures in the two eyes were the same and appeared in
reverse depth when the pictures with disparity were reversed
to the two eyes.
James F.lliot, a mathematician in Edinburgh, had the
idea in 1834 o f constructing a stereoscope but did not co n ­
struct one until 1839. He was n ot aware of W h eatston es
work until 1852. Elliots stereoscope consisted o f a box
that allowed each eye to see one ot a pair o f stereographic
 /kf Jj /«Г/J
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F.fiirc 2.S9. W h e a tsto n e S stereogram s. (From P ('x !w p h c .< : ТУ.ап4хИ4Ш c f t h e R*yd S n i f f y , l&tt)

pictures. It contained no mirrors or lenses (see Elliot 1852). arms allowed him to vary convergence while keeping
Figure 2 .6 0 shows a modified version o f E liots stereoscope disparity constant, and thus show that impressions o f
made by Lockett (1 9 1 3 ). depth do not depend on disparity alone. The invention ot
The essence o f any stereoscope is that it allows one to the stereoscope inaugurated the modern study o f stereo­
control the image in each eye separately. An experimenter scopic vision.
can thus isolate binocular variables and study their effects In 1852, W h eatston e presented a paper to the Royal
quantitatively— it provides an experimenter with dichoptic Society. He described the pseudoscope, which reverses
control. W ith his new instrument, W h eatston e dem on ­ the inputs to the two eyes. This reverses the sign ot
strated the relationship between binocular disparity disparity and makes concave surfaces appear convex and
and depth perception. His stereoscope with adjustable vice versa. In a communication to the Microscopical Society,

F.Sorc2 .60 . E llio t’s slerc o seo p eo f I S3 9. M odified by L o c k e tt in 1 9 1 2 .
(F ro m L a d e n 1 9 1 »
W heatstone ( 1 8 5 3 ) described the binocular microscopes
made by Pere Cherubin d’Orleans in 1677 and by Riddell
in 1853.
2 .1 1 .2 c B re w ster
Sir David Brewster (Portrait Figure 2 .6 1 ) was born in
Jedburgh, Scotland, in 1781, the son o f the rector o f the
grammar school. He died in 1868. He wrote many papers
on optics, especially on the polarization o f light, and
invented the kaleidoscope. He was a scientific editor, the
Figarc2 .6 i. Sir David Brew ster.
college principal at St. Andrews University, and secretary
to the Royal Society o f Edinburgh. His statue is outside
the Chemistry Departm ent o f Edinburgh University.
A lenticular stereoscope can be seen protruding trom his
gown.
Brewster witnessed W h eatsto n es demonstration o f a
mirror stereoscope at the meeting of the British Association
in 1838. He bought a model with which he began his own
experiments. At a meeting o f the Royal Scottish Society of
Arts in Edinburgh in March 184 9 he described a stereo­
scope in which two side-bv-side pictures were placed in a
box and viewed through prisms made from h a lf lenses,
which fused and magnified the images. He described the
instrument in his book The Stereoscope, published in 1856.
Brewster made his first prism stereoscope by cutting a
convex lens in h a lf and arranging each h a lf with its vertical
cut edge on the temporal side of an eye. Figure 2 .6 2 shows
an early version. Mr. Loudon, an optician o f Dundee, made
prism stereoscopes for Brewster. Brewster sent several to
members o f the nobilitv.
j
Examples of early stereograms produced for the prism
stereoscope are shown in Figure 2.63. The prism,or lenticu­
lar, stereoscope is still referred to as the Brewster stereo­
scope, although W heatstone had made one in 1832, before
Brewster. The subsequent development o f stereoscopic
instruments in general is described in Chapter 24.
Brewster wrote an anonvmous / letter to the London
Times in O c to b e r 1856. He disputed W h eatsto n es claim to
have invented the stereoscope and to have discovered the
principle o f stereoscopic vision. W heatstone effectively
refuted Brewster and the two men engaged in an acrim oni­
ous correspondence in the Titnes. At a meeting o f the
Photographic Society o f Scotland in 1860, Brewster
attacked W h eatston e again. He claimed that Euclid in the
3rd century B C and Giovanni della Porta in the 16th
century had described the principle o f stereoscopic vision.
! inure 2 .62 . E arly Rrtruutcrprism stereoscope ( IS 6 2). A m irror in chc hinged
panel reflects lig h t o n to the stereogram .

Figure2.63. E arlyplrotographicsterw gran u . The upper stereogram is a
p h otog rap h o f the W h e a tsto n e family, taken by A n to in e C lau d et
probably in i lie m id -1 850%. (R ep rod u ced by pcrm i.w ion o f th e N ational
P o rtra it G a llery ) T h e low er stereogram s arc views o f th e G reat
E x h ib itio n o f 1851 in the C rystal Palace, L o n d o n . T h e stereogram s
should be viewed w ith a stereoscope o r w ith divergent fusion.
Brewster described the pair o f pictures shown in
Figure 2 .6 4 by the Florentine artist Jacopo C him cnti
( 1 5 5 4 - 1 6 1 4 ) . They are in the Musee W icar in Lille, France.
Brewster received a description o f the pictures in a letter
written by Alexander Crum Brown, professor o f chemistry
at Edinburgh, who saw them on a visit to Lille. C ru m Brown
claimed that the binocularly fused drawings create a 3 -D
picture.
Although Brewster had not seen the pictures, he pub­
lished a letter in the Photographic Journal, in which he
claimed that they were stereoscopic images (Brewster
I8 6 0 ) . W h eatston e obtained photographs o f the drawings
in I8 6 0 . He showed that they did not produce depth in
Figm 2.64 tw o draw ings by Ja co p o C him cn ti (7 5 5 4 1614). Brew ster claim ed
th a t the draw ings arc stereogram s.
a stereoscope. Brewster obtained photographs in 1862 and
wrote, “The full stereoscopic relief o f C h im cn tis pictures
was seen and acknowledged by all” (Brewster 1862).
F.dwin Emerson ( 1 8 6 4 ) o f Troy University made
detailed measurements of the C him cnti photographs and
showed that the differences between the drawings were
accidental and n o t related to binocular disparity. For lively
accounts o f this debate sec Wade and O n o ( 1 9 8 5 ), O n o and
Wade ( 1 9 8 5 ), and Wade ( 2 0 0 3 ). The works of W heatstone
and Brewster have been edited by Wade ( 1 9 8 3 ). Gill ( 1 9 6 9 )
described early stereoscopes.
In the 1850s, the science o f binocular vision boomed.
During this decade, the percentage o f papers in vision
devoted to binocular vision increased from about 19 to
30% . About 7 0 % o f these papers were written by Germans,
including W undt, Helmholtz, Hering, Dove, Panum, von
Graefe, Meissner, and Nagel (Turner 1993).
2 .1 1 .3 STEREO PH O TO G RA PH Y
Johann Schulze ( 1 6 8 7 - 1 7 4 4 ) , a German physician, pro­
duced the first photographic images in 1725. He did this by
shining light on cut-out letters placed on a bottle contain­
ing a mixture o f chalk and silver nitrate. Tom Wedgwood,
son o f the potter Josiah Wedgwood, produced images o f
botanical specimens on sensitized silver salts in 179 6 (see
Pollack 1 977). However, these men did not know how to
fix the images. Joseph Nicephore Niepce, Cardinal of
Amboise ( 1 7 6 5 - 1 8 3 3 ) , produced the first photograph in
about 1826, and Louis Daguerre produced his first
successful daguerreotype photograph in 1837 (Portrait
Figure 2 .6 5 ). Figure 2 .6 6 shows the first American patent
for a camera registered to Alexander W olcott, dated 1840
(see Schimmelman 2 0 0 2 ) . The principle o f making a trans­
parent negative from which positives can be produced was
introduced by che Englishman Fox Talbot in 1840 (see
Arnold 1977).
 Louis Daguerre
Jn rtrtZ o r

I .*•>«* 1 .66. F irst A m erican p a ten tfo r a cam era. T h e image is produced by a
con cave m irror.

W h eatston e realized that two photographs taken from

different positions would appear three-dimensional when
viewed in a stereoscope. In 1840, he asked T albot to take
stereo photographs, but the camera separation was too large
to produce the appropriate binocular disparities (Klooswijk
1991). In 1841, W h eatston e employed two photographers,
Richard Beard and Henry C.ollcn, to help him produce the
first effective stereophotograph, which was a portrait o f
Fox Talbot Charles Babbage, the inventor o f the first calculatingcnginc.
The following year, the Parisian photographer Antoine
Claudct produced daguerreotype stereophotographs tor
W heatstone, but these were not satisfactory because o f the
reflective surface ot the prints.
The first stereophotographs were taken by moving a
single camera through the interocular distance. Because
early film required long exposures, the subject had to be sta­
tionary for a long period. For example, W h eatston e’s young­
est child had difficulty sitting still, as evidenced by her
blurred image in Figure 2.63a.
In 1853, the Parisian photographer A. Q u in c t made the
first stereocamera, which he called the Quinetoscope.
Figure 2 .6 7 shows a patent for a stereocamera by Silas A.
Holmes o f New York in 1854. In 1856, J. B. Dancer inde­
pendently made a stereocamera in Manchester, F.ngland. It
is illustrated in Figure 2.6 8Л .
Nicephore Niepce
In 1896, the French company Jules Richard produced
KiSo i c P i o n e e r s o t photography. the “ Verascope.” This was the first mass-produced stereo

7fitnrjJAX,
Z/ue/i&s
* -
Fifiur 2.6 ?. Stcrco ca m cra p atented by S . A . H o lm es in 1 8 5 4 .
camera. Kodak introduced their stereo camera in 1901.
These stereo cameras consisted o f two cameras side-by-side.
In 1853, F. Barnard produced an attachment, known as the
stereo reflector (Figure 2 .6 9 ) that converted a single-lens
camera into a stereo camcra. The left-eye and right-eye views
are reflected so that they project through the same lens and
fall on opposite halves o f the film. In the Leitz stereo attach­
ment, prisms replaced the mirrors. The attachment for the
C o n tax camcra contains a reflecting system and two minia­
ture lenses. The normal lens is replaced by the attachment.
The distance between the reflecting system and the lens for
proper separation o f the images is proportional to the lens
aperture and inversely proportional to the tangent o f the
angular field o f the lens.
Further developments in stereophotography
described in Maude (1 9 7 8 ).
By 1846, stereophotographs were being sold in James
Newmans shop in Soho Square, London. However, stcrco-
photography did n ot arouse much interest because stereo­
scopes were expensive. Brewster took his prism stereoscope
to Paris in 185 0 and engaged the optician Jules D uboscq to
built a number o f them, together with a set o f daguerreo­
type stereophotographs. These stereoscopes were shown in
London at the Great Exhibition o t 1851. O n e was made
for Q ueen Victoria who took a great interest in the device.
She was amused! W ith in three months, nearly a quarter o f
a million prism stereoscopes were sold in London and Paris.
Stereoscopic views o f the G reat Exhibition o f 1851, such as
those in Figure 2 .6 3 , were popular because people who
could not get to London were able to sec the exhibits.
Duboscq patented the prism stereoscope in 1852, but
the patent was successfully challenged and annulled in
1857. Claudet devoted him self to the improvement o f ste­
reoscopic photography. He patented a folding version ot
the prism stereoscope on 22 March 1853. This was the first
British patent for a stereoscopic device.
Figure 2 .7 0 shows a pocket stereoscope patented in
America on 8 M arch 185 3 by Jo h n F. Mascher ot
Philadelphia. Mascher also patented the miniature stereo­
scope shown in Figure 2.71. A rotary stereoscope holding
50 or 100 views was made in England in 1854. Figure 2.72
is an 1857 American patent tor a device ot this kind.
Stereoscopes made for the wealthy became very elabo­
rate. Examples are shown in Figure 2.73, including a mirror
stereoscope built in 1856 and a prism stereoscope o f 1862.
In 1854, George Swan Nottage, a man o f humble origin
and limited education, founded the London Stereoscopic
Com pany with the m otto “N o hom e without a stereo­
scope.” By 1858 the company had sold over half a million
stereoscopes and its traveling photographers had produced
V
100,0 00 stereoscopic photographs o f famous places from
many parts o f the world. Nottage became Lord Mayor o f
London and died in 1885, a wealthy and honored man.
Stereoscopic photography was introduced into the United
States in 1854 by W illiam and Frederick Langenhcim. They
founded the American Stereoscopic C om pany in New York
in 1861.
The idea for stereoscopic book illustrations was pat­
ented by P. B. (io d e t in 1857. The first book illustrated with
stereoscopic photographs was Charles Sm yths account o f
Tenerife, published in 1858. Another early book entitled
Stereoscopic Vietcs am ong the Hills o f New Ham pshire was
published by the Bierstadt Brothers o f New Bedford,
Massachusetts, in 1862. Viewing stereograms in a book
requires an open type ot stereoscope, which can be placed
on the surface o f the book. Joh n Parker ( 1 8 5 8 ) described a
pair o f prisms with a partition extending from the bridge ot
the nose to the stereogram, like the one included with
Volume 2 o f this book. In the same m onth, J. B. Spencer
are (1 8 5 8 ) described a similar stereoscope for use with books.
In 185 9 a Mr. Bennett o f London described the
“Clairvoyant Stereoscope,” which was an open-sided hand­
held prism stereoscope with a sliding picture holder. Joseph
Beck ( i 8 6 0 ) patented an improved version in September
1859. Oliver Wendell Holmes, essayist and Harvard profes­
sor o t medicine, designed a similar handheld version ot the
prism stereoscope in 1863. In 1864, his friend Joseph Bates,
added a sliding picture holder. The instrument was mass-
produced for home entertainment in America and
Europe. It is readily available in antique shops, and is still
iif.urc 2.м llarlv stereoscop ic dcviccs. (Л ) Stereoscop ic cam era by J . B. D an ccr. 1 8 5 6 . (B ) A stcrcosco p ic cam cra by Lucicn B u ll. 1 9 0 3 . ( C ) Edison's
K in eto sco p e, 1 8 9 4 . ( D ) Ives K rom skop. lh rc c stcreop ositives w ith red, green, and blue filters co m b in ed to produce a co lo red stereoscop ic pictu re.
(S o u th K en sin g ton Scien ce M useum . Scien ce and S o ciety P icture Library}

manufactured. W endell Holmes (1 8 5 9 ) wrote three enthu­
siastic articles in the Atlantic Monthly about stereoscopic
pictures. He wrote,
The time will com e when a man who wishes to see
any object, natural o r artificial, will go to the
Imperial, National, or City Stereographic library
and call tor its skin or form, as he would for a book
at any com m on library, (p. 3)
The Oliver Wendell Holmes Stereoscopic Research
Library is maintained by the National Stereoscopic
Association. The association publishes the bimonthly mag­
azine Stereo World ( www.stereoview.org).
In 186 2 Henry Swan (1 8 6 3 ) patented stereoscopic m in­
iatures, which became known as “Swan cubes.” Transparent
positives were mounted on two small prisms so that they
created a 3-D image when viewed from the correct posi­
tion.
Ives built the device shown in Figure 2 .6 8 D for produc­
ing colored stereoscopic pictures. Three pairs o f pictures
taken through red, green, and blue filters were viewed in a
stereoscope containing rhe same three filters.
By 1862, more than a thousand professional photogra­
phers were producing stereoscopic photographs, which
were sold by the million. The Keystone View Company of
America acquired its main rival, Underwood and
Underwood, and dominated the market. Until the advent
 R ight-eye Left-eye
view view IT

F.guie 2.69. I b c stereo rcfltitor. A system o f m irro rs attach ed to a single lens

cam era con v erts it in to a stereo cam era in w hich the left-eye and right- I
eye views arc p ro jected to op p osite halves o f the film .

o f chc cinema, chc sccrcoscopc was the optical wonder o f

the age. Ic allowed people to see the world in 3 -D in the
co m fo rt o f their own living rooms (sec Earle 1979).
In 1880 the physicist August Fuhrmann opened the
Kaiser Panorama on the Untcr den Linden in Berlin. It
remained open until 1939. A 5-mccer diameter cylinder i:i*mrc2.7o. P o ck ct stcrcosco p c patent by J. I:. M asch cr, 1 8 5 3 .
housed 25 viewing stations, as shown in Figure 2.74.
Stereoscopic slides rotated past the viewing stations at
intervals o f a few minutes. Many photographers were there was a resurgence o f interest in stereoscopy with the
employed to collect photographs o f exotic places and advent o f the random-dot autostereogram, described in
headline-making events. Ac one cime chere were 2 5 0 Section 2 4 . 1.6.See Judge ( 1 9 5 0 ),D a r r a h (1 9 6 4 ),G e r n sh e im
Kaiser stereoscopic panoramas throughout Germany, The ( 1 9 6 9 ), and Morgan and Symmes ( 1 9 8 2 ) tor more details
German kaiser, the sultan o f Turkey, and the pope had on the history and methods o f stereoscopic photography.
copies o f the photographs for private viewing. Several thou­
sand o f these stereoscopic pictures were published in
2 .1 1 .4 S T E R E O S C O P IC M O V IE S
1915 in a book entitled Goldenes Rtich der 7entrale fu r
K aiser pun or am en . Joseph Plateau ( 1 8 0 1 - 1 8 8 3 ) was a Belgian scientist best
Stereoscopic peep shows lost their wide appeal when known in visual science for the Talbot-Plateau law and the
illustrated magazines becam e widely available. In 1992, Plateau spiral aftereffect. In his doctoral dissertation at the

Я Г * # .*

Figure 2.71. M in ia tu re stcrcosco p c p a ten t by J. F. M aschcr.

 Л / 7

Fijere г.гу M u lti-im ag e stereoscope p aten t by Л . B cckcrs.

Fijpr« 1.73. Early dom estic Stcrcoscopc*. (Sm.ih К*п*.п|;».--> Some* Miiuum So#n«
*nd Society pirturr Library)

Fitmc 2 ."». W }eК л Ь сг Рлпоглт а. Tw enty*five people view ed 5 0 stereoscop ic slides th at changed p osition every few m in u tes inside the 1 5 -fo o t
d iam eter cylinder. ( Ь т О с и п ш ^ п 1 9 9 7 )
University o f Liege in 182 9 he observed that continuous
motion can be created trom a series o f intermittently viewed
objects. Michael Faraday ( 1 8 3 1 , p. 2 1 0 ) made similar obser­
vations using superimposed toothed wheels rotating in
opposite directions. O n the basis o f these stroboscopic
effects, Plateau developed the “phenakistiscope* in 1833. It
consisted ot a disc with slits around the rim and a series o f
pictures in a ring concentric with rhe slits. The rotating disc
was held in front o f a mirror, and the observer looked with
one eye through the passing slits at rhe pictures reflected in
the mirror. A picture trom the moving sequence appeared
each time a slot passed before the eye. The intermittent
sequence o f pictures appeared as a single moving picture. At
the same time, Simon Stampfer independently developed a
similar device in Vienna.
A device that became known as the “zoetrope” was
invented by W illiam Horner ( 1 7 8 9 - 1 8 3 7 ) in Bristol in
about 1834. A series o f pictures was placed on the inside o f
a rotating cylinder and viewed through a sequence ot slits in
the opposite wall o f the cylinder. Several people sitting
round the cylinder could view this device at the same time.
In 1853, Baron Uchatius mounted a rotating picture disc
and sectored shutter on a magic lantern to create moving
images. See Deslandes ( 1 9 6 6 ) and C o e ( 1 9 8 1 ) for accounts
o f the history o f cine photography.
In 1849, Plateau proposed that a binocular phcnakisti-
scope would produce 3-D moving images, an idea he cred­
ited to W heatstone. However, there is no record o t this
(b ) S tereo p ee p sh ow .
b y W illia m Shaw in 1860.
ti£urc2 .7 $. Early d cv iccs for prod ucing m ovin g stereoscop ic images.
device having been made. In a letter to the journal L a
Iwniere in 1852, Antoine Claudet described how he had
constructed a stereoscope in which one sees moving images
and wrote that W heatstone was attempting to construct a
similar instrument. Although he announced that a full
description o f these instruments would be published, the
publication never materialized (sec Gcrnshcim 1969 and
Gosser 1977). It fell to rhe Parisian optician Jules Duboscq
to patent the first stereo moving picture device in 1852
(Duboscq 1857). He called it rhe “stereofantascope.” ltc o n -
sisted ot Plateaus phenakistoscope and two mirrors, which
stereoscopically com bined 12 pairs o f photographs, with
each pair placed along the radius o f a revolving disc. The
radial arrangement introduced some distortion because
the pictures tor the two eyes moved at different velocities.
The followingycar Claudet (1 8 6 5 ) took out a British patent
tor a similar device involving a prism stereoscope rather than
a mirror stereoscope (see Gosser 1977). Czermak made a
similar instrument in 1855 (H elm holtz 1910, p. 357).
In 1859, Henri D u M o n t, a French civil engineer, pat­
ented a series o f instruments tor showing moving stereo­
scopic images. In the version shown in Figure 2.75a pictures
arc placed on the outside o f two drums and viewed through
mirrors and slits in discs, which rotated with the drums. In
early I8 6 0 , W illiam Shaw, in Middlesex, England, co m ­
bined a zoetrope with a mirror stereoscope and with a prism
stereoscope to produce a moving stereoscopic peep show
(Shaw 1861). In the version shown in Figure 2.7 5b the pairs
(c) Kinem Moscopo.
Patented b y Sellers in 1861
o f pictures were mounted on chc sides o f a rotating occago-
nal drum and viewed through cone-shaped apercures in a
rocating cylinder so chat vision was cut ouc between pic­
tures. O n e o f his displays was o f a moving train. He called
this instrument chc “sccrcotropc" and showed ic ac the
Incernational Exhibition o f 1862. In February o f I8 6 0 ,
Pierre H . Dcsvignes from Lewisham, Kent, patented a
similar device and also used a train as one o f his pictures. He
proposed che use o f intcrmicccnc illumination со overcome
the problem o f image blur, buc there is no record o f his
having built such a device.
Coleman Sellers ( 1 8 2 7 - 1 9 0 7 ) , an American engineer,
com bined a vertical zoetrope with a prism stereoscope in
1861, со make a stereoscopic peep show called chc “kinema-
toscope” (Figure 2 .7 5 c). This was an advance on earlier
devices because, instead o f lining a cylinder, the cards c o n ­
taining the pictures radiated out from a central shaft so that
their motion was along the line ofsighc rather than orthog­
onal to it. This reduced image blur. The cards came into
view one ac a cime as che shaft rotaced. Ac chc same cimc, an
oucer cvlinder
/ with a series o f slots rotated between the
cards and the stereo viewer, so chac vision was blanked out
between cards. Sellers built only one model, which he kept
at home as a toy (sec Gosscr 1977).
In about 1870, W heatstone, also, constructed a stereo
zoetrope wich pictures arranged round the inside o f a rotat-
ing cylinder. He added a pawl device, which moved the cyl­
inder intermittently so that it was stationary when each pair
o f pictures was seen. H e was noc the first to use this impor­
tant principle. He did not use a shutter system to interrupt
viewing between pictures (see Gosser 1977).
Interest in stereoscopic moving images lapsed in the
period after 18 7 0 , when modern cinematography was being
developed. Eadweard Muybridge began his career as a p h o ­
tographer o f stereoscopic views o f N o rth America. During
che 1870s he developed a chronophocographic sysccm for
recording animals in mocion (Muybridge 1899). Ic involved
an array of 4 0 cameras, which were triggered in sequence
along chc path o f m otion. The resulting sequence o f images
is whac is required tor cinephocography. He mounted the
sequence o f photographs round the rim o f a wheel and pro­
jected them with a magic lantern to produce a brief moving
image. Hut the moving display lasted only abouc one second.
He attempted to make stereo versions ot these pictures.
Rcicnnc Marcy made a chronophocography sysccm using a
single camera in which a sequence ot piccures could be caken
in quick succession on a rotating glass plate. He used two
cameras rather than 4 0 to produce moving stereoscopic
images (Marcy 1895). But his use o f a glass plate severely
limited the duration o f che projected picture. The develop-
menc ot flexible film was che key to further success.
Louis Le Prince, a Frenchman living in Leeds, England,
seems to have been the first to use flexible film that moved
intermittently to produce moving projected piccures (see
C o e 1981). He pacenced his device in Leeds in 1888.
In 1890, Frederick Varley, a civil engineer in London, work­
ing with phocographer W illiam Friese-Greene, patented
the first stereo cine camera using a roll o f celluloid film
(Varley 1890). The unperforated Eastman film was about
17 cm wide and 7 yards long with at most five exposures per
second. This low exposure lrcquency severely limited the
quality o f the moving image. Furthermore, the machine was
not suitable for commercial exploitation. In 1903 Lucien
Bull built the high-speed stereo camera shown in Figure
2 .6 8 B . A rotating drum triggered a series o f flashes.
The first working cine projector was developed by Louis
and Auguste Lumicrc. They obtained celluloid film from
Eastman and coated it in their own factory in Lyons. They
opened the worlds firsc movie house in Paris in D ecem ber
1895. The first film showed them feeding a baby. Many
ocher invencors were involved in chc macuracion ofcin cp h *
otography into its present form.
Edison patented a stereoscopic version o f che kineto-
scope, buc chcre is no record that it was built. In 1903,
Auguste and Louis Lumicrc exhibited, in France, an
anaglyph stereo movie entitled Larrivee du train. It lasted
onlv a few seconds. In 1915, the Famous Plavers Film
i 4
Com pany (later the Paramount Picture Corporation)
released three short anaglyph stereo films produced by the
cinem a pioneer Edwin Porter (Hayes 1989). However,
there seems to be no record o f where these films were
shown.
Harry K. Fairall produced the first commercially suc­
cessful stereo movie The Power ofL ov e , which opened at the
Ambassador Hotel Theater in Los Angeles in September
1922. In the same year, Educational Pictures released a
group o f short stereo films called Plastigratm. They were
made by Jacob Levenchal and Frederick Ives and shown in
New York. Also in 1922, W illiam Van Doren Kelley exhib-
iced his shore movie Plasticon at the Rivoli Theater in New
York (Kelley 1 924). In 19 3 5 , Mecro-Goldwyn-Mayer
released a series o f shore stereo movies called Attdioscopiks.
These were che first stereo movies with sound (Norling
1939). All these movies used color anaglyphs. This mcchod
does n ot allow che use o f color in the film.
In 1935 F.dwin Land demonstrated a stereo film in color
using the polaroid method of separating the images. A t the
New York World Fair in 1939 the Polaroid C om pany exh ib­
ited In Time u ith Tomotrow , a 12-minute 3 -D film ot a
Chrysler car assembling itself. The Zeiss-1 kon C om pany o f
Germany developed this process in the 1930s. It was used
by Raymond and Nigel Spottiswoodc, who produced the
first stereo film in full color and wich stereo sound for che
1951 Festival o f Bricain in London.
In 1922, Laurens Hammond and W illiam F. Cassidy o f
che Teleview Corporation demonscraced a short science fic­
tion film called Radio M ania at che Selwyn Theater in New
York. This film used che "Teleview” sysccm, in which altcr-
nating left- and right-eye views o f a movie were projected on
a large screen. Each member ot the audience viewed the
screen chrough a rotating shuccer synchronized wich chc
alcernacion o f chc images on chc screen. In a modern version
o f chis sysccm, used by chc Imax Company ofToronco, m em ­
bers o f che audience view alcernacingpiccures on a wide-angle
screen chrough eleccricallyoperaccd liquid-cryscal shucccrs.
In Russia in the 1940s, Semyon Pavlovich developed a
scereo cinema syscem using a parallax gracing. The sysccm
used 3 0 ,0 0 0 silver wires, weighing six cons, suspended in
front o f che screen. Ic did noc require che use of viewing
glasses, buc had several drawbacks, including darkening o f
che image, image diffraction, and dependence on viewing
position. Also in che 1940s, Professor Noaillon o f Belgium
developed a radial converging grill with wide slits, which
were rendered invisible by a rapid oscillation o f chc grill in
its own plane. Stereoscopic pictures were projecced through
chc grill onco a screen so chac a m ember o f chc audience saw
alcernace strips ot each picture presented to the two eyes.
The Frenchman Francois Savoye patented a similar system
in 1942. Jennings and Vanet ( 1 9 5 2 ) developed a version o f
this system in which an inclined cylinder o f black bars and
slits, tapered trom top to bo ttom , rotated rapidly about its
central axis. Alternating left- and right-eye vertical strips o f
two stereoscopic images were projected chrough chc slits
onco a screen inside the cylinder. The tapered cylinder pro­
jected a scries o f radiating zones into the audience area. All
viewers in this area saw the alternating images correctly. The
rotation speed o f the cylinder was set to avoid stroboscopic
effects between the grill and the projector. A small system
called the cyclostcreoscope was made for home use by
A. Mattey o f Paris (Blum 1983).
Projection systems using lenticular screens have been
used for stereo cinematic projection, but screens for large
pictures are expensive, and several projectors are required.
T he construction and projection o f lenticular-sheet stereo­
grams are described in Section 24.1.3b.
There was a boom in stereo films based on the use o f
polaroid glasses in the 1950s and again in the early 1980s.
The recent Imax 3 - D films, based on the shutter system,
have been very popular. Stereoscopic television and video
films have not been successful. Recent developments are
described in Section 24.2.6.
This completes this historical review. Historical back­
grounds to particular topics will appear in various parts ot
the book.
 3

P S Y C H O P H Y S I C S AND ANALYSIS

3.1 Psychophysics 92 3.2.6 Signal analysis 109

3.1.1 Psychophysical methods 92 3.3 Linear control theoryв 110
3.1.2 Dctcciion 100 3.4 Analysis o f nonlinear systems Hi
3.1.3 Resolution 100 3.5 Tim e series IN
3.1.4 Discrimination Ю1 3.6 Bayesian inference 116
3.1.5 Temporal thresholds №1 3.7 Concepts o f geometry IIS
3.2 Analysis ot linear systems 104 3.7.1 Symmetry and groups IIS
3.2.1 Nature o f linear systems
* 104 3.7.2 Types o f geometry 1 1 $
3.2.2 Fourier analysis 105 3.7.3 Non-Euclidcan geometries 124
3.2.3 Transfer functions 106 3.7.4 Analytic geometry /25
3.2.4 Point-spread and line-spread functions 10S 3.7.5 Differential geometry 127
3.2.5 The contrast sensitivity function iOX

3 .1 P S Y C H O P H Y S IC S Defined displays o f random dots have been used to investi­

gate the effects o f binocular disparity on the perception
o f motion-in-depth (Section 3 1 .3 ). O n the other hand,
3 .1 .1 P S Y C H O P H Y S IC A L M E T H O D S
a stimulus domain might be a set o f natural objects such as
3 . 1 . 1 a B asic Terms human faces.
An experimenter with an incomplete or incorrect
Traditionally, psychophysics is the quantitative study o f
knowledge o f a stimulus domain from which stimuli are
how people o r animals detect, resolve, discriminate, iden­
drawn produces incorrect data and false theories. An
tify, or categorize defined stimuli. This section provides
observer who responds to stimulus features outside the
only a brief outline ot psychophysics, with an emphasis on
stimulus domain o f interest to an experimenter produces
those methods used in the study o f depth perception.
misleading data.
Psychophysics was established with the publication o f
A response dom ain is the set o f measured responses
Fechner s Elcmente der Psychopbysik in I8 6 0 . For fuller
evoked by defined stimuli. There arc four main types o f
accounts see Guilford ( 1 9 5 4 ) , Torgcrson ( 1 9 5 8 ) , Swets
response.
( 1 9 6 4 ), Green and Swets ( 1 9 6 6 ) , Carterette and Friedman
(1 9 7 4 ), Falmagnc (1 9 85 ), and Gescheider (1997). Computer
1. Performance o f a psychophysical ta*k The basic
programs have been developed for designing stimuli for
psychophysical tasks arc detection, resolution,
psychophysical experiments (Brainard 1997; Pelli 1997).
discrimination, categorization, identification, and
A stimulus dom ain is a defined set o f stimuli from
description. These tasks are defined later in this section.
which stimuli used in an experiment are drawn. It is a set ot
Performance may be indicated by a verbal response,
objects or events with defined features and selected values
which can range from a simple “yes” or “no” to a
o f those features. It may also contain rules o f composition
description o f a sensory experience. Otherwise,
and transformation o f those features and values. A defined
performance may be indicated by a physical response
stimulus domain is used to investigate some property ot a
such as pressing a key, an adjustment o f a stimulus, or
sensory or perceptual system.
sorting stimulus objects. In animals and preverbal
Stimuli mav4 be constructed in the laboratory.
i For exam- infants, responses consist o f such things as a
pie, Stiles ( 1 9 7 8 ) used two 10" patches illuminated with
change in gaze direction, pointing, or a conditioned
light o f various luminances and wavelengths to establish
response.
the standard observer for color discrimination. Defined
sets ot shapes viewed at various inclinations in depth have 2. Speed * accuracy, or precision o fa motor response This
been used to investigate shape constancy (Section 29.4). could be a simple reaction time to a stimulus onset.
 O r ic could be chc accuracy or precision o f pointing со
or tracking a stimulus.
3- Involuntary reflex The response may be an involuntary
reflex such as pupil dilation, eye accomm odation, or
optokinetic nystagmus. These responses require no
prior training and few instructions.
4. N euronal activity The response may be the activity o f a
neuron or a group o f neurons in response to defined
stimuli.
Behavioral responses to defined stimuli may be corre­
lated with neural responses within the sense organ or within
the brain (Ju n g 1961). For example, the psychophysical!)'
determined contrast-scnsitivity function may be related to
responses o f retinal ganglion cells.
The basic p ara m eters o f p erfo rm a n ce on any task
involving a response to a stimulus are accuracy, precision,
magnitude, sign (e.g., near-far, move left:-move righc),
and speed. In a simple psychophysical task, the basic param­
eters are accuracy and precision. Take the task o f setting
one object (the variable) to appear at the same distance
as an o b ject at a fixed distance (the standard). The p o in t
o f o b jectiv e equality ( P O E ) is the objective distance
o f the standard, Each setting o f the variable indicates
the distance o f the variable from the P O E , signed positive
when the standard is beyond the standard and negative
when it is nearer than the standard. The p o in t o f subjective
eq u ality (P S E ) is the signed mean o f a scries o f settings.
A ccu racy is the signed difference between the P O E and
the PSE. Accuracy is synonymous with co n sta n t error
and bias.
After the P S E has been determined, the unsigned dis­
tance o f each setting from the PSF. is calculated to yield a set
o f deviation scores. Precision is indicated by the mean o f
the unsigned deviation scores. Precision may also be indi­
cated by the variance, given by the mean o f the squared
deviation scores, or by the standard deviation, given by the
square root o f the variance. Precision is synonymous with
sensitivity, variability, and variable error.
The term ’ accuracy” is often used where “precision” is
mcanc. Precision is also often used inappropriately со sig­
nify the mean o f unsigned deviation scores with respect to
rhe P O E . This measure confounds accuracy and precision,
and should be avoided. Accuracy and precision are inde­
pendent, or orthogonal, measures.
In assessing human performance on a detection or dis­
crimination task, it is useful to have some measure o f the
theoretical limit that can be reached by an ideal detector.
A detector that performs at chc theoretical limit is known
as an ideal observ er for that task. For instance, it is possible
to calculate the performance o f an ideal observer for the
detection o f a spot o f light, given the number o f light quanta
in the signal and the “noise" within which the signal is
presented (Barlow et al. 1971). The ideal observer for a
particular task provides a yardstick for assessing the perfor­
mance o f a human observer on the same task. An ideal
observer for stereopsis is described in Section 18.3.5.
In a class A psychophysical p roced u re the subject is
presented with a discontinuity such as a luminance bound­
ary in a bipartite field or an olfset between to lines (vernier
stimulus) (Brindley 1970). The subject adjuscs chc stimulus
until the discontinuity is no longer detectable. At the end
point, the two halves o f the stimuli arc indistinguishable in
every way. It is assumed that, under these circumstances, the
signals arising in the sense organ from the two halves o f the
stimuli are identical. Even though the sensory signals arc
identical, the stimuli producing them may not be physically
identical. For example, two patches may perfectly match in
color and generate identical signals in the eye but have very
different wavelength compositions. This is metamerism
(Section 4.2.7).
Brindley stated that, when identical signals are sent to
the brain, the sensations they produce are indistinguishable.
This is known as the psychophysical lin k in g hypothesis.
In practice, it is difficult to determine whether two signals
arc identical (Boynton and O n Icy 1962). It is logically pos­
sible for a difference between two signals in a sense organ to
be lost at a higher level. For example, there is some evidence
that foveal stimuli are detected more rapidly than periph­
eral stimuli but chat the difference is compensated for at a
higher level.
A class A procedure removes virtually all ambiguity from
the task because the subject performs like a null-reading
instrument. A well-administered Class A psychophysical
experiment is the most sensitive measure we have for reveal­
ing what is detected, resolved, or discriminated. Under the
m ost favorable circumstances, sensory thresholds are near
the theoretical limit o f efficiency defined by the ideal
observer.
W h en we say an o b ject is detected or that two stimuli
arc resolved or discriminaced, wc say noching abouc whac
subjcccs experience, ocher chan chat they experience a dis­
continuity. W c do not calk abouc sensory “qualia,” such as
red patches and che like. We firsc use an inscrumcnc со mea­
sure defined stimuli by a scandard procedure o f known
accuracy and precision, which we call che physical measure.
For example, wc measure chc phocomecric luminance o f
stimuli relative to a physically defined standard. We then
map the physical measurements o n to the probability that
an observer detects each of a set of stimuli.
If wc have no instrument finer than a given sensory
system, we can n ot measure the sensitivity o f that sensory
system. For example, people who tcsc wool quality by couch
or tea or wine by caste outperform all instruments so that it
is not possible to measure what they are doing in terms o f an
ideal observer. O n e can measure only cheir repeat consis­
tency and consistency across testers. We can also compare
precision measured under one condition with that mea­
sured under another condition. W ith o u t some independent
measure we cannot compare accuracies. Som e sensations,
such as pain, have no quantifiable stimulus so that questions
o f precision and accuracy do nor arise.
In a class В p ro ced u re the subject matches or compares
two things with respect to some defined feature, while the
things dilier in some other feature. For instance, an observer
who adjusts the lengths ot the two halves o f the Miillcr-I.yer
illusion to appear equal is performing in a class B experi­
ment. It is class В because, after the lines have been matched,
the two halves o f the figure still differ with respect to the
arrows on their ends. In class В experiments it may be
difficult to be sure which aspect o f the stimuli the subject
is responding to. The literature can be contused, with a
welter o f conflicting theories and contradictory evidence.
Examples are provided by the literature on the m oon illu­
sion (Section 2 9 .3 .5 ) and shape constancy (Section 29.4).
Som e ot this contusion is due to the tendency to regard
a perceptual phenom enon as due to a single process at one
level in the system. For example, the apparent motion o f a
stationary o b ject seen against a moving background is
known as induced m otion. But the effect can arise from
processes in at least three levels in the nervous system
(Section 2 2 .7 ). The topic o f levels o f perceptual processing
is dealt with in Harris and Jenkin (2 0 0 2 ).
The assumption that one can tap a particular process
has worked well in class Л experiments. For instance, wc
have the beautiful coincidence between the psychophysical
spectral sensitivity curve and the physically determined
absorption characteristics o f extracted visual pigment. As
soon as subjects arc required to isolate the stimulus features
being judged from among other features, they bring to bear
a repertoire o f sensory, perceptual, and linguistic functions
and skills. We no longer have a null instrument but a
knowledgeable strategist.
3 .1 .1 b B a s ic P sy ch o p h y sica l M e t h o d s
In the m eth o d o f ad ju stm en t the subject adjusts a variable
stimulus until it is detected or matches a standard with
regard to a specified feature.
In the m eth o d o f lim its the experimenter increases or
decreases the variable stimulus until the subject detects it or
indicates that it matches a standard. The mean signed error
o t settings with respect to the standard is the constant error.
The variability o f settings about the signed mean measures
the precision o f the judgments, and reflects the sensitivity
o f the sensor y system.
I he method o fad ju stm ent and the method o f limits are
especially useful for measuring steady-state constant errors.
For instance, to measure how an inclined surface affects the
apparent inclination o f a superimposed test line, subjects
are asked to set the line to the apparent vertical with and
without the surfacc. The difference between the mean
signed errors indicates the extent o f the induced inclina­
tion. Errors ot anticipation and habituation are avoided by
averaging settings from trials in which the line starts at vari­
ous angles on either side o f the vertical.
The m ethod o f c o n sta n t stim uli is used for measuring
transient effects, such as aftereffects, which typically fade
exponentially. The method is also used when it is important
to avoid presenting stimuli in an ordered sequence.
W h en the method o f constant stimuli is used to
measure a threshold, values o f the stimulus around the
threshold are repeatedly presented in random order, and
subjects report whether o r not the stimulus is present. The
probability ot detection plotted as a function o f stimulus
magnitude yields a psychom etric fu n ctio n , like that in
Figure 3.1. As stimulus strength increases, the probability
o f detection increases. A t first it increases slowly because o f
noise in the sensory system. Detection rate then accelerates
and finally levels o f f to a probability o f one. Thus, the func­
tion is usually an S-shaped curve in the form o f a cu m u la ­
tive norm al d istribu tion , or normal ogive. The threshold is
usually defined as the stimulus value that is detected on
5 0 % o f trials.
The method o f constant stimuli may also be used to
measure discrimination thresholds. For example, one can
measure the accuracy and precision o f setting a variable
stimulus to match a comparison stimulus. About seven
values o f the variable stimulus are selected around the PSE.
O n each trial, one o f these stimuli is presented briefly and
the subject indicates whether, by a defined criterion, it is
greater or less than a comparison stimulus. The comparison
stimulus may be presented with the test stimulus or just
before it. Subjects are asked to make a decision, even when
the two stimuli look alike. The order o f presentations is ran­
domized and each stimulus is presented many times. The
percentage o f trials in which the variable stimulus is judged
to be greater than (or less than) the standard stimulus is
plotted on the jy-axis against stimulus magnitude on the
л -axis to yield a p sy ch o m etric fu n ctio n like that shown in
Figure 3.1.
The value o f the stimulus that yields 5 0 % “greatcr-than”
judgments is th e PSE. O ver the middle part o f the psycho­
metric function, the probability o f a response is a linear
function o f stimulus magnitude. The 5 0 % point may there­
fore be derived by linear interpolation. The difference
between the PSE and the P O E is the constant error.
The value o f the stimulus that yields 7 5 % o f "greater than”
judgments is usually taken as a measure o f the upper dis­
crimination threshold. The 2 5 % point defines the lower
discrimination threshold. The difference between the PSE
and one or other o f the discrimination thresholds is the just
n oticeable d iffercnce, or J N D.
P rob it analysis (Finney 1971) is used to improve the fit
o f a cumulative normal curve to a set o f data, and thus
to derive more precise estimates o f the parameters o f the
function. The ordinate (response probability) and abscissa
(stimulus strength) are first transformed into standard
scores (standard-dcviation units). This tends to render the

В M agnitude of test stim ulus
С S tim ulus intensity
H ypothetical fiy ib im c tr k fu m tiw s . (A ) D eriv in g a threshold from
a co n sta n t stim ulus p ro ced u re. ( B ; D eriv in g th e PSF. and d iscrim in ation
thresholds from a co n sta n t stim ulus procedure. ( C ) D eriv in g a threshold
from a fo rced -ch o ice procedure.
psychometric function linear. Weights are then assigned to
each datum point in inverse proportion to its standard
error, which means that greater weight is given to points in
rhe upper part o f rhe psychometric function. In addition,
datum points near the center o f the psychometric curve arc-
weighted more heavily because they contribute more to rhe
determination o f the position o f the curve than do points
at cither end o f the curve. The best-fitting line is then
determined by weighted linear regression.
Psychometric functions may be fitted with a W cibull
fu n ctio n o f the form:
i//(r) = l-c.\ p (- a c K)
where V7 (c) is the probability o f detection o f a stimulus o f
intensity с , (X represents the effect o f the stimulus on the
sense organ, and /3 represents the effect o f noise (Wcibull
1951; Mortensen 2 0 0 2 ) . This function often fits data
well and ir models the effects o f probability summation
(Section 13.1.1).
Foster and B isch o f ( 1 9 9 7 ) developed a bootstrap proce­
dure for improving the accuracy o f thresholds derived from
psychometric functions, when the number o f trials is not
large. W ich m an n and Hill (2 0 0 1 a , 2 0 0 1 b ) reviewed proce­
dures for estimating parameters from psychometric func­
tions, assessing errors ot these estimations, and testing
goodness o f fit between models and data.
3 . 1 .1 c S ta ir c a s e M e t h o d s
The method o f constant stimuli is a nonadaptive procedure
because the stimulus presented on a given trial does not
depend on the way the subject responded to previous stim­
uli. In an adaptive p roced u re the value o f the stimulus on
any trial depends on previous responses. Judgments about
stimuli that lie some distance from the P SE are less informa­
tive than those about stimuli near the PSE. It is therefore
best to concentrate stimuli near the PSE. Stimuli should
also be symmetrically arranged around the PSF. so as to
avoid biasing the results. Л derivative o f rhe method o f
limits, known as the staircase m ethod, is an adaptive pro­
cedure that provides an efficient way to achieve these
two goals.
In a simple staircase, stimuli are presented in ascending
or descending order until the response of the subject
changes. The order o f stimulus progression is then reversed
until the response changes again. Usually, after between six
and nine reversals, stimulus values converge on the PSE. If
the step size between successive stimulus presentations is
too great, the subject merely alternates between “yes” and
"no” judgments. If the step size is too small, time is wasted.
It is a useful strategy to start with a large step size and reduce
it during the course o f the experiment. Л simple rule is to
halve the step size when the su bjects response reverses, and
double it again i f a specified number ot similar responses
occur in succession (Levitt 1971). The threshold is the
mean ot a criterion number ot trials after the judgments
have reached a constant level o f fluctuation. The difficulty
o f deciding when a constant level has been reached can be
avoided by defining the threshold as the stimulus value
above which 5 0 % o f rhe judgments are “yes.”
W ith a simple staircase, the subject can anticipate when
to change the response. For instance, if several “yes” judg­
ments have been made in succession, the subject may guess
that it is time to say “no,” even though no change in the
stimulus has been detected. The d o u b ic-sta ircasc m ethod
reduces the effects o f sequential dependencies. In this
m ethod, two staircase sequences are run at the same time
with stimuli from the cwo sequences interleaved in random
order (Cornsw eet 1962).
Several variations o f the scaircasc m ethod have been
devised. Taylor and Creelman (1 9 6 7 ) devised P E S T (param­
eter estimation by sequential testing). Watson and Pelli
(1 9 8 3 ) developed Q U E S T (quick estimate by sequential
testing), in which the initial stimulus value is determined
by chc mode (maximum likelihood) o f the experimenters
prior knowledge o f the probability density function ( P D F )
o f threshold values over the population. The subject’s
response is then used to construct a new P D F using Bayess
rule (Section 3 .6 ). The next stimulus is presented at the new-
most likely threshold. At the end o f the procedure, the
mode o f the final P D F is considered the best estimate o f chc
threshold. King-Sm ith et al. ( 1 9 9 4 ) developed a modified
version o f Q U E S T . Kontsevich and Tyler 1 9 9 9) developed
a Bayesian adaptive procedure in which stimulus intensity
on each trial is sec according со boch che expecced mean
chreshold and the expected slope o f the psychometric
function. These methods require a fast compucer wich
adequace memory.
3 .1 .Id S ig n a l D e t e c t i o n P ro ce d u re s
An absolute chreshold is che smallest magnitude o f a stimu­
lus thac can be dccecccd on a given percencage ot trials. In
che classical procedure, a scimulus is presenced on every crial
and subjects reporc whether or noc chey have detecced it. In
the chreshold region, subjcccs are necessarily uncertain
abouc che presence ot che stimulus. They may improve their
rate o f detection by adopting a lax criterion in which they
report the stimulus when they are unsure. O n the other
hand, chey may lower cheir dececcion race by adopcing a
scriccer criterion in which chey reporc che scimulus only
when chey are sure. Classical psychophysical mechods do
n ot distinguish between a change in the detectability o f a
stimulus and a change in the willingness o f the subject to
report its presence (the criterion level). The method o f
signal d e tectio n measures the separate contributions o f
these two faccors (Green and Swecs 1966). Thurscones
(1 9 2 7 ) law o f com parative ju d g m en c was a precursor со
signal dececcion theory.
A signal is a physical spatial or cemporal disconcinuicy
chac a sensory system is attempting to detect. The basic idea
is that neural discharges created by a signal are accompa­
nied by noise arising from other stimuli or in the sensory
svstem.
t It is assumed that the noise level fluctuates over time
at random around a mean value with a given variance. Ic is
also assumed chac che sensory response generaced by a signal
varies ac random around a mean value, wich che same vari­
ance as for noise alone. Responses on different crials are
assumed со be independent, and chac performance is scable
over a sec o l crials.
The deccccability o f a given stimulus is defined as che
difference bccween che mean of che probability distribution
o f responses generated by noise alone and the mean o f the
distribution ol responses generated by noise plus signal,
divided bv the variance o f the distributions. Detectability is
4 4
denoted by the symbol d ’ {d prime).
W ith in the threshold region, a subject is necessarily
uncertain about whether a weak sensation is due to a signal
or to noise. The subjects task can be described as that o f
estimating the likelihood chac che sensory accivicy on agiven
crial arises from noise plus signal, relative со che likelihood
chat ic arises from noise alone. The ratio o f chese cwo likeli­
hoods is che lik e lih o o d ratio and forms chc most efficient
basis for a detection task.
The way a person responds in an uncertain situation
depends on the perceived rewards and penalties (payoff )
associated with each o f four types o f response. These are:
( l ) correctly detecting a stimulus (h it), (2) saying a stimulus
is present when it is n ot (false positive), (3 ) n ot detecting a
true signal (miss), and (4) not reporting a stimulus when it
is not present (correct rejection). The payoff associated with
each type o f response is known as a p ay o ff matrix. For
example, i f one suspects that the house is on fire it is better
to raise chc alarm rather than delay until one can see che
4
flames. O n che other hand, a d octor might wish to obtain
more evidence before telling a patient he is going to die
o f cancer. The level o f sensory activity above which an
observer reports a signal is the crite rio n level, denoted by
the symbol /3.
The method o f signal detection separates the effects o f
che observers criccrion, /3 , from changes in che detectabil-
icy o f che stimulus, d\ Signals o f varying strengch in the
region o f chc chreshold are presenced in random order,
along wich cacch crials in which chere is no signal but only
noise in chc sensory sysccm. A record is kepc o f chc race ac
which cargccs are dccecccd in a given number of crials (hie
race), and che race ac which cargccs are reporced when none
is present (false-positive race). These data are plotted on a
graph wich hie races along che у -axis and false-positive races
along che x-cixis. A curve, known as che receiver operating
ch a ra cteristic, or R O C curve, is then ficced со che daca, as
shown in Figure 3.2.
W h en che hie rate increases in simple proportion to che
false positive rate, the R O C curve is a diagonal line. This
signifies that the observer was merely guessing, since an
improved hit rate was achieved only by an equal increase in
false positives. At one extreme the subject never reports a
stimulus, thus avoiding false positives buc scoring no hits.
Ac che ocher excreme che subject reporcs che stimulus on
every trial, thus scoring che maximum number o f boch hies
and false positives. W h en mosc of che signals are detecced
wich few false posicives, che curve rises steeply from che
diagonal before leveling off'. The area between the R O C

False positive rate
Figure 3 .2 . A bypotht'diAtl set o f R O C atrtes. Sym bol d ' signifies chc
d ccccta b ilitv* o t chc stim ulus, liach curve is a locus o f co n stan t
d etectability. Ih c p osition a lo n g e a c h curve represents [ i. th e criterion
a t w h ich the su b ject is operating.
curve and the diagonal indicates the detectability o f the
stimulus. The area corresponds to the probability o f detec­
tion in a two-alternative forced-choice task. It is a nonpara-
metric measure that does not rely on assumptions about the
distribution o f responses. The criterion is given by the point
along the R O C curve at which the subject is operating.
Macmillan and Creelman ( 1 9 9 1 ) wrote a users guide for
signal detection theory.
Signal detection methods can be used to plot the
probability o f response o f single neurons in the visual
cortex to well-defined stimuli o f variable strength to yield a
n eu ro m ctric fu n ctio n (Parker and Newsome 1 9 98 ) (sec
Section 4.3.1a).
3 . 1 . 1 c F o rce d C h o i c e M e t h o d s
Blackwell ( 1 9 5 2 ) designed a simple procedure for ensuring
that a measurement o f a threshold is not affected by changes
in the observers criterion. Bergmann had proposed a simi­
lar procedure in 1858 (see Fcchncr I8 6 0 , p. 2 4 2 ) . Subjects
are presented with two stimulus windows,either at the same
time or sequentially. In the case ot simple detection, one
window contains a stimulus while the other is blank.
Stimulus strength and the relative positions o f the two win­
dows are varied at random over a series o f trials. O n each
trial, subjects are forced to say which window contains the
stimulus; hence the name tw o-alternative fo rced -ch o ice
( 2 A F C ) procedu re. A two-alternative decision is indepen­
dent o f changes in criterion, since subjects are forced to
choose on each trial. The percentage ol correct responses is
plotted on the у-axis against the value o f the stimulus on the
x-axis, to generate a psychometric function, like that shown
in Figure 3.1. Since the chance level o f performance is 50% ,
ordinate values run between 5 0 and 100%. The stimulus
value correctly identified 75 % ot the time is taken as the
threshold. The 7 5 % point is the mean o f the psychometric
function based on the forced-choice procedure. The slope
o f the function indicates the rate at which performance
improves as stimulus strength is increased. It is the recipro­
cal o f the standard deviation o f the distribution o f responses.
The standard error ol judgments lor each stimulus value is
calculated by the equation tor the standard error o f a pro­
portion. The standard error is largest when subjects arc
most uncertain in their judgments, which is when the test
and comparison stimuli are most similar. As the percentage
ot correct responses increases, the standard error tends
to decrease. M cK ee e t al. (1 9 8 5 ) have described these
statistical procedures.
An observer who is forced to choose between two stim­
uli that ditter in more than one respect may base choices on
a feature other than the one being studied. Thus, the forced-
choice procedure produces spurious results when the exper­
imenter believes that observers are using one criterion when
in fact they are using another.
Psychophysical procedures that involve identification
and description are discussed in Section 4.6.
3 .1 . I f S c a lin g P ro ce d u res
Scaling is used for measuring the magnitude o f a percept
such as the brightness o f a patch o flig h t, the loudness o f a
sound, or the distance o f a seen object. In simple scaling,
subjects judge the magnitudes ot a stimulus attribute in
terms o f a familiar scale such as feet, o r ounces. However,
we do not have well-learned scales for sensory qualities such
as loudness, brightness, or velocity. In such cases, it may be
possible to teach subjects a scale. Another procedure is to
ask subjects to rate stimuli with respect to the mean value
o f a series o f stimuli o f different magnitudes. Otherwise
they can place stimuli in order. The ordering can be a simple
rank ordering, an equal-interval ordering, or an equal-ratio
ordering. It can be on a one-dimensional continuum such
as size, velocity, or distance, or in a multidimensional fca-
ture space. Thus, in addition to discriminating between
stimuli, subjects arrange them in bins or in order. Readers
are referred to Torgerson ( 1 9 5 8 ) , Garner ( 1 9 6 2 ) , and
Falmagne (1 9 8 6 ).
3 .1 .1 g S tim u lu s P ro b es
A stimulus probe is a comparison stimulus that creates the
same percept as a test stimulus but through the mediation
o f a distinct sensory system. For example, the test stimulus
could be a depth interval between two objects created by
perspective alone. The probe could be a depth interval cre­
ated by binocular disparity alone. Subjects adjust the dis­
parity o f the probe until the depth interval o f the probe
appears to match the depth interval o f the test stimulus.
 A probe may interfere with che cesc scimulus when probe
and stimulus are presented at the same time. To avoid this
problem, the probe may be presented just after che test scim­
ulus, and che subject may be allowed to go back and forth
between che two stimuli until satisfied that they arc well
matched. However, even when well matched with regard to
the stimulus feature of interest the tw o stimuli still differ
physically and may still appear to differ wich regard со ocher
features.
A probe does nor indicate che absolute perceived mag-
nicudc o f a cesc scimulus buc only how accuracely and pre­
cisely ic is judged relative со chc probe. Theoretically, a probe
would indicace the absolute perceived magnitude o f a test
stimulus i f the probe were perceived with perfect accuracy
and precision. But this is never the case.
A probe can n ot be used to measure che effect o f a
variable on a given stimulus when the probe is subject to
che same variable. For example, a depch probe defined by
disparity cannot reveal whether the slant o f a surface
defined by perspective declines over time. This is because
slanced surfaces, however chey are defined, appear less
slanced over time.
Probes can be useful for investigating the consistency ot
judgments o f a given stimulus feature defined by distinct
cue systems. For example, we will see in Chapter 3 0 that
probes have been used to study relationships between depth
judgments based on distinct depth cues.
O n e may chink chac one has uncovered che crucial scim­
ulus variable responsible for a particular percepcual effecc.
However, changes in cheselecced variable m ay be incidencal
со changes in anocher factor thac one has noc considered. Ic
is often difficulc со change one feacure o f a scimulus wichouc
changing ochers. For example, one may conclude chac che
perceived size o f a surface parch is a funccion o f che density
o f texture elements. But the crucial factor may be the change
in the total number o f elements in the patch rather than
density.
It has often been claimed that Figure 3.3a demonstrates
that vertical extents arc overestimated relative to horizoncal
excencs. Buc che horizoncal element is partitioned into three
sections while the vertical element is not. A partitioned line
appears shorter than a clear line, whatever the orientation
o f che figure, as shown in Figure 3.3 (Finger and Spelc 1947).
The visual field excends much furcher horizontallyШ chan
vertically, as dcpicced in Figure 3.3. A vertical line cherefore
A. The vertical e le m e nt a pp e ars longer than the horizontal line.

3 .1 .1 b P h e n o m e n o lo g ic a l A nalysis

Many perceptual phenomena can be investigated by simply

asking subjects to describe what they see. Before the nine­
teenth century, most investigations o f the functioning o f
the visual system relied on this method. The G estalt psy­
B . The stem o f aT appears longer.w hatever its orientation .
chologists used chc m ethod extensively in che early part of'
che 20ch cencury. Mosc visual phenomena were discovered
by chance observation or by an inspired guess chac a given
phenomenon may occur ifscimuli arc arranged in a particu­
lar configuration.
For instance, Celeste M cC ollo u g h , extrapolating from
some work on chromatic aberration, ancicipaced chac some­
thing ot inceresc would be seen i f alcernacing gratings were
paired wich alternating colors. Thac led со che discovery o f
one o f che firsc concingenc aftereffcccs (Sections 4 .2 .9 c and C . A pp a re nt le ngths m ay be influenced by the oval visual field.

13.3.5). W heacscones discovery o f che scereoscope and his

qualicative observations wich a variecy o f stereograms
revealed che basic characceriscics o f chc human stereoscopic
syscem.
O n ce a visual phenomenon has been discovered, the
stimulus conditions that give rise to it can be established
by comparing rhe probability o f its appearance under
ditferenc experimenral condicions. Powerful inferences can
be made abouc mechanisms underlying visual processes
D. A circular a perture rem oves the e ffe ct o f the oval visual field.
from qualicacive observacions made under cleverly devised
circumscanccs. Figure y \ 7be reTticahh&rizonbd illusion.
occupies a larger proportion o f the visual field than docs a
horizontal line o f the same length. There is little i f any illu­
sion when a cross is viewed through a circular aperture
(Kunnapas 1 959). Even if there is a residual illusion it
remains to be decided whether it occurs in a gravitational
frame of reference or in a retinal frame ol reference.
The question ot frames ot reference is illustrated by
Figure 3.4. Tw o o f the discs look like mounds, and two look
like hollows. W h en the figure is inverted, mounds become
hollows and hollows becom e mounds. In most textbooks, it
is concluded that the eonvexitv* or concavitv/ ot a shaded
region is interpreted in a way consistent with the light
source being above with respect to gravity. However, when
Figure 3.4 is viewed with the head upside down, impres­
sions o f convexity and concavity are determined by the ori­
entation o f the dark and light areas relative to the head
rather than to gravity. But even this is not the correct
account, 'rhe figure can be viewed with head upright but
with the figure at a steep angle beneath the chin so that the
part o f the picture that is “top” with respect to gravity
and to the head is upside-down on the retina. Now the co n ­
vexities and concavities arc interpreted in a retinal frame o f
reference (Howard et al. 1990).
A given response may be mediated by distinct stimuli
processed by distinct neural systems. For example, the
pupils dilate in response to a reduction in illumination,
relaxation o f accommodation, a change in convergence ot
I.*«€ 3.4. Fram es o freferen ce in sh ap efrom shading. W h e n the figure is
inverted , the m ou nd discs change in to hollow s, and vice versa. V iew in g
the figure w ith inverted head reveals th at the cru cial facto r is
orien ta tio n o } the discs to the head rather than to gravity. W h e n the
figure is viewed below the c h in alm o st parallel w ith body, with head
e re ct, the cru cial fa c to r turn s o u t to be the retinal orien tatio n o t
the discs.
the eyes, and an emotional stimulus. Also, a given percep­
tual effect may be mediated by distinct sensory channels
involving different neural processes. Thus, an impression
o f depth can be created by binocular disparity or by
motion parallax. Several distinct processes may contribute
to more complex visual phenomena such as the Miiller-
I.ycr illusion. Just because a perceptual effect has a name
does not mean it is due to one neural process. For example,
processes occurring at distinct levels in the nervous
system may generate brightness contrast (Section 22.4).
Also, there are three distinct forms ot induced visual
motion (Section 22.7).
O n ly vigilance and imagination in designing control
conditions can prevent one from failing to recognize a cru­
cial variable. Perhaps half the perception literature consists
o f claims that investigators have neglected crucial variables
and of counterclaims that the neglected variables were not
crucial or were controlled for.
3.1 . l i A n alysis o f Illu sio n s
Many visual phenomena arc designated illusions. But what
is an illusion? The most general definition is that an illusion
is a judgm ent about an o b ject or event that does n ot agree
with a judgm ent based on a more reliable m ode o f observa­
tion. For example, in the Miiller-Lyer illusion, the estimate
o f the relative lengths o f two lines does not agree with mea­
surements made with a ruler.
Classical geometrical illusions, such as rhe Miiller-Lyer,
Zollner, and Poggendorft illusions, have been classified into
illusions o f direction and size, with various subdivisions
(sec C oren et al. 1976). Illusions may also be classified in
terms o f their known or assumed causes.
1. Physical illusions
A stick half immersed in water appears bent.
A layer o f hot air may appear like water.
2. O ptical dcfccts
Diplopia arises from lens aberrations.
3. Projcctivcly equivalent stimuli
The Ames room (Section 29.2.2b).
The double nail illusion (Section 15.4.6a).
4. Peculiarities o f retinal processes
Dark adaptation. Troxler fading.
Afterimages.
5. Peculiarities o f processes in VI
T ilt contrast. Hering and Zollner illusions.
Induccd motion (Scction 22.7).
 The m otion aftereffect.
C o n trast o f size. The D e lb o e f illusion
6. Peculiarities ot processing at higher levels
The m oon illusion (Section 29.3.5 ).
Reversible perspective (Section 2 6.7).
7. C onflicting intersensory stimuli
Ventriloquism (Section 4.5.4b).
Vection (Section 22.7.3).
Visually-induced illusions o f self-tilt.
8. Visual pathologies
Anomalous correspondence (Section 14.4.1).
Phantom limb and neglect (Section 32.1.1).
3 . 1 .2 D E T E C T IO N
A stimulus is said to be detected when, over a series o f trials,
an observer reports its presence at above chance level.
A persisting patch o f light isdctcctcd when chc mean rate at
which quanta fall on the patch is discriminably different
from the rate at which quanta fall within the surrounding
region (Section 5.1.5). A b rief patch o f light is detected
when the quanta per unit area on the patch is sufficiently
different from the quanta per unit area on the surround.
Because ot diffraction and other lens aberrations, the image
o f a sharp spot or line is spread across several receptors, so
that detection reduces to detecting a luminance gradient.
In a typical detection task, a line o f a given length and
luminance, on a background o f a different luminance, is
varied in thickness until it is detected. For an illuminated
line on a dark background, no line is so thin that it cannot
be detected. This is because luminance can be increased to
compensate tor any reduction in width to generate a dis-
criminable luminance gradient. O n e can talk about the
minimum resolvable thickness ot an illuminated line onlv it в
the contrast between line and surround is specified. It has
been estimated from frcqucncy-of-sceingcurvcs that a short
line o f light seen against a dark background is detected at
above chance level i f two quanta o f light are absorbed within
a critical area and within a critical time period o f about
10 ms. Stimulus energy is completely summed within this
critical area (R icco ’s law) and critical time (B lo ch s law).
T he critical area and critical time vary with light wavelength
and retinal location (Boum an and van den Brink 1952;
Schwarz 1993).
A black line seen against a bright background must be at
least 0.5 arcmin wide to be detected, however bright rhe
background (H ech t and M intz 1939). A visual target can
also be the boundary between two unequally illuminated
regions. In all cases, performance depends on the ability to
detect a luminancc gradient— the subject is not required to
respond to any other attribute o f the stimulus.
3 .1 .3 R E S O L U T IO N
3 . 1 .3 a W i d t h R e s o lu tio n
As two superimposed fine lines are separated, the two dis­
tributions o flig h t over their images separate to form a wider
distribution. This creates the impression o f a line increasing
in width. As the lines separate further, the two peaks o f
light distribution becom e sufficiently distinct to allow the
two lines to be seen. Thus, two spatially separated lines can
be distinguished from two perfectly superimposed lines
before they are far enough apart to be seen as two distincc
lines. This type o f resolution is width resolution. It exceeds
the limits set by the Nyquist or Rayleigh criteria described
in the next section. In color, width resolution shows itself as
a loss o f saturation as a m onochromatic light is replaced by
two m onochrom atic lights that produce the same hue as
the original m onochromatic light. W id th resolution in
stercopsis is discussed in Section 18.11.2.
3 . 1 .3 b R e s o lu tio n o f S tim u lu s S e p a r a tio n
Two stimuli are fully resolved when they are detectable
as two stimuli. For spatial resolution, the stimulus must
excite two distinct detectors at a discriminably higher level
than it excites a third detector in an intermediate location.
Thus, a set o f detectors in a regular lattice can resolve a peri­
odic stimulus, such as a black-white grating, only it the spa­
tial period o f the receptors is no more than half the spatial
period o f the grating (distance between two black bars).
This is known as the Nyquist lim it. A related statement is
that, tor a diffraction-limited system, two point sources can
just be resolved when the peaks o f their images are sepa­
rated by the radius ot the inner bright regions ot their dif­
fraction patterns (A irys disc), as illustrated in Figure 9.3.
This is known as the Rayleigh criterion . For green light
( 5 4 0 nm) and a numerical aperture o f 1.4, this criterion
imposes a resolution limit o f 2 4 0 nm. Resolution acuity is
discussed further in Section 9.1.
For temporal resolution, the excitation incurred by the
first stimulus must subside sufficiently before the second
stimulus is presented. The limiting factors are the speed ot
stimulus onset and the time constant o f the sensory
system.
The color system has only three channels— red, green,
and blue cones. They have very wide and overlapping wave­
length tuning functions. Since neither che Nyquist limit
nor the Rayleigh criterion is satisfied in a system with only
three channels, our capacity to resolve wavelengths is zero.
No matter what the wavelength composition o f a patch o f
light, we see only one color. The color we see depends on
the relative extent to which the different color channels are
excited. I f two lights with different wavelength com ponents
excite the three channels in the same ratios, those lights
appear identical. The lights are said to be metameric
matches. Л m eta m eric stim ulus is a com bination o f physi­
cal stimuli within a stimulus continuum that produces a
sensation o f a single value within that continuum, even
though the com ponent stimuli produce distinct sensations
when presented separately.
T he wavelength componencs o f two lights become
discriminably different when they are presented one at a
rime or in distinct locations.
Metamerism arises only in sensory systems consisting o f
detectors with overlapping band-pass tuning functions
along a stimulus continuum. All visual features, other than
luminance, contrast, and flicker, are processed by multi­
channel systems and are therefore metameric, at least to
some extent.
The visual local-sign system is metameric only locally. It
has about one million channels (ganglion cells). At the th e­
oretical limit we can resolve a black and white grating with
bars as narrow as the diameter o f ganglion-cell receptive
fields. In other words, resolution is limited by the ability o f
the neighboring receptive fields to detect differences in
luminance contrast. Tw o stimuli falling wholly within a
local retina region where the excitatory regions o f neigh­
boring receptive fields mutually overlap appear as one stim­
ulus in a position that depends on the mean or centroid o f
the total luminance distribution. This occurs when two
short parallel lines are presented together within an area o f
about 2 arcmin, which is about rhe size o f the smallest
receptive fields in the retina (W att e t al. 1 9 8 3 ; Badcock and
Westheimer 1985). This metameric merging o f stimuli
occurs over larger distances in the peripheral retina, where
receptive fields are larger. M etameric merging accounts for
the limit ot grating resolution, at which adjacent lines o f a
grating merge into a grcv patch. W h en lines are presented
to distinct locations or successively, their separate positions
can be discriminated to much finer limits, just as wave­
lengths o t light can be discriminated when colored patches
are presented in different spatial locations. Spatial discrimi­
nations beyond the Nyquist limit are referred to as hypera­
cuity, as wc will see in Section 3.1.4.
3 . 1 .3 c R e s o lu tio n o f S e c o n d a r y Featu res
Resolution is more difficult to investigate in secondary
spatial or spatiotemporal features— features derived trom
the initial coding ot intensity, color, local sign, and time
(Section 4.2.4). 'I his is because all secondary features can be
also resolved by the million-channel, local-sign system. For
example, even i f orientation detectors could n ot resolve the
angle between two long intersecting lines, the lines would
still be perceptibly distinct because they fall on distinct
regions o f the retina.
Given that orientation is coded in the visual cortex by
detectors with overlapping tuning functions, it follows that
two neighboringor intersecting short lines at slightly differ­
ent orientations should metamerize their orientations—
they should appear asoneline.it an intermediate orientation.
Parkes et al. ( 2 0 0 1 ) showed that neighboring patches o f
grating differing in orientation all appear orientated at
the mean orientation o f the set. Superimposed long lines
differing in orientation do not metamerize because they
stimulate distinct regions o f the retina.
For similar reasons, metamerism should be evident in
visual m otion, and there is evidence that it is. A display o f
short-lifetime dots moving in different directions in the
same general direction appears as a set o f dots moving in a
mean direction. The discrim inability ot a change in the
mean direction o f motion tor a mixed display o f dors was
the same as tor an array o t dots all moving in the same direc­
tion (Watamaniuk et al. 1989). W h en the directions o f
motion are widely separated and dot trajectories do not
intersect, the two motions are discriminated.
Furthermore, an array o f short-litetime dots moving in
the same direction at different speeds resembles an array o f
dots moving at the mean speed o f the set (W atamaniuk and
Duchon 1 9 9 2 ). Averaging o f direction or speed does not
occur when the dots have a long lifetime because the differ­
ences between the com p on ent dots arc then discriminated
on the basis o f relative changes in position o f identifiable
dots. These results can be explained in terms o f metameric
processes within the motion-detection system that arise
because the tuning functions o f motion channels overlap.
Using similar methods, W illiam s et al. ( 1 9 9 1 ) estimated
that the direction tuning functions o f human m otion detec­
tors have a half-bandwidth at half amplitude o f about 30".
They proposed that with a channel spacing ot 30°, the
motion system consists o f 12 channels. Recording from
motion-sensitive cells in monkey V I yielded a similar
bandwidth (Section 5.6.4).
Metamerism is discussed further in Section 4.2.7.
Metamerism in the disparity system is discussed in
Section 18.8.
3 . 1 .4 D IS C R IM IN A T IO N
3 .1 .4 a B a s i c F eatu res
Tw o stimuli are discriminable it one is detectably dilferent
from the other, given that they have been resolved as two
stimuli, either in space or in time. A metameric system with
poor resolution can have exquisite discrimination. For
instance, even though rhe wavelength-resolving power o f
the human eye is zero, we can discriminate between many
hundreds o f spectral colors (or their meramers), as long as
they are presented sequentially (resolved in tim e) or to
different regions o f the retina (spatially resolved).
Spatial resolution requires detection o f a difference
between rhe means o f two overlapping and simultaneous
distributions o f activity along the sensory continuum.
Since chc cwo distributions o f accivicy arc presenc ac chc
same time, performance is subject to the Nyquist limit and
metamerism.
Discrimination depends on the detection ot a difference
in the mean response o f one set o f dccectors and chc mean
response of either che same detectors at a different time or
o f a set of detectors in a different location on the sensory
surface. There is no well-defined theoretical limit to chc
precision with which che mean o f a single distribution ot
excitation across a set o f detectors can be registered when
no confounding stimuli are present.
The precision w-ich which che locacion o f a single scimu­
lus can be registered depends on the square root ot the
num ber o f phocons and cheir spacial discribucion. In neural
cerms, precision depends on che race o f change ot response
across chc sec o f dececcors. The precision wich which che
location o f a stimulus can be detected by two detectors with
overlapping tuning functions depends on che steepness o f
the cuning functions ac che poinc on che stimulus con tin ­
uum where che cuning funccions overlap. Thac is, ic depends
on che relative race o f change o f che signal in each o f che two
dececcors as che scimulus is moved over che scimulus co n ­
tinuum. Resolution depends mainly on che signal-co-noise
ratio, and on chc cuning widch and dcnsicy o f sensory chan­
nels along the sensory continuum. The noisiness o f the indi­
vidual channels seems to be less important tor discrimination
than it is for resolution (Bowne 1990).
The fineness o f discrimination compared wich resolu­
tion explains hyperacuity. Examples o f hyperacuicy are
dececcion o f a change in separation becwecn cwo neighbor­
ing buc discincc points, and dececcion o f an offsec bccwccn
cwo abuccing lines (vernier acuicy). Boch chcsc acuities
are several times finer chan rhe mean spacing o f recep­
tive fields. Another example is the task o f setting a point
midway between cwo ocher points, which has yielded
chresholdsof approximately 1 arcscc (Klein and Levi 1985).
The key idea is chac if cwo simultaneous stimuli arc sepa­
rated by less than about 5 arcmin they meeamerize. In a
resolution cask, chc stimuli arc necessarily crowded cogecher.
In a hyperacuicy cask they are spatially separated (Gcisler
1984).
The distinction between resolution and discrimination
(hyperacuity) in a locally mecameric spatial modality can be
vividly illustrated on the skin. W h e n the back is prodded
simultaneously by cwo poinced objeccs abouc 1 cm aparc,
che stimuli meeamerize into apparently one objecc ac an
incermediace position. The apparenc position o f chc fused
stimuli depends on cheir relative screngchs. Bekcsy ( 1 9 6 7 )
used che cerm “fu n n elin g ” for mecameric averaging. If chc
objeccs are presenced sequentially wich che same separation,
their distinct posicions can be discriminated (I.oom is and
Collins 1978). Metamerism is evident in the summation o f
responses ot cells in the somatosensory cortex ot alert m o n ­
keys when neighboring points are applied simulcaneously
со the skin (Gardner and Costanzo 1980).
Gcisler ( 1 9 8 4 ) described an ideal observer tor acuity
and hyperacuity. Snippe and Kocnderink ( 1 9 9 2 ) developed
an ideal observer for width discrimination and hyperacuity
in mecameric sensory systems.
3 . 1 . 4 b D i s c r im in a t io n F u n c tio n s and
D ip p e r F u n c tio n s
In general, a d iscrim in atio n fu n ctio n defines the discrimi­
nation threshold as a function o f the range o f values o f a
given stimulus feature. Л stimulus is detected most effi­
ciently when it excites a detector at che peak o f its cuning
function. However, a difference between two stimuli on a
feature continuum is discriminated best when che scimuli
tall on the steep Hanks o f the overlapping tuning functions
o f neighboring detectors. Ac such poincs che discrimination
chreshold falls со a m inimum. Thus, in any multichannel
system, chc discrimination chreshold should be lowesc
where che cuning functions overlap and highest at che
maxima o f che cuning funccions. The number o f undula­
tions will depend on che number o f overlapping channels
devoced со che dececcion o f chac feacure. A dip per function
is a dip in a discrimination chreshold as one moves over a
scimulus continuum.
Thus, che basic reason for a dipper funccion is chat che
responses to two values o f a given feature are most differ­
ent at the point on the stimulus continuum where che
tuning functions o f adjacent detectors intersect. This is
where the signals in che dececcors change most rapidly. The
huc-discrimination function shown in Figure 3.5 is che
best-known example (H urvich 1981).
O n e m ight expect the spatial-frequency discrimination
function to show peaks at spatial frequencies where the
tuning functions o f channels cuned со differenc scimulus
periodicities overlap. However, cells tuned со differenc spa­
cial periodicities are noc discributed evenly over the recina.
For a gracing o f reasonable size this lack o f homogeneity
W avelength (nm)
Fipr«M . 7 be h u e d iscrim in atio n fim tio ri. T h e w avelength d ifferen ce
required to p ro d u ce a just n o ticeab le d ifferen ce bccw ccn th e tw o halves
o f a b ip a rtite stim ulus. (Adapted from Hurvich 1981)
would mask modulations o f the contrast sensitivity func-
4
tion. Also, optical aberrations produce modulations ot the
contrast sensitivity function (Section 9.6.2b)
The visual position-detection system has one million
channels (ganglion cells). Modulations o f position discrim­
ination would therelore be evident only/ locallv.
* There has
been some debate about whether sensitivity to changes in
rhe separation o f two lines shows peaks and troughs, as the
distance between the lines is varied (Hirsch and Hylton
1982; Westheimer 1 984). W ilson (1 9 8 6 ) interpreted data
from Klein and Levi ( 1 9 8 5 ) as showing peaks and troughs
like those in the hue-discrimination function.
Consider the task ot discriminating a difference in blur
between a test edge and a comparison edge with fixed blur.
As blur ot the comparison edge is increased, the discrimi­
nation threshold declines to a minimum before climbing,
as shown in Figure 9.22. This is a dipper function tor
blur discrimination. Similar functions occur in contrast
discrimination.
Dipper functions have a special significance in multi­
channel systems centered on a physical norm (oppositional
systems). These include motion with the norm o f no
m otion, orientation with the norm o f vertical, and binocu­
lar disparity with the norm o f zero disparity. A stimulus
that is not the norm is said to be on a pedestal. I f detect­
ability is maximum at the norm then discrimination should
peak at values on either side o f the norm. In other words,
discrimination should improve as the comparison stimulus
is placed on a pedestal, rhat is, moved some distance from
the norm. In such a case the dipper function shows as a drop
in the discrimination threshold (rise in discrimination sen-
sitivity) as the pedestal value ot the comparison stimulus
is increased followed by an increase in che threshold at
4
higher pedestal values. This is illustrated in Figure 3.6 tor a
hypothetical opponent sensory dimension.
Regan and Price ( 1 9 8 6 ) found undulations in sensitiv­
ity to changes in line orientation as che line was set in vari­
ous orientations. The highest sensitivity to changing
orientation occurred at the vertical and the horizontal,
which suggests that the tuning functions o f orientation
detectors intersect at these salient values. This means that
the peaks ot the tuning functions occur on either side ot the
main meridians.
Dipper functions in discrimination o f binocular dispar­
ities are discussed in Section 18.3.3b.
Physiological evidence reveals the difference between
peaks o f detection and peaks o f discrimination. In the visual
cortex o f the cat, cells tuned to stimulus orientation
responded most reliably со stimuli oriented at the peak o f
the tuning function, but sensitivity to changes in orienta­
tion was greatest on the flanks o f che tuning function
(Scobey and G abor 1989).
Motion-sensitive cells in V 2 and in the middle temporal
area ( M T ) o f the alert monkey had directional tuning func­
tions with a half-width o f 50° at half-height. Although each
C hannel tuning functions
S tim ulus 1
va lu e (S) |
I
M axim um
difference
Z ero
В
d ifferen ce
M axim um
i change
С
M inim um
change
Pi$aK3.& D etection a n ild iio im in a tia i. (A ) H yp oth etical tu n in g fu n ctio n s
o f three d e te cto rs cen tered on a n o rm . ( B ) Sign ed d ifferen ce in firin g
rate o f n eig h b o rin g d etecto rs as a fu n ctio n o f the value o f the stim ulus.
( C ) T h e fu n ctio n derived by d ifferen tiatin g the d ifferen ce signal. The
d iscrim in ation signal (relative rate o f change) is stron gest a t th e p oin ts
where th e tu n in g fu n ctio n s arc steep est and in tersect.
cell fired most vigorously to motion at the peak o f its
cuning function, it was most sensitive to changes in motion
direction (as little as 1 .Г ) when the stimulus fell on the
flank of its tuning function (Snowden e t al. 1992).
3 . 1 . 4 c D is c r im in a tio n w ith R e s p e c t
to a N o rm
Oppositional stimulus continua are centered about a neu­
tral value, or norm . We can ask what is che lease departure
from the physical norm that can be detected. For example,
we can measure the threshold for detection o f offset o f a
point from the straight ahead, tilt ot a line relative to verti­
cal, or departure o f two stimuli from coplanarity. O n ly one
stimulus need be present, because the internalized norm
serves as the comparison. A norm, such as no m otion, grey
in the red-green opponent system, o r zero disparity in a
crossed'uncrossed disparity scale, is an inherent physical
value in an oppositional scale. But the internalized values
chat we develop for each o f these norms arc subject to tem­
porary modification (Section 4.2.9b).
An experimenter may define an arbitrary norm that che
subject is required to learn such as the mean o f a set o f
repeatedly exposed stimulus values. Subjects are chen asked
whether each o f several stimuli is greater than or less than
the memorized norm.
Isolated stimuli that are displaced with respect to a
norm tend to appear closer to the norm than they are. This
process is discussed in Section 4.2.9b.
This completes the general discussion of detection and
discrimination. Recognition, identification, and descrip­
tion arc discussed in Section 4.6.
3 .1 .5 TEM PORAL TH RESH O LD S
Temporal aspects o f sensory processing have been studied
with a great variety ot procedures. O nly a brief outline o f
these methods is provided here.
W ith a suprathrcshold stimulus, one can measure the
time required to detcct it. In a typical experiment, subjects
press a key as quickly as possible after a stimulus is presented
to provide a measure o f the reaction tim e. The reaction
time includes the time taken for the stimulus to be pro­
cessed stimulus (latency) and the time taken for the response
to be prepared and executed. If the same response is used for
different stimuli, differences between reaction times pro­
vide a measure ot differences in sensory processing time.
These procedures have been used to study effects o f learning
on the processing time for stereopsis (see Section 18.14).
In some cases, the results o f temporal processing o f sen­
sory inputs are reflected directly in a spatial percept. For
instance, a difference in arrival ot sounds at the two ears ot
a few milliseconds causes an apparent shift in the position
o f the sound source that subjects can identify by simply
pointing in the appropriate direction, raking as long as they
wish. Similarly, in the Pultrich stcrcophenom cnon, a target
moving in a frontal plane appears to move in depth when
image processing in one eye is delayed by introducing a dark
filter in front o f that eye. Л very precise mapping o f inreroc-
ular time differences into disparities can be obtained by
simply asking subjects to indicate the depth o f the path o f
the moving target (Section 23.1).
In another temporal procedure, the duration o f time for
which the stimulus is presented increases gradually on suc­
ceeding trials until the subject reports either the presence o f
the stimulus or some defined change in the stimulus. The
resulting measure is known as the tem poral threshold. The
temporal threshold tor stereopsis is discussed in Section
18.12.1. Subjects arc not required to respond rapidly but
are merely required to say on each trial whether or not the
stimulus occurred, o r in which o f two windows it occurred.
As the luminance intensity ot a stimulus is increased, the
temporal threshold becomes vanishingly small. As the stim­
ulus is weakened, rhe temporal threshold increases up to a
limiting value that depends on the capacity o f the sensory
system to integrate stimulus energy over time. This thresh­
old reflects the tem p o ral in teg ration tim e. The capacity o f
a sensory system to integrate stimuli over time can also be
investigated by presenting brief stimuli in succession with
variable interstimulus intervals. This topic is discussed in
more detail in the next section.
3 .2 A N A L Y S IS O F L I N E A R S Y S T E M S
3 .2 .1 N A T U R E O F L IN E A R S Y S T E M S
A system is any device that transforms inputs into outputs
to perform some specified action. A function that defines
how well-defined inputs are transformed into specified o u t­
puts is a tran sfer fu n ctio n . The aim o f systems analysis is to
design systems or to determine transfer functions o f exist­
ing systems. O n e must first specify the system. Human-
made systems usually have well-defined inputs and outputs
and well-defined com ponents, or modules, which can be
investigated independently. Any natural system, such as the
eye, has a large number o f com p on ent systems and is itself a
com ponent in a great number ot larger systems. O n e must
specify the stimuli that one wishes to study. In the visual
system, these could be a set o f stationary black-white grat­
ings, a set o f colored patches, a set o f objects at different
distances, o r any other stimuli that evoke responses. O n e
must then specify the responses and the features o f the
responses that one wishes to study. In the visual system, one
can measure the precision or accuracy o f detection, discrim­
ination. or recognition, or one can measure various attri­
butes o f eye
i movements, or ot neural activity
4 at some
specified sire in the nervous system.
In a given experiment, a defined system is a "black box,”
the internal structure o f which can be inferred only from
specified responses to a given set ot stimuli. Paradoxically, it
is easier to infer the order in which subroutines are executed
in a nonlinear system than in a linear system. This is because
linear systems are commutative so that rhe same outcome can
be achieved by doing things in different orders, whereas non ­
linear systems are often noncommucative. In a linear system,
one can independently determine the transfer functions ot
subsystems and combine them mathematically to predict the
transfer function o f the larger system. The transfer functions
o f in-series modules are combined by multiplication, and
those o f parallel modules are combined by addition. Modular
systems that combine in a linear fashion are easy to construct
(or to program genetically) and malfunctions are easy to
trace and treat locally. However, a linear system cannot per­
form operations such as multiplication or division, o r .my o f
the other nonlinear operations that are known to serve
important functions in the nervous system (Section 3.4).
Many biological systems, such .us the heart, kidney, and
liver are modular units that can be made to operate in rela­
tive isolation. The visual system has certain obvious struc­
tural-functional modules, such as rhe two eyes, the lens, rhe
pupil, and the extraocular muscles. Physiological and psy­
chophysical investigations have revealed what look like
modular structures in the neural structures o f the visual
sysccm, such as the various cell cypcs in che recina, che LCiN,
and che various in-series and parallel processing screams in
che cencral nervous sysccm. However, no physiological
sysccm is strictly linear and che performance o f che whole
sysccm is noc predictable from che responses o f modules
studied in isolation.
O n e may say chac die aim o f visual science is со identify
and characterize functional modules, and со derive cheir
cransfer funccions and che rules governing cheir inccraccions.
This is an ambitious encerprisc. Consider che bewildering
array o f pocencial modular componencs chac one can choose
со invesrigace. O n e can select a pigmenc molecule, any recep-
cor cell, amacrine cell, bipolar cell, o r ganglion cell, or any col­
lection o f chese retinal cells, or any synapse or collection o f
synapses, or che optic nerve or any o f che large number o f
visual cencers in che brain. For each componenc one muse
choose che stimuli and responses deemed to be ot inceresc.
The visual sysccm and each o f ics componencs is sensitive со
an unspecifiably large number o f stimuli and responds in an
unspccifiably large number o f ways. For example, a retinal
recepcor is responsive со light, pressure, chemical changes,
and electricity, and responds by changing ics membrane
pocencial, cemperacurc, optical properties, oxygen consump­
tion, and chcmical composicion. In addition, no cwo cclls
and no cwo eyes are exacdy alike. The visual system changes
over cime, because o f adapcacion, learning, and aging. Ic is
also an evolvingsyscem wich a hiscory and, we hope, a fucurc.
An invescigacor muse decide which aspcccsof che sysccm
со scudy and ac whac level o f generality and abscraccion.
There is no such ching as a complecc analysis o f any natural
syscem. The visual syscem is whac ic is. The descriptions and
cheories thac we erecc are human conscruccs based on an
arbicrary selection o f some aspecc o f che syscem derived for
some specific purpose and based on cercain assumptions.
Even when a funccional description has been found chac
mimics some aspecc o f the visual syscem, ic may noc specify
che physiological scruccures involved. The reason for chis is
chac a given function can be implemenced in many differenc
physical syscems. Conscruccing a functional description is
like defining che algorichm ot a process chac can be executed
by discincc machines, or hardware (see Marr 1982).
Syscems fall inco cwo main classes, linear and nonlinear,
each requiring very differenc experimencal and machemaci-
cal procedures. In very general cerms, a linear syscem is one
in which che response со input// plus input В is equal со chc
sum o f che responses со A and В separacely. This is chc p r in ­
ciple o f su p erp osition . Also, in a linear syscem, chc response
со a given inpuc is che same whenever ic is applied. This is
che principle o f cime invariance. In practice, any sysccm is
linear only over a cercain range o f scimulus values. A co m ­
plex sysccm such as chc eye behaves as a linear sysccm in
some respeccs and as a nonlinear syscem in ocher respeccs.
Componencs ot a syscem may be highly nonlinear and
yec produce a linear response when working cogecher. For
example, an amplifier may be nonlinear and produce a
discorccd oucpuc buc be linear when an error feedback signal
is added. The following provides only a very general guide
со syscems analysis and indicaces sources from which more
detailed information can be obcained. The analvsis of
concrol syscems is discussed in Seccion 3.3.
3 .2 .2 F O U R I E R A N A L Y S IS
The fundamencal assumption underlying linear syscems
analysis is chac che cransfer function o f a syscem is fully c h a r ­
acterized by ics responses to a sec ot sine-wave inpucs. In a
linear syscem,a sine-wave inpuc produces a sine-wave oucpuc
wich che same frequency. The signal can be shifted in phase
and ics amplicude eichcr acccnuaced or amplified. O ver che
pare o f che frequency spectrum tor which che change in
amplicudc is conscanc, che syscem is said со have a flac
response. A low-pass system accenuaces responses above a
specified frequency, and a high-pass syscem accenuaces
responses below a specified frequency. A band-pass sysCem
cransmics inpucs over only a limiced band o f frequencies. In
practice, che response o f any natural syscem begins со
weaken and evencually scops as che frequency o f che inpuc is
increased bevond a cercain limic. Thus, all nacural svscems
i *
arc eicher low-pass or band-pass syscems.
In 1807, Fourier escablished a fundamental cheorem,
which is used excensively in linear syscems analysis. His
paper was rejected and n ot published until 165 years laCer.
The core idea is chac anv wavctorm can be synthesized by
i t a
com bining a specified sec o f pure sine waves o f appropriace
amplicudes and in appropriace phase relationships. A pure
sine wave in che cemporal domain extends forever; ic has no
beginning o r end. A pure sine wave in chc spatial domain
extends indefinicely in space. If a complex waveform is peri­
odic and rcpeacs ac a frequency ot F H z, che componenc
sine waves include one wich a frequency o f F Hz (che funda­
mencal) plus sine waves wich frequencies chac arc multiples
of/-'. For example, che sine wave componencs o f a repecicive
square wave are a sine wave wich a frequency, F, equal со
chac o f che square wave, plus all odd harmonics ( 3 F, 5 F,
7 F , . . . ) wich amplicudes decreasing in inverse proportion со
frequency. Thus, che frequency componencs o f a repecicive
wavctorm are a series o f discrete componencs described
machemacically by a Fourier series.
If che waveform is aperiodic, che frequencies o f che co m ­
ponenc sine waves vary continuously and are described
machemacically by a Fourier incegral. In eicher case, che
F ou rier cransform o f a signal gives che amplicude and phase
ot each sine wave componcnc ot che original waveform.
The amplicudc o f each com poncnc sine wave as a func­
tion o f ics frequency is che am p litu d e speccrum o f che
signal. The phase o f componcnc sine waves as a function o f
frequency is che phase spectrum o f che signal.
A transient signal is known as an impulse, or delta
function. The Fourier amplitude spectrum o f an impulse is
particularly importanc. For example, chc Fourier spectrum
o f a sound pulse consists o f pure cones o f all possible Period

frequencies, all o f equal amplitude. The set ol pure tones

coincide (arc in phase) at only one m o m ent in time. At all
other moments they mutually cancel because they are out o f
phase. A narrow vertical line is a spatial impulse, which, in
the Fourier domain, consists o f an infinite number ol verti­
cal spatial sine waves o f equal amplitude, which arc in phase
only at that particular location. At all other locations, rhe
sine waves cancel со a constant (dc) luminance level.
The F ou rier power spectrum o f a signal is formed by
P hase angle
squaring the amplitude o f each frequency term in the
Fourier transform. The power spectrum has peaks at the ri*4c* Л.7. Sine a n d o>unefu?i\ tio)is.
frequencies to which the system responds most vigorously.
For a mathematical treatment o f Fourier analysis see
Bracewell ( 1 9 7 8 ) and Brigham (1 9 7 4 ). Applications o f W hen spatially modulated signals are used we have the spatial
Fourier analysis to the visual system are discussed in amplitude transfer function and the spatial phase transfer
Section 4.4.1. function. The spatial amplitude transfer function is often
referred to as die modulation transfer function, or M T F .
The simplest spatially modulated signal is a black and
3 . 2 .3 TRANSFER FUNCTIONS
whicc grating in which luminance is spatially modulated
The transfer function o f a svstem
i is some measure ot the according со a cosine or sine funccion. O ver a phase interval
oucpuc plocced against the same measure o f che inpuc. O n e from 0° to 360° che cosine function is symmetrical and chc
imporcant measure ot a linear system is its gain. Gain is the sine funccion is asymmetrical, as shown in Figure 3.7. That
magnitude o f some feature o f che output divided by the mag­ is why they are somccimcs referred со as even-symmetric
nitude o f the feature o f the input that drives the outpuc. and odd-symmetric functions. The spatial frequency o f a
A m plitude gain is the amplitude o f che oucput divided by grating is the number o f complete white-black cycles in one
rhe energy level o f che inpuc. For example the amplitude gain degree o f visual angle, expressed as cycles per degree (cpd).
ot a visual receptor is the amplitude o f che generator potencial The spatial period ot a grating is the reciprocal o f its spatial
divided by che intensity oflighr falling on it. Velocity gain is frequency, or che angular subtense o f one cycle o f che
the velocity o f some response o f the system divided by the gracing. The luminance amplicudc ot a grating is che differ­
velocity o f some input signal. For example, the velocity gain ence in luminance between che peaks and troughs. The
o f the visual pursuit syscem is the velocity o f an eye move­ M ich clso n co n trast o f a grating is the difference between
ment divided by the velocity o f the moving stimulus. In depth the maximum and minimum amplitudes divided by the
perception, gain is the judged distance o f an object divided by sum ot the two amplitudes, as shown in Figure 3.8.
its actual distance. A gain o f zero indicates that there is no
output and a value o f 1 indicates that the output equals the
inpuc. A gain greater than 1 indicates amplification. A nega­
tive gain indicates that the sign ot the input has been reversed.
In particular, a gain o f - 1 indicates that the output is the
exact opposice ot the input. Gain is sometimes expressed in
decibels. For amplitude gain,£, one decibel (dB) = 20logj g .
Thus, a ratio gain o f 1 is equivalent to a decibel gain o f zero.
A second im portant measure o f a linear syscem is its
phase shift. W h en a system is stimulated by a sine wave,
phase shift is defined as the phase o f the output minus that
o t the input, indicated by degrees or radians. W h en the
oucpuc is delayed wich respect со chc input we have a phase i C baracteriitkt o f л tine-w avegrating. Sp atial freq u en cy is the
lag, and when the output anticipates the input we have a n u m b er o f lu m in an cc m od u lation s per degree o f visual a n g le— the
phase lead. A 180“ phase lead or lag brings che input and recip rocal o f th e p eriod . T w o levels o f co n tra st arc illustrated.

output into antiphase. A 3 6 0 n lead or lag brings che inpuc L m ax + L m in

and output into phase again. M e a n lu m in a n ce = -----------------------
2
Sinusoidally modulated inputs are used to measure rhe
L u m in a n c e m o d u la tio n = L m a x - L m in
transfer functions ot a system. W hen che input is a temporally
L m a x — L m in
modulated signal we have che temporal am plitude transfer M ic h c ls o n c o n tr a s t = ----------------------
fu n ctio n and the tem poral phase tran sfer fun ction . L m a x + L m in
 Consider che image o f a sinusoidal gracing formed by an
optical system. The amplitude o f luminance modulation o f
the image is attenuated by the summed effects o f optical
aberrations, light loss, and light scatter. The am p litu d e
atten u ation produced by an optical system is the reciprocal
o f the gain o f the system. The spatial modulation transfer
function ( M T F ) o f the eye is the amplitude of luminance
attenuation o f the image o f a glaring on rhe у-axis as a func­
tion o f the spatial frequency o f the grating on the x-axis. In
any practical optical system, amplitude attenuation is co m ­
plete for all spatial frequencies above a certain value. This
simply means chac chc system can n ot resolve gratings above
a certain spatial frequency whatever their contrast.
The concept o f amplitude attenuation can also be applied
to the visual system as a whole, including the optics and the
neural processes involved in a persons ability to detect the
stimulus. In particular, human observers, like optical systems
are insensitive to gratings above a certain spatial frequency.
But they are also insensitive to gratings below a certain spa­
tial frequency— they have a band-pass characteristic. The
range o f resolved frequencies for a grating ot a given contrast
is the sp atial-frequcn cy bandw idth o f the human visual
system at that contrast. Gratings with frequencies outside
the spatial bandwidth appear as homogeneous grey patches.
From Fourier’s theorem it follows diat a visual display,
however complex, in which luminance is modulated along
only one spatial dimension, can be synthesized by superimpos­
ing parallel sinusoidal gratings, with suitable frequencies,
amplitudes, and phases. The gratings constitute the spatial
Fourier components ot the display. In practice, luminance
cannot be modulated about zero since there is no negative
light. All spatial patterns therefore contain a certain mean level
o f luminance, which can be regarded as a dc, or zero spatial-
trequency component added to the Fourier transform.
Any two-dimensional visual scene can be synthesized by
superimposing sets ot sine-wave gratings, with each set ori­
ented at a different angle in the plane o f the display. I f a set o f
spatial sine waves is transmitted through a spatially homoge­
neous linear system, the image consists o f a set o f sine waves
with the same spatial frequencies. The amplitudes ot com po­
nent spatial frequencies can be changed by different amouncs
in a linear system. A linear system may also displace, rotate, or
invert the image, because such transformations do not affect
spatial frequency. Strictly speaking, a linear system cannot
magnify or minify the input, with all frequencies scaled up or
down proportionally. However, most optical systems either
minify or magnify the image. This need not violate the
assumption ot linearity, since it is only the linear dimensions
o f the image that are minified or magnified, not the angles
subtended at the nodal point o f the optical system.
The spatial amplitude transfer function o f an optical
system is derived by using a photoelectric probe to measure
the luminance modulation ot the stimulus grating and ot the
image o f rhe grating at each o f several spatial frequencies
within the spatial bandwidth ot the system. The luminance
modulation o f a retinal image o f a grating is measured by
scanning a photometer over the reflection o f the image. The
ratio o fth e amplitude o f luminance modulation o f the image
to that o fth e stimulus defines contrast transmission, or gain.
This is plotted .us a function o f the spatial frequency o f the
grating to produce the spatial modulation transfer function
o f the optics o f the eye. This function indicates how effi­
ciently the eve’s optical system transmits spatial sine waves.
The modulation transfer function o f a linear system can be
used to predict the quality o f the image o t any pattern.
To specify an image in terms o f its Fourier components,
a Fourier analysis o f t h e stimulus pattern is first performed.
Each sine-wave component is then amplified or attenuated by
an amount determined by the modulation transfer function
o f the system. W hen the pattern is restored by Fourier synthe­
sis, it defines the spatial properties o f the image produced by
the system. The image is the result o f passing the visual display
through a set o f sine-wave luminance filters, each with an infi­
nitely narrow bandwidth. For a full specification ot the image,
one must also know the spatial phase transfer function. The
optical transtcr function is derived trom the amplitude and
phase transfer functions. W hen defined for all orientations o f
the image, it fully specifies the performance o f a linear optical
system in transmitting spatial information tor a given aper­
ture and optical axis. The temporal properties o f a system arc
specified by the temporal amplitude transfer function and the
temporal phase transfer function. O n e can combine two spa­
tial dimensions and time to produce a spatiotemporal
Fourier transform . This transform specifies the unique set ot
dritringsincwavc gratings at each orientation that arc required
to synthesize a given moving display. The spatiotemporal
transfer function o f a linear system is a complex-valued
function o f spatial and temporal variables.
Although a linear system can be formally described by a
Fourier transform, one need n ot assume that the system
contains distinct components that actually carry out these
operations. Any system capable o f detecting the spatial
Fourier components o f complex patterns efficiently must
fulfill three requirements:
1. It must possess a set o f independent and linear detectors
each ot infinite size and very narrow spatial-trequcncy
bandwidth.
2. It must be spatially homogeneous.
3. It must cncodc both amplitude and phase.
The visual system does not satisfy these conditions.
Receptive fields arc comparatively small and arc noc narrowly
tuned to spatial frequency. Also, they arc not homogeneous,
since they become larger and less dense in the peripheral
retina (Section 4.4.1a).
For an introduction to linear systems, see Toatcs (1 9 7 5 ).
For more details see Bracewcll (1 9 7 8 ), Cooper and M cG illem
( 1 9 6 7 ), and Brigham (1 9 7 4 ).
 3.2.4 P O IN T-SPR EA D AND LINE-SPREAD syscem produces. In an opcical sysccm, chc oucpuc is an
FUNCTIONS image chac can be measured with a physical instrument. The
methods used со decermine chc modulation transfer func­
The po in t-sp read function is a measure o f the optica!
tion of che eye are described in Section 9.1.3b.
quality o f an image. Ic is related to che modulation cransfer
Several mechods may be used со measure chc modula­
funccion. Ic is che distribution o f lighc incensicy over the
tion cransfer function o f che visual system as a whole, includ­
image o f a poinc o f light. Even wich a well-focused image,
ing neural processes. The amplicude ot the output can be
diffraction o f light by die pupil, optical aberrations, and
derived from objective responses in the form o f eye move­
light scatter in the eye cause each o b ject point to project as
ments or the responses o f a neuron or o f a set ot neurons at
a blurred disc in chc image. The image disc produced by a
a specified level in the visual system. O n the ocher hand, che
brighc poinc o f lighc, however small, necessarily tails across
oucpuc may be indicaccd by psychophysical judgmcncs
abouc seven cones (see Sections 5.1.5 and 9 . 1.3).
made under specified conditions. De Lange ( 1 9 5 8 ) was che
T he discribution o f lighc over che image o f a chin line o f
firsc со apply linear syscems analysis со psychophysical daca,
light is the line-spread fun ction . A thin line in che spatial
in his investigations o f visual flicker.
domain is a spatial impulse, or delta fu n ctio n in the Fourier
Cam pbell and Robson (1 9 6 8 ) first applied these m eth­
domain. Impulses are used widely in testing nacural and
ods to psychophysical data derived from che use o f spatial
man-made communication syscems because the Fourier
pacccrns modulaccd in luminance. In chis application, che
transform o f an impulse is a sec o f equal-amplicude sine
oucpuc o f che visual syscem is defined as che luminance con-
waves extending across che whole frequency spcccrum. The
crasc required for detection o f a sine-wave grating at some-
crescs o f all che waves o f the sine waves coincide at che loca­
specified criterion for detection. Threshold concrasc plocced
tion ot the impulse. A t all other places, crescs and croughs
as a function ot spatial frequency is the co n tra st sensitivity
cancel. A spaciocemporal impulse is a scimulus confined
fu n ctio n , or C S F . It may be regarded as the spatial transfer
boch spatially and in time.
function o f the contrast-dctection mechanism o f the visual
W h en che eye is exposed со a chin line, ic is as i f a com ­
syscem as a whole ac che concrasc chreshold. A cypical
plete- sec o f parallel spatial sine waves were simulcaneously
concrasc sensitivity function is shown in Figure 3.9.
injecced into the visual syscem. The amplicude cransfer func­
W e will see in Chapter 18 that an analogous sensitivity
cion o f che eye determines how each componenc is attenu-
function relates the threshold for detection o f a modulation
aced, and che Fourier integral o f the amplitude cransfer
o f depth in a textured surface to the spatial frequency o f
funccion o f a linear syscem is ics response to a spatial impulse
depth modulation. In general, the spatial amplitude trans­
(che line-spread function). Put another way, chc spatial
fer funccion ot a syscem is a mapping o f chc amplicude o f che
amplitude cransfer funccion is the Fourier transform o f the
oucpuc onco che amplitude o f sinusoidal inputs o f varying
line-spread function. The line-spread function and the
spatial frequency. The temporal amplitude transfer func­
transfer funccion are chus equivalenc represen rations o f a
tion is a mapping o f che oucpuc onco sinusoidal inputs o f
linear visual system. This mathematical relationship forms
the basis o f many inferences abouc che performance o f the
eye, corcical cells, and che visual syscem as a whole.
The line-spread funccion resulting from diffraction
imposes an upper limic on che spatial frequency o f a gracing
that can be imaged on the recina. This limic in cycles per
degree is called che c u c o ff frequ en cy and is given by:

„ rrr d К
Cutoff frequency = — X -------
1 ; A 180

where d is pupil diamcccr and A is che wavelengch o f the

lighc. Aberrations ocher chan diffraction reduce che cucoff
frequency below chis chcorctical limic. and we will see
in the next section chac che finest grating chac a person can
d etect is further limited by neural factors beyond the optics
o f che eye.

3.2.5 THE CONTRAST SENSITIVITY

FUNCTION
The m ethod used со decermine che amplicude o f che sys­
tem s output must be adapted со che type o f output chac chc
S patial frequency (cpd)
Figure V9. C ontrast sensitivity function. C o n tra s t sensitivity o f a hum an
observ er fo r a sinc-w avc g ratin g , w ith a lu m in an ce o f 5 0 0 cd / n r.
(Adapted from Campbell and Robson 1% 8)
varying temporal frequency. At suprathreshold contrasts,
the output o f t h e visual system is assessed by asking observ­
ers to match the contrast o f gratings at different spatial
frequencies (Georgcson and Sullivan 1975).
3 .2 .6 SIGNAL ANALYSIS
3 . 2 .6 a B asis F u n c tio n s
Any mathematical analysis applied to inpur or output sig­
nals is known as signal analysis. In applying such methods
one docs not necessarily assume that the system is linear.
The first task is to decompose the stimuli being considered
into a set o f basis functions. For example, sine waves o f dif­
ferent frequencies provide a set o f basis functions. Any well-
behaved complex function can be synthesized arbitrarily
closely by a set of sine and cosine functions, summed over a
range o f frequencies and phases. A lso ,a complex function
can be analyzed into its com ponent sine-cosine functions.
We can then ask whether the visual system as a whole ana­
lyzes complex visual stimuli in terms o f a specified set o f
basis functions. For this purpose, basis functions can be
regarded as a set o f filters applied to the visual input, o r we
can talk about a set o f visual channels or coding primitives.
Physiologically, a visual primitive in the space domain is
the sensitivity profile o f the receptive fields o f a set o f simi­
lar cells at the level o f the visual system being considered.
For example, at the level o f ganglion cells, the visual primi­
tives are the types o f receptive fields o f ganglion cells
(Section 5.2.2). The idea can be generalized to the spa-
tiotemporal response profiles o f cortical cells in V I or
higher in the visual system (Section 5.6.4).
It is important that the ser o f coding primitives is co m ­
plete. A set is complete with respect to a defined stimulus
domain when each discriminablc stimulus within that
domain can be represented by a distinct weighted sum o f the
primitives. For example, zero crossings (regions o f maximum
change in luminance) do n ot form a complete set o f visual
primitives because there are textures that appear different but
produce the same representations in terms ot zero crossings
(see Daugman 1990). G abor functions, described in Section
4.4.2, provide a complete set o f basis functions (Young 1987;
Koenderink 1990). In a complete coding system, the number
o f independent degrees ot freedom in the code is at least as
large as the dimensionality o f t h e stimuli.
A second important attribute o f coding primitives is
their linear independence. A coding process is optimally
efficient when the primitives are independent, so that each
primitive captures a property o f the input not captured by
any other. Independent primitives are often described as
orthogonal but, mathematically, primitives that are noc
orthogonal can be independent.
In biological sensory systems, detectors for distinct
sensory attributes are generally independent. For instance,
the color o f a line is noc affected by the lines orientation.
However, sensory detectors for a given feature arc n ot inde­
pendent— they overlap. For instance, visual orientation
detectors have broad and overlapping tuning functions,
which undersample the stimulus dimension to produce
metamerism. Such detectors are inefficient for resolution
but are efficient for discrimination, as explained in Section
4.2.7. They also econom ize on space within the detector
array.
A third attribute o f good coding primitives is their abil­
ity to exploit redundancies in stimuli, and thus economize
on signal transmission and processing (Barlow 1961). In a
nonrcdundant visual world, each point varies in luminance
over the full range ot values in a totally random fashion and
independently o f the luminance o f neighboring points.
Visual white noise has these characteristics. There is no way
to compress the signal from such a stimulus. Since long lines
are rare in a white-noise world, there would be no point in
having detectors tuned to line orientation. There would be
nothing to perceive in a white-noise world. In facc, natural
visual scenes contain redundancies, since points with simi­
lar luminance tend to cluster along lines or within areas and
persist over time.
For infinitely large homogeneous (shift invariant) detec­
tors, Fourier com ponents are the most efficient way to
transmit inlormation about spatially redundant stimuli
(Bossomaier and Snyder 1986). However, for detectors
with receptive fields o f finite size, like ganglion cells, wave­
lets based on oriented G abor patches with overlapping spa­
tial scales are well suited to exploit simple redundancies in
natural images. As explained in Section 4.4.2, they achieve
an optimal compromise between information preservation
and econom y ot sampling over each stimulus dimension
(Sakitt and Barlow 1982; Field 1987; Olshausen and Field
1996). Little attention has been paid to the most efficient
way to exploit temporal redundancy in natural images.
3 . 2 . 6 b C o n v o lu tio n
O n ce the sensitivity profile o f a linear detector is known,
the magnitude ot its response to any stimulus can be speci­
fied. The distribution o flig h t intensity across the receptive
field o f the detector is plotted. At each location across the
detector, stimulus magnitude is multiplied (weighted) by
the local value o f the sensitivity profile o f the detector.
The resulting function is the con volu tion fu n ctio n for
that detector. In general, the convolution function derived
from two continuous functions f{ t ) an d ^ (r) tor t > 0, is:
/ ( ') * „ ? ( ') = \ f { t - u ) g { u ) d u
The order ot the opcracions makes no difference, or f\ t)g {t)
g {t) f { t ) . Calculation o f a convolution function and its
inverse is eased by the fact that the Laplace transform o f a
convolution equals the product o f the Laplace transforms
ot the two functions (see the next section). The convolution
funccion can be integraced со yield a single number, which
represents the response o f that detector to that stimulus at
chat instant. Keeping the stimulus in che same locacion, the
procedure can be repeated for each o f the set o f detectors
that overlap the locacion o f che stimulus. The resulcing
numbers plotted against the positions o f the centers o f the
detectors yield a one- or two-dimensional spatial response
profile to that stimulus over chac region o f chc recepror
surface. O n e could convolve the spatiotemporal sensitivity
functions o f a sec o f cells wich rhe spatiotemporal distribu­
tion ot stimulus intensicy to derive a function that repre­
sents the total response o f the syscem to a stimulus over a
defined time interval.
3 .3 LINEAR C O N T R O L T H E O R Y
C o ntro l theory was developed in response to che need to
design physical systems that achieve some specified goal in
response to changing conditions. The syscem may be a
simple thermostac, an automatic pilot in an aircraft, or
the cleccric grid system. The branch o f control theory
concerned with understanding how human operators inter­
act with a physical control system is known as human
factors.
C o ntro l theory is also concerned wich che design o f
models that simulate the responses o f a naturally occurring
system to specified inputs. In it simplest form, a ' model” is
rhe transfer function o f che whole syscem. The svscem is
treated as a single "black bo x” with a single transfer func­
tion. Finer levels o f analysis can be achieved by dividing rhe
model into a set ot in-series or parallel components. Each
com ponent is a “black box” specified only by its transfer
function. Its internal structure is undefined. The combined
transfer functions o f subcomponents equal che cransfer
tunction o f the whole linear system. There is no theoretical
limit to the extent to which a model can be subdivided.
O n ce a model has been designed it is implemented by a
sec o f physical com ponents with the same transfer functions
or by a computer program. The model is assessed by measur­
ing how closely its outputs to specified inputs resemble
those o f the system being modeled. A model consists o f an
input stage, with appropriate filters, one o r more in-series or
parallel controllers with defined transfer functions, and an
oucpuc chat changes the state o f the thing being controlled.
The thing being controlled may be a defined part o f the
system, known as the “plant,” an external object, or another
svstem.
The flow o f signals from che input to the output is
the forward loop o f che syscem. Feedback loops convey
error signals trom some later stage in che system to one
o r more com ponents ac earlier stages. An error signal
usually modifies che response o f a com ponent so as со
rescore the oucpuc o f che system со som e defined goal stace
(Figure 3.10).
кinure У Io. B asic d em en ts o f a lin e a r сon h o ! system .
In proportional error control, the feedback signal is pro­
portional со the error. W ith constant input, proportional
control results in a steady-state error. The sceady-stace error
may be reduced by incegracing chc error signal over a time
interval (integral control). However, this renders che syscem
insensicive со rapid fluctuations in input— it lowers its fre­
quency response. Differenciacion o f the inpuc improves che
frequency response buc renders che system insensitive со
constant inputs. Models usually contain both integral and
differential elements. The stability and accuracy o f a concrol
syscem m aybe improved by adding appropriate filters in the
forward loop or feedback loop. C om puter programs, such
as C A D software can be used to design appropriate filrers.
The error is sampled ac defined intervals in a sampled data
system, and continuously in a continuous sysccm.
Many biological systems can be described by a differen­
tial equation. For example, the force ( f ) required to rotate
an eye or move an arm is the sum o f three forces.
1. Force со overcome elascicicy, which is resistance chac
depends on posicion 0 .
2. Force to overcome viscosity, which is resistance that
depends on velocity, d9 jdr.
3. Force to overcome inertia, which is resistance chat
depends on acceleration, d O/dt'.
A coefficient is the value o f a tunction when the variable is
set at unity. If che coefficient o f elasticity is E, that o f viscous
resistance is К and that o f inertia is M (mass), then:
F -_E e + v < * ^
dr dr
A first-order system contains no terms higher than the
velocity ccrm, and a second-order system contains an
inertial term.
Differential equations are not easy со solve because chc
terms are not algebraic quantities that can be added or sub­
tracted. The differencial of an exponential function equals
the value o f the function, so that if we convert the terms o f
a differential equation into exponential functions then we
can creac chem as algebraic quantities. This is whac che
L ap lace tra n sfo rm docs. Mathematically, the Laplace
transform is derived from rhe convolution o f the function
to be solved, f ( 0 ) , and an exponential function, i'° with
exponent s9 . The function с 0 is known as che kernel,
and the Laplace transform is denoted by F(*). It is the area
under the curve formed by multiplying the function and T a b le /. SO M F. F U N C T IO N S A N D L A P L A C E

the kernel at each value ol в This process is represented by TRA N SFO RM S

the formula:
L a p la c e
••
In p u t fu n c tio n s tra n s fo rm
F U ) = \ ' - * f( e ) d e
0
Im pulse у = infinity
W h en fO is zero for negative values o f в and the real at x = 0

parr o f the complex variable s is zero, Laplace and Fourier

transforms are the same. I
S te p у = К for x>0
The Laplace transform o f each term in a differential у = 0 for x<0 s
equation is found in a table. The overall solution of the
equation is then obtained by algebraic procedures. The
Linear ram p К
у = Kx
resulting Laplace transform is converted back into non -
г.aplacian form by again looking in the table. In general, all
bounded continuous functions have a Laplace transform.
In most practical cases, a function has a unique Laplace E xponential decay у = e -ax I
s+a
transform and a transform has a unique inverse function.
For example, the Laplace transform o f an exponential
function, e ‘l is Sine w ave sin (wf) ot
*■* K I 7 s2+tu2
F ('" ) = \ e “/ ( e " ) *

E xponential e - w sin (lvt) ш

Since s is not a function o f time, it is treated as a constant. dam ping ( s + 0 ) 2 +- ft»2

F (e" )= | « dt
t -i)
1 r
s— a
1
s -a
Table 3.1 shows examples o f Laplace transforms o f input
functions and of transfer functions that describe the way
the system transforms the input.
For example, let the input be a step and the transfer
function be integration. In Laplace terms the input is 1/s
and the transfer function is 1/s. The output is the product,
namely 1/s2, which is the Laplace transform o f a ramp. Thus,
a step passed through a system that integrates produces a
ramp output.
I f a system contains several linear processing stages in
series, the overall gain is the product o f the com ponent
gains and the overall phase lag is the sum o f the com ponent
phase lags. Also, the Laplace transform o f an in-series set o f
com ponent transfer functions is che product of the Laplace
transforms o f the separate transfer functions. The Laplace
transforms of linear in-parallel cransfer functions may be
summed. ’I hus, a single transfer function can be derived for
the whole linear system. The Laplace transform o fth e input
times the Laplace transform of the transfer function o f a
system gives the Laplace transform o f t h e output.
A mismatch between the output and some specified
goal state generates an error signal, £ . This signal can feed
back to the input with sign reversed. This brings the output
closer to the goal state, which reduces the error signal.
T ra n s fe r fu n c tio n s
dy
Differentiation
dx
2nd deriva tive d 2y
dx2
I
Integration M t)d t s
This process continues until the output hovers about chc
goal state. The Laplace transform o f t h e error signal fc'CO
equals the Laplace transform o f t h e input, л(.'), minus che
Laplace transform o f t h e output, y(s). For an introduction
to Laplace transforms see Grove ( 1991) .
The e lo sed -lo o p gain,£(.<) o f a system is the amplitude
o f some attribute o f t h e output divided by che amplicude o f
che same attribute o f che input when the system is operating
under feedback control. For example, the closed-loop gain
o f vergence can be defined as the vergence movem ent o f the
eyes divided by the opposed angular displacement o f che
images in the two eyes. G ain may also be defined in terms
o f other attributes o f the stimulus and response, such as
velocity. Gain in decibels is 2 0 times the logarithm o f p ro­
portional gain. Thus, a proportional gain o f 1 is equivalent
to 0 db.
The o p c n -lo o p gain, G(s) o f a system is the amplitude
o f t h e oucpuc divided by che amplicude o f che inpuc when
che feedback loop is cut. For example, this can be done by
feeding che signal from an eye-movemenc monicor to a
mechanism that controls the m otion o fth e stimulus, so that
che image does not move when che eyes move. There is
a simple relationship between G(s) and the closed-loop
g a in ,^ ):
e{s) = x { s ) - y { s )
y{s) = G(s)e{s)
;( .( ) = G ( .« ) [.v ( i) - y ( i) ]
;'U )| l + C ( j) ] = 6'(i).vU )
M - G{S) ( \
A s) I ^ ( 7)xU)
y{s)
^ = <?(*)
x{s)
G{s)
Therefore =
+ G(s)
If the feedback mechanism has rhe transfer function H(s)
then the closed-loop gain is:
G(s)
# (* ) =
Thus the closed-loop gain equals the open-loop gain divided
by the open-loop gain minus one. For example, if I/(s) is 1
and the closed-loop velocity gain o f visual pursuit is
0.9 then the open-loop gain is 9. Thus the eyes will move at
9 times the velocity o f the visual target if the feedback loop
is cut. If the closed-loop gain is 0.5 the open-loop gain is 1.
I f a sinusoidal signal is applied to a linear control system
the output is also sinusoidal, with the same frequency. The
amplitude o f rhe output may be larger (positive gain) or
smaller (negative gain) than that o t the input. Also, the gain
may vary with the frequency o f rhe input. A graph o f gain
against the frequency o f the input to a system is known as
rhe gain B o d e plot.
The phase lag ot a linear control system is the extent to
which rhe output lags the input, measured by rhe phase
angle between a sinusoidal input and the corresponding
sinusoidal output. A plot o f phase lag against rhe frequency
o f the input is the phase B o d e plot. If phase lag is a co n ­
stant fraction o f the period o f rhe input it is a constant
time lag.
Many processes, such as a swinging pendulum, have a
natural frequency o f sinusoidal oscillation. W h e n the driv­
ing function o f an oscillating system is switched otf, the
amplitude o f oscillation decays because o f friction and vis­
cous damping. The amplitude, в ot a damped oscillation ot
frequency ft» can be described as the product o f a sinusoidal
f unction and an exponential damping function, as shown in
Figure л. 11, and described by:
9 = ac * sin со/
where a and b are constants. The rime taken for a sysrem to
reach a steady state after a stimulus has been switched on
Пцхи* у 11. A dam pin gfu n ction . R ep resen tin g che ex p o n en tial d ecay o f a
sinusoidal oscillacion .
also depends on the damping ot the system. It damping is
set to a critical value, the system changes from one state to
another without sinusoidal oscillations. If a system is over­
damped, it reaches the steady state more rapidly than a
critically damped system. An undamped system will either
oscillate indefinitely, or become unstable. A system will be
unstable if the gain o f the feedback loop is greater than 1 or
if the phase lag of the feedback loop exceeds a critical
value.
The stability o f a linear system can be investigated
by plotting gain against phase on polar coordinates,
a graph known as the Nyquist diagram . It can also be inves­
tigated by the roo t locus procedure (lTAzzo and Houpis
1995).
Many neural systems show spontaneous or stimulus-
initiated oscillations. Two coupled oscillators are phase
locked when the phase between them is constant. Two cou­
pled phase-locked oscillators in antiphase arc in push-pull
mode and their combined output is the difference between
their amplitudes. Tw o oscillators in phase are synchronized.
A chain o f coupled phase-locked oscillators can generate a
traveling wave. For example, the m otion ot a snake is gov­
erned by a traveling wave o f neural activity. Synchronized
neural systems are discussed in Section 4.3.4.
Exponential functions describe the time course o f many
natural processes. Any natural process has a tim e co n stan t,
which indicates how rapidly it reaches a new steady state
when disturbed.
The general exponential function, as graphed in
Figure 3. 12 is^ = a t* . C onstan t a defines the intersection
ot the tunction on the у -axis. Constant b defines the
slope o f the function. W h en b is positive, the function
describes a growth process and when b is negative it describes
a decay process. The number e is the base o f natural loga­
rithms and equals 2 .7 1 8 . It equals che sum ot the following
series:
1 1 I 1 1
e - — I— H— H------ h— ...
0! 1! 2! 3! 4!
 I f г equals one second, che function falls со 1 o f ics initial
value in one second. The cime constant is a measure ot how
long it cakes a process со decay. Many natural physiological
and perceptual processes obey an exponential funccion
approximately. For examples o f models applied со vcrgcnce
eye movements see Section 10.5.11.

3 .4 ANALYSIS OF N O N L IN E A R
SYSTEMS

The response o f a linear syscem to any inpuc can be calcu-

laced when ics response со each o f an appropriate sec o f sine
waves (or, equivalencly, its response со an impulse) is known.
This is because any signal can be rep resen ced as a sec ot sine
waves o f appropriace amplicude and phase. This is noc crue
ot a nonlinear syscem. There are many cvpes o t nonlinearity,
and there is no general method for characcerizing all non ­
linear systems. However, several procedures have been
Raised to a power .v, it becomes: applied to the visual syscem. Types o f nonlinearicy in che
0 1 2 * 4
visual system are listed in Section 4.4.4.
. .V .V X X X
с = ----- 1------ 1-------1------ 1----- In chc Volccrra mechod ic is assumed chac nonlinearicies
0! 1! 2! 3! 4! arise trom inceraccions becween impulses occurring ac dif­
W h en e* is differentiated, the series is unchanged since each ferenc times. For a single dececcor generating impulses ac n
term bccom cs the term before ic: differenc cimes, che potential interaction between impulses
J x 01 2 5 4 is proportional to che produce o f cheir inccnsicies. The con-
de x x x x x
——= — i— н-------1------ 1— ... cribucion o f interactions to the response o f the syscem ac
dx 0! 1! 2! 3!4! cime t is che producc o f impulse inccnsicies over che sec o f
This means chat the slope, or differential, o f an exponential cime intervals multiplied by a function o f the n time inter­
function, is everywhere equal со the value o f the function ac vals, a function known as a Volterra kernel. The svstem is
chac poinc. characterized by the integral o f these products over che sec
ot n impulses. The zero-order cerm, or kernel, indicaccs che
response when no scimulus is presenc. For low-amplicude
dx stimuli the firsc-order cerm (n = 1) dominaces che response,
In ocher words, rhe race o f growth or decay ot an exponen­ and che kernel is che linear componenc o f che sysccm.
tial funccion is proportional со the presenc magnitude o f A linear syscem has no cerms higher chan che firsc. Higher
the funccion. For example, if rabbits were lefi to reproduce rerms indicacc deviacions from linearicy, which become
unhindered, the increase in numbers would follow an expo­ more apparent as signal size increases. The mechod can be
nential funccion because the race at which chey reproduce generalized со a system o f multiple inpucs.
would be proportional со che number o f rabbics. During World War II, W iener developed the mechod ot
My = t then .v= log^y. Thus, an exponential function is W iener kernels for invcscigacing nonlinearicies in re flee ced
che inverse o f a lo g a rith m ic funccion. sonar signals. The mechod is defined in Cerms o f a system’s
In the time domain, a*, in the equation у = equals response со whice noise and can be used for syscems chac
cime, t. Let b =1 /Т where г is che time conscanc. Then an (1) do noc change rapidly over cime and (2 ) becom e linear
exponential function o f time is: as signal screngch is reduced. Firsc, chc response o f chc
syscem со Gaussian (whice noise) stimuli is measured. Then
i
che W ien er kernels arc calculaced. These are essentially
y —ae r
orchogonal cerms in a power series. O n ce che kernels arc-
W h ere a is che value o f у ac cime zero (a^ = a, since = 1) known, chc response o f che syscem со any inpuc waveform
and r is che cime ac which у = ae'\ W h en t - x , can be calculated.
The zero-order cerm represencs che response o f che
у —ле 1——■- —- — —0.368л syscem со a scacic inpuc. The firsc-order cerm represencs che
* 2.718
linear characceriscics ot che response, and higher cerms rep-
Thus, after cime г che value o f the exponential function rcsenc nonlinearicies. The values o f the kernels depend on
falls со abouc one-chird o f chc value ic had ac cime zero. che nacure ot che scimulus. Ideally, responses со an infinitely

M a i e p i a n , за х и щ е н и й а в т о р с ь к и м прав ом
long Gaussian white-noise stimulus allow one to predict the
response o f the system to any stimulus, because all stimuli
are contained in white noise. In practice, one must use finite
stimuli o f limited spatial and temporal bandwidth (for
details see Marmarelis and Marmarelis 1978).
Л variant ol the W ien er kernel m ethod, which has
improved signal-to-noisc ratio, involves testing a system
with a small set o f superimposed sine waves rather than
white noise (B en n ett 1933). V ictor ( 1 9 7 9 ) used this proce­
dure to analyze responses o f single neurons in the visual
pathway (see Section 5-6.4).
In another approach, the stimulus consists o f a spa­
tiotemporal sequence ot binary signals in the form o f a grid
ofblack and white squares modulated in time (Sutter 1992).
The display is constructed from a repeating binary sequence
o f length 2n - 1, known as a maximum length shift-regiscer
sequence, or M -seq uen ce. The order o t n is made suffi­
ciently large so that the repeating sequence is not apparent.
Such a sequence approximates a white-noise stimulus, since
all spatial and temporal frequencies are represented equally.
The stimulus is easy to generate and allows tor rapid calcula­
tion o f the first- and higher-ordcr W ien er kernels. For
example, a two-dimensional M-sequence display has been
used to map the spatiotemporal structure o f t h e receptive
field o f a cortical cell (Reid et al. 1997).
The structure o f the stimulus determines which aspects
o f a cell’s receptive field are revealed. For a linear system, a
sparse stimulus is sufficient, because only the first W iener
kernel is relevant. For nonlinear systems a reasonably dense
stimulus is required to reveal the higher-ordcr kernels. For
example, more details o f a cells receptive field are revealed
with finer stimuli modulated at higher temporal frequen­
cies. However, a finer stimulus has less stimulus energy and,
it the stimulus exceeds the resolving power ot the visual
system, it becomes indistinguishable from uniform grey.
The overall transfer function o f a linear system does not
reveal the presence or nature o f linear com ponents because
the same overall transfer function can arise from a multi­
tude o f equivalent components. To explore the inner work­
ings ot a linear system one must probe the input-output
relations o f each com ponent.
For a system consisting ot a cascade ot linear and n o n ­
linear components, the characteristics o f the nonlinear
com ponents can uniquely determine the response charac­
teristics o f the whole system (Spekrcijse and Re its 1982;
Korenberg and Hunter 1986). For example, when stimu­
lated with superimposed stimuli o f frequency F x and F ,, a
nonlinearity, such as rectification, produces cro ss-m o d u la ­
tion produ cts, or complex harmonics, o f the general form
nF{ ± for integral values o f я and m. The relative ampli­
tudes ot these terms depend on the nature o f the non lin­
earities.
Regan and Regan ( 1 9 8 8 , 1989) provided a mathemati­
cal analysis o f these methods and applied it to the process­
ing ot binocular signals (Section 11.7). This method is more
immune to che effects o f noise than arc W ien er kernel
methods.
Nonlinear systems may also be studied by building an
analogcomputer with similar nonlinear features, and having
it compute outputs to defined inputs. The analogcomputer
constitutes a model o f those aspects o f the system being
studied. The adequacy ot the model is tested by seeing how
well it simulates the behavior o f the system with previously
untested inputs. Also, a digital computer can be pro­
grammed to simulate a nonlinear system. For example,
Lehky et al. (1 9 9 2 ) characterized the nonlinear receptive
fields ofcom plcx cells o fth e monkey visual cortex by record­
ing the responses o f cells to a great variety of patterned
stimuli. An artificial neural netw ork was then created for
each neuron, using an iterative optimization algorithm. The
responses o f t h e ccll to some stimulus patterns defined the
training set for the neural network. The cell’s responses to
patterns n ot used in the training set were predicted with a
median correlation o f 0.78.
For discussions of ncural-network methods see
Rumelhart and M cClelland ( 1 9 8 6 ) , H inton ( 1 9 8 9 ), and
Miller et al. ( 1991) .
Neural network models can be used to characterize the
reccptivc-ficld structure o f cells, but do not indicate the
function o f the cells. Network models o f binocular dispar­
ity processing are discussed in Section 11. 10.2. For a discus­
sion o f nonlinear visual processes see Pinter and Nabet
( 1 9 9 2 ).
3.5 TIM E SERIES
The above discussion o f analysis o f events over time is part
of the broader subject known as tim e series analysis. A
time series is a scries o f measurements o f a defined process
made over time. T im e series analysis is designed to reveal
trends and recurring events in a single process (univariate)
or relationships between two or more processes (bivariate
or multivariate). The methods also apply to series o f mea­
surements made over space.
The first task in analyzing a time-varying or space-vary­
ing signal is to distinguish between signals due to changes
in the input to the system from those due to noise fluctua­
tions. Noise often consists o f high-frequency random fluc­
tuations, which can be removed by taking a moving average
over successive sets o f data points. This is tantamount to
passing the data through a low-pass filter.
'I he effects o f noise can also be reduced by applying
a well-defined stimulus many times and averaging the
responses over many cycles o f stimulus repetition. Signal
averaging emphasizes com ponents in the response that are
time-locked to the stimulus, and attenuates com ponents
due to noise, which average out over several cycles o f stimu­
lus repetition because they arc nor correlated between one
repetition and the next.
 Standard signal-averaging procedures overlook episodic
noise such as bursts and oscillations. Thcscr events can be
characterized by phase-locked spectral analysis, which
measures the dilierence between responses to each cycle
o f a periodic stimulus and the response average. Standard
signal-averaging procedures also tail to register stimulus-
engendered variations in response to particular cycles o f a
periodic stimulus. Episodic activity generated by the stimu­
lus, but not time-locked to it, can be revealed by power
spectrum analysis or as peaks in the autocorrelation func­
tion, as described below (Schitf et al. 1 999). Long-term
variations can be removed by passing chc data through a
high-pass filter. Signal averaging has been used extensively
in the analysis o f cortical activity (Section 11.7).
Trends can be revealed by fitting the data to a defined
polynomial function by the least mean squared error proce­
dure. W h en data are passed through two filters in series, the
final output is obtained by the process o f convolution,
which was described in Section 3.2.6b. These procedures
can be found in any textbook o f statistics.
The au to co rrelatio n fu n ctio n is one ot the main tools
for revealing recurrent patterns in a process. The correlation
coefficient is derived between N observations made at
repeating intervals o f time o r space and the identical set o f
observations displaced by a lag interval of k. W h en к is zero,
the correlation coefficient is necessarily 1. This value is
ignored. The correlation coefficient, >y between the set o f
measurements made at interval t (.v) and those made at
interval t + 1 (x + , ) is firsr obtained. This is essentially the
mean ot the products ot the paired deviations from the
mean divided by the sample variance. It is a measure o f how
similar the value o f the function at interval / + 1 is to its
value at interval r. In this case, the lag interval, k, is 1, and
the coefficient measures any tendency for neighboring
events to be related. Then measurements two intervals apart
(к = 2) are correlated to give and so on for values o f X-
usually no greater than N /4. Each o f the к correlation coef­
ficients, rt, can be plotted as a function ot the lag interval
(k) to give the autocorrelation function, or correlogram.
The process should be stationary; that is, it should n ot co n ­
tain long-term trends. For a random series o f events, all
coefficients tor £ > 0 varv
/ randomly
/ about zero. Л series
containing short-term dependencies, in which neighboring
values tend to be the same, shows large coefficients for small
values o f к. Л scries with a regular alternation shows coeffi­
cients that alternate in sign. The coefficients o f a sinusoidal
series also vary• sinusoidallv.
* Peaks in the autocorrelation
function can represent the contributions o f different tem ­
poral o r spatial frequency components. Autocorrelation
functions will be encountered in Sections 11.10.1 and
13.1.4b.
I chastic process does nor allow short-term predictions while
he power spectral density fu n ctio n o f a process rep­
resents the contribution o t each sinusoidal spatial or tem ­ a chaotic system does. Also, the autocorrelation functions
poral frequency to rhe variance o f a series o f measurements.
The area under the whole spectral density function is
the variance o f the whole time scries. The spectral density
function is in the frequency domain, and the autocorrela­
tion function is in the time or space domain. However, they
are closely related. A spectral density function based on a
total variance normalized to 1 is the Fourier transform o f
the autocorrelation function.
In bivariatc analysis, a scries o f measurements o f one
process can be correlated with measurements o f a second
process over lag intervals trom 0 to some specified value to
produce a cro ss-co rrela tio n fun ction . After allowance has
been made tor contaminating effects o f autocorrelations in
each process, the cross-correlation function reveals comm on
fluctuations in the two processes over time or space. For
example, the visual system can be said to cross-correlate the
images in the two eyes over a spatial transformation to
reveal how one image should be matched to the other
(Section 15.1).
A cross-spectral density fu n ctio n is the Fourier trans­
form o f the cross-correlation function between two pro­
cesses. There are several forms o f the cross-spectral density
function. The cross-amplitude spectrum measures how the
amplitudes o f two processes are related, and the cross-phase
spectrum indicates how their phases arc related.
The c o h e re n ce fu n ctio n is the frcqucncy-domain
analog o f the squared cross-correlation coefficient. It
expresses the extent to which two processes covary as a
function o f frequency and has been used in the analysis o f
synchronous neural activity (Scction 4.3.4g).
A c h a o tic system is one in which a small change in its
state at time zero leads to an exponential growth in uncer­
tainty about its future state. The Earths atmosphere is
chaotic. C ortical neural networks with recurrent excit­
atory and inhibitory circuits m aybe chaotic (Van Vreeswijk
and Sompolinsky 1996). Chaos imposes a limit on our
ability to predict behavior. Short-term predictions are to
some extent possible in a chaotic system, but not long-term
predictions.
The French mathematician Rene Thom developed a
branch o f mathematics known as ca tastro p h e theory. The
theory has been used widely in biology, sociology, eco n o m ­
ics, and psychology to dcscribc systems that undergo sudden
changes o f state, like the stock market, outbursts o f anger,
and nerve impulses. However, many o f the models based on
catastrophe theory have come under attack because o f their
lack o f mathematical rigor and their disregard for empirical
evidence (Kolata 1977). There seem to be no applications
to space perception.
A stoch astic svstcm
¥ is formed from a multitude ot
independent interacting factors. The output o f a stochastic
system resembles that o f a deterministic chaotic system, and
it is difficult to distinguish between them. However, a sto ­
o f the two types o f system differ. Stochastic analysis has
been applied to binocular rivalry (Section 12.10).
 For a general account o f time series analysis see Chatfield
( 1 9 9 7 ). T im e series analysis can be applied to the dynam ics
o f n on lin ear systems. This branch o f mathematics has not
been applied to any o f the topics discussed in this book. For
an introduction to nonlinear dynamics see Kaplan and
Glass ( 1 9 9 5 ) and W ilson (1 9 9 9 a ).
3.6 BAYESIAN IN FER EN C E
In 1763 T . Bayes published a theorem concerning how
people make judgments when playing games. The modern
form o f Bayess theorem was developed by Laplace ( 1812) .
Sec Dale ( 1 9 8 2 ) for an account o f the early history o f Bayess
theorem.
Bayesian analysis applied to perception has its roots in
Helm holtz’s theory ot unconscious inference, which is
summed up by the statement, “such objects arc always imag­
ined as being present in the field ot view as would be there
in order to produce the same impression on the nervous
mechanism, the eyes being used under ordinary normal
conditions" (H elm holtz 1910, vol. 3, p. 2).
Bayesian inference is based on conditional probabilities.
A conditional probability o f event A, given a particular
value o f state В is expressed by p { A \ B ) . A conditional
probability o f event A can be expressed over a range o f
values o f state В to yield a probability distribution o f
event A over variable B. For example, we could state the
probability o f a man’s being bald at each age between 1 and
100 years.
Like any other account o f perception, Bayesian analysis
starts by defining a stim ulus d o m a in ( S D ) . A visual stimu­
lus domain is a set o f objects or events defined with respect
to specified visible features and selected values ot those fea­
tures, plus the rules o f composition and transformation of'
those features and values. The stimulus domain is not merely
a stimulus that happens to be present at a given mom ent but
rather the defined set from which particular stimuli are
drawn.
The complete stationary visual stimulus domain is the
set o f discriminably different scenes. If the scene were
broken down into a 1,000 by 1,000 pixel array with each
pixel occurring at one o f 10 discriminably distinct levels o f
luminance, the stimulus domain would contain 1 0 : :" " li:
displays. F.ach display would, in theory, produce a distinct
response. A world consisting o f random sequences ot such
arrays would concain no redundancy and no structure.
There is no point in thinking about such a domain except to
measure the ability to detect whether cwo such displays are
correlated (Section 15.2.1).
For a synthetic stimulus domain, such as displays on a
computer monitor, rhe rules o f feature com position and
transformation may or may n ot conform to those in natural
scenes. Stimulus domains defined with respect ro natural
objects or events necessarily conform to natural rules o f
composition and transformation. However, it is only
selected features o f objects, not the objects themselves that
arc in a visual stimulus domain used in an experiment. Any
natural object has an unspecifiably large number o f features,
many o f which, such as temperature, atomic structure, and
weight, are not visible unless transduced by an instrument.
Thus, an unspecifiably large number o f stimulus domains
can be defined over a given set o f natural objects. Scientific
instruments reveal ever more properties o f natural objects
but they have n ot revealed all rhe properties o f any natural
object.
Each member o f rhe set o f static or dynamic visual dis­
plays in a well-defined stimulus domain has a certain pro b­
ability o f occurrence. The distribution o f probabilities over
the set o f displays is the prior probability distribution o f
the stimulus domain, or d o m ain prior, denoted by p{SD).
A domain prior may be defined in terms ot a set ot stimuli
used in an experiment o r in terms o f the probabilities o f
occurrence o f specified objects or events in a given context
in the natural world.
Consider an observer who makes certain assumptions
about a given stimulus domain. The set o f assumptions, cor­
rect o r incorrect, about the set o f stimulus objects is the
o b serv er’s stim ulus d o m a in , (OD). I f some o f the assump­
tions are correct, the observer knows something about the
domain. For an observer with correct and complete knowl­
edge o f the domain, SD = OD. The observer may have
assumptions about the relative probabilities o f various dis­
plays in the stimulus domain. The distribution o f assumed
probabilities over the set of displays is the observer s prior
probability distribution, or observer prior, denoted by
P(OD).
A particular retinal image can arise from more rhan one
object. For example, an inclined circle and a frontal ellipse
can produce the same retinal images. Identical images p ro­
duced by distinct distal stimuli are essential am bigu ities ot
the stimulus domain. Image ambiguity can also arise because
o f noise in the visual system, such as optical opacities, light
dispersion, distortions, scotomata, or eye tremor. Som e o f
these sources ot noise can be allowed for. For example,
the effects o f chromatic aberration can be discounted
(Section 4.2.9c) and so can the effects o f eye tremor. O th er
forms o f noise, such as defects o f accommodation, involve
loss o f information, which cannot be restored. These are
essential sources o f noise. However, an observer may know
what type o f information is missing and thereby estimate
the degree o f uncertainty introduced by an essential source
ot noise.
The distribution o f the relative probabilities o f obtain­
ing a given image, /, overall displays in the stimulus domain
is the dom ain lik elih o o d fu n ctio n , denoted by p ( l \S D ) .
'Ihe domain likelihood function can be derived onlv
/ by
* a
person with complete knowledge o f the stimulus domain
and o f the transmission characteristics o f the visual system.
The likelihood function derived from whatever assumptions
chc observer makes about these things is the o b serv er lik e ­
lih o o d fu n ctio n , denoted by />(/ 1OD) .
A visual system has access to only the retinal image and
must decide which display in the stimulus dom ain most
probably produced that image. C onsider an observer with
com plete knowledge oi the stimulus dom ain and of the
image form ing system. Each display o f the stimulus domain
will have a certain probability o f producing a given image.
The distribution o f these probabilities over all displays o f
rhe dom ain is the posterior probability distribution for a
given image, or simply the dom ain p o ste rio r, denoted by
p\SD |/ ) . The probability that a given image has been pro­
duced by display X rather than by display Y will depend on
the relative probabilities o f occurrence o f the two displays,
p{SD), and on how likely it is that each display could pro­
duce that image, p ( l \S D ) . M ore precisely,
p (S D \ l)ap (l\ S D )p {S D )
Dividing by a norm alizing factor />(/) we obtain the basic
Bayesian formula.
/>(/)
The norm alizing factor is simply the integral o f all products
o f likelihood functions and priors.
’Ihe dom ain posterior indicates the probabilities that
each o i the possible stimulus displays could produce a given
image in a given visual system. The final decision about
which display is present will depend on the gain fu n ctio n ,
that is, risks or costs involved in m aking particular errors o f
stimulus identification. C h oo sin g the mode, o r maximum
o f the posterior distribution, maximizes the chance o f
selecting the correct stimulus. O n the o ther hand, choosing
the mean o f the distribution m inim izes the least square
error ot the estim ate. The range o f proximal stim uli that are
accepted as arising from a given o b ject also depends on the
gain function. For example, it is better to falsely conclude
that a dangerous o b ject produced an ambiguous image than
to falsely conclude that a harmless o b ject produced the
stimulus.
A fully determ ined stimulus dom ain is one that can be
в
fully described in term s o f either specified features or speci­
fied rules o f com position. For example, the five regular
polyhedra are fully specified by their sides, edges, and co r­
ners. Linear perspective is an ideal dom ain specified by rules
o f transform ation because projections from three to two
dim ensions can be fully specified (Section 2 6 .1 .1 ). The
inverse projection is underdetermined because a given
image can be produced by different objects. An ideal per-
ceiver is one that has com plete knowledge o f a stimulus
dom ain and o f che uncertainties introduced by visual noise
and essential am biguities (Section 4 .6 .3 ). Such a perceiver
can identify displays accurately w ithin lim its set by essential
ambiguities. Hum an observers fall short of the ideal when
they have lim ited knowledge o fth e stimulus dom ain or o f
visual noise. The perform ance o f a human observer can be
assessed with respect to that o f t h e ideal perceiver only for
stimulus dom ains that can be fully specified by the experi­
menter, that is, when the dom ain prior can be specified.
O pen sets ol objects, features, o r events in natural scenes,
such a faces, distances, or velocities can n ot be fully speci­
fied. For natural scenes, the best an experim enter can do is
observe a large sample and derive a statistical probability
distribution o f the o bjects, features, or events, and use this
as the prior probability.
Bayesian methods arc useful in artificial visual systems
in which the designer can fully specify the optical system
and knowledge com petence o f the machine. Bur difficulties
can arise even in m achine vision. If the m achine is operating
with natural scenes, the stimulus dom ain and the prior
probabilities are difficult to specify. Even a simple and well-
defined stimulus dom ain can be problem atical, as illustrated
by Bertrand s paradox in which tw o m ethods ot measuring
the probability that a randomly selected chord o f a circle is
longer than the side o f an inscribed equilateral triangle give
different results (Bertrand 1889). A lbert (2 0 0 0 ) showed
that similar problems arise in defining the prior probabili­
ties o f directions o f m otion o f a point moving at random in
3-D space (secjep so n et al. 1996).
An observer’s best Bayesian estim ate o f a given stimulus
p{O D |/ ) is derived from the observers prior, p(OD), and
likelihood fu nction, p { ! |OD) . For a human observer, the
q u an tities p(O D ) and p(l\ O D ) are, typically, difficult to
estimate because the experim enter must know what the
observer assumes or knows about che stimuli and abouc
uncertainties in the visual system. But one may question
whether human observers have even an approximate idea o f
the relative probabilities ot scenes in any significant stim u­
lus dom ain. Even i fp(O D ) and p( l \OD) can n ot be quan­
tified, it may be possible to com pare the perform ance o f an
observer on a visual recognition task with that o f an ideal
perceiver.
Assuming a noise-free visual system, an ideal-perceiver
analysis can be used to define the least am ount ot inform a­
tion in the retinal image required for the specification o f
displays in defined stimulus dom ains. For example, it has
been shown that the com plete 3 -D m etric structure o f a
scene can be recovered trom just three views o f four nonco-
planar points (U llm an 1 9 7 9 ), or from just tw o views o f
eight points (Longuet-H iggins 1981) (Section 2 8 .2 .2 ).
Applications o f Bayesian statistics to pcrccption arc dis­
cussed in Knill and Richards (1 9 9 6 ) and in Mamassian et al.
(2 0 0 1 ). W itk in ( 1 9 8 1 ) used Bayesian m ethods to develop a
model o f the perception o f shape from texture. Read (2 0 0 2 )
developed a Bayesian model o f stereopsis. Yang and Purvcs
(2 0 0 3 ) developed a Bayesian model o f errors o f perceived
distance in term so f the probability distribution ofd istanccs
in defined scenes. Knill (2 0 0 3 ) developed a Bayesian model
o f the differential probabilistic structure of depth cues.
 3.7 CO N CEPTS OF GEOM ETRY
3 .7 .1 SYM M ETRY AND G RO U PS
In the m ost general sense, a symmetrical pattern is formed
by the repetition o f a pattern over space or tim e according
to a simple transform ation rule that preserves the m etric
structure o f the pattern. A linear transform ation o f an ele­
m ent creates a frieze pattern; a rotation creates circular
structures; reflections create bilaterally symmetrical pat­
terns, as shown in Figure 4 .1 5 . D ilatation and shear are not
included because they are not isom etric transformations.
M ost objects contain one or more ot these symmetries,
and symmetries occur in the fundamental subatom ic
processes responsible for the structure o f the universe.
O u r visual system is particularly sensitive to symmetries
(see Section 4 .6 .3 c).
G roup theory is a branch o f m athem atics dealing with
symmetries and other simple transform ation. A group is a
set o f things (elem ents) and a binary operation th at can be
applied to any pair o t elem ents in the set. The binary opera­
tion can be m ultiplication, addition, a rotation, a transla­
tion, or any other operation that, when applied to any pair
o f elem ents, maps in to another elem ent o f the group. The
binary operation betw een two elem ents a and b can be rep­
resented by the sign tor m ultiplication, ab, or by the sign for
addition, a I b. A group must satisfy the following axioms:
1. The operation that defines rhe group must be clo sed ,
which means that it must not produce elements outside
the defined set. For example, the odd integers are not
closed under addition, and therefore do not torm a
group with addition. The even integers form a group
under addition.
2. The set must contain an id en tity elem en t, e. The group
operation applied t<> the identity elem ent and any other
clem ent, a, leaves a unchanged. Thus ae = a. For
example, e for the group form ed by m ultiplication o f
natural numbers is 1. For addition, г1is zero. For
rotation, e is zero degrees.
3. Each elem ent, a, has an inverse e lem en t, a 1. Th e group
operation applied to any elem ent and its inverse
produces the identity elem ent. Thus, ал 1 = e. For
example, in addition, - 2 is the inverse o f 2, so that
2 + - 2 = 0 , the identity elem ent.
4. The operation m ust be associative. Thus, ( ab)c = a{bc).
A group may or may n o t be com m utative. Thus, ab may
or may n o t equal ba.
The p erm u tatio n group o f a set o f numbers represents
all ways in which the set may be mapped onto itself.
Th e perm utation group o f all num bers contains all other
groups as subgroups (C a lcy s theorem ). A group in which
n repetitions o f the same operation return the group to its
original state is a cy clic g rou p o f o rd er n. Thus, successive
rotations o f a line by 6 0 c form a cyclic group o f order 6 (C 6).
It is a subgroup o f the group o f rotations through 30" (C , J .
The order ot any subgroup ot a group o f order n is a factor
o f n (Lagrange’s theorem ). I f n is prime, there are no sub­
groups.
Croups with the same abstract structure are isom orp hic.
Tw o problem s that appear different on rhe surface may be
isom orphic. For example, the problem ot why o n e s reflec­
tion in a m irror is reversed left to right but nor top to
bottom is isom orphic with the follow ing problem . Place
twro pennies heads up and one penny tails up. By turning
the pennies two at a time make them all tails up. C an you
continu e turning pairs o f pennies until they are all heads
up? The m irror problem is discussed in Section 4.6.3e.
G roup theory is beautifully explained in Grossm an
and M agnus (1 9 6 4 ), Budden (1 9 7 2 ), and Shubnikov and
Koptsik (1 9 7 4 ).
G roups formed by continuous, or infinitesim al, trans­
form ations are known as I.ie g rou ps (H offm an 1966).
A Lie group is a differentiable m anifold. The local differen­
tial operators o f Lie groups are know n as o rb its and occur
in orthogonal pairs: horizontal and vertical grids tor defin­
ing translations, concentric and radial patterns tor defining
rotations and dilations, and orthogonal hyperbolic patterns
for defining hyperbolic rotations. The operators can be
commutatively com bined by summation and multiplication
to form a Lie algebra.
Patterns o f optic flow and som e processes in spatial
vision, such as size and shape constancy, can be described in
terms o f Lie orbits (sec S ection 4 .7 ).
3 .7 .2 T Y P E S О F G E О M F. T R Y
Every group o f transform ations has an associated geometry.
Each geom etry describes the properties o f patterns under
a defined group o f transform ations. The transform ations
must satisfy the group axioms o f closure, identity elem ent,
inverse elem ent, and associativity. The following geom etries
arise from different groups ot transform ations.
3 .7 .2 a G e o m e tr ie s B ased on C o n g r u e n c e ,
Iso m etry , an d S im ila rity
Two shapes are congruent when they can be exactly super­
imposed. C o n g ru en ce is a null transform ation, and a geom ­
etry based on congruence allows one to plot shapes on axes
and specify their internal dim ensions and positions. But it
does not allow for translation o r rotation.
Iso m etric g eo m etry adm its rigid m otions, namely
translation, rotation, and m irror reflection. It preserves
shape and size, but n o t position or orientation, as in
Figure 3.13a. In this geom etry, any tw o isom etric shapes
can be brought inco exact congruence by an appropriate
translation and/or rotation.
 Sim ilarity g eo m etry admits rigid motions plus dilations/
con traction . It preserves shape, but not size, position, or
orientation, as in Figure as in Figure 3 .1 3 b .
In the visual constancies, we readily recognize an object
whatever che position, orientation, or size o f its retinal
image. These are the transform ations that define isom etric
and sim ilarity geometries, and, in some sense, the visual
system muse carry ouc chese cransformacions. Any cwo sim i­
lar shapes can be brought into congruence by translation,
rotation, and change o f size. Euclidean geomecry is based
on the transform ation group o t similarities.
3 .7 .2 b A ffine G e o m e tr yi
Affine geom etry adm its rigid m otions, dilations/contrac­
tions, plus shear. Ic preserves collinearity, parallels, che ratio
(a) Isom etry
(b) S im ilarity
(c) A ffine transform ations
(d) Point perspective
Figure 3-D- Types o fp ro jectiv e tran sform ation .
o f lengths along a line or o f segments on parallel lines, and
che ratio o f areas o f any two figures in a plane. It does not
preserve angles, size, or the ratios o f noncollinear distances,
as shown in Figure 3 .1 3 c. The fundam ental theorem o f
affine geom etry is that any triangle in an o b ject plane can be
projected o n to any triangle in any image plane, given that
one is allowed to arrange the two planes at an appropriate
angle.
Shadows cast by the sun provide an example o t an affine
transform ation, since che lighc rays are effectively parallel.
C ertain types o t binocular disparity involve affine transfor­
mations o f shear, as we will see in Section 19.3.3.
3 .7 .2 c P ro je ctiv e G e o m e tr y
Projective geom etry adm its rigid m otions, dilations/con­
tractions, shear, and nonparallel projection. It preserves co l­
linearity, concurrence, and order o f points, buc noc parallels,
lengths, or angles, as shown in Figure 3.13d . The notion ot
angles betw een lines has no m eaning, and all triangles are
projectively equivalent, as are all rectangles.
Projective geom etry grew out o f the geomecry o f che
conic sections. These are the projection s ot a circle o n to a
plane. The theory o f co n ic sections was developed by
M enaechm us, Euclid, and Apollonius in the 3rd and 4th
centuries B C , and by Pappus o f Alexandria in the 3rd cen­
tury A D . Interest in projective geom etry was fostered by
che developm ent o t drawing in perspective in 15th-century
Italy (Section 2 .9 .3 ). The foundations o f modern projective
geom etry were developed by the French mathem aticians
Gerard Desargues ( 1 5 9 3 - 1 662), Blaise Pascal ( 1 6 2 3 -1 6 6 2 ) ,
and J. V. Poncelet ( 1 7 8 8 - 1 8 6 7 ) , and by the 19th-century
G erm an m athem aticians Carl Gauss, Karl Von Scaudt,
Felix Klein, and G eo rg Riem ann; the Hungarians Farcas
Bolyai and his son Janos B olyai; and the Russian Nikolai
Lobachevsky.
Projective geom etry is imporcanc in vision because che
retinal image is a projection o f the scene. Each visible point
is mapped by a straight projection line to one poinc in che
image plane. W h en che projection lines are parallel (parallel
projection) and the image plane is flat we have an affine
geometry, which preserves parallels and ratios ot lengths,
bu t not angles. W hen the projection lines pass through one
point (polar p ro jection ), we have a projective geometry,
which preserves collinearity, concurrence o f intersecting
lines, and relative order o f points, but not parallels, lengths,
areas, or angles.
In projective geometry, ratios o f distances along a line
are not preserved, buc cro ss ra tio s o t distances am ong tour
collinear points are preserved, as shown in Figure 3.14.
A p ersp ectiv ity is a mapping ot a defined set o f points by
projection onto a second set o f points on an image plane.
A p ro je ctiv ity is a mapping o f a sec o t points onto another
set by one or a sequence o f perspectivicies. A projectivity
can chus be che product ot tw o or more perspectivities.
 А' Figm M6. The S iobiu s net. S ta rt by draw ing lines throu gh chc fou r black
n o n co llin c a r p oin ts. M ark th e new p o in ts w here these lines in tersect.
. , .. _ AC AD
C ross ratio (or line AD = ----- / ------ D raw lines throu gh chc new p oin ts to form yet m ore poincs. I f the
BC BD process is continued» th e p o in ts eventually hll chc w hole surfacc.
А ' С ' A ' D'
C ro ss ratio for line A ’D’ = ---1 - / ------------------------
B ’ C* B 'D *
lines intersect. The points have a defined position, since
AC AD A ' C ' A 1D'
By the rule o f cro ss ratios ----- / ------------------- = ---- / -- each is collinear with two intersecting lines. By continuing
BC 8 D B ' C ' B'D'
to link up the newly form ed points the whole surface is
F ijn r t 3. 14. The cross ratio. eventually filled w ith points in determ ined positions. This
is known as the M obiu s n e t (Figure 3 .1 6 ).
Dcsarguess theorem is another fundamental theorem
The set o f successive perspectivities are said to be in projec­ o f projective geometry. It states that, for triangle ARC, and
tive correspondence. Por example, in Figure 3 .1 5 , the points its projection A R'C\ the intersections o f the three pairs o f
on line 1 are in projective correspondence w ith points on corresponding sides are collinear. The p ro o f is easy to visu­
line 3 because they arc both projections o f the points on alize by applying the following principles:
line 2. W h en tw o people in different positions look at the
same o b ject, the images in their eyes are in projective co r­ 1. The images o f any tw o coplanar lines intersect.
respondence.
2. Л line and its projected image lie in the same plane as
Sets o f col Iinear points arc in projective correspondence
the center ot projection.
when they have the same cross ratio. In general, any set o f
four points on a straight line has the same cross ratio as their 3. Two nonparallel planes intersect in a straight line.
images formed on any flat image plane.
The fundam ental theorem o f projective geom etry is that L et triangle A B C and its image A ’B ’C' projected from
tour points, with no three collinear, com pletely determ ine point 0 lie in nonparallel planes, as in Figure 3.17.
a projective transform ation. To prove this, jo in any four From (2 ), each pair o f corresponding sides o f the triangles is
noncollincar points by lines to create new points where the coplanar with O. From ( l ) each pair o f sides must meet. But
the triangles lie in distinct perspective planes that, from (3),
must m eet in a line. Therefore, all pairs o f corresponding
sides m eet in the same line. The intersection o f two perspec­
tive planes is the perspective axis. The theorem is true

figure 3.IS- P rojcctive I'orrapw fU ncc. T h e p o in ts on lin e I a rc in p ro jectiv e

co rresp o n d en ce w ith th e p o in ts o n line 3 bccau.sc b o th sees o f poincs arc F ig « M7. Desarp<es ’ theorem . C o rresp o n d in g sides o f projcccivclv
p ro jectio n s o J th e p o in t* on lin e 2 . eq u iv alen t triangles converge o n th e sam e straight line.
for any polygon because any polygon can be divided into О
triangles.
W h en we p roject a circle from a point, rhe projection
lines form a double cone. The projections o f a circle on
planes passing through the cones form chc co n ic sectio n s,
as shown in Figure 3 .1 8 . The projection is a hyperbola when
the plane cuts both cones. It is an ellipse when the plane
cuts only one cone. It is a parabola when che plane is parallel
to one o l the projection lines, but it reduces to two straight
lines when the surface passes through che apex o f che cone.
It follows that the circle, hyperbola, ellipse, and parabola are
projeccively equivalent. ЛИ these shapes can be described
analytically by equations o f the second degree.
M any people falsely in tu it chac an oblique seccion o f a
cone is egg-shaped racher chan elliptical. The G erm an artist,
A lbrecht Diirer, made this mistake (Panofsky 1971, p. 2 5 6 ).
The Belgian m athem atician G . P. D andelin, in 1882, pro­
duced the following elegant p ro o f chac che cross section o f a
cone is an ellipse (see C ou ran t and R obbins 1956).
Let a plane cut a cone to form surface E, as in Figure 3.19.
Place tw o spheres w ithin the cone so that they touch the

C ircle

cone along parallel circles C t and C, and touch surface E at

points /•’ and From any point P on the circum ference o f
E draw lines to and F ,. Also from P draw a line to the
cone apex, 0 and through points 5 , and 5 , on circles C, and
C , Now P F { = PS, because they are tangents to the same
sphere. Similarly, PF, = P S It follows that:

P F X+ P F : = P S , +PS,

b.Rurc з. i s. 7b e to n ic section s.
Buc PS{ + PS, = SlS„ which is che discance along che surface
o f the cone betw een the parallel circles. This distance is
independent o f che position o f P on the circum ference
o t E. Therefore, P F { + PF, is constant for all positions of P
on E. But this is the definition o f an ellipse, namely chat che
sum ot che distances from che two foci to the edge o f an
ellipse is constant. Therefore E is an ellipse and F } and F, arc
its foci.
The notion o f the cross ratio can be extended to points
on a curve. Any sec o f four points on a circle preserves che
same cross racio when projected o n to any line through any
other poinc on the circle. Also, the pencil o f rays to a sec o f
poincs on a circle trom another point on the circle is co n ­
gruent (form che same angles) wich the pencil o f rays to the
same points trom any o ther point on the circle, as shown

Fi*«rc 3 .20 . Cross ratios o f poin ts on л circle. I he cross ratio o t any set o f tour
p o in ts o n a circle, such as p o in ts А , В , C . and D . is preserved w hen they
arc p ro jected throu gh any o th er p o in t on the circle, such as p o in ts P I
and P 2 . A lso , the angle form ed by the rays from any p o in t P o n a circle
to a given pair o f p oin ts on the circle rem ains th e sam e w herever p o in t P
is o n the circle.
in Figure 3 .2 0 . This follows from Euclid’s theorem thac rhe
angles subtended by the cord o f a circle to any point on the
circum ference o f the circle are equal. This theorem forms
the basis for the locus o f single binocular vision, or horopter
(see S ection 14.5). In general, a set o f four points on any
co n ic section preserves the same cross ratio when projected
through any other point on the conic section.
A co n ic section may also be defined as the set o f inter-
sections o f projcctively related lines. For example, a locus o f
equal vergence o f the eyes is a locus o f intersections o f visual
lines from centers o f rotation o f the eyes that m eet in a co n ­
stant angle. Also, a locus o f isoversion is a hyperbola defined
by the locus o f intersections o f visual lines that rotate from
equal angles in opposite directions (see Figure 10.10).
For an introduction to projcctivc geom etry see C oxctcr
(1 9 6 4 ). For applications to vision see Section 26.1.1.
3 .7 .2 d T o p o lo g y
Topology is rubber-sheet geom etry in which a pattern may
be deformed in any way as long as it is not cu t or join ed to
another pattern. It adm its rigid m otions, dilations, con trac­
tions, shear, nonparallel projection, plus elastic deform a­
tion. It preserves connected neighborhoods and edges, and
also relative order o f points and routes between points.
M etric properties such as lengths, angles, areas, or cross
ratios are not preserved. In topology, one cannot distinguish
between a doughnut and a coffee cup! A topological trans­
formation preserves all points and their neighbors. Thus all
mappings are b iu n iq u e (one to one) and con tin u ou s.
Topological transform ations obey the following rules.
1. As the distance between two points reduces to zero, the
distance between their images also reduces to zero.
2. If you can go from a to b through a defined set o f points
in a given order then you can go from the image o f /г to
the image of/» through the images o fth e same points in
the same order.
3 . Points in a surface remain in the surface in the
transform ed image. Points outside remain outside.
4. Points on the boundary o f a surface remain on the
boundary in the transformed image.
5. A surface is closed if it is finite but has no boundaries,
like the surface o f a sphere.
Jo rd a n ’s theorem states that a simple closed line (one
with no ends) divides a plane into an inside and an outside.
All points on the same side o f the line have the same p o la r­
ity, and all points on opposite sides have opposite polarity.
Any two points with the same polarity are co n n ected . They
arc simply connected i f there arc no holes in the surface.
Jord an’s theorem is im plicitly embedded in the figure-
ground m echanism o t the perceptual system, w hich allows
us to recognize the difference between the inside and o u t­
side o f a figure. The perception o f figure-ground relation­
ships can be difficult with a com plex figure like that shown
in Figure 3.21. W c must use a cognitive strategy o f tracing
round the figure to solve the problem. We may recognize
when Jord an s theorem has been violated, as in Figure 3.22,
even though we may not be able to say why.
Jord ans theorem is true on a spherical surface but not
on other 3 -D surfaces. For example, not all closed lines on a
torus divide the surface into two. W h en the M obius strip,
shown in Figure 3 .2 3 is cut along the full length o f the
dotted line the strip remains single. The surprise generated
when the strip is cu t in this way and yet remains conncctcd
indicates that our perceptual system assumes that Jord an s
theorem holds in this case.
KiguK3 .21 . I h e M insky spiral. It is d ifficu lt to see th at the figure on the
left con sists o t tw o spirals w hile th at o n the rig h t con sists o f o n ly one.
The d ifferen ce can be d etected on ly by m en tally tracin g round the
figure. (From Minsky and Papcrt 1969)
 Fi*«rc 3.2*. I b e М оЫ ш strip. A M obiu s scrip is a real o b jc cc wich o n ly on e
edge and o n e surface. Ic co n trad icts chc assum ption chac a com p lete
edge defines tw o surfaces. W h e n c u t alo n g th e d o tted line the strip
Fцигс 3 .22 . - in im possible object. re m a in s o n e lo o p .

The geom etries listed above form a hierarchy, because
theorem s true in any one o f them arc also true in those ear­
lier in the lisc. Each set o f transform ations is a subset o f
those following it, as shown in Figure 3.24. Topology is the
m ost general geom etry because its theorem s are true in all
other geom etries.
In any geom etry, the features o f patterns chat remain
unchanged are invariants. The paccerns arc said to be equiv­
alent over the set o f transform ations that are allowed in the
geomecry, and are called au tom orp h s. For example, in iso­
m etric geom etry, chc different orientations o f a shape arc
automorphs. In projective geom etry, all shapes that project
chc same image arc autom orphs. In cach ease, the au to­
morphs form an equivalence class. A n equivalence relation
is reflexive (any elem ent is equivalent to itse lf), symmetrical
( i f a is equivalent to b then b is equivalent to a ), and transi­
tive ( i f a is equivalent to b and b is equivalent to с then a is
equivalent to r).

Allowed tran sform ations Pre se rve d properties

S ym m etry transform ations

Identity, connections, collinearity, parallels, angles, size, orientation, position

S ym m etry

Translation

Identity Identity, connections, collineanty, parallels, angles, size, orientation

Rotation

Isom etric Identity, connections, collinearity, parallels, angles, size

Sim ilarity Identity, connections, collinearity. parallels, angles

S hear

Affine Identity, connections, collinearity. parallels

P erspective

Projective Identity, connections, collinearity

Elastic

Topological Identity, connections

X R andom
motion

Random > Identity

m otion

F ig u re 3 . 24 . Geometries an d transforsnationgroups.
 A co n fo rm a l tra n sfo rm a tio n preserves continu ity and
local angles but does n o t necessarily preserve collinearity or
parallels. Ricm annian geom etry on curved surfaces can be
defined in terms o l conform al transform ations o f Cartesian
coordinates.
The projection o f each h a lf o f the retina onto the surface
o f the visual cortex is basically a conform al transform ation.
So is rhe projection o f the sense organs in rhe skin onto
the sensory hom unculus in the somatosensory cortex.
Hem idecussadon involves a discontinuous mapping o f the
nasal and tem poral hem iretinas so that the retina as a whole
is n o t mapped onto the visual cortex topologically. The way
organs change in shape during em bryology or evolution can
often be described by conform al transform ations that arise
through differential rates o f growth (allom etric grow th).
For example, shapes o f shells in related genera o f molluscs
and shapes ot prim ate skulls (see Figure 4 .1 0 ) can be
described by conform al transform ations. D ’Arcy W entw orth
Thom pson described these transform ations in his book
On Growth an d Form (Thom pson 1952). They were also
described by Julian Huxley in Problems o j Relative Growth
(1 9 3 2 ).
O u r ability to recognize cartoon drawings and family
resemblances betw een faces suggests that our visual system
is capable of carrying out conform al and topological
transform ations o f visual stimuli.
3 .7 .2 e B e y o n d T o p o lo g y
A more general geom etry than topology would be one that
preserves spatial and tem poral continu ity o f points but not
connected neighborhoods and edges, or relative order ot
points o r routes betw een points. M olecules undergoing
Brow nian m otion, particles in a dust storm , or a swarm ot
locusts would conform ro such a geometry.
A still m ore general geom etry would be one in which
point identity is preserved but nor spatial and temporal
continuity. Points would be allowed to move discontinu-
ously. The values o f stock in the stock market would co n ­
form to such a geometry.
Finally, o n e could have a geom etry in which som e or all
points are n o t preserved. Q uantal noise and the distribu­
tion o f men in battle would conform to such a geometry.
3 .7 .3 N О N - E U С L ID E A N G E О M E T R IE S
In Euclidean geom etry, length and angles have meaning.
Accordingly, geom etries based on isom etries and similari­
ties are Euclidean. In this sense, affine and projective geom ­
etries are non-Euclidean. In Euclidean geometry, there is
only one line through a given point that is parallel to a
second line. This is the p o stu la te o f the u n iq u e parallel.
All attem pts to prove it have tailed, since it is not derived
from the other postulates o f Euclidean geometry. The paral­
lel postulate asserts that parallel lines do n o t m eet even at
infinity. It is the only postulate o f Euclidean geom etry that
deals with points at infinity.
N on-Euclidean geometries are consistent with the pos­
tulates o f Euclidean geom etry except the parallel postulate.
These geom etries were developed in the 19th century by the
G erm an m athem aticians C arl Gauss, Karl Von Staudt, Felix
Klein, and G eorg R icm ann; the Hungarian m athem atician
Janos Bolyai; and the Russian m athem atician Nikolai
Lobachevsky,
In non-Euclidean geometries, there can be many parallel
lines through a point. For example, in the non-Euclidean
hyperbolic geom etry developed by Klein, all real points occur
inside a circle. Each cord o f the circle is defined as a straight
line o f infinite extent and distances arc defined in terms o f
cross ratios. Two lines intersect if thev/ m eet inside the circle.
But lines that meet on the circumference o f the circle are
defined as parallel because all points on the circumference
are defined as being at infinity. By this definition, there is an
infinite number o f lines through a point inside the circle that
are parallel to a line not passing through the point.
In non-Euclidean geometries, the axes are curved. A space
o f positive curvature is elliptical, and the coordinates o f a
Riemannian elliptical geometry lie on the surface o f a sphere
or ellipsoid. These geometries are elosed, since an ellipsoid
and a sphere lorrn closed surfaces. A space o f negative curva­
ture is hyperbolic, and the axes o f a Riemannian hyperbolic
geom etry lie on a hyperbolic cone, or saddle (C oxeter 1961).
This geometry is not closed. Einsteins theory o f the curva­
ture o f space-time under the influence o f gravity is the best
known application of non-Euclidean geometry.
In any geom etry, rhe shortest distance between two
points is called a geodesic and is defined as a straight line. In
Euclidean geom etry, geodesics arc conventional straight
lines and all straight lines are geodesics. Parallel straight
lines never m eet. In Riem annian geometry, geodesics
(straight lines) are curved when considered trom the point
o f view o f Euclidean geometry. For example, in spherical
geom etry constructed on the surface o t a sphere, all straight
lines (geodesics) are great circles, or equatorial circles that
cut the sphere in half. The shortest distance between two
points on the surface o f a sphere is along the great circle
through the points. That is why airplanes navigate along
great circles on long journeys.
All great circles on a sphere intersect, like lines o f longi­
tude on the E arth , so that no two straight lines in this
geom etry can be parallel in the sense ot n o t m eeting. In
vision, the images o f all Euclidean straight lines fall on great
circles o f the spherical retina. Therefore, the retinal images
o f two noncollinear straight lines in o b je ct space can n o t be
parallel. The images o l any pair o l parallel straight lines, it
extended, converge in both directions onto points on op p o­
site ends o f a diam eter o f the eye. O n e can draw concentric
circles on a sphere, like lines ot latitude, but, except tor the
equatorial line, such circles are not geodesics. A n image
that does n o t lie wholly on a great circle on the retina is
necessarily chc image o f a curved or hcnc objccc. The image A2

o f a curved line tails on a great circle only when the line lies
wholly in a plane chrough che nodal poinc o f chc eye.
In Euclidean geom etry, the angles o f a triangle sum со
180“. In a Riem annian geomccry chey sum со more o r less
than 180". For example, in spherical geometry, the angles o f
a triangle form ed by the intersections o t three great circles
sum со more chan 180°.
Spherical geomerries used to specify retinal locations
and binocular disparities arc described in S ection 14.3.2.
The geom etry ot visual perspective is discussed in Section
26.1. The application o f non-Euclidcan geomecry со chc
description ot 3-D shapes is discussed in Seccion 26.6.1.
Accemprs со conscruct a non-Euclidcan geom etry o f visual
space are described in S ection 4 .7 .2 .

3 .7 .4 A N A L Y T IC G E M E T R Y

In analytic geomecry, locations o f poincs are specified by

coordinates. Lines, curves, and surfaces and relationships
betw een them are specified by algebraic equacions. The
C a rtesia n c o o rd in a te s ot a point are specified by its dis­
tance along each o f tw o or three orthogonal axes. The p o lar
co o rd in a te s o f a point are its distance trom a central point
and ics radial direction wich rcspecc со chc ccncral poinc.
Polar coordinates are used to specify locations o f points on
the retina (Seccion 14.3.1) and directions o f eye positions
(Section 10.1.2d ). Axis syscems used to specify binocular
disparity arc described in Section 14.3.2. In these systems
there is no way to represent points and lines at infinity in
the extended plane ot projective geometry. For this purpose
we use hom ogeneous coordinates.
H o m o g en eo u s c o o rd in a te s were invented by M obius
in 1827. O riginally they consisted o f che sides o f a criangle
Л >Л„ЛХ,as in Figure 3 .2 5 . The position ot any point in the
triangle is specified by its distance from each o f the three Figa>< H om ogeneous coordinates. (Л ) I he bar y ccn tric coord inatcs
apexes. It, at each apex, a weight is placed proportional со o f a p o in t arc the d istan ces from each o f three apexes o r each o f three
sides o f a triangle. T h e three d istan ces can be norm alized to 1.
che discance o f che poinc from chc apex, chen che position o f
(B ) H om ogen eou s co o rd in ates in a triangle cu ttin g 3 -D co o rd in a te s set
che poinc is che center ot gravity, or cencroid, o f che criangle. a t 60". T h is system is used to p ro je c t ab solu te ( X , Y, Z ) p o in ts in 3 -D
Thac is why criangular hom ogeneous coordinaces arc called co lo r space (red lines) in to relative (x , y, z) values in a 2-L ) ch ro m aticity
b a rv cen tric co o rd in ates. diagram (b lu e lin es). ( C ) H om ogen eou s co o rd in ates in a rectangular
plane, H , parallel to th e X , Y plane o f 3 - D C a rte sia n axes. The
The position o f a point may also be specified by its
co o rd in ates o f p o in t P, w here a lin e through th e origin (O ) in tersects
perpendicular distance from each side ot che triangle. plane H , arc (x h , yh, w ). \v is th e h eigh t o f H above the X , Y p lan e. A ll
Triangular hom ogeneous coordinates are used for speci­ p o in ts on the line О and 1* have the sam e h om og en eou s coordin ates.
fying trichrom atic color values in the C IE color system. In
this system, the x-,y~, and г -axes o f 3 -D color space arc used
to represent the absolute lum inances o f standard red, green, origin (O ) and che point. The coordinates ot che poinc in
and blue m onochrom atic wavelength com ponents in a chc chromacicicy plane arc chc chree perpendicular discanccs
given color specim en. The x-,y-, and г -axes may be set at 6 0 ” from each o f che three sides o f che triangle, namely x,y, z , as
rather than at 90°. In this case a plane placed across them in Figure 3 .2 5 b . The values o f x, у , and z arc normalized to
form s an equilaceral triangle, as in Figure 3 .2 5 a . The height add up to 1. The coordinates represent the relative propor­
o f the chrom aticity plane above the origin signifies lum i­ tions o f red, green, and blue in chc color specim en. In chc
nosity. Any 3 -D point in X, Y, Z space can be projected center o f the triangle, there are equal amouncs o f red, green,
onto the chrom aticity plane by drawing a line chrough rhe and blue so che color chcrc is gray.
 The above examples show that 2-1) hom ogeneous axes
arc a projection o t 3 -D axes into a plane. Thus, in 2-D h om o­
geneous coordinates a point is specified by three numbers
rather than bv the two numbers o f 2 -D Cartesian coordi-
nates. Hom ogeneous coordinates express only relative values,
since all points on a line through the origin have the same
hom ogeneous coordinates. They all project to the same point
in a plane. That is why they are called homogeneous coordi­
nates. In general, hom ogeneous coordinates are a projection
o f n-dimensional coordinates into an n-1 dimensional space.
Absolute values are lost, leaving only relative values.
H om ogeneous coordinates can be used to indicate
movements or projections ot objects in space. L et the coor­
dinates o f a point with respect to orthogonal 3 -D Cartesian
axes be (лг, j', z). [.et H be a plane containing hom ogeneous
axes. Plane H can have any position and orientation relative
to the 3 -D axes. It has alreadvi been noted that the chrom a-
ticity plane cuts all three axes o f 3 -D color space to create a
triangular plane.
For representing spatial transform ations it is usual to set
plane H parallel to the X - , _y-axcs and orthogonal to the
г -axis o f 3 - D space, as in Figure 3 .2 5 c. For example, an artist
sets the easel orthogonal to the depth dim ension ot the
scene being painted. W h en the easel is set at an angle, the
painting is anam orphic (sec Section 2 .9 .5 ). Let the height
(position on the г -axis) o f plane H above the x ,у plane be
w. For sim plicity, plane H is confined to the positive quad­
rant ot space. A line through the origin ^point O ) of the
Cartesian axes intersects plane H in point [xh,y t ,(o). 'Ihese
are the hom ogeneous coordinates o f the point. Therefore,
as in any polar projection, each point in plane H is associ­
ated with a line passing through the origin ot 3 -D axes. Each
line is associated with a point in a given plane.
The 2-D hom ogeneous coordinates ot a point are
represented by the triplet [xb,yh,(o) where x b - x /0 )
and y b= y /(Q . Tw o points are the same in h om o­
geneous coordinates if they are proportional. Thus
[xb>yb,0)) = {axh,ayb>a(0). Scaling moves plane H along
the z-axis. W e arc free to give 0) any value. For many
purposes it is convenient to make CO= 1 .
Any line in plane H is defined by the intersection o f a
plane through О and plane H. Since any line is the locus o f
points that satisfy a linear equation,
ax+ by+ c = 0
we can call the ordered set o f three coefficients [ayb , and f]
rhe hom ogeneous coordinates o f a line. For the line at infin­
ity (the horizon) W = G. In general, points and lines in
hom ogeneous coordinates are both represented by three
numbers. This reflects the duality o f points and lines in pro­
jective geometry. For every theorem about points there is an
equivalent theorem about lines.
In hom ogeneous coordinates, geom etrical theorem s can
be reduced to algebraic theorems. For example, the projection
o f a point in plane H onto a second plane H ’ can
be represented analytically by the following set o f linear
equations,
X / = a ,x b + b ,y 4 + c , (0
Уь = ai xb+bzy t +c 2(0
(o'=axxh + biy t +C f(0
Theorem s in projective geom etry becom e theorem s about
num ber triplets defined by these transform ations. Tliis
branch ot mathematics is an aly tic g eo m etry . Theorem s can
be easier to prove when expressed in algcbraic form , but one
may lose sight o f the spatial structures that the equations
represent. In visual sciencc the spatial structures arc the
im portant things.
Suppose one wishes to translate, rotate, o r shear a shape
in a 2 -D com puter graphics display. In a plane defined by
tw o-dim ensional Cartesian axes, point \x,y) can be carried
to point [x',y') by the following transform ations:
Translation through Tx and Ту
x' = x + Tx>/ = у + Ту
Scaling by Sx and Sy
x' = x Sx,y' = у Sy
Rotation about the origin through в
x' = x cos в - у sin 0, у ‘ - у cos О+хмпО
Transform ations o f a plane figure can be achieved by carry-
in gou t these calculations for cach point o f chc figure. In any
transform ation, directed line elements (vectors) that map
into line elements with the same direction are eigenvectors,
and che scalar m ultiple chat transform s an eigenvector into
its image is an eigenvalue. Eigenvalues arc the n roots o f the
equations representing chc transform ation.
These calculations can be carried o u t more efficiently by
expressing chc poincs in hom ogeneous coordinaccs and chc
cransformacion as a m ultiplication o f two matrices. The
hom ogeneous coordinates o f the point in its original posi­
tion form a one-dim ensional matrix {x,y, CO). The coeffi­
cients o f the three cransformacion equations arc arranged in
a 3 by 3 matrix that characterizes that transform ation.
M ultiplying the point m atrix by chc equation matrix gives
the matrix o f the transformed values o f the point {x\y\(o').
The rules o f matrix m ultiplication arc described in any
textbook on m atrix algebra. These matrix rules represent,
in com pact form , the operations that solve a set o f linear
equations.
The 3 by 3 matrices that represent the movements and
rotations o f a point in a plane are as follows:
I 0 0
Translation = (,v'. y',l) = Ia,^,I| 0 I 0
T T 1
 i' 0 0 W c let (0 = z j d + 1, which denotes the magnification
o f t h e projection (S ectio n 2 4 .1 .1 ). The coordinates o f a
Scaling = ( x ' . f Л) = \х,уЛ) 0 s о
point in the plane are related to those o f a point in 3-D
О О 1
space by:

cos#
Rotation = [х '.у , 1) = [дг, у, 1] —sin#
О 0
The equations may be expressed in short forms:
p ' = r r ( r / r y )
r = P S (,,s ,)
P ' —P R ($ )
sin# 0
[дг', у', z\w ] = [xjlO, у /10, zj (0 ,1]
cos# О
1 These procedures are used in com puter graphics to move
objects w ithin a display or to create 2 -D displays from 3-D
scenes. C alculations are faster if objects are represented by
polygons. A m ovem ent or projection o f an o b jcct can be
achieved by transform ing only rhe apexes o f the polygons.
For more details on these methods see Hearn and Baker
(1 9 8 6 ), Foley c t al. ( 1 9 9 0 ), and Faugeras (1 9 9 3 ).

Successive translations and rotations o f a point can be 3 .7 .5 D IF F E R E N T IA L G E O M E T R Y

derived by adding the transform ation matrices. Successive
In differential geom etry one defines a basic set o f local
scalings o f a point can be derived by matrix m ultiplication.
differential operators, namely translation, rotation (curl),
Adding or m ultiplying matrices is known as co m p o sitio n .
dilatation (div), and tw o types o f shear \def) which can
C om position yields a single m atrix that represents a set o f
be com bined algebraically to describe any continuous
transform ations in a com pact form . This provides consider­
transform ation o t points on a surface or in a volume.
able econom y o f com putation. For small rotations, substi­
D ifferential geom etry is used extensively in analyzing
tuting 1 for c o s0 achieves further economy.
airflow in aerodynamics.
In general, m atrix com position is n o t com m utative—
W hen we move through a visual scene the retinal image
the order o f operations affects the result. However, the sim ­
undergoes continuous transform ations known as o p tic
ilarity com positions o f translation, scaling, and rotation arc
(low, which can be described in terms o f the operators o f
comm utative.
differential geom etry (W crkhovcn and K ocndcrink 1990).
The m ethod can be generalized to three dim ensions. In
O p tic flow inform s us about our self-m otion and about the
this case, we project 4 -D C artesian coordinates o n to 3 -D
3-D layout ot objects in the visual scene (C hapter 2 8 ). We
hom ogeneous coordinates. Therefore, each p o in t is repre­
are very sensitive to changing patterns o f optic flow, which
sented by four numbers (л-, у, z, «•)* or vx f( 0 , y / t 0 , zjO), 1).
suggests that our visual system em bodies continuous space-
Transform ations are now represented by 4-by-4 matrices.
time transform ation operators. There is physiological evi­
For example, the m atrix for rotation o f a point in 3-D space
dence that visual centers in the brain contain cells that
about the z-axis becom es:
respond selectively to the differential operators o f geom etry
co40 —sin 0 0 0
(Section 5.8.4e). We do not know which set o f primitive
sin 9 cosd 0 0 transform ation operators the visual system uses. I Iotfman
KZ(B)=
0 0 10 (1 9 6 6 ) suggested that the system uses rhe differential opera­
0 0 0 1 tors o f Lie groups. K ocndcrink (1 9 9 0 ) has proposed that
we use the similar set o f basic operators o f differential geom ­
etry. Perhaps different geom etrical operators arc used for
Th e projection o f p o in t {x,y, z, 1) in 3 -D space o n to point
different purposes in different p a rtso fth e brain. Differential
(.v/, y',z',(0) in a plane norm al to the z-axis and distance d
operators have been applied to the analysis o f patterns o f
from the origin is represented by:
binocular disparity (Section 19.3.3).
■1 0 0 0 1 Also, in differential geometry, one defines various types
0 10 0 o f curvature that can be used to describe sm ooth 3-D
[x,y,z,l\' objects. Applications to visual perception arc described in
0 0 0 1f d : S ection s 2 0 .4 .2 and 26.6.1.
00 0 1J The brain is, am ong other things, a geom etry engine.
 4
SENSORY CODIN G

4.1 Stimuli and sense organs 12S 4.5.2 Relationships within a feature system 163
4.1.1 Specification o f stimuli 128 4.5.3 Jointly tuned detectors 165
4.1.2 Structure o f sense organs 129 4.5.4 Associations bccwccn distinct features 16$
4.2 Types o f sensory coding 130 4.5.5 Stimulus covariance 167
4.2.1 The nerve impulse 130 4.5.6 Nested sensory systems 168
4.2.2 Analog processing 131 4.5.7 Multicue systems 170
4.2.3 Monopolar and bipolar dececcors 132 4.5.8 The sice and order o f visual processes 175
4.2.4 Primary coding 133 4.5.9 Multistable percepts 177
4.2.5 Secondary coding 136 4.5.10 Rules o f visual structures ISO
4.2.6 Feature detectors 139 4.6 Types o f perceptual judgment 1S2
4.2.7 Metamerism 141 4.6.1 Detection, resolution, and discrimination 1S2
4.2.8 Sen so rv opponencv 143 4.6.2 Categorization, scaling, and identification 183
4.2.9 Contrast effects and normalization 144 4.6.3 Perceptual descriptive processes 18$
4.3 Temporal coding 145 4.7 Geometry applied to visual space 193
4.3.1 Temporal characteristics o f neural spikes 145 4.7.1 Implicit principles o f visual geometry 193
4.3.2 Temporal coding in single neurons 146 4.7.2 The geometry o f visual space 193
4.3.3 Detection o f rime intervals 147 4.8 Mechanisms o f attention 195
4.3.4 Temporal synchrony of neural activity 148 4.8.1 The nature o f attention 195
4.3.5 Temporal coding o f spatial features 154 4.8.2 Stimulus factors in attention 106
4.4 Coding primitives 155 4.8.3 Attention and stimulus crowding 19S
4.4.1 Fourier components 156 4.8.4 Attention and consciousness 201
4.4.2 Gabor functions and wavelets 158 4.8.5 Stimulus externalization 203
4.4.3 Other visual primitives 15* 4.9 Plasticity o f basic visual functions 203
4.4.4 Nonlinear visual processes 159 4.9.1 Basic findings 203
4.5 Higlicr-order sensory systems 162 4.9.2 Causes o f cxpcricncc-dcpcndcnt plascicicy 204
4 .5 .1Types o f sensory proccssi ng 162

4 .1 S T IM U L I A N D S E N S E O R G A N S to describe the physical nature o f what che environm ent

4 .1 .1 S P E C I F I С AT I О N О F S T I M U 1.1
The firsc seep in investigating sensory systems is to define
pr i mar y stimuli. These are light, sound, heat, chem icals,
m echanical stimuli (pressure, tension, vibration, and
inertia), electricity, and magnetism.
Any primary stimulus has a set o f local properties. For
example, all light signals have intensity, direction, wave­
length. polarity, duration, and phase. For stim uli distrib­
uted over space or tim e, each local property can have spatial
and temporal derivatives. For light, derivatives include
contrast, patterns o f lum inance and color, and m otion.
We then ask what stim uli are available in an anim als
environm ent and which are m ost relevant to the survival ot
the animal. Jam es G ibson (1 9 7 7 ) used che word “afFordancc”
offers an animal wich respecc to how che anim al behaves.
For exam ple, the ocean affords fish with a fluid within
w hich chey can swim. Sound waves afford a basis for echo-
locacion, and electric fields in water afford a basis for clec-
crolocation. The idea o f afFordances is related to the idea o f
constraints. For exam ple, a horizontal surface in a gravita­
tional field affords support buc constrains m otion to one
plane. Binocular disparity affords stereoscopic vision but
constrains it со a limiced range o f distances. AfFordances
and constraints are com plem entary ideas.
'th e next seep is со understand how stim uli impinge
on sense organs. Any sense organ is designed to dececc
only one prim ary stimulus. Thus, each prim ary stimulus
requires ics own sense organ. The scimulus seleccivicy o f a
sense organ depends on ics structure. In the eye, it depends
on the cornea, lens, and visual pigments. In audition ic
depends on chc structure o f chc pinna, ear ossicles, and
cochlea.
W c muse chen explore ways in which a primary scimulus
could, in theory, be detected. A nim als can use only m echa­
nisms that arc achievable by living tissue. For example, ani­
mals can not d etect electrom agnetic signals outside a narrow
range o f wavelengths.
Given chat a prim ary stimulus has been detected, we
muse then explore how che local properties o f that stimulus
may be dccecccd. For example, a visual recepcor can n ot reg­
ister che phase ot light because che frequency ot lighc waves
is too high. Any light d etecto r should be able to register
light intensity. The direction o t a light source can be
detected only if the detector is in a pit, or is associated with
a waveguide or lens. There are tw o ways to d etect wave­
lengths o f lighc. A colorim eter uses a prism to spread wave­
lengths out. The human eye detects chrom atic aberration in
the same way and uses it со code che sign o f accom m oda­
tion. But the best m ethod for color vision is to use pigments
with different absorption characteristics.
The next step is to theoretically explore ways in which
the spatial and tem poral derivatives o f signals may be
detected. O n e way is to have receptors with com plex recep­
tive fields. Each rcccptor responds only when a particular
spatial or temporal pattern falls on the receptive field. This
would require a large num ber o f recepcors, mosc o f which
would be inactive at a given tim e. A better way is to have
receptors sensitive to only primary stimulus features and
then converge rhe outputs o f these d etectors in different
ways o n to detectors at a higher level. D ifferent first-order
spatial or tem poral derivatives could be detected in parallel
in distinct neural centers. Higher order spatial or temporal
derivatives could be detected by a succession o f converging
outputs over an in-series set of neural centers.
W e will sec that these processing strategics have been
adopted by many animals for che detection o f spatial and
tem poral derivatives o f many types o f prim ary signal. For
exam ple, visual patterns o f sensory stim ulation trom human
eyes, patterns from the ears o f bats, and patterns o f electric
fields trom the electric sense organs o f fish are all detected
by parallel and in-series neural centers at various levels in
the central nervous system. In all cases, the neural centers
have a similar multilayered scruccure.
4 .1 .2 S T R U C T U R E OF SEN SE O RG A N S
M osc sense organs consist o f receptors arranged on a sen­
sory epithelium supported by a m echanical structure. The
epithelium and supporting structure have intricately
designed m echanical properties, w hich serve the following
four purposes:
1. Filtering appropriate stimuli Each sensory end organ is
sensitive to several primary stim uli. For instance, in
addition to light, retinal receptors are sensitive to
pressure applied to the eyeball, vibration, and electric
pulses. However, the m echanical structure o f a sense
organ is designed to preferentially transm it one type o f
stimulus energy, called the ad eq u ate stim ulus. Thus,
the m echanical properties o f the eyeball, orbical tissues,
and receptors norm ally shield the eye from form s o f
energy other than light. Similarly, the m echanical
properties o f the skull and the cochlea protect rhe
receptors on the basilar mem brane ot the ear trom
form s o f energy other than sound. The semicircular
canals respond preferentially to head rotation because
their sensory hair cells project into a fluid-filled
annulus, and the utricles respond preferentially to head
tilt because their sensory hair cells have heavy crystals
attached to them.
2. Efficient collection o f stimulus energy Structures
associated with sense organs are designed for efficient
transmission o l a specific type o f energy to the sensory
epithelium . For exam ple, the ossicles in the middle car
act .is a lever that m atches the im pedance o f air to that
o f the fluid in the inner car. In som e sense organs,
muscles direct the receptors to different positions or
directions. M obile hands, eyes, and pinnae arc examples.
The m echanical structure o f sensory end organs ensures
that stimulus energy is efficiently collected. For
exam ple, the outer segm ent o f a retinal recepcor form s a
waveguide in which lighc reflects trom che inner wall.
This prevents lighc from escaping (Section 5.1.2a). The
dense hexagonal packing o f cones in the central retina
and their alignm ent with the center o f che pupil also
facilitates efficient collection o f lighc. Light absorption
in retinal recepcors is facilicaccd by che placcm cnc o f
pigm ent molecules on a folded membrane.
3. Spatial distribution o f stimuli The simplest sensory
systems consist o f a single detector that increases its rate
ot response m onotonically as stim ulation strength
increases. The simple eyespots o f some invertebrates arc
o f this type. M ore com plex sensory systems, such as the
skin, eye, and ear, have many receptors distributed over
a m em brane. In the skin, stim uli are applied directly to
differenc locations, w hich ensures chat che spatial
distribution o f receptors corresponds to che spatial
distribution o f stimuli. The car has a basilar membrane
chat is sensitive to traveling waves and creates an
ordered distribution o f frequencies over the hair cells.
The sem icircular canals o f the vescibular system are
arranged in orthogonal planes so that different
directions o f head rotation are coded distinctly. Th e lens
o f the eye ensures a faithful distribution o f light to form
an image. O u r two laterally separated eyes produce
images that contain binocular disparities tor the coding
o f depth. Vergence eye movements bring the images in
the tw o eyes into spatial correspondence.
4. Trophicfunctions an d protection Som e structures
associated with sense organs, such as blood vessels and
glands, serve trophic functions. Sense organs arc
designed so chat these structures do not interfere with
stim ulus d etection. Thus the cornea and lens do not
contain capillaries. Instead, they have highly specialized
trophic mechanisms. The capillaries o f the retina are
kept away from che fovea and are placed so that chey do
n o t form sharp shadows. The audicory system filters out
auditory effects o f blood circulation. Associated
structures or muscular systems protect sense organs
against injury or sensory overload. The eyelids,
epiderm is, and the muscles o f the middle ear arc
examples.
4 .2 TYPES OF SENSORY CODING
A sensory end organ transduces a spatiotem poral pattern o f
stimulus energy into a corresponding pattern o f electro­
chem ical activity, w hich produces neural discharges in
a sensory nerve. In the sim plest case, neural discharges
from a sense organ are linked m ore or less directly to a
response m echanism . For example, in che simple phocotaxic
response o f a m aggot, changes in light intensity as the
animal moves its head from side to side causes chc head со
cum in che direction o f least stimulus intensity (Fraenkel
and G unn 1 961). The coding process consists essentially ol
a simple transduction and som e am plification. N o features
o f the stimulus are extracted, other than its tim e varying
intensity.
A higher level o f com plexity is illustrated by the response
o f the sem icircular canals o f the vestibular svstem to head
rotation. The responses cause the eyes to rotate in the op p o­
site direction to chc head. The time-varying response from
each canal and che spatial stim ulation over the three canals
are processed, but nothing else. Signals reach the extraocular
muscles through a three-neuron pathway.
In the vertebrate visual system, light triggers certain
simple responses with a m inim um o f processing. For
instance, changes in light intensity evoke the pupillary light
reflex, and image blur evokes lens accom m odation. These
responses are involuntary and do not involve pattern vision
or conscious perception. Like the eye, a cam era autom ati­
cally operates the diaphragm and the focusing mechanism.
Inform ation abouc all visual feacures is contained in the
bundle o f light rays entering the eye (chc optic array). The
spaciocemporal paccerns o f lighc reaching che retina are
transduced in to spatiotem poral patterns o f neural activity.
We often sav chac visual features are coded in che neural dis-
charge. O n e could say equally well that a scene is coded by a
digital camera or a symphony is coded into grooves in a
vinyl disc. At this level it is best to say that the stimulus is
transd uced in to neural activity. A perceptual m echanism ,
unlike a cam era, involves com plex filtering processes that
analyze the neural signals into a m ultitude o f simple fea­
tures such as position, color, m ovem ent, and size. Simple
features are com bined into com plex features. At this level,
neural processes can be said to co d e stimulus features.
Finally, we generate percepts (descriptions) and store them
in memory, where they can be compared with current stim ­
uli or used to construct abstract ideas. At this level, neural
processes can be said to rep resen t o b jects and events, real or
imaginary.
A t a particular time, we process only those parts or fea­
tures o f the visual scene to which we are attending, even
though nonattended stimuli are transduced in the retina
and reach the visual cortex. Thus, m echanism s o f perceptual
awareness can be decoupled from the early stages o f visual
processing. They may also be decoupled from response
m echanism s because we can perceive w ithout responding
and we can learn to respond in a multitude o f ways to che
same stimulus.
The following discussion starts with a description o f
sensor y transduction processes. This is followed by a descrip­
tion o f processes responsible for extraction o f inform ation
from the neural discharge.
4 .2 .1 T H E N E R V E IM P U L S E
Sensory receptors are analog devices that respond to stim u­
lus energy by a graded change in mem brane potential,
known as a g en erato r p o ten tial (Section 5.1.2a). Graded
potentials also occur at synapses throughout the nervous
syscem, where they are know n as p oscsynaptic p o ten tials.
G eneracor potentials produce all-or-nonc a ctio n p o te n ­
tials, or nerve impulses. A nerve impulse is the basic unit
for long-range cransmission o f inform ation in the nervous
syscem. Transduction o f lighc energy inco nerve impulses
involves a com plex sequence of m olecular mechanisms
chac cake abouc 0.2 s, as described in Section 5.1.2b . These
m olecular m echanism s am plify the signal and provide a
feedback gain-concrol m echanism .
The auditory system must operate with much shorter
latencies because it resolves sounds with frequencies up to
abou t 2 0 kH z. Accordingly, the transduction process in
the hair cells o f the cochlea is more direct and does not
involve such a com plex sequence o f m olecular messengers
(H udspeth 1989). In the interest o f speed, the auditory
system relinquishes the am plification and gain control
provided by the slower visual transduction process.
An action potential is a transitory change o f about
9 0 mv in the standing potential across the cell m em brane o f
a neuron. The standing potential is due to a concentration
o f positive ions outside the cell, w hich is m aintained by
m etabolic activity. An action potential is triggered when
positive sodium and potassium ions migrate through pores
in che cell m em brane and briefly reverse che sign o f the
mem brane potential. The total current generated by ion
migration is modeled by the H o d g k in -H u xley eq u atio n s
(H odgkin and Huxley 1 952). The action potential travels at
up to 2 m/s in unmyelinated axons, and up to hundreds o f
m eters per second in myelinated axons. Velocity increases
with increasing axon diameter. In myelinated axons, action
potentials jum p betw een gaps (nodes) in the insulating
myelin. This increases speed o f conduction. In a given
neuron, all action potentials have the same am plitude and,
on that account, are said to obey the a ll-o r-n o n c law.
In the visual system, action potentials are first form ed in
retinal ganglion cells. The axons ot ganglion cells carry
action potentials to the thalamus, where they are relayed to
neurons that p roject to the visual cortex o f the brain.
Л typical cell in the visual cortex has a structure consisting
o t a tree o f branching dendrites, each with a multitude
o f dendritic spines, and a single outgoing axon. Incom ing
nerve impulses impinge on synapses on the dendritic spines.
Excited synapses convey graded potentials to the cell body
(som a) o f the neuron. A ction potentials generated in the
soma or the initial segm ent o fth e axon convey signals to the
next neuron in the chain.
Slowly rising action potentials mediated by calcium ions
are also generated in dendrites. D endritic spines are active
elem ents th at are capable o f am plifying or filtering excit­
atory potentials. Slight local changes in the m orphology o f
spines can m odulate their functional properties (Tsav and
Yuste 2 0 0 4 ).
A ction potentials also propagate back from the soma
into the dendritic tree. W e will see in Sections 6 .4 .3 and 6.5
that backpropagating action potentials are involved in syn­
aptic plasticity (Stuart and Sakm ann 1 9 9 4 ; M agee and
Johnston 1 997).
Because it has fixed am plitude, an action potential is a
qu antized signal. A system that transmits signals as a tem ­
poral string o f quantized impulses is an im p u lse-cod e. An
im pulse-code is used tor long-range transmission in the
nervous system, ju st as it is in the digital com puter. An
efficient im pulse-code has the following requirem ents:
1. It must use quantized signals ot fixed amplitude. Such
signals are relatively im m une to the effects o f noise
w ithin the system because they are stronger than all but
the m ost severe noise.
2. Signals should get neither weaker nor stronger during
transm ission. An axon with a diam eter o f 1 mm has a
resistance o f about 1 0 “ ohm/cm, which is abou t 10
times higher than that o f metal. I f signals in an axon
relied on electrical condu ction, they would fade w ithin
a few millim eters. Nerve impulses are boosted to a fixed
amplitude at the nodes o f Ranvicr, which occur along
myelinated axons at intervals proportional to axon
diameter.
3. D uring transm ission, signals must not coalesce and
must preserve their temporal order. Two properties o f
nerve condu ction ensure that these tw o requirem ents
are m et. First, the velocity o f conduction o f impulses
along a given axon is constant. Sccond , after an impulse
has been transm itted, the cell is unresponsive, or
refractory, for a few m illiseconds. Consequently, nerve
impulses are discrete and cannot get out o f order. Also
the refractory period lim its the upper frequency o f
nerve condu ction to about 5 0 0 impulses/s.
S ince the ampli rude o f a n eu r a 1spike is fixed, an impu lse-
code system cannot use amplitude modulation tor trans­
m itting inform ation. In the single axon, inform ation can be
transm itted only in terms o f the tim e o f occurrence ot
impulses or as a tem poral frequency or a m odulation o f
tem poral frequency.
C om pu ters use an impulse code to constru ct a digital
(num ber) code. In a defined tim e interval, an electrical
signal signifies the binary num ber 1, and the absence o f a
signal signifies 0. Each signal codes one b it ot inform ation.
A message is conveyed as a string o f binary numbers, o f
defined length (a word). A clock defines the tem poral posi­
tion o f each binary num ber in a word. H ence both tim e and
signal strength are quantized in a digital code.
Neural impulses do n o t occur in discrete tim e intervals.
So there is no digital coding in the nervous system. Sensory
nerves do not transm it inform ation about w hether an
impulse did or did not occur in a defined tim e interval.
However, synchrony betw een signals in different neurons is
used in neural signaling (see Section 4 .3 .4 ). A single recep­
tor transm its inform ation about the state o f depolarization
o fth e receptor, w hich depends on stimulus m agnitude. 'I he
generator potential is lawfully related to the logarithm o f
stimulus intensity, and the frequency o f impulses in a sen­
sory neuron is a m o n o to n ic function ot the generator
potential over the linear range.
4.2.2 ANALOG PROCESSING
Axons are designed for long-range transmission o f inform a­
tion. However, the m ost im portant coding processes do not
occur in axons but at synapses, where signal transmission
obeys very different rules, and inform ation trom many
sources can be com bined using operations such as addition,
subtraction, m ultiplication, and mutual in hibition . These
operations are typically analog, local, and nonlinear. In a
com puter, logical operations are perform ed by and-gates
and or-gates, which are perfectly structured connections
betw een binary elem ents. The nervous system does n o t pos­
sess perfect structures o t this kind. W hatever logical opera­
tions it perform s arise from a statistical and changeable
weighting o f a m ultitude o f inputs at synapses (M el 1994).
Inform ation can be transm itted at a much higher rare
by an analog neural signal than by neural spikes (de Ruyter
van Steveninck and Laughlin 1 9 9 6 ). Also, analog pro­
cesses occurring in parallel w ithin a large netw ork can be
perform ed much m ore rapidly than equivalent in-series
digital processes executed in com puters (K o ch e t al. 1986).
Analog processes are dedicated to a particular task, whereas
com puter programs may be m odified. Lack o f flexibility is
not a disadvantage in a system that subjects all inputs to the
same lim ited range o l translorm ations, and for which speed
o f processing is im portant. However, we will sec in che next
chapter that parallel processes in neural netw orks possess
some flexibility. Flexibility is achieved by growth processes,
by serial processing performed at a later stage, and by atten ­
tion mechanism s. Stim ulus-contingent changes at synapses
allow for som e short-term flexibility in processing and for
long-term learning.
Synaptic transmission is graded rather than quancal.
Each cortical neuron is studded with up to 2 0 0 ,0 0 0 syn­
apses arranged on a com plex o f branching dendrites. Analog
processes convey signals to the cell body (som a) o f a cortical
neuron. However, all-or-none neural spikes mediated by
calcium ions also convey signals from dendrites to the soma.
These spikes are slower than sodium spikes that travel along
axons. Also, action potentials backpropagate from the soma
to dendrites o f cortical pyramidal cells. These potentials can
prom ote subthreshold calcium action potentials initiated
by excitatory inputs (Larkum et al. 1 9 9 9 ). This coupling o f
action potentials facilitates detection o t coincidence ot
inputs arriving at a pyramidal cell from different layers o f
the visual cortex. The m agnitude o f this coupling depends
on the proxim al-distal distribution o f dendritic branches
(Schaefer et al. 2 0 0 3 ). The extent and distribution o f back-
propagation trom soma to dendrites are more restricted
after several action potentials have occurred in sequence
(Spruston ec al. 1 9 9 5 ; Yuste and D enk 1 9 9 5 ).
Shore inh ibitory interneurons cransmic signals in an
analog fashion. These signals inhibit rather than excite the
cells they impinge on. Excitatory and inhibitory interac­
tions at a given synapse depend on the relative locations ot
inputs on che dendrites, on ionic currents released by stim u­
lation, and on the m agnitude ot m em brane conductances.
We will see in Section 5.5. I f chat glial cells, w hich o u t­
number neurons, are also involved in cortical activity
(Nedergaard 1994). N eurohorm ones carried in the blood
o r cerebrospinal fluid regulate neural activity at target sites
throughout the nervous syscem. O th er influences, known
as n eu rom o d u lators, modulate neural transmission, rather
chan evoke neural impulses. For example, axons originacing
in subcortical centers such as the locus coeruleus carry neu­
rom odulator у signals to m ost parts o f che cerebral cortex
(Section 5 .5 .2 g ). O th er neurom odulatory signals arise in
the cerebral cortex (K atz and Frost 1 9 9 6 ). For example,
corticofugal impulses from che visual cortex to che laceral
geniculate nucleus m odify the response characteristics ot
geniculate cells.
There is a great variety o f dendritic patterns in cortical
neurons (see Figure 5 .2 0 ). Stellate cells, pyramidal cells, and
inhibitory/ intcrneurons in the visual cortex have distinct
dendritic patterns. Differcnc patterns serve distinct fu n c­
tions such as addition, m ultiplication, and gain control
(Silver 2 0 1 0 ).
For example, there are cells in the mammalian brain­
stem that acc as coincidence detectors for sound localiza­
tion. They respond maximally when inputs from one ear
arrive at one cluster o f dendrites at the same tim e as inputs
lrorn the other ear arrive at a distinct cluster ol dendrites.
Th e separation o f the cwo dendritic clusters increases signal
strength because signals arriving on neighboring dendrites
show nonlinear saturation, and hence have a high thresh­
old, while those arriving on distinct dendrites sum linearly
and have a low threshold (A gm on-Sn ir et al. 1 9 9 8 ). A sim i­
lar m echanism could d etect coincidence o f stim uli within
or between the eyes.
Synapses on local branches o f che dendricic cree o f pyra­
midal cells form distinct processing units. Each unit could
be sensitive to a particular spatiotem poral paccern o f inpucs
representing a particular com plex feature. Also, the co u ­
pling betw een each dendritic branch and che soma o f che
cell is su bject to m odification (see S ectio n 6 .5 .5 ).
Thus, che real work o f che nervous system is achieved by
nonlinear analog processes within clusters o t synapses on
the dendritic branches o f each neuron. T h equantal impulse-
code system is simply a way to get inform ation along an
axon from one synaptic cluster со che next w ithout loss.
C om puters are quantal and digital throughout, both tor
transmission o f signals and for signal processing.
4 .2 .3 M O N O P O L A R A N D B IP O L A R
DETECTORS
Som e stimulus features have direction as well as magnitude.
They are said со be oppositional, or b ip o la r stim u lu s fea­
tures. For exam ple, visual m otion along a given axis is a
bipolar feature, since the m otion can be in either o f two
directions. Som e receptors are b ip o lar d e te cto rs because
they produce a bipolar response to bipolar stimuli. They are
thus able to code both the magnitude and direction o f b ip o ­
lar features. For instance, a hair cell in a cupula ot a sem icir­
cular canal hyperpolarizes when the head rotates one way
and depolarizes when it rotates the other way. Since there
are no negative nerve impulses, neurons can produce b ip o ­
lar responses only with respect to a resting state o f m ain­
tained discharge. Thus, afferent fibers from che sem icircular
canals m aintain a steady discharge that decreases when
the head turns one way / and increases when it turns che
ocher way.
Lighc intensity is a m onopolar stimulus since there is no
negative light. Retinal receptors do n o t generate bipolar
receptor potentials— they all hyperpolarize when stim u­
lated. The stimulus feature o f light-on as opposed to lighc-
o ff is bipolar, but light-on and light-off responses are
achieved in two discincc secs o f bipolar cells into which the
receptors feed. They are called bipolar because ot their
structure, not because o f their function. Functionally, each
bipolar cell is m onopolar. It acts as a half-wave rectifier,
since it responds to alternate half-cycles o f a stimulus oscil­
lating in lum inance. A bipolar cell does not respond to a
steady stimulus. A cell producing distinct signals for light
increase and light decrease would have to m aintain a con­
stant discharge when there is no change in illum ination.
Similarly, m ost sim ple cells in the visual cortex have
little or no m aintained discharge. They act as half-wave rec­
tifiers with respect to the distribution o f dark-light stimuli
falling on their receptive fields. Each cell responds to only
one half o f the cycle o f stim ulation produced by a dark-light
grating m oving over the receptive field o f the cell. The full
range o f stim ulation is covered because cells occur in pairs
in quadrature spatial phase (S ectio n 5 .5 .3 ).
There are several reasons why it is m ore efficient to
d etect a bipolar feature using oppositely tuned m onopolar
detectors rather than a bipolar detector:
1. M onopolar detectors do not need a maintained
discharge.
2. Any disturbance o f m aintained discharge upsets the
calibration o f a bipolar detector. For instance, alcohol
upsets the m aintained discharge o f vestibular receptors,
with well-known consequences.
3. Tw o m onopolar detectors have double the dynamic
range o f a bipolar detector.
4. O utputs o f m onopolar detectors can be com bined to
produce a difference signal or ratio signal that is
independent o f changes in a stimulus feature to which
both detectors are equally sensitive. For instance,
if the output o f a cell in the visual cortex that is tuned
to one orientation is subtracted from that o f a detector
tuned to another orientation, the resulting signal
is independent o f the overall luminance o f the
stimulus.
5. N onlinearities in each detector may be canceled when
tw o opposed signals arc com bined. An example o f this
is provided in S ection 3 1 .4 .1 .
There is a price to pay for detecting a bipolar feature
with m onopolar detectors. There must be twice as many
m onopolar as bipolar detectors. Also, there must be an
opponcncy m echanism that com bines the tw o half-wave
rectified signals in to a unitary signal. D etecto rs (hair cells)
in the sem icircular canals arc bipolar and do not rectify the
head-acceleration signal. For them , the need to econom ize
on the num ber o f detectors and subsequent analysis o u t­
weighs the disadvantage o f m aintaining a discharge when
the head is n o t moving. Also, these detectors respond to
only one stimulus feature and do no need an opponent
mechanism to discount the effect o f stimulus intensity.
Sim plicity and speed o f processing are im portant for
vestibular detectors because they control eye-stabilizing
reflexes and postural responses, which must be rapid.
4.2.4 PRIMARY C O D IN G
4 .2 .ч а In tro d u c tio n
There are two basic coding processes in the nervous system.
The first is response coding, w hich is defined by the char­
acteristics o frh c response o f a receptor or neuron. It includes
variation in the strength ot the response as a function ot the
strength o f the stimulus. Thus, in the eye, light intensity
affects the strength o t the generator potential o f rods and
cones. Stim ulus onset, offset, and duration affect the tem ­
poral m odulation o f receptor potentials. These responses
becom e coded in terms o f tem poral characteristics o f neural
spikes in ganglion cells.
The second basic coding process is labeled-line coding.
It is defined in terms o t which o t a set o t receptors or neu­
rons is responding. A t the receptor level, labeled-line coding
depends on there being dillerent receptors. For example,
position is a primary labeled-line feature coded in terms
o t the location o t receptors on the retina. C ones are diller-
cntiallv tuned to long, m edium , and short wavelengths to
produce labeled lines lor color processing.
A coding process evident at the level o f single receptors
will be referred to as a prim ary coding process. A stimulus
feature coded by a primary sensory process is a primary
feature. Secondary features are coded at a level beyond the
receptors.
The outputs o f primary coding in retinal receptors are
elaborated by neuronal processing in the retina. The elabo­
rated signals code secondary features such as local lumi­
nance contrast and color opponency. These features are
coded in the responses o f ganglion cells. The coding o f other
secondary features, such as movement, orientation, and
binocular disparity, is delayed until the visual cortex.
Still other secondary features, such as complex patterns o f
optic flow and higher spatial derivatives o f disparity, are
coded in higher visual centers. All processes representing
secondary or higher features are derived from primary
coding processes.
Philosopherssince Aristotle have distinguished between
prim ary sensations and secondary sensations. Primary sen­
sations, like seen length and size, were said to resemble the
stim uli that give rise to them . Secondary sensations, such as
warmth and taste, were said to differ from their stimuli. Hut
this is a misleading distinction. Sensory inputs are related to
some aspect o f the stim uli that create them . That is why
they contain inform ation. For example, sensations o f tone
bear some relationship to the frequency o f sound vibra­
tions, even though tone is basically coded by the location o f
excitation along the basilar m em brane o f the inner ear.
The distinction betw een prim ary and secondary sensa­
tions gave rise to a futile debate betw een idealists, who insist
that sensations are all we know, and realists, who believe in
an objective world that transcends sensations. The problem
arose because sensations were treated as isolated idealized
entities, such as pure red, and pure tones. But there is no
unique relationship between a given sensation o f “red” and
a particular wavelength o flig h t. The same co lo r sensation
can be produced by many wavelength com binations. Also,
the sensation produced by a given com bination varies with
the spatial and tem poral features o f surrounding stimuli.
Nevertheless, perceptual experiences and the actions associ­
ated with them form consistent and coherent patterns
com m on to all people. W e experience paradoxes, illusions,
and delusions. But we can reveal errors by observing rela­
tionships betw een events and finding percepts that are m ost
consistent and reliable. By and large, our perceptual systems
are effective in detecting the structure o fth e local environ­
m ent and controlling our behavior in that environm ent.
Primary and secondary features and prim ary and sec­
ondary sensory coding that will now be discussed have
nothing to do with the primary and secondary sensations o f
the philosophers.
4 .2 .4 b C o d in g Stim u lus Intensity
The physical intensity o f an adequate stimulus is the energy
falling on unit area o f a sensory surface in unit time. W hen
an adequate stimulus varies in intensity bu t nor in any other
respect, the frequency o f nerve impulses generated in an
afferent sensory neuron is typically some m o no to n ic, satu­
rating iu nction ot stimulus intensity, modified by effects ot
spatiotem poral interactions betw een sensory inputs and by
sensory adaptation. The firing rate o f many sensory affer­
e n t declines exponentially when a constant stimulus is
applied to the receptor. These are p h asic sen so rs that trans­
m it inform ation abou t changes in stim ulation, rather than
about its absolute level. C ells that m aintain a response to a
steady-state input are to n ic sensors.
The direction from which a stimulus impinges on a
receptor may also affect its power to evoke a response. For
instance, a retinal cone is m ore sensitive to light that arrives
from the direction o f t h e cen tcr o f the pupil than to light
arriving trom other directions— a phenom enon known as
the S tiles-C ra w fo rd effcct.
Under certain conditions, the response o f the visual
system depends on the total physical energy falling w ithin
the area and tim e interval over which stimulus energy is
integrated. In the psychophysical dom ain, the area relation­
ship in vision m anifests itself as R ic c o ’slaw . This states that,
tor a stimulus of fixed short duration and with a diam eter ot
less than about 2" o f visual angle, the detection threshold is
inversely proportional to the product o f the area and inten­
sity o fth e stimulus (G raham et al. 1 9 3 9 ). The rime relation­
ship m anifests itself as B lo c h s law, which states that, tor a
stimulus o f a fixed small area and a duration o f less than 0.1
s, the threshold is inversely proportional to the product ot
tim e and intensity (R ouse 1952). A similar law in p h o to ­
chem istry is known as the Bunson-Roscoe law.
Each retinal ganglion cell receives inputs from several
receptors through a com plex cellular net work. The netw ork
defines the rccep tiv c field o f the ganglion cell. F.ach co rti­
cal cell receives inputs from several ganglion cells, which
define the receptive field o fth e cortical cell. The response o f
a retinal ganglion cell or o f a cell in the visual cortex is deter­
m ined by the spatiotem poral structure ot stim uli tailing
within its receptive field and nor merely by the total stimulus
energy (S ectio n 5 .5 .3 ).
Although lum inance changes by 10 log units between
starlight and sunlight, visual receptors have a dynam ic
range o f only abou t 3 log units. Furtherm ore, a ganglion
cell can transm it up to a frequency ot only about 8 0 0
impulses per second. The cells refractory period prevents it
from firing at a higher rate. At least tour m echanism s serve
to allow the visual system to com pensate tor the lim ited
dynamic ranges o f the receptors and transmission system.
1. Pupillary responses The pupils control o f the am ount o f
light entering the eye.
2. Nonlinear compression o f response sensitivity at high
lum inance. This is due to such causes as saturation o f
bleached visual pigm ent and o f neural responses.
3. General or local adaptation The visual system adapts its
sensitivity as a function o f local or mean level o f
luminance. This process is equivalent to placing a neutral
density filter over the whole or part o f the visual scene.
4. Subtractive adaptation This arises from lateral
inhibition betw een the “O N ” and “O F F ” regions o f chc
receptive fields o f ganglion cells. Ic reduces responses to
even areas o f even lum inance com pared with responses
to spatial or temporal contrast boundaries. This type o f
visual process is responsible for sim ultaneous and
successive contrast.
5. Segregation of 'ON an d 'OFF ganglion cells Th is
doubles the dynamic range o f che visual system.
4 .2 .4 c P rim a ry L a b e le d -L in e C o d e s
A primary labeled-line code depends on the sensory rcccp-
cor stim ulated. The main sensory m odalities, such as vision
and audition, arc labeled lines because receptors in each
m odality respond to one primary scimulus and evoke dis­
tin ct sensations. The concept o f labeled line receptors is
related to the concept o f sp ecific nerve energies associated
wich Johannes M uller (1 8 4 3 ), although the idea originated
before M uller (see Boring 1950, p. 8 0 ; and Rose 1999).
However, we now know that different sensory systems p ro ­
duce distinct sensations by virtue o f the centers o f the brain
into which they feed rather than by virtue o f differences in
neural activity.
 ЛИ detectors operating in a labeled-line system have a
band-pass tuning function, in which the firing rate at first
increases and then decreases as che value o f the labeled-line
feature is varied over the detection range o f the detector.
For example, the response o f a single retinal cone increases
and then decreases as a point ol light is moved across it. The
spatial tuning function is thus two-valued, which in tro­
duces an essential ambiguicy into che response o f any single
labeled-line detector. The tuning function ot a receptor to
changes in stimulus intensity is a single-valued function.
A nother reason for am biguity in a labeled-line detector is
chat a change in response can be due со either a change in
stimulus intensity or to a change in the labeled-line feature
to which the detector is tuned.
W ith in any sensory system, there are two basic types o f
labeled-line systems. The first is defined by the spatial loca­
tion o f the receptors on the sensory epithelium . These are
to p og rap h ic co d es. In the eye and the skin the topographic
code indicates spatial location. In the ear, it codes frequency
and is referred to as a to n o to p ic cod e. The second primary
labeled-line system is defined by the filter characteristics o f
different recepcors. In the eye these arc the rods and the
three types o f cone. This system codes achrom atic stimuli
and long, m edium ,and short wavelengchs o f light. Differenc
types o t receptor in the skin code pressure, temperature,
and pain. These types o f labeled-line system will be referred
to as recep to r-ty p e co d in g . G eneral types o t coding will
now be discussed in m ore detail.
4 .2 .4 d P rim a ry T o p o g ra p h ic C o d in g
A sensory m odality can have only one to p o g rap h ic labeled -
lin e system . This is because each receptor in a given
system has a distinct position on the sensory epithelium .
Topographic sensory inputs project o n to che cerebral cortex
to torm a to p o lo g ica lly co n tin u o u s m apping. Stim ulation
o f a given receptor evokes an impression o f a given value on
a sensory continuum , which is the lo cal sign o t the recep­
tor. The local sign o f a sensory cell is a function o f how it is
connected in the central nervous system, rather than o f its
position in che sensory m em brane. However, sensory recep­
tors do not change their positions on the sensory epithe­
lium and the order o f receptors is preserved in the cortex.
Therefore, one may talk about receptors coding location on
the sensory surface.
A sensory system can devote its topographic system to
only one sensory feature, which is the local sign, or to p o ­
graphic, feature for that sensory system. This will be called
the lo cal-sig n exclu sion rule. For both vision and couch,
position is the local-sign feature. For audition, it is frequency,
and for the utricles it is direction o f head acceleration.
The retinal image has a precise geom etry, w hich can be
encoded only it receptors m aintain a fixed spatial order.
O n ce the spatial attributes o f an image have been coded into
nerve impulses in ganglion cells, a fixed spatial ordering o f
the axons in optic nerves is no longer required. It is only
required that the specific connections that each neuron
makes be preserved until spatial inform ation is encoded
into a nontopographic form , or evokes a response. The fact
that the visual hemificlds are represented in different hem i­
spheres or that the mapping o f the retina o n to the cortex
can be described as a conform al logarithm ic function
(Section 5.5.4d ) has no significance for spatial coding. In
the nervous system, only the con nection s that cells make
with ocher cells are relevant. The geomecry o f che disposi-
cion o f cells on the cortical surface is irrelevant tor coding
o f topographic inform acion, although ic is im portant for
econom izing on the lengths o f neural connections.
There has been a long debate abouc whecher local signs
are innate o r calibrated through experience (see Section
2 .8 .3 ). The debate centered on the restricted idea o f a one-
to -o n e correspondence between retinal location and per­
ceived visual direction. Hut a richer set o f concepts emerges
when one considers the topology o t visual space. C onsider
the follow ing propositions regarding retinal local sign.
1. A point stimulus evokes a sensation o f only one point.
N point stimuli evoke a sensation ot N points when
they arc sufficiently well separated.
2. Closely adjacent stimulus points are perceived as
connected.
3. The relative order o f stimulus points is preserved in the
percept.
4 . The greater the distance between stim ulus points, the
greater the pcrccivcd distance between them.
5. C o llin car stim ulus points appear collinear.
6. A stronger version o f proposition 5 is that images
arising from straight lines are perceived as straight. This
carries the corollary that a line perceived as straight
when imaged on one part ot the retina is perceived as
straight when imaged on any other part.
7 . The relative directions o f stimulus points are preserved
in the percept.
The first five propositions arise from innate mechanisms
chat are noc modified by experience. Even H elm holtz, the
arch em piricist, believed chat proposition 3 depends on
innate processes. The last two propositions are not necessar­
ily true and are modified by experience. Tims a period o f
exposure to curved lines induces straight lines to appear
curved. G eom etrical illusions attest to the fact that proposi­
tions 6 and 7 are su bject to short-term experience.
4 .2 .4 e R c c c p to r -T y p e C o d in g
All labeled-line systems in a given sensory modality,
other than the local-sign system, are n o n to p o g rap h ic.
They depend on differences betw een che filter characteris­
tics o f different receptors rather than on positions o f
receptors on the sensory epithelium . They could be called
rcce p to r-ty p c la b eled -lin e codes. N ontopographic sen­
sory inputs p roject onto the cerebral cortex to form
d iscrete m aps rather than continuous topographic maps.
O n e such system is the three-cone color system, in
which the receptors act as differential filters for wavelength.
For a given intensity of light, the response of a retinal cone
is a bell-shaped function o f the frequency (wavelength) o f
the light. C o lo r is not a posicion-dependcnt stimulus fea­
ture. A com plete set o f color receptors must be present at
each location o f the local-sign system, which itself has only
one com plete set o f channels. This imposes a constraint on
the num ber of color channels. I f color were coded by many
channels, only a subset o f these channels would be activated
at a given tim e by a given stimulus. This would degrade the
spatial resolution o f the local-sign system. Also, i f there
were many color channels, the retina would have to be
impossibly large. It was this logic th at led Thom as Young
(1 8 0 2 ) to propose that there are only three types o f
receptor for color, and that they have widely overlapping
wavelength tuning functions.
The only way to escape this constraint is to devote one
part o f the eye to color coding and a distinct part to spatial
resolution. The m antis shrimp has eyes o f this type. A cen­
tral set o f low-density om m atidia contains at least ten types
o f color pigm ent, which filter the incom ing light. They are
thus capable o f resolving the chrom atic spectrum . Two
flanking sets o f high-densitv achrom atic om m atidia resolve
the image spatially. The three sets o f om m atidia in each eye
converge on che same location in space. See Section 33-2.1
for m ore details o f these remarkable eves.
4
O th er nontopographic labeled-line systems include
olfactory and taste receptors.
A ll primary sensory features in a given sense organ are
coded in term s o f (1 ) the tem poral features o f responses
such as latency and frequency, (2 ) local sign, or (3 ) recep­
tors with d istin ct tuning functions for a nontopographic
feature. In the visual system, this means that receptors can
signal only intensity, tem poral changes in intensity, oculo-
cencric direction (local sign), and wavelength. C od ing for
o ther features must be deferred to beyond the receptors.
Types o f sensory coding are listed in Table 4.1. D eferred, or
secondary, coding will now be discussed.
4 .2 .5 SEС О N D A RY С О D IN G
S eco n d a ry stim ulus features are those features that are noc
coded in terms o f responses o f single sensory receptors.
They are spatial or spattotem poral derivatives of primary
stimulus features. C o d in g processes that require the co o p ­
erative activity o f several receptors or o f several neurons at a
later stage o f processing arc secon d ary co d in g processes.
Since secondary coding involves integrating inform ation
from several receptors o r neurons, it is refereed to as
p o p u latio n co d in g (Section 4.6 .2 b ).
Secondary coding starts in the recina. O n e retinal system
consists o f O N -bip o lar cells and O F F -b ip o lar cells (Section
5 .1 .3 ), which com bine to create the receptive fields o f gan­
glion cells that code local contrast. C o lo r is initially coded
ac che level o f chree types o f cones. However, the secondary
feature o f color opponency is coded at the ganglion-cell
level, and color constancy is coded at the cortical level.
O rientation could be coded by receptors that differ in shape
or by ganglion cells wich elongated receptive fields. But
visual receptors and ganglion-cell receptive fields have c ir­
cular cross sections. Single receptors are incapable ot coding
m otion direction o r binocular disparity. C od in g o f visual
features such as m orion, oriencacion, and disparity is delayed
until the visual cortex.
We are able to see the m otion, orientation, and relative
depth ofstim u li ateach location in the visual field. Therefore,
tor each location in the visual field, there must be a co m ­
plete set o f secondary detectors for each o f these features.
However, secondary features do not require dedicated reti­
nal receptors because the outputs from a given set o f recep­
tors can be configured in different ways to code different
secondary features. The form ation o f d istinct channels for
secondary features can occur in the retina or can be p ost­
poned until inputs reach the visual cortex. In a com plex
visual system, it helps to postpone coding o f secondary
features because there is more room in the brain than in the
eye for che necessary neural processes.
There are two basic types o f secondary coding. The first
is response coiling, which involves the temporal character­
istics o t neural responses. This is discussed in Section 4.3.
The second is labeled-line coding, or m ultichannel coding,
which will now be discussed.
4 .2 .5 a M u ltip lc -C h a n n c l Systems
It is unfortunate that the word “channel” is n o t well defined.
People talk about the visual channel as opposed to the audi­
tory channel, the visual m otion channel as opposed со che
color channel, and about the red, green, and blue channels
w ithin che color svstcm.
i
In this section a m ultichannel
system is defined as one composed o f an array o f labeled-
line detectors for a given stimulus feature. Typically, each
d etecto r has a bell-shaped cuning function with a response
peak and two flanks over which the response falls to zero,
and som etim es to below zero. For instance, a retinal cone
shows a band-pass response when the wavelength o f a light
o f fixed intensity is varied, or when che position o f the scim­
ulus is varied. Also, a hair cell in che auditory cochlea shows
a band-pass response as the frequency o f a tone o f fixed
intensity varies. However, for any detector with a band-pass
tuning function, two stim uli lying on opposite flanks o f che
cuning function generate the same response. Therefore the
responses o f single detectors are ambiguous.
 The universal solution to this problem is to have d etec­
tors tuned to different bu t overlapping bandwidths within
the stimulus continuum . D etectors with the same band­
width and peak sensitivity constitute one channel ol a
m ultichannel system. D etectors in different channels dirfcr
in their peak sensitivity and span different ranges o i the
stim ulus continuum . For color, there are three channels—
red, green, and blue cones. For retinal position, rhere are
about one m illion channels (ganglion cells). W c can say
that all secondary m ultichannel coding involves com bining
the responses from a set ot detectors with overlapping
tuning functions. D etection o fth e value o f a particular stim ­
ulus depends on the com bined output ot the stimulated
detectors.
A lthough the response o f any channel is ambiguous
across the two halves o f its tuning function, the com bined
responses ot the set ot activated channels provides a unique
output tor each value o f the stimulus continuum . Thus, a
particular value o t a stimulus feature evokes a particular
com bination o f responses in a particular set o f overlapping
channels, w ithin the lim its o t resolution. For example, each
wavelength o f the visible spectrum evokes a unique response
in the set ot red, green, and blue cones.
A single channel o f a m ultichannel, labeled-line system
can determ ine the value o f a stimulus with a precision no
finer than h alf the width o f its tuning function. This pres­
ents no problem it there are many channels, as in the
m illion-channel local-sign system o f the eye. However,
according to the local-sign exclusion rule, there can be no
more than one m ultichannel local-sign system in a given
sense organ. But fortunately, ir is not necessary to have
many narrowly tuned channels to achieve good discrim ina­
tion. The value o f a stimulus can be detected with great pre­
cision from the outputs o f a tw o-channel system. The
G erm ans used this fact during World War II. Their b o m b ­
ers navigated down the locus o f equal volume o f signals
from tw o overlapping radio beams. Any departure from
this locus was immediately detected by a change in the
strength o f t h e signal from one beam relative to that from
the other. For this type o f system to work, the tuning func­
tions o f t h e channels must overlap, but the output o f each
channel must retain its identity.
All multichannel systems are presented with the following
sources o f am biguity:
1. Metamerism Any detector system with only a few
overlapping tuning functions is able to d ctcct the value
o f a single stimulus but has reduced capacity to resolve
tw o or more stimuli presented at the same tim e to the
same set ot detectors. Such systems arc m etam eric
sensory systems. For example, the same color
impression can be created from different com binations
o f wavelengths and luminance. There is no cure tor this
type o f am biguity in a primary sensory system such as
the color-detection svstcm. The metamerism is
S E N S O R Y C O D IN G
obligatory. However, in a secondary coding system,
metamerism in one spatial feature may be compensated
by another spatial feature. For instance, different
orientations o f a set o f lines may n o t be resolvable by
the orientation-d ctection system but may be resolved by
the position-detcction system.
M etam erism is discussed in more detail in Section 4.2.7.
2. Confounding effects o f intensity The response o f a
d ctcctor in a m ultichannel system is ambiguous because
changes in the stimulus feature to which the detector is
tuned arc contoundcd with changes in stimulus
intensity. The am biguity can be resolved by using the
difference in response ot tw o neighboring dctcctors
(Section 4 .2 .8 ), or by norm alizing the response o f a
given ceil by dividing its response by the mean response
o f neighboring cells (Section 5.5.3).
3 . Confounding one feature with another A given neuron in
the visual co rtex is tuned to more than one stimulus
feature. l;or example, many cells in rhe visual cortex are
tuned to both the direction ot m otion and the
orientation o f a stimulus. However, the spatial
distribution o f neurons tuned to one feature differs
trom that o f neurons tuned to another feature.
The visual system is therefore able to com bine
independently the outputs that arise trom the different
stimulus features. This is an econom ical process.
If each neuron in the visual cortex were tuned to
only one o f N stimulus features instead o f to all the
features, the num ber o f neurons would have to be
multiplied by N.
There are at least two reasons why it is better to cover a
wide stimulus continuum with several detectors rather than
with only one.
In the first placc, the design o f an efficient detector for
one end o f a teaturc continuum usuallv differs trom that ot
i
a detector at the other end. For example, a detector for high
spatial frequency (fine patterns) is fundam entally different
from a detector for low spatial frequency (coarse patterns).
Also, a detector o f vertical lines has a vertically oriented
receptive field, w hich renders it relatively insensitive to hor­
izontal lines. Even tor trcqucncy-coded detectors o f stim u­
lus intensity, the stimulus range is typically partitioned
am ong several detectors with S-shaped tuning functions at
different positions along the stim ulus-intcnsity continuum .
Thus, rods operate at low intensities and cones operate at
high intensities.
In the second place, m ultichannel systems are less sub­
je c t to the effects o f noise. This is because the effects o f noise
arc reduced when signals with independent sources o f noise
arc com bined. O n e can think o f the ou tp u t o f each channel
o f a m ultichannel system as a vector w ith length determ ined
by signal strength and direction by the peak value o f the
• 137
cuning funccion o f chac channel. The veccors of' all active
neurons are com bined со form che population veccor, which
forms che escimacor for coding chc scimulus. An optim al
cscimacor should, on average, produce che correcc value
(ic should be unbiased) and ic should have minimum vari­
ance (noise). Deneve ec al. (1 9 9 9 ) developed a biologically
plausible neural necwork chac simulaced a m ultichannel
syscem for dececcion o f scimulus orientation. By making
cercain assumptions abouc chc cuning functions and che
cype o f noise, chey showed chac chc model perform ed as
an ideal dececcor. See Abbocc and Dayan (1 9 9 9 ) for a dis­
cussion o f che effects o f correlated noise in m ultichannel
svsccms.
4 .2 .5 b C h a n n e l T u n in g Funccions
Tlie cuning funccions ofseparate channels in a m ultichannel
syscem arc measured by ploccing che response frequency of
single neurons as a funccion o f changes in che value o f a
given fcacure. C hannel bandwidch is usually specified by
h a lf che widch o f che cuning funccion ac h alf ics heighc.
Channel bandwidch may be measured by four psychophysi­
cal procedures:
1. Range o f adaptation In chis procedure o n e measures
che range o f values o f a cesc scimulus for w hich che
dececcion chreshold is elcvaccd by previous adapracion
со a similar scimulus o f fixed value. The procedure
can be repeaced for differenc values o f che adapting
stim uli (Blakem ore and C am pbell 1 9 6 9 ). Ic is assumed
chac che cffcccs o f adapcacion cransfer from one
channel со anocher only when cheir cuning funccions
overlap.
2. Range o f subthreshold summation C onsider a variable
feacure such as oriencacion, velocity, or disparicy chac is
dccecccd by cells wich overlapping cuning funccions.
Discincc subchreshold stim uli chac fall wichin che
bandwidch o f che cuning funccion o f a cell may
summace со produce a suprachreshold scimulus— an
cffccc known as subthrcshold sum m ation. By varying
che relacive values o f cwo simulcaneous stim uli over a
sensory continuum , one can decermine the stimulus
range o f subchreshold sum m ation. This reveals che
bandwidch o f channels dcvoccd со a Оgiven sensorv/
feacure. For example, che cuning bandwidch o f
oriencacion dececcors has been inferred from che
range o f orien cations over w hich subchreshold
sum m ation o f cwo differencly oricncaccd stim uli
occurs (Thom as and G ille 1 979). Similarly, che spatial-
frequency bandwidch o f dececcors has been inferred
from the range o f spatial frequencies over which
subchreshold summacion o f gracing acuicy occurs
(G raham and Nachm ias 1 9 7 1 ; Sachs cc al. 1971;
W ilso n and G elb 1 984). The application o f
subchreshold summacion со sensory processing
o f 2 -D spatial concrasc stim uli was reviewed by
G raham (1 9 8 9 ). Subchreshold summacion in binocular
vision is discussed in S ection 13.1.
3. Range o f masking A briefly presenced suprachreshold
stimulus elevaces che chreshold for a briefly presenced
stimulus presenced in che same or a neighboring
location, ac che same cime or in close rcmporal
contiguity. This is known as masking. For exam ple, one
can determ ine the range o f spatial frequencies over
which a masking grating elevates the chreshold o f a
superimposed test grating (Stroineyer and Julesz
1 9 7 2 ; W ilso n et al. 1983). After allowing for
probability sum m ation and nonlinear interactions,
the results suggest chac chere are ac lease six spatial-
scale channels with a half-am plitude bandwidth o f
abouc 2 .2 occaves for che lowesc spacial-frequency
channel, and about 1.3 octaves for the highest channel
(W ilso n 1991a)- Binocular masking is discussed in
Section 13.2.
4 . Comparison o f detection thresholds with identification
thresholds I f cwo stim uli on a given sensory continuum
stim ulate discincc sensory channels, the idencicy o f each
scimulus should be apparcnc at the same contrast at
w hich it is dececced. This is because each labeled-line
channel produces a d istinct sensation. Two such stimuli
arc said со be perfeccly discrim inated. Stim uli chac are
not perfectly discrim inablc stim ulate channels with
overlapping tuning functions. For example, Nachmias
and W eber (1 9 7 5 ) found that gratings o f 3 and 9 cpd
were perfectly discriminaced at the contrast at which
they were just detected. Using this m ethod, W atson and
Robson (1 9 8 1 ) concluded that there are abou t seven
channels devoted to the detection o f spatial frequency
(S ectio n 5 .6 .3 ).
O n e can also ask how many channels span che total
bandwidth o f a detection system for a given sensory feature.
For color there are three, and for local sign there are about
one m illion. Estimaces o f the num ber o f channels for
m otion, spatial scalc, and binocular disparity vary betw een
three and about 20. A related question is what proportion
o f the bandwidth o f a detection system docs the mean
bandwidth o f d etectors occupy. This proportion is not
the reciprocal o f the number o f channels, since channels
overlap.
It is generally assumed chat a m ultichannel system is
more sensitive to a change in the value o f a stim ulus feature
when the tuning functions are narrower. In investigating
this question Pouget et al. (1 9 9 9 ) used che facc chat che
ju st noticeable change o f a stimulus value is proportional
to the square root o f Fishers measure o f inform ation (see
Brunei and Nadal 1998). For a population o f N neurons
with Gaussian tuning functions distributed evenly over a
stimulus continuum and with independent noise with
variance a2, Fisher inform ation is given by:
where f ( 0 ) is the mean activity o f neuron i in response to
stimulus value 0, and f ( 0 ) is its derivative with respect
to 0. It follows from this equation that the inform ation,
and therefore stimulus discrim inability, increase as tuning
width decreases. A ccording to their analysis the optim al
tuning curve has a width equal to 1/N. Pouget et al. also
showed that sharpening tuning functions by inhibitory
interactions at a higher level does not necessarily improve
discrim ination because the process introduces correlated
noise am ong neurons. In o ther words, processing occurring
beyond the initial stage o f detection cannot increase the
inform ation con ten t o f a stimulus. Pouget et al. (1 9 9 8 )
developed a nonlinear recurrent network model o t popula­
tion coding.
4 .2 .5 c C h a n n e l H o m o g e n e ity
C onsider a detection system in w hich, for each location
in the visual field, there is a set o t band-pass detectors
(channels) that covers the detectable range o f the stimulus
feature. The ch an n el h om o g en eity o f such a system can be
defined with respect to each o f the follow ing criteria:
1. Homogeneity oftuning functions 'I he tuning functions o f
channels for a given feature are hom ogeneous when
they are sim ilar over the total area o f the sensory
epithelium where the detectors occur. For exam ple, for
each type o f cone, the chrom atic absorption function is
the same wherever the cones occur in the retina. The
discrete nature o f the three chrom atic channels is
revealed by humps and dips in the hue-discrim ination
fu n ction , since hue discrim ination is best where the
tuning functions ot neighboring color channels overlap
(Section 4 .2 .7 ). H ue-discrim ination functions are
derived from stimuli subtending 2°. However, since the
visual pigments are rhe same over wide areas o f the
retina, the peaks ot the discrim ination tu nction should
occur at the same wavelengths wherever the stimulus is
placed.
The detectors o f the m otion-detection system do not
have hom ogeneous tuning functions. M otion detectors
based on small receptive fields in the central retina are
sensitive to low velocities, while m otion detectors based
on large receptive fields in the visual periphery are
sensitive to high velocities. A lthough the m otion-
detection system may be a three-channel system in rhe
sense that three detectors span the velocity bandwidth
o f rhe system at any locarion, rhe bandwidrhs vary in a
continuous fashion over the retina.
Locally, a sensory system can have a sm all num ber o f
channels with distinct tuning functions but show a
continuum o f tuning functions over the retina. In this
type o f system one would expect to find undulations in
the discrim ination function for small stim uli that
stim ulate a local discrete set o f detectors, but a sm ooth
discrim ination function for large stimuli that stim ulate
a wide range ot d etecto r types over a large area. C olor
may be the only visual feature coded by channels with
overall hom ogeneous tuning functions.
Visual features derived from spatial coding, such as
m otion, spatial scale, and orientation are grossly
in hom ogeneous because o f the steep increase in the
size o f the receptive fields o f ganglion cells as one
moves away from the fovea. For the same reason,
binocular disparity is coded by channels with
inhom ogeneous tuning functions. This issue is
discussed further in S ection 11.4.2.
2. Relative distribution ofdifferent types o f receptor The
color system is inhom ogeneous in this respect since the
proportions o f red, green, and blue cone types vary
from one locarion to another. The oricntation-d ctcction
system is probably hom ogeneous in this respect.
4 .2 .6 FEA TU RE D E T E C T O R S
4 .2 .6 a D e fin itio n o f F eatu re D e te c to r s
A featu re d e te cto r is a neuron whose firing rate varies as a
function o f a change in a defined stimulus fearure. The cells
tuning tunction to a particular stimulus feature is measured
by recording irs firing rate as rhe feature is varied for a stim ­
ulus presented in the cell’s receptive field. A stimulus feature
is ch an n eled at a specific level in the nervous system when
detectors for that feature exist at that level. In other words,
the feature is represented explicitly at that level (Man-
1982). Light intensity is channeled at the receptor level,
since a change in light intensity changes the response o f
receptors. O th er prim ary visual features channeled at the
receptor level are position, flicker, stim ulus duration, and
wavelength. C ontrast and color opponcncy are channeled
in the retina at the ganglion-cell level. M otion is channeled
at the ganglion-cell level in the frog and rabbit, but in pri­
mates it is first channeled in the visual cortex. O rientation
and disparity are, also, first channeled in the visual cortex.
In the retina they are u n ch a n n elcd .o r d istrib u ted .
It is inefficient ro have more than rhe m inim um num ber
o f features channeled at the receptor level. It many specific
features were encoded there, m ost receprors would be inac­
tive m ost o f the tim e and this would degrade acuity. It is
better ro have a ser o f receptors with m ore or less rhe same
broad response characteristics so that gradients o f light
intensity may be detecred at all rerinal locations. It is also
undesirable to channel many features at the ganglion cell
level because chis would increase chc size and complexicy o f
the eye. It is better to channel secondary features in the cen­
tral nervous system, where there is more room and where
cells can be specialized for detection o f specific secondary
or higher-ordcr stimulus features.
4 .2 .6 b C o d in g D e n sity and P opu lation C o d in g
Л system in w hich each neuron responds to only one stim u­
lus exhibits highly specific, or lo cal co d in g . A com puter
keyboard uses local coding. M ost o f the time, m ost neurons
would n o t respond and chc system could represent only
N stim uli. A system in which inform ation is represented by
che com bined activity o f all neurons exhibits d en se co d in g .
The coding is called dense because, with mosc natural visual
scenes, each neuron would have a high probability o f firing.
In dense coding, inform ation is present in the spatioccinр о­
га I paccerns o f accivity, as in a hologram . For N neurons,
each signaling a binary stace, a dense code could represent
2 s patterns. A system in w hich each neuron responds to a
few stimulus features exhibits sp arse co d in g with respect
со those feacures. Sparse coding com bines efficiency wich
reasonable capacicy to carry inform ation. A nything that
increases the feature specificity o f cells narrows their tuning
functions and increases the sparseness o f coding. A t the
same tim e, the informacion con ten t o f responses o f indi­
vidual cells increases and che responses o f neighboring cells
becom e decorrelaced. This decreases coding redundancy
and cherebv improves m etabolic efficiency.
Each recinal receptor responds to a m ultitude ot visual
features, and coding is therefore dense with respect со stim ­
ulus features. The only specificity is with respect to simple
features such as position, lum inance, and wavelength. Many
cells in the striate and peristriate areas show selective tuning
to contrast, length, color, m o tio n , orientation, and binocu ­
lar disparity. Their coding is therefore sparser than that ot
retinal recepcors. These feacurcs are m ore com plex chan
chose coded locally in che retina. The single co rtical cell
can n ot be said со code any o n e o f chese feacures unam bigu­
ously, since variations in firing rate may be due со a change
in any one or any com binacion o f chem. A t higher levels o f
visual processing, coding becom es sparser because cells
becom e selective со even m ore com plex feacures (Barlow
1961). For example, cells in the infcrotem poral cortex
respond selectively to faces. Sparse coding econom izes in
energy consum ption (Levy and Baxter 1996). This is im por­
tant in the brain, which accounts for up to 50% o fth e total
energy consum ption o f the body.
It is believed that particular stimulus features are distin­
guished in a sparse coding system by che cooperative acciv­
ity o f populations o f cortical cells tuned to that feature. This
is known as p o p u lation co d in g . For example, che orienta-
cion ot a line may be uniquely coded by the output o f the set
o f orientacion-sensicive cells chat che given stimulus excites.
The direction o f m ocion o t che same line could be coded by
che oucpuc o f the sec o f m otion-sensitive cells that it excites.
Since che two sets o f cells are at least partly distinct, each
stimulus feature is coded distinctly, although n o t necessar­
ily in the activity o f individual cells (see A b b o tt and
Sejnow ski 1 9 9 9 ). However, this simple view must be m odi­
fied because evidence reviewed in S ection 5 .6 .7 shows that
the same pattern o f response o f cortical cells can be p ro ­
duced by stim uli possessing different com binations o f
mocion direccion and orientation.
The response specificity o f a cell in che visual cortex
varies as a function o f che responses o f other neighboring
cells outside the classical receptive field. Thus, efficiency o f
inform ation transmission ot cells in che visual cortex o t alert
monkeys increased as m ore o f a patch o f a com plex scene
was exposed (V in je and G allant 2 0 0 0 , 2 0 0 2 ). Recurrent
influences arising from attention and learning also increase
the response selectivity o f co rtical cells (Section 5.6.8).
Rao and Ballard (1 9 9 9 ) argued that a cortical neuron
that is influenced by stim uli outside its receptive field detects
the difference between an inpuc signal and che predicccd
value o f thac signal. O nly the difference between the signal
and its predicted value is transmitted to higher centers. This
predictive coding reduces redundancy of transmission.
Z ohary (1 9 9 2 ) developed an algorithm tor determ ining
how many cells in an ensemble o f cortical cells, each tuned
to two stimulus dimensions, is required to match the psycho-
physically determ ined perform ance of che animal.
4 .2 .6 c In te r a c tio n s B e tw e e n F eatu re D e te c to r s
Feature detectors do noc form a neac set o f discincc parallel
m odules, each serving a discincc stimulus attribute. They
interact in che following ways:
1. Spatial an d temporal binding o f a given feature
N eighboring scimuli and scimuli in temporal sequence
tend со be correlated because objects tend to have
spatial and tem poral extension. O n e can regard cortical
cells that respond to spatially or tem porally extended
stimuli, such as angles or specific patterns o f m otion,
as reducing the redundancy o f natural images
( Rao and Ballard 1999). This issue is discussed in
Section 4.5.2b .
2. Rinding distinct features O b je cts possess parcicular
concatenations o f distinct visual features that must be
recognized as belonging to the same objecc. Ihis issue is
discussed in S ection 4 .5 .4 . Also, objects defined by
different feature com binations must be perceptually
segregated from each other and from the background
(Section 5 .6 .7 ).
3. Compositefeatures The outputs from feature detectors in
discincc stimulus dom ains may be com bined ac an early
scagc o f processing со form dedicated com posite feature
detectors. For example, signals from m otion dececcors
 and signals from disparity detectors feed into m otion-
in-depth detectors (Section 3 1 .3 ).
4 . Inter featurefacilitation The location and shape o f a
visual contour may be defined in terms o f lum inance,
color, m otion, texture, or binocular disparity. The
precision o f localization o f a contour improved as more
attributes were added (Rivest and Cavanagh 1996).
M cG ra w c t al. (2 0 0 3 ) found that the apparent location
o f a small patch coincided with the centroid o f the
distribution o f luminance or o f texture w ithin the
patch. W hen the tw o distributions were skewed in
opposite directions, the apparent location ot the patch
depended on the relative contrasts o f the tw o stimulus
features. However, precision was poorer than when only
one feature was present. Thus, consonant features
improve the precision o f localization while conflicting
features degrade it.
Poom (2 0 0 2 ) found that subjects could d etect aligned
edge segments em bedded in random ly oriented
segments when the segments were defined by
lum inance, by m otion, or by disparity. However, adding
m ore features did not improve perform ance. Perhaps
these features would facilitate each other when near the
detection threshold.
5. Cue invariance W c can d etect the m otion o f edges
defined by lum inance, texture, color, or disparity
(Regan 1 999). F.ach o t these feature systems could have
its own m otion-detection m echanism. However, in
cases like this, it is m ore econom ical to converge the
outputs o f the various feature detectors on cue-invariant
cd gc-dctcctors before the detection o f m otion
(Cavanagh e t al. 1 990). Som e cells in V I o f the c a t and
m onkey responded to boundaries defined by texture,
lum inance, or contrast (Leventhal et al. 1998). This
suggests that cue invariance occurs initially at the level
o f edge detection rather than at the level o f m otion
detection.
D epth can be detected by cues such as vergence,
perspective, m otion parallax, or disparity. In this case,
cue invariance cannot occur at the level o f contour
detection because these are not all contour-detection
processes. Each cue system must have its own depth-
d ctcction m echanism . Their weighted outputs then
converge o n to a cue-invariant depth detection system at
higher levels in the visual system (Section 11.5).
6. Cross talk Repeated exposure to particular
com binations o f features can cause one feature to affect
the perception o f another feature. The chrom atic
aberration o f the eye produces color fringes along
black-w hite borders. However, we do n o t see these
color fringes because the visual system applies a
correction at a neural level. Prisms produce color tringes
that disappear after the prisms have been w orn for a few
days. Again, the neural system com pensates for them.
TIi is adaptation process is reflected in the M cC oIlough
effect, in which exposure to gratings with particular
com binations o f color and orientation produces
long-lasting coupling betw een perceived co lo r and
orientation (Sections 4 .2 .9 c and 13.3.5).
7. Mutual dependency The interpretation o f o n e feature o f
an o b ject can depend on the value o f associated features.
For example, the perception o f relative m otion depends
on the perceived relative depth and transparency o f
objects (Section 2 2 .5 .3 ). These effects depend on
com plex and highly nonlinear feedback processes by
w hich the outcom e o f one perceptual process influences
other processes.
4.2.7 M ETAM ERISM
A m cta m erie stim u lu s is a com bination o f physical stimuli
within a stimulus continuum that produces the same
sensation as another com bination o f stim uli w ithin that
continuum . The com pon ent stimuli com prising the m cta­
merie stim uli are discrim inable when presented separately.
M ctam crs arc physically different stimuli that create the
same sensation. M etam ers form an equivalence class under
the operation o f resolution but not under the operation o f
discrim ination. For example, the same color can be pro­
duced by many m ixtures o f m onochrom atic lights. W e
can n ot resolve the wavelength com ponents o f a colored
area but we can discrim inate betw een these com ponents
when they are presented one at a tim e o r in different
locations.
M etam ers arc som etim es confused with p ro jcctiv ely
eq u ivalen t stim u li. A frontal square is projectively equiva­
lent to a family o f slanted tapered shapes and, under reduced
conditions, they look the same (Section 2 6 .1 .1 b ). The
equivalence is produced by the geom etry o f visual rays pro­
jectin g o n to a tw o-dim ensional retina. In contrast, meta-
meric stimuli arise because o f the way stimuli arc processed
by the receptors and nervous system. In both cases there is
loss o f inform ation about the distal stimulus.
M etam ers should also be distinguished from stim ulus
eq u ivalen ce in m u lticu e system s. For example, binocular
disparity creates sensations o f depth that resemble those
created by m otion parallax. However, the basic detectors
are very different. They pool their inform ation but the pool­
ing does not involve metamerism.
Inferences from the use o f metameric stim uli are based
on two assumptions. First, once stim uli have been co m ­
bined m etamerically, inform ation about the com ponent
stim uli is lost in that fcature-dctection system. Second, two
stim uli that produce identical sensations generate identical
physiological activity at som e location in the nervous
system. It follows from these assum ptions that the identical
appearance o f tw o metamerieally m atched stimuli can n ot
be disturbed by any change applied equally to the metamer-
ically com bined neural signals. I f two metamerieally
matched stimuli remain matched for all possible changes
applied equally to both , then the m ctam cric process must
be at the initial site o f processing o f that sensory system.
Conversely, if a change applied equally to tw o stimuli
disturbs a meram eric march, a process that detecrs rhe
applied sensory change m ust precede the merameric pro­
cess, or there is a nonlinear feedback betw een later and ear­
lier stages o f processing. Thus, we infer that trichrom acy is
achieved at rhe fron t end o f rhe visual system from the facr
that merameric color m atches continu e to match tor all
states o f adaptation o f the eve (G rassm anns third law). For
a m ore detailed analysis o f this logic see Brindley (1 9 7 0 ).
Also, the shape o f the m eram eric m atching function for
color (the C IE color ch art) provides a basis tor inferences
about the nature o f the cone m echanism s responsible for
trichromacy.
M etamerism arises only in sensory systems consisting o f
detectors with mutually overlapping band-pass tuning func­
tions along a particular stimulus continuum . All m ultichan­
nel sensory systems o f this type produce some degree o f
metamerism. All visual features,other than lu m inance,con­
trast, and flicker, arc processed by m ultichannel systems and
are, at least to som e extent, merameric.
The degree o f metamerism in a sensory feature depends
on the following tw o factors.
1. The num ber o f channels devoted to the feature At one
extrem e, rhe receptor stage o f rhe color sysrem is wholly
m eram eric, since it has only three overlapping channels
over the whole stimulus continuum . The system has no
wavelength resolution it ca n n o t exceed the Nyquist
lim it.
The orientation system is only partially merameric,
because it has m ore than three channels. O rientations
are metamerized only when they fall in a region o f
channel overlap. C ells in the visual cortex have
orientation tuning functions with a half-am plitude,
half-height bandwidth betw een 15° and 30° (S c ction
5 .6 .2 ). Intersecting short lines at slightly different
orientations therefore m etam erize and appear as one-
line at an interm ediate orientation (Parkes er al. 2 0 0 1 ).
Lines that differ sufficiently in orientation appear
distinct.
For rhe same reason, m orion is only partially merameric.
There seems to be general agreem ent chat the direction
tuning functions o f m otion sensitive cells in the visual
cortex have a half-height at halt-am plitudc o t about 30°
(Section 5.6.4a). For a 5 0 % overlap between channels
this would give six channels. Studies o t m otion
metamerism have yielded a sim ilar value
(Section 3 .1.3).
Binocu lar disparity detectors arc also partially
merameric (Section 18.8.2).
A t the other extrem e, the visual local-sign system
contains one m illion channels (one m illion ganglion­
cell receptive fields). Each channel has a tuning tunction
defined as response am plitude as a function o f rhe
location o t a stimulus wichin che recepcive field. This
system is merameric only w ithin each sm all region
where the receptive fields o f ganglion cells overlap.
Two stim uli falling tn an overlap region appear
as one stimulus at che centroid o f the total
lum inance distribution. O th er stim uli are
resolved.
Similarly, the frequency coding system in audition is
merameric only locally w ithin each critical band— a
region along the basilar mem brane over which hair-cell
tuning functions mutually overlap.
2. The number o f processes for detecting the feature
O n ce color signals are metam erized, there are no
subsequent visual processes that can recover the
com ponent signals. Also, once tw o neighboring stimuli
have been metamerized inco one stimulus in an
interm ediate location there arc no processes that can
resolve them . Tw o short lines metamerize o n to one
line at an interm ediate orientacion. Buc the
orientations o f long lines do not metamerize because
the orientacion o f a long line may be detected by the
local-sign system. Similarly, short-duration elements
moving in dilfercnt directions may metamerize in to one
elem ent m oving in an interm ediate direction. But
long-duration moving elem ents do not metamerize
because their d istin ct trajectories are detected by the
local-sign system.
In any system o t detectors with overlapping cuning
functions, any one detector produces an ambiguous
signal because it responds to any stimulus w ithin its
tuning range. The outputs o f several detectors must be
com bined to produce a precise signal. W h en a stimulus
does nor excite a representative sample o f detectors for a
given feature, that feature will be misperceived. For
exam ple, rhe color o f a stimulus confined ro a small
central area is not correctly registered because it tails to
stimulate all three types o fc o n e . This effecr is known as
small-field tritanopia. Similarly, the perceived
orientation o f a sh o rt isolated line fluctuates over a
range o f about 30*, presumably because it fails to
stimulate a balanced set o f orientation detectors
(Andrew s 1967). A similar process may explain the
autokinetic effect, in which a stationary isolated bright
spot appears to move erratically.
M ctam cric systems exhibit several relaced propercies,
which are discussed in subsequent sections o f this chapter.
 4.2.8 SEN SORY O P P O N E N C Y
An opponent, o r bipolar, stim ulus feature has a natural bal­
ance point, or norm . For instance, “v e rtica lly ” is a norm
for orientation, “equidistance” is a norm for relative depth,
and “stationarity” is a norm in a scale o f m ovem ent from
o n e direction to the opposite direction. O ppositional stim ­
ulus features are detected by opponent sensory systems.
Strictly speaking, an opponent sensory system extracts the
difference betw een inputs from tw o oppositely tuned detec­
tors for a bipolar sensory continuum . However, the term
“opponency" is often used to denote any sensory m echa­
nism in which a difference signal is generated, even i f the
stimuli do not form a bipolar sensory continuum .
4 .2 .8 a O p p o n e n c y a t th e L evel o f R c c c p to r s
The sim plest sensory opponent mechanisms occur at the
level o f the sensory end organ. Such end organs are bipolar
receptors that m aintain a resting potential. For example, the
end organs in the sem icircular canals o f the vestibular system
operate as bipolar receptors. Turning the head in one direc­
tion deflects the cupula in the opposite direction and hvper-
polarizes the sensory hair cells. Turning the head in the
opposite direction depolarizes the hair cells. W hen the head
is stationary, the hair cells m aintain a resting potential.
R etinal receptors do not m aintain a resting potential
and are therefore n o t bipolar receptors. There is one excep­
tion to this rule. Lizards have a p arietal eye on top o f the
head. Each receptor contains a green-sensitive opsin that
causes the receptor to depolarize in green light and a blue-
sensitive opsin that causes the cell to hyperpolarize in blue
light (Solcssio and Engbretson 1 993).
4 .2 .8 b O p p o n e n c y a t th e P r e c o rtic a l L evel
Th e vestibular system contains a sccond opponency m echa­
nism at the level ot the vestibular nuclei in the brainstem.
Inputs from the three m atching pairs o f sem icircular canals
on opposite sides o f the head com bine in a push-pull tash-
ion in the vestibular nuclei to signal the direc tion o f head
rotation (see Howard 1 982).
In the trichrom atic color-detection system, inputs from
red cones and green cones are com bined in an antagonistic,
o r seesaw fashion, as are those from blue cones and yellow
(red plus green) detectors. This process occurs in the retina
to produce the opponent center-surround organization o f
the receptive fields o f parvocellular ganglion cells. Since
a change in lum inance affects members o f each opponent
pair equally, color opponency produces signals that vary
with hue, independently ot changes in lum inance. The
lum inance signal is derived by adding rhe inputs from red
cones and green cones.
T h e olivary nucleus in the brainstem contains a type
o f opponency m echanism that detects differences in the
intensity and tim e o f arrival o f sounds at the two ears. This
mechanism codes the direction and distance o f t h e sound
source (Section 3 5 .3 ).
4 .2 .8 c O p p o n e n c y a t th e C o r tic a l L evel
W e will see in Section 5.1.3 that midget bipolar cells in the
retina arc divided into O N -bipolar cells, w hich respond to
light increase, and O FF-bip olar cells, which respond to light
decrease. In spite o f their names, these cells arc not op p o­
nent cells, since each cell responds only to either light
increase or light dccrcase. Their outputs arc com bined in the
visual cortex. It has been claimed, but not confirm ed, that
inputs from ganglion cells converge in push-pull fashion on
double-opponent cells in the visual cortex (G ouras 1991).
Single cells that respond selectively to orientation,
m otion, or binocular disparity occur first in the visual
cortex. Although each o f these stimulus features is opposi­
tional, the detectors are not. For example, an orientation
detector responds maximally to stimulus tilt in only one
direction, and m otion detectors respond to m otion in only
one direction. Similarly, disparity detectors arc not op p o­
nent detectors, since they do n o t maintain a resting dis­
charge (Scctio n 11.4.1). However, there arc good reasons
for concluding that outputs o f detectors tuned to stimuli
on either side o f a norm are com bined in the cortex to pro­
duce a difference signal. A difference signal is advantageous
since it is n o t affected by changes in contrast. A change in
contrast affects both d etectors equally.
In the dom ain o f visual orientation, opponency makes
orientation discrim ination independent o f co n trast over
a wide range o f concrasts (Regan and Beverley 1985).
Independence o f contrast has also been reported for discrim­
ination ot spatial frequency (Regan 1982), speed (M cKee
c ta l. 1986), and temporal frequency (Bow ne 1990).
Judgm ents o f either the orientation, spatial frequency,
or contrast o f a grating presented with different com bina­
tions o f the three attributes were just as precise as when the
grating varied in only the attribute being judged (V in cen t
and Regan 1995). Thus, subjects precisely judged one
sensory feature when the stim ulus varied with respect to
features n o t being judged. Since individual cortical cells
respond to changes in many features, the ability to isolate
one feature must depend on opponent processes between
sets o f differently tuned cells. The ratio o f responses o f two
detectors can be used for the sam e purpose.
D etectio n o f binocular disparity is largely independent
o f lum inance and contrast (S cctio n 18.5.1), which suggests
that opponency between crossed and uncrossed disparities
is registered at a higher level in the nervous system. In
C hapter 2 0 wc will see that the extraction o f other types
o f difference signals w ithin rhe disparity system renders
stereoscopic vision immune to the effects o f misconver-
gence, image m isalignm ent, and unequal m agnification o f
the images in the two eyes.
 Binocular rivalry is a type o f sensory opponcncy operat­
ing betw een distinct stim uli in the two eyes. This topic is
discussed in C hapter 12.
Л related mechanism for rendering the response o f fea­
ture dc tec tors invariant to changes in contrast is to scale
(divide) the response o f each cell by the pooled response o f
neighboring cells. This type o f autom atic gain control is
called response n o rm alizatio n (H eegcr 1992a; Carandini
and H eeger 1 9 9 4 ). The term “norm alization” is also used to
describe processes in opponent systems, as discussed in the
next section.
4.2.9 C O N T R A ST EFFECTS AND
NORMALIZATION
4 .2 .9 a C o n tr a s t and A ssim ilation
In many instances the way a stimulus appears is affected by
adjacent stim uli presented at the same time. For example,
a grey patch appears darker when next to a lighter patch
than when next to a brighter patch. In in d u ccd visual
m o tio n a stationary spot appears to move in the opposite
direction to a moving background. Also, when parallel lines
are slightly further apart than about 4 arcm in they appear
to repel each other (K oh ler and W allach 1 9 4 4 ; Badcock
and W estheim er 1 9 8 5 ). These are sim ultaneous co n tra st,
o r repu lsion , effects.
C ontrast effects also occur in the spatial-frequency
dom ain (see Howard 1 9 8 2 ). In the dom ain o f orientation,
simultaneous contrast reveals itself as geom etrical illusions
such as the H ering illusion. C o n trast effects in the percep­
tion o f depth are discussed in Section 2 1 .4 and those in
m otion-in-depth in Section 3 1.7.
Under other conditions, adjacent stim uli may attract
each other. For example, gray bars in a pattern may appear
brighter when next to w hite bars than when next to black
bars (S ectio n 2 2 .4 .1 ). Also, the discance betw een two paral­
lel lines is underestimated when they are separated by a gap
slightly greater than is needed to resolve them (Bad cock
and W csdicimcr 1985). These are assim ilation, or attraction,
effects.
It is generally believed that simple contrast effects occur
because o f spatial overlap betw een inh ibitory regions o f the
tuning functions o f detectors for a particular visual feature.
Consequently, neighboring d etectors engage in mutual
inhibition. C ontrast effects enhance signals associated with
changes in stim ulation, relative to signals associated with
regions o f steady stim ulation. Assim ilation could be due
to spatial sum m ation o f excitatory signals from adjacent
feature detectors o f the sensory continuum . In general, co n ­
trast effects operate over a greater spatial range than do
assimilation effects. Presumably,
Ф
this is because the inhibi-
tory regions o f the tuning functions o f feature detectors
extend beyond the excitatory regions. Also, inhibitory lat­
eral con nection s between cortical cells extend further than
excitatory connections.
Physiological correlates o f sim ultaneous and successive
contrast effects have been revealed in the responses o f single-
cells in the visual cortex (see Saul and Cynader 1989).
Psychophysical measurement o f contrast and assimila­
tion provides inform ation about the properties o f feature-
d etection systems, such as the num ber and bandwidth o f
channels coding a given feature.
Successive contrast effects can o ccu r betw een stimuli
presented successively. For example, a line appears to be dis­
placed away from the location o f a previously seen line in
an adjacent location. Effects o f this kind were first described
by G ibson (1 9 3 3 ). K ohler and W allach (1 9 4 4 ) gave them
the name figural aftereffects (see Sections 2 1 .1 .2 and
2 1 .6 .1 b ).
4 .2 .9 b N o rm a liz a tio n
It is characteristic o f oppositional stimulus dim ensions that
inspection o f a stimulus displaced from the norm causes
th at stimulus to appear more like the norm and induces a
coherent apparent shift o f stim uli over the whole stimulus
dim ension. Jam es J. G ibson used the term “norm alization”
to refer to the tendency for stimuli in an oppositional scale
to regress to chc norm . Thus, when one looks at a tilted line,
it gradually appears more vertical. This is tilt n o rm aliza­
tio n . After tilt norm alization has been induced, a vertical
line looks tilted in the opposite direction with respect to
the induction line. This is the tilt aftereffect. The aftereffect
can be as large as 5° when che test stimulus is presenced for
100 ms (W olfe 1984). W ith continued observation, curved
lines com e to look straighter, and o b jects at different dis­
tances appear more equidistant. In m otion norm alization, a
m oving display appears to move more slowly. After m otion
norm alization has been induced, a stationary stimulus
appears to move in the opposite direction to chac o f the
induction stimulus. This is the m o tio n aftereffect.
O ver tim e, in natural scenes, stim uli in an oppositional
dim ension are symmetrically distributed about the norm,
w hich is che mean value. A persiscenc asymmetry o f stim u­
lation with respect to a norm signifies that there is a system­
atic distortion o f visual processing. Rescaling responses over
the sensory continuum adjusts the system to the distur­
bance. For example, on average, the natural world contains
as many lines slanting or curving one way as lines slanting or
curving another way. Even if a natural o b ject in the world is
slanted, the slant it creates in the retinal image balances out
as che observer moves abouc and views ic from different
directions. A persistent slant or curvature over the whole
visual field signifies that the visual system is wrongly cali­
brated and in need o f correction. A fter a w hile, systems
thac detect orientation, curvature, or m otion automatically
adjust themselves. The prevailing mean value o f stimuli
on an oppositional scale is subtracted from the value o f
ocher stimuli chac may be presenc. For example, a vercical
line appears tilted in the opposite direction to a tilted
surrounding frame. Thus, norm alization can be regarded as
an autom atic rccalibration, or error-correcting mechanism
(Andrew s 1964).
The term "norm alization” is- also used to refer to the
neural process o f dividing the response o f a feature-detector
by the pooled response o l neighboring cells so as to render
the response o f the feature detector invariant to changes
in stim ulus contrast. This process implies division, rather
than subtraction.
A plausible physiological explanation for Gibsonian
norm alization can be provided in terms o f adaptation
w ithin opponent mechanism s. O n e must assume that the
tuning functions ot detectors tuned to opposite sides ot the
norm intersect at the position o f the norm and that a stim u­
lus appears at the norm when the distribution o t activity in
the set o f detectors is symmetrical. For instance, after a line
just o tf the vertical has been inspected tor some tim e, it
should appear displaced toward the vertical because the
detector on that side o t vertical will have becom e adapted,
o r fatigued, relative to che one on the other side o f vertical.
Inspection o f a vertical line has no effect because it excites
the two detectors equally. Similarly, the opponent colors
red and green norm alize coward gray, whereas inspection o f
an equal mixture o f red and green (gray) does n o t produce
norm alization.
The tuning functions o f channels in oppositional sen­
sory systems are symmetrically disposed about the norm . If
the norm occurs ac the peak o f che tuning tunction o t the
cencral channel, d etection would be optim al for a stimulus
at the norm but sensitivity to change would be greatest on
either side o f rhe norm . If the norm occurs where the tuning
functions o f tw o channels intersect, sensitivity to change
would be greatest ac che norm , buc detection would be
optim al on either side o f the norm (see Figure 3.6).
N orm alization is due ro selective adaptation o f ch an­
nels, but its effect on a particular stimulus depends on the
num ber and tuning widths o f channels along a sensory
continuum .
4 .2 .9 c C o n t in g e n t A fte re ffe cts
Sensory adaptation can elevate the threshold for a few
minutes. There are also adaptation processes chac can last
davs
i o r even weeks. The besc known o f chese are che co n cin -
gene aftereffects. For example, a period o f exposure со
red vercical lines alternating with green horizontal lines
produces a long-lasting aftereffect in which vertical lines
look slightly green and horizontal lines look slightly red
(M cC o llou g h 1 9 6 5 ). S ee Vul et al. (2 0 0 8 ) for a discussion
o f transient and long-lasting aftereffects.
Long-lasting adaptation effects have also been reported
after exposure to single visual features such as spiral m otion
(Favreau 1979) and visual tile (W olfe and O ’C onnell
1986). In these cases, long-lasting effects occur when test
trials do not im mediately follow the induction stimulus.
However, these seemingly simple effects may be specific to
incidental features o f the induction stimulus, such as its size
or the surroundings. I f so, they may be best described as
contingent aftereffects. C o n tin g en t aftereffects last a long
tim e because the normal visual environm ent does not co n ­
tain persistent com binations o f the particular features that
produce contingent aftereffects.
There is evidence that cells in the visual cortex o f
monkeys adapt specifically to stimulus contingencies.
However, this was shown only for linked stim uli w ithin the
single visual dim ension ot orientation (C arand ini et al.
1997). The m ost significant contingencies are probably
those between distinct stimulus dimensions.
Concingenc aftereffects can be understood as m echa­
nisms to correct tor cross talk between feature-detectors.
The orientation-color contingent effect may be responsible
tor the tact that we are n o t aware o t chrom atic aberration in
the optical syscem o f che eye, or in speccacle lenses chac we
use habitually (Section 9 .6 .5 c). The visual system treats co n ­
stant chrom atic aberration as arising from som e feature o f
the visual system
Ш
rather than from the environm ent. The
relevance o f contingent aftereffects to binocular vision is
reviewed in S ection 13.3.5.
Som e stimulus contingencies arise from recurring struc­
tures and events in the visual environm ent (Section 4.5 .5 c).
For example, an approaching o b ject produces loom ing o f
che retinal image and changes in disparity (Section 3 1 .2 .2 ).
Buc che coupling o f loom ing and disparicy is noc fixed like
che coupling of color and oriencation in chrom atic aberra­
tion. The visual system develops specialized m ulticue detec­
tors for rapid detection o f rhe variable coupling between
such recurring stimulus complexes.
4 .3 T E M P O R A L C O D IN G
4. 3 . 1 TEMPORAL CHARACTERISTICS
OF N E U R A L SPIKES
4 .3 .1 a N e u ro m e tr ic F u n c tio n s
The probability o f response o f a sensory neuron plotted
against stimulus strength forms o f a cum ulative probability
curve, or n cu ro m ctric fu n ctio n . A similar psychometric
function is obtained when the probability o f seeing is p lo t­
ted against signal screngch in a psychophysical cxpcrimenc
(Section 3.1 .1 b ).
Fitzhugh (1 9 5 7 ) obtained the first neurom etric fu n c­
cion from signal-dececcion analysis o f responses o f ganglion
cells in the cat to flashes o f light. Extensions o f this approach
are described in Section 5.1.5.
This linkage betw een neural responses and psychophys­
ical responses has been extended to responses o f cortical
cells. For exam ple, the sensitivity o f cortical cells tuned to
binocular disparity has been compared with psychophysically
determ ined depth thresholds (Section 1 1 .4 .1 ). This type
o l investigation forms the basis o l the growing field ol
co g n itiv e n eu ro scien ce (Parker and Newsome 1998).
The threshold o f the m ost sensitive single cells in the
visual cortex corresponds to the behaviorally determ ined
contrast threshold (Barlow et al. 1987; DcValois and
DcValois 1 9 8 8 ). The m ost sensitive cells in the visual cortex
o f anesthetized cats signal differences in spatial frequency
o r orientation that are only slightly larger than the differ­
ence thresholds determ ined psychophysically (Bradley e t al.
1987). Similarly, the orientation discrim ination o f monkeys
determ ined psychophysically is sim ilar to the sensitivity o f
cortical cells to changing orientation obtained in the alert
monkey (Vogels and O rban 1 990). In monkeys, the thresh­
old o f cells in M T and M S T to the degree o f coherent
m otion in a display o f random dots is sim ilar to the
psychophysically determ ined threshold (Section 5.8.4b ).
These facts do n o t mean th at single cells unambiguously
code variations in one stimulus feature.
4 .3 .1 b R esponse Variability
The frequency o f response of a neuron anywhere in the
visual system is not precisely the same when a given stim u­
lus is repeated. Any such variance in response is called
in trin sic noise. The ability o f any detector to d etect a signal
depends on the ratio o f signal strength to variance due to
noise— the sig n a l-to -n o ise ratio. There are two basic types
o f intrinsic noise. A dditive n oise is a constant level o f noise
added to signals o f any strength. For additive noise, the sig-
nal-to-noise ratio declines as signal strength is reduced and
may exceed signal strength in the neighborhood o f the
stimulus threshold. M u ltip licativ e n oise is proportional to
signal strength, so that the signal-to-noise ratio remains
constant as signal strength is varied. There has been some
debate about w hether m ultiplicative noise is an intrinsic
property o fth e way single neurons respond or w hether it is
due to properties o f neural netw orks.
The variability o ft h e spike count o f a neuron is charac­
terized by the ratio o f the variance to the mean (F a n o ratio).
For a random Poisson process the expected ratio is 1. Several
investigators have reported that the firing ot neurons in
V I is highly variable, and conform s to a Poisson function
(see Softky and K och 1 993). However, Kara et al. (2 0 0 0 )
found that response variability o f cells in the visual cortex o f
the anesthetized cat to be m uch lower than previously
reported. Nevertheless, they found that variability o f firing
increased from retina to L G N to visual cortex. G ur and
Snoddcrly (2 0 0 6 ) recorded trom retina, L G N , and V I ot
alert monkeys in response to optim ally oriented bright bars.
For suprathrcshold stimuli, response variability was no
higher in the cortex than in the retina, when rhe effects o f
eve m ovem ents were taken into account. The mean Fano
ratio was only 0 .3 , both in cortical layer 4 and in other
cortical layers.
The lower the response variability, the smaller will be
the num ber o f cells required to reliably indicate the pres­
ence o f a given stimulus. W ith highly variable responses,
optim al decoding would require deriving a weighted sum ot
neuronal responses (see Jazayeri and M ovshon 2 0 0 6 ).
4 .3 .1 c A dap tation and D iscrim in ab ility
The sensitivity ot retinal receptors is an inverse function
o f retinal illum ination. C ells in the visual cortex exhibit
contrast adaptation, in which response frequency is adjusted
to the prevailing level o f contrast. This prevents response
saturation to high-contrast stimuli and increases dynamic
range.
C om plex cells in the visual cortex o f the monkey
also show pattern-specific adaptation. A b rief presentation
ot a grating in a specific orientation causes a temporary
shift in preferred orientation o f cells in the same neighbor­
hood away / trom the orientation o fth e induction stimulus
(M uller e t al. 1999; Felsen et al. 2 0 0 2 ). Loss o f responsiv-
ity to a persisting stimulus conserves m etabolic energy
and increases discrim inability for orientations in the neigh­
borhood o f the adapted orientation. Stimulus-specific
adaptation improves discrim inability because it reduces
the correlation between signals arising from stimuli with
sim ilar orientations.
4 .3 .2 Т Е M P О RA L С О D I N G 1N
S IN G L E N E U R O N S
Visual stim ulation produces receptor potentials in retinal
receptors and a m odulated release o f glutamate neuro­
transm itter m olecules from bipolar cells. A ganglion cell
transforms such signals trom the set o f bipolar cells in its
receptive field into bursts o f one ro six action potentials
(spikes) separated by quiescent periods. This pooling pro­
cess reduces the variability o f neural responses to a given
stimulus. D iscrete bursts o f firing o f ganglion cells o f rab­
bits, cats, and primates recur with high precision when the
same stimulus is repeated (Berry et al. 1 9 9 7 ; Uzzcll and
C hichilnisky 2 0 0 4 ; Freed 2 0 0 5 ).
C o rtical neurons show stereotyped differences in the
waveforms and repetitive firing properties o f their action
potentials. Neurons in the mammalian neocortex can be
classified into four types according to their temporal dynam­
ics. These are: "regular spiking,” "tast spiking,” "bursting,”
and “intrinsic-bursting” neurons (Section 5.5.1c).
B u rstin g cells in the visual cortex show characteristic
bursts o f stimulus-evoked activity containing up to about
six spikes w ithin a 25-m s period. Som e pyramidal cells in
layers 2 to 6 ot the visual cortex of the cat respond with svn-
chronized bursts with a burst frequency o f betw een 3 0 and
5 0 H z in response to depolarizing current. They have been
called ch a tterin g cells (Gray and M cC o rm ick 1996;
C ardin et al. 2 0 0 5 ). Bursts are more reliably related to the
oriencacion and spatial frequency o f che stimulus chan arc
single spikes (see Lisman 1 9 9 7 ). Single spikes can arise
spontaneously, and therefore represenc noise. M ultiple
spikes rarely occur spontaneously. Also, m ultiple bursts are
more likely со trigger a postsynaptic response than arc single
spikes, especially when the bursts converge on a given syn­
apse. C hattering pyramidal cells send collaterals into other
cortical layers and ocher cortical regions and may play a key
role in generating synchronous co rtical activity, discussed
in S ection 4 .3 .4 (see Sam onds and Bonds 2 0 0 5 ).
It is generally assumed that single neurons convey infor­
mation in terms o f spike frequency and chac che probabilicy
o f an action potential per unit tim e is proportional to firing
race. This is known as che Poisson m odel. W ith refractory
periods betw een 5 0 and 100 m s, the maxim um rate of trans­
mission is betw een 10 and 2 0 spikes/s. The bandwidch o f a
spikc-trequcncy system is therefore very lim ited.
The Poisson model docs not account for why ganglion
cells tend to respond in discrete bursts o f spikes rather than
at a continuously varying race. Theoretically, a discrete burst
o t spikes can convey up to 3.6 bits ot inform ation per spike.
This is much more than is conveyed by spike frequency
alone. Uzzell and C'hichilnisky (2 0 0 4 ) found that spike-time
variability in primate ganglion cells decreases wich increasing
stimulus strength, probably because o f lim itations imposed
by the refractory period.
The inform ation that can be coded by frequency o f dis­
charge o f a single neuron is limited by the highest frequency,
which is typically less chan 100 Hz. A lso, it takes tim e to
obtain a reliable estim ate o f discharge frequency. These lim ­
itations apply where the frequency o f neural spikes codes
stimulus intensity. They could also apply in a labeled-line
coding system in which the value o f a stimulus feature is
coded in terms o f the relative frequencies ot responses across
a set o f distinctly tuned channels.
Precise detection ot spike frequency requires detection
o f interspike intervals. It is not clear how a ccll codes such
intervals or how a postsynaptic cell is influenced by the
spike frequencies o f several im pinging neurons. A less pre­
cise but more plausible coding ot spike frequency could be
the simple spike count in the interval over which a postsyn-
aptic cell integrates spikes. The higher the count the greater
the probability that the postsynaptic ccll would fire. For a
single neuron, the num ber o f spikes w ithin an integration
tim e o f say 5 0 ms would be very few. However, it is possible
that recurrent collateral con nection s in a neural network
could extend the integration tim e to 5 0 0 ms (see R olls e ta l.
2 0 0 6 ).
O th er aspects o f temporal coding have been reviewed
by D inse et al. ( 1 9 9 0 a ).
4 .3 .3 D E T E С T I О N О F T 1M E IN T E R V A L S
W h en coding involves com paring the tim ing o f responses
o f detectors, tem poral phase rather frequency is used.
Much higher tem poral resolution can be achieved by phase
coding than by frequency coding. In the first place, phase
coding may be based on ju st cwo spikes. Secondly,
phase coding is not lim ited by the upper frequency o f
neuronal firing.
C om pu ter sim ulations o f cortical pyramidal cells have
revealed that they could, in theory, d etect coincidence
betw een single spikes in the subm illisecond range (Sofiky
1994).
4 .3 .3 a T em p o ra l C o d in g by P aired S e n se O rg a n s
A given stim ulus may arrive at one sense organ betore it
arrives at another sense organ. For example, the relative
tim es ot arrival o f sounds at the tw o ears depends on the
direction o f the sound source (Section 3 5 .3 ). Auditory
afferents converging in the superior olive form a delay line
in which the tim ing o f inputs from the tw o ears is co m ­
pared. This system requires submillisecond tim in g o f binau­
ral coincidence. This is achieved by regulating the distances
betw een axon nodes (see Sabatini and Regehr 1999) and by
a gradient o f potassium channels (M athew s et al. 2 0 1 0 ).
Echolocation is a special case. For example, dolphins use
the interval betw een the emission o f a click and che arrival
o t the reflected sound to estimate the distance o l an o b ject
(Section 3 5 .8 .3 ).
Electric fish d etect the phase o f electric signals pro­
duced by their own electric organs relative to the phase o f
signals produced by other fish with a resolution o f 1 0 c,s
(Section 3 6 .1 .2 ). This remarkable perform ance has been
modeled in terms o f the Hodgkin-H uxley equations o f spike
generation in single neurons (Takagi and Kawasaki 2 0 0 3 ).
There is some evidence that synchrony betw een inputs from
the two eyes is involved in stereopsis (Section 23-3).
A m oving o b ject stimulates neighboring receptors
sequentially. For example, a m oving spot o f light stimulates
retinal recepcors sequentially, which d iggers a response in a
m otion detector. For a review o t m echanism s o f m otion
detection see Sm ith and Snowden (1 9 9 4 ) and Section 5.6.4.
4 .3 .3 b S e n so ry S c a n n in g
A sense organ may scan a stationary o b ject, cither interm it­
tently or continuously. In vision, scanning consists o f inter­
m itten t saccadic eye movements, which occur at a velocity
o f about 6 0 0 7 s . The eyes move sm oothly only when pursu­
ing a moving o b ject. Visual inputs are somewhat suppressed
and images are severely blurred during saccades. The eyes
are reasonably stationary during intcrsaccadic intervals,
which are typically about 2 0 0 ms. W h ile the general struc­
ture o f a visual scene can be registered during one fixation,
several fixations are required for the detection o f che detailed
structure o f large o b jects or scenes. A person first registers
the general layout o f a scene and then concentrates fixations
on regions o f greatest interest. The detailed structure o f a
scene can be registered when che image is moved at random
into different positions, as long as the image dwells in each
position for about 2 0 0 ms. In o ther words, inform ation can
be presented to the fovea in any order as long as the overall
structure o f the scene remains constant. Furtherm ore, in
vision, changes to the general structure o f the environm ent
can be detected w ithout making an eye m ovem ent, as long
as the change does n o t occur in an unattended locarion or
during asaccadc. The order o l fixations is im portanc only in
the special case o f reading, where m eaning is conveyed by
the order ot a long string o f letters and words, although not
by rhe exact form o f the letters (M cC o n k ie and Z ola 1979).
Also, when scanning a norm al stationary scene it is n o t nec­
essary to register the m ovem ents o f the eyes. Registration o f
eye m ovem ents is required only tor estimating the m otion
o f an isolated o b ject or o f the whole scene. People with
tunnel vision must register eye m ovements to build up a
coherent impression o f a scene.
W h en we recognize an o b ject by touch, the fingers typi­
cally scan continuously over the o b ject. It is not necessary
to hold the hand still. In fact, a stationary o b ject is difficult
to recognize because the skin sense organs adapt rapidly.
Unlike vision, the tactile senses cannot detect the general
structure o f the environm ent w ithout exploratory groping
movements. In an unfam iliar environm ent, impressions
gained from successive tactile encounters with o b jects must
be integrated with inform ation about the direction and
extent o f m ovem ents o f the hand. W h en the hand moves
over a stationary o b ject, inform ation about rhe direction
and extent o f m otion ot the hand is provided by the tem po­
ral sequence o f inform ation from the skin senses. W hen rhe
hand moves from one o b ject to another, intorm ation about
the m ovem ent o f the hand is provided by kinesthesis and/
o r ctfcrcnce. In either case, an impression o f the size and
shape o f an o b ject or about the layout o f o b jects in the envi­
ronm ent depends on intorm ation about the m otion ot the
hand. In touch, the order in which inform ation is picked up
by skin receptors in relation to movements o f the hand or
fingers is the crucial tactor.
4 .3 .3 c D ifferential L aten cies o f D e te c to r s
In a m ultichannel system, the different detectors are tuned
to different values ot a particular feature. For example, some
cortical cells show a peak frequency in response to stimuli
in one orientation while other cells respond m ost vigor­
ously to other orientations. The orientation o t a given stim ­
ulus is said to be coded in term s o f the relative frequencies
o f the responses o f all the detectors that are excited by the
stimulus. In this system, rhe frequency o f response o f each
detector must be registered.
Thorpe et al. (2 0 0 1 ) argued that this process is too slow
to account for the speed with which com plex stimuli are
recognized. Ihey proposed that rhe latency o f each detector
o f a m ultichannel svstem varies as a tunction o f the value o f
the stim ulus feature. For different detectors, the minimum
latency would occur at different values o f the feature. Thus,
instead o f frequency tuning, the orientation detectors
would show laten cy tu n ing, in which the latencies rather
then the frequencies o f the responses o f the excited d etec­
tors are com pared. The crucial stimulus becom es the order
in which the detectors respond. This is a rapid process
because it requires the registration o f only one spike in each
detector.
The latencies o f the first spikes can be used only on the
initial presentation ot a stimulus. It would help if a stimulus
were sampled interm ittently. M icrosaccadcs may serve this
purpose. Perhaps the visual system uses latency tuning for
rapid initial registration o f features and frequency tuning
tor subsequent processing.
Although there is no physiological evidence o f latency
tuning in the visual system there is evidence o t such tuning
in the somatosensory system. Johansson and Birznieks
(2 0 0 4 ) recorded responses o t afferents trom skin receptors
in the human index finger. A small flat or spherical object
was moved over the finger in different directions with d if­
ferent applied pressures. For all afferents, response fre­
quency and the latency o f the first spike varied as a function
o f the direction o f movement. For slow-acting afferents
arising from Ruffini corpuscles, frequency and latency
varied together as m otion direction changed. For other
afferents, the two response features varied independently
and presumably conveyed different types o f inform ation.
D ifferent afferents showed m inim um latency for different
directions ot m otion. The direction o f stimulus m otion
could therefore be derived from the pooled response laten­
cies o f a set ot afferents that a given stimulus excites. The
response latency o f each afferent was reasonably constant
when the same stimulus was repeated.
W h ile latency tuning may be used in the initial coding
o f sensory features, it is less plausible at higher levels o f
visual processing, where differential condu ction tim es are
likely to influence the tim e o f arrival ot spikes.
Rolls et al. (2 0 0 6 ) recorded sim ultaneous responses o f
groups o f cells in the monkey interior tem poral cortex to
each o f a set o f com plex stimuli. A Bayesian probability pro­
cedure was used to estim ate the inform ation contained in
the tim es o f arrival o f the initial spikes in neighboring neu­
rons, in the spike co u n t over the initial 2 0 ms, and in che
relacive order o f spikes. M ore informacion was contained in
the spike co u n t than in the initial spikes. The order o f arrival
o f spikes contained no effective inform ation.
4 .3 .4 TEM PO RA L SY N C H R O N Y OF
N E U R A L A C T IV IT Y
4 .3 .4 a S o u rc e s o f S y
j
n c h ro n iz e d A c tiv ityv
Synchrony o f firing o f subcortical or cortical neurons to a
given stimulus has been studied by recording trom a pair o f
neurons, and deriving a time-averaged measure o f the
tem poral correlation betw een spiking events. It is possible
to measure synchrony o f firing in a large num ber o f cells
in great detail, and to distinguish betw een synchronous
firing arising from direct stim ulation, that due to lateral
interactions, and that due to feedback from higher centers
(G erstcin and A crtscn 1 9 8 5 ; A crtsen e t al. 1 9 8 9 ; Vaadia
e t al. 1 9 9 5 ; Sm ith and Kohn 2 0 0 8 ).
R etinal ganglion cells and L G N cells respond with pre­
cise spike tim ing to tem porally fluctuating visual stim uli. In
the cat, the precision o f tim ing is the same lor cells o f a given
type ( X or Y ). Tem poral precision increases as stimulus
contrast is increased (Reinagel and Reid 2 0 0 2 ). Cells in the
recipient layers o f t h e visual cortex also respond with pre­
cise spike tim ing, but the precision o l tim ing decreases in
higher visual centers. Thus inform ation conveyed by spike
tim ing could be conveyed to the visual cortex (see Ticsinga
e t al. 2 0 0 8 ).
C ells in the visual cortex exh ibit spontaneous synchro­
nized oscillations and weaker stimulus-driven synchronous
oscillations. These could originate in the retina or lateral
geniculate nucleus (Ariel et al. 19 83; G hose and Freeman
1 9 9 2 ). M ultielectrode recordings in the L G N revealed
synchronized oscillations o f 6 0 to 114 Hz evoked by
large spatially continuous stationary or moving stimuli
(Neuenschwander and Singer 1 9 9 6 ). The oscillations origi­
nated in the retina, but it was argued that they alone could
not account for oscillations at the cortical level. Projections
from subcortical centers to cholinergic and G A BA ergic
cortical synapses m odulate the frequency, am plitude, and
phase o f cortical oscillations (Rodriguez e t al. 2 0 0 4 ).
A second source o f stimulus-driven synchronous
* co rd -
cal activity could be the subthreshold oscillation o f rhe
m em brane potentials o f many cortical pyramidal cells
in layer 5 o f rhe visual cortex and other cortical areas
(G utfrcund et al. 1 9 9 5 ; Gray and M cC o rm ick 1 9 9 6 ). These
oscillations would potentiate the responses o f cells when
they are phase locked with the frequency ot incom ing stim ­
uli. O n e type o f subthreshold oscillation is mediated by a
regenerative voltage-gated m odulation o f calcium conduc­
tance across the cell m em brane. A second type is mediated
by m odulation o f sodium conductance. Both types o f oscil­
lation can trigger spikes if the m em brane is sufficiently
depolarized.
Third, stimulus-driven or spontaneous synchronous
cortical activity could be generated by lateral connections
betw een cells, by tim e delays in recurrent inh ibitory loops
in the cortical netw ork (Freem an 1 9 7 5 ), or by feedback
trom higher centers. There is evidence chat precise temporal
synchrony o f cells in V I extends over about 3 mm and arises
trom lateral connections, while slow synchronous m odula­
tions extend at least 10 mm and involve feedback from
cxtrastriate cortex (Sm ith and Kohn 2 0 0 8 ).
‘Ih crc is evidence that oscillatory activity originates in
inhibitory interneurons in cortical layer 4 with collaterals
SEN SO RY C O D IN G
ram ifying in layers 3 and 4 (I.linas et al. 1991). In the
absence o l stim ulation, these oscillations have an amplitude
o f 5 mv and arc in the 5 to 2 0 Hz range. C om puter m odel­
ing indicates that during stim ulation, and with appropriate
synaptic coupling, much higher frequencies could be gener­
ated (Silva et al. 1 9 9 1 ). D ifferent types o f inhibitory
interneuron respond preferentially to different input fre­
quencies (Pike et al. 2 0 0 0 ). Thus, an oscillatory input may
be decom posed into distinct frequency com ponents pro­
cessed bv d istinct neural networks. M ost interneuronal
connections are local. However, it requires only a few long-
range interneurons to trigger synchrony betw een distant
locations (Buzsaki e t al. 2 0 0 4 ).
The use o f synchrony in the responses o f paired sense
organs was discussed in the previous section. It has been
proposed that synchrony o f firing o f subcortical or cortical
cells could also provide sensory inform ation, improve sensi­
tivity, aid stimulus binding, serve as an attention m echa­
nism, and provide a basis tor learning. Let us now consider
these possible functions o f synchronous firing.
4 .3 .4 b S y n c h ro n o u s F irin g an d S tim u lu s T u n in g
Visual stim ulation causes groups o f adjacent cells in the
visual cortex ot both anesthetized and alert cats to discharge
in synchrony at frequencies o f between 3 0 and 8 0 Hz (Gray
and Di Prisco 1997). This so-called gam m a frequency is
outside the frequency range o t spontaneous background
activity responsible for rhe alpha rhythm or the 4 - to 7-H z
tlieta waves that occur during sleep (G ray and Singer 1989;
M unk et al. 1 9 9 6 ). C o rtical cells fire in high-frequency
bursts containing two to tour spikes at intervals o f 15 to
3 0 ms, w hich is approximately one period o f the gamma
cycle.
A visual stimulus evokes synchronous responses in cells
ot the prim ary visual cortex separated by up to 7 mm. Such
cclls have nonoverlapping receptive fields. The responses o f
cells with similar tuning to orientation, m otion, or spatial
frequency are m ore closely synchronized than the responses
o f cells that differ in tuning (B raiten bcrg 1985; Konig
et al. 1995). This correlated activity is mediated by
lateral connections in the visual cortex (Section 5.5.6).
Synchronized discharges o f nearby pairs o f cells in the cat
visual cortex are stimulus dependent and not a simple co n ­
sequence o f t h e responses o f the separate cells. Although
the optim al tuning o t cell pairs to spatial and temporal
frequency and velocity was found to be sim ilar to that o f
the com ponent cells, the receptive fields o f cell pairs were
narrower and their responses were briefer (G hose et al.
1994a). This suggests that synchronized discharges o f
neighboring cells achieve a higher spatial and tem poral res­
olution than is achieved by single cells. The precision o f
response synchrony o f neighboring cells in the monkey
visual cortex is reduced as stimulus contrast is reduced
(K ohn and Sm ith 2 0 0 5 ).
• N 9
 Synchrony o f firing o f spatially aligned ganglion cells
could facilitate the response o f cortical cells tuned to
stimulus orientation (A lonso c t al. 1996; M eister 1996).
Correlated activity betw een cells with different tuning
characteristics could help to resolve the am biguity in the
response of single cells. For example, cells that respond both
to dark and light bars may fire in synchrony only in the
presence o f a dark bar (C h ose c t al. 1994a).
Dan et al. (1 9 9 8 ) showed theoretically and experi­
mentally that more inform ation can be extracted from а
pair of neurons that tend to fire in synchrony than from the
firing rates o f a sim ilar uncorrelated pair o f neurons.
Synchronous inputs are more likely to drive cortical cells
through Hebbian synapses that act as coincidence detectors
(Section 6 .5 .1 ).
O n the other hand, C ardoso de O liveira c t al. (1 9 9 7 )
found that responses o f cells in M T and M S T becam e syn­
chronized ju st before an expected stimulus was presented.
Firing becam e desynchronized as a function o f stimulus
contrast at the onset o f a stimulus moving at up to 2 9 7 s
with respect to a stationary background. They concluded
that m otion direction is coded by differential rates o f firing
rather chan by synchronization alone. Desynchronization
o f firing in the region o f an attended moving stimulus,
whatever its direction, relative to synchrony in the back­
ground could be used со segregate che scimulus from ics
background.
Tem poral synchrony o f the pattern of neural activity
evoked by a given stimulus, coupled with desynchroniza­
tion betw een one pattern o f activity and others, could allow
the same network to code discinct stimuli in rapid succes­
sion and distinguish betw een several temporally or spatially
overlapping scimuli (M iln er 1 9 7 4 ; von der M alsburg and
Schneider 1 9 8 6 ; Singer and Cray 1 9 9 5 ). W allis and Rolls
(1 9 9 7 ) have shown chac a hierarchically organized syscem
o f feature extracting processes o f this type can build repre­
sentations o f objects that are independent o f position, size,
and aspect.
4 .3 .4 c Syn ch ron ou s Firin g and Stim u lus B in d in g
Singer and G ray (1 9 9 5 ) proposed that spatially separated
neurons in che visual system fire in synchrony at gamma fre­
quencies ( 3 0 - 8 0 H z) when stim ulated by a single o b ject
o r by a set o f stimuli chac are pcrcepcually grouped inco a
single o b ject. This may be called the b in d in g -by-sy n ch ron y
hypothesis. Synchronized firingcould enhance the response
o f a pool o f cells chac respond со che same scimulus objccc.
Such activity could bind responses coconnecccd or grouped
scimulus elem ents spanning many receptive fields. Ic could
chus be pare o f a m echanism for figure-ground segregation
and figural grouping. The following evidence supports che
binding-by-synchrony hypochesis.
Tw o parallel bars scim ulacingcorcical cclls wich discinct
receptive fields evoked widespread synchronous activity
when the bars moved in aco m m on direction (se e G ra y c ta l.
1 9 9 1 ). Pairs o f cells with different preferences for m otion
direction in M T o f the alert m onkey responded in syn­
chrony when stimulated by a single o b ject m oving at up to
6 .7 7 s , but not when stim ulated by d istin ct moving objects
(K reiter and Singer 1996).
A set o f cortical cells with overlapping receptive fields in
the cat visual cortex responded in synchrony when stim u­
lated by a single bar. However, when stimulated by two d if­
ferently oriented superimposed bars, the cells segregated
into assemblies according to orientation preference. The
cells in each assembly were synchronized but there was no
correlated firing betw een the assemblies (Engel et al. 1991).
O n e long bar induced scronger synchrony chan cwo smaller
collinear bars in che same location (Ncuenschwander and
Singer 1996).
A 4 0 -H z com ponent o f the human visual evoked p o ten ­
tial (V F.P) was stronger in response to a coherent figure
than to a spatially noncoherent figure (Tallon-Baudry et al.
1 9 9 6 ). Rodriguez et al. (1 9 9 9 ) presented subjects with a
pattern that could be perceived as meaningless shapes
or as a face. Synchronized V E Ps at the gamma frequency
occurred at widely separated regions o f che human scalp
when the person reported seeing a face. The physical stim u­
lus remained the same, only the percept changed. The
responses becam e desynchronized as the person made a
m otor response.
C ells in widely differenc corcical areas and in different
hemispheres responded in synchrony with near zero phase
lags at betw een 35 and 8 5 Hz to a stimulus to which che
cclls were similarly tuned (Hckhorn c t al. 1 9 8 8 ; Jagadcesh
et al. 1 9 9 2 ). This cype o f synchronous activity was m ost
pronounced in response to stim uli w ith continuous co n ­
tours and com m on m otion, as one would expect ot a system
that helps to bind distincc feacures o f a given o b ject (C ray
et al. 1 9 9 1 ; Freiwald ec al. 1 9 9 5 ). The oscillations need not
themselves codc stimulus-specific inform ation. They could
serve to coenergizc sets ot feature detectors for che form a­
tion and consolidation o f ccll assemblies in the process o f
learning. O n ce a cell assembly has been consolidated, syn­
chronous activity could activate it for the purpose o f object
recognition. Synchronous activity in a distributed set ot
cells can be evoked quickly enough to allow a fam iliar o b ject
to be recognized in a fraction o f a second (Gray et al.
1 9 9 1 ).
Vaadia et al. (1 9 9 5 ) found correlated spatiotemporal
patterns o f firing in the frontal lobe that varied according to
the task thac che monkey was perform ing. The possible role
o f synchronized
i
activitvi in binocular rivalry
4
is discussed in
Section 12.10.2.
However, other evidence does n o t support the binding-
by-synchrony hypochesis. Young ec al. (1 9 9 2 ) found no
evidence o f stimulus-evoked synchronous accivicv in che
• i
3 0 со 6 0 Hz range in che prim ary visual corcex or in chc
middle-cemporal area ( M T ) o f eicher the anesthetized or
alert monkey. Som e signs o f oscillation were found in the
inferotem poral cortex, but only in the alert monkey. C hose
and Freeman (1 9 9 2 ) could find no consistent relationship
betw een discharges in cortical cells and specific features ol
the stimulus other than stimulus strength, as reflected in
the mean firing rate o f cells. Engel et al. (1 9 9 2 ) suggested
that oscillatory responses m ight have been missed in these
studies because the responses were not strictly periodic and
contained a broad band ot frequencies.
Synchrony o f firing betw een pairs o f neurons in monkey
V I was found to be no greater when both receptive fields
lay in a figure region than when one receptive field was in
the figure and one was outside it (Lam m e and Spekreijse
1 9 9 8 ). Also, R oelfsem aet al. (2 0 0 4 ) found no synchrony in
the 3 0 - 8 0 H z range betw een cells in V I that responded to
different locations along a continuous line. However, the
mean firing rate o f the cells was elevated when the monkeys
attended to the line.
Thiele and Ston er (2 0 0 3 ) measured the degree o f syn­
chrony in the response o f cells in M T o f the alert monkey.
O rthogonally m oving gratings elicited less synchrony when
they were biased to form a coherent plaid pattern than
when they form ed separately m oving gratings. This is the
opposite o f what one would expect from the hypothesis
that stimulus binding is fostered by synchrony.
Palanca and D eA ngelis (2 0 0 5 ) pointed out that syn­
chronous activity is to be expected between cortical neu­
rons with overlapping receptive fields or betw een neurons
with collinear receptive fields and lateral connections.
A strong test o f the binding-by-synchrony hypothesis
would be the presence o f synchrony between neurons with
receptive fields that do not overlap and arc n o t collinear.
They found that rhe synchrony o f responses o f pairs o f well-
separated neurons in monkey M T was no greater when the
cells were stimulated by d istin ct closed figures than when
they were stimulated by a single closed figure. In a second
test, the stimulus was a parallelogram moving past four
apertures that occluded the corners o t the figure. W h en the
apertures were made visible against the background, the
parallelogram appeared com plete. W hen the apertures were
cam ouflaged, the shape becam e disconnected. Responses o f
pairs o f cells were slightly m ore highly synchronized when
the apertures were visible. However, the same increase in
synchrony occurred in a control condition in which only
the apertures were presented w ithout m oving stim uli. Thus,
the increased synchrony may have been due to an increase
in the num ber o f figural elem ents rather than to the
perceived organization ot the elements.
Ray and Maunsell (2 0 1 0 ) argued that if the gamma
rhythm is to play a role in stimulus binding it must be
consistent over cortical regions coding the given feature.
However, they found that gamma oscillations in V I o f alert
monkeys varied with stimulus contrast. Furtherm ore, the
gam ma rhythm is weak or absent for stim uli o flo w contrast,
small size, or low spatial frequency.
It is not clear how synchrony o f firing in distributed
neurons arising from a given stimulus can be distinguished
from synchrony arising from responses to o th e r stim uli that
are presented at the same tim e (Shadlen and Movshon
1999).
4 .3 .4 d S y n c h ro n o u s F irin g
an d T e x tu re S e g re g a tio n
The results o f som e psychophysical experim ents support
the idea that neural synchrony is involved in figure-ground
segregation. It has been claim ed that a texturcd region can
be detected w ithin an identical textured surround when the
two regions are presented sequentially at rates betw een 12
and 4 2 H z, if the phase difference is at least 10 ms (Leonards
et al. 1996). A set o f collinear line elem ents was more easily
detected w ithin a set ot randomly orientated elements
(see Figure 4.5b ) when the two sets were presented asvn-
chronously (U sher and D onnelly 1998). The interplay
betw een depth cues is influenced by the degree o f temporal
synchrony betw een con flictin g cues (see C hapter 3 0 ).
O th er psychophysical evidence argues against the role
o f synchronized neural activity in texture segregation. Kiper
et al. (1 9 9 6 ) found that perform ance on a texture segrega­
tion task was not affected by whether the texture elements
in the regions to be segregated were flickered in phase or in
antiphase. Lee and Blake (1 9 9 9 ) reported that subjects
could d etect a textured figure that differed trom the back­
ground only in tem poral synchrony. A textured region in
which elements reversed m otion direction in synchrony
stood out from the background in w hich reversals o f direc­
tion were n o t synchronized. However, Farid and Adelson
(2 0 0 1 ) showed that a simple tem poral band-pass filter could
convert the difference betw een the two regions o f the dis­
play into a difference in contrast. W h en they elim inated
this factor, subjects could not d etect a textured figure
defined by a difference in tem poral synchrony.
In spite o fd o u b ts about the use o f widespread synchrony
o f neural activity in visual coding, there can be no doubt
that relative tim ing o f inputs to the two ears or eyes affects
spatial coding. Also, synchronous inputs at particular syn­
apses are involved in tuning cortical cells during early devel­
opm ent and in perceptual learning, as we will see at various
points in this chapter and in C hapter 6 (see Trotter et al.
1992).
4 .3 .4 e S y
J
n c h ro n iz e d A c tiv ityJ and A tte n tio n
In states o f reduced attention and sleep, large cell popula­
tions in the co rtex engage in high-am plitude synchronous
activity ac less than 10 H z. D uring arousal, the reticular
activating system o f the brainstem disrupts this synchro­
nized activity but facilitates stimulus-dependent oscillatory
activity at frequencies in excess o f 3 0 Hz ( Munk et al. 1996).
A ttcntional processes are probably very im portant in
organizing neural activity into unitary patterns. Sillito
et al. (1 9 9 4 ) reported that synchronized activity in the
visual cortcx o f the cat induccd sim ilar high-frcqucncy
synchronized spike potentials in relay cells o f the LG N .
They suggested th at this feedback mechanism conccntratcs
neural circuitry o n to the stimulus. However, they found
that this activity could arise trom slow corticallv induced
covarying resting potentials rather than from covarying
spike potentials (Brody 1998).
T h e strength and pattern ofsynchronized firing between
widely different parts of the cat cerebral cortex have been
shown to depend on the stimuli to which the cat is attend­
ing (C ardoso de O liveira et al. 19 9 7 ; Roelfsem a ct al. 1997).
For example, cells in cat cortical areas 17, 7 , and 5 fired in
synchrony in the 4 to 12 H z range when the visual stimulus
was one associated with a learned action but nor when the
stimulus was novel (von Stein et al. 2 0 0 0 ). This suggests
that synchronization is associated with top-down neural
processing. Perhaps the fam iliar stimulus attracts more
attention than the novel stimulus. Fries c t al. (2 0 0 1 ) found
that neurons in cortical area V 4 ot the monkey showed
increased synchronization in the 35 to 9 0 Hz range and
decreased synchronization in the < 17 H z range when the
stimulus was one to which the animal was attending.
Synchronization could increase the efficiency o f synaptic
transmission o f specific inform ation passing from V 4 to the
inferior tem poral cortex, where pattern inform ation is p ro ­
cessed. W e are still left with the problem ot how patterns ot
activity in cell assemblies are accessed (Engel et al. 1992).
Trcism an (1 9 8 8 ) proposed that visual attention must be
directed serially to each o b ject in a display whenever more
than one feature is used to distinguish an object trom other
o b jects (P ortrait Figure 4 .1 ). C rick and Koch (1 9 9 0 ) pro­
posed that attention based on stimulus position binds
neural activity arising from diverse features o f an object,
and that this process is facilitated by tem poral synchroniza­
tion o f the responses o f neural centers activated by the
various features of the o b ject. There is evidence involving
fM R I in humans that the parietal cortcx is involved in
directing attention to particular locations when multiple
o b jects arc shown in different locations but not when they
are shown sequentially in the same location (Shafritz et al.
2002 ).
Synchronized activity could involve feedback loops that
help to sustain a pattern o f neural activity responsible for
short-term memory. Tallon-Baudry et al. (2 0 0 1 ) observed
sustained synchronized activity betw een regions o f the
extrastriate cortex o f tw o human subjects when they were
required to memorize a pattern and com pare it w ith a
second pattern presented after an interval o f up to 2 s.
4 . 3 . 4 f S y n c h r o n o u s A c tiv ity an d L e a rn in g
H cbb (1 9 4 9 ) speculated that learning depends on com peti­
tive reinforcem ent o t synaptic contacts. He proposed that
».i. A nne Trcism an. She o b tain ed а В .Л . trom C am brid ge
U n iv ersity in 1 9 5 7 and a P h .D . in psychology from O x fo rd U niversity
w ith C . O ld field in 1 9 6 2 . A fter w ork in g in the M .R .C .
P sych olin gu istics Research U n it in O xfo rd and the Bell L ab oratories in
N ew Jersey* she was ap p oin ted lectu rer in psychology at O xfo rd
U niversity in 1 9 6 8 . She was professor o f p sy ch ology a t the U niversity o f
B ritish C o lu m b ia from 1 9 7 8 to 1 9 8 6 and at the U n iv ersity o f
C a lifo rn ia at Berkeley from 1 9 8 6 to 1 9 9 4 . Sin ce 1 9 9 л she has been the
Jam es S. M cD o n n e ll Professor o f P sychology a t P rin ceto n University.
She w on the Spearm an m edal o f the B ritish Psychological S o ciety in
1 9 6 3 and the H ow ard C ro sb y W arren M edal o f t h e S o cie ty o f
E xp erim en tal Psychologists in 1 9 9 0 . She was elected a Fellow o t the
Royal S o ciety in 1 9 9 0 and a m em b er o t the N atio n al A cadem y o f
Scien ces in 1 9 9 4 .
synaptic contacts are strengthened when activity in a
prcsynaptic cell is tem porally correlated with activity in a
postsynaptic cell. Synaptic con tacts arc weakened when
activity in the two cells is n o t correlated. Synapses behaving
in this way are known as H cb b ian synapses. D etails about
H cbbian synapses arc provided in Scction 6.5.1.
W hen two prcsynaptic cells converge on the same
postsynaptic m em brane, the activity in either prcsynaptic
cell is more highly correlated with that in the postsynap­
tic cell when the inputs arc synchronous rather than asyn­
chronous. This is because the postsynaptic membrane
summates potentials from synchronous signals more effec­
tively than from asynchronous signals. Neural impulses in
two axons converging on a simple cell in the c a t’s visual
cortex produce a stronger postsynaptic response when
they arrive w ithin about 7 ms o f each other (Usrey et al.
2 0 0 0 ). Thus, correlated activity in two or more afferent
pathways gains preferential access to the nervous system,
and, over tim e, leads to increased transmission efficiency in
that pathway.
Persisting increases in synaptic transmission arc known
as lon g-term p o te n tia tio n (L T P ). W h en converging inputs
arc persistently uncorrclatcd the synaptic strength o f the
one mosc highly correlaccd wich che postsynaptic pocencial
increases ac the expense o f the synaptic strength o f the other.
Furtherm ore, L T P in one group o f synapses can be associ­
ated with lon g -term depression (L T D ) o f responsiveness
in neighboring inactive synapses, mediated either by ch em i­
cal ditFusion o r by lateral dendritic con nection s (Scanziani
e t al. 1 996).
These processes have been studied m ost extensively in
the hippocampus, a region o f the cortex involved in memory.
Long-term potentiation has also been recorded in the
auditory cortex o f adult monkeys (Ahissar ct al. 1992).
W h en neighboring neurons in chc auditory cortex were
induced to fire at the same tim e, the connection between
them increased. Asynchronous stimulation reduced the co n ­
nection betw een them. However, these changes occurred
only when the monkeys were accending to chc audicory
stimuli.
A neural net wich a broad distribution o f conduction
and synaptic delays could use the H ebbian rule to learn
static patterns (ccll assemblies) and tem poral sequences
such as tunes (H erz c t al. 1 989).
A Hebbian synapse strengthens synapses when converg­
ing inputs are synchronized. It can therefore be thought o f
as a covariance detector responding to w hat is com m on
betw een tw o inputs. Som e sensory systems act as difference
d etectors since chcv respond to what is different between
two inputs— they decorrelate the input (D an et al. 1996).
For instance, a ganglion cell does n o t fire when ics receptive
field is evenly illum inated but does fire when there is a
lum inance gradient across the receptive field. Ganglion
cells work this way because o f mutual inh ibitory co n n ec­
tions w ithin the inner plcxiform layer o f the retina
(Section 5.1.4e). The advantage o f this system is that mes­
sages are transm itted to the brain only from regions where
spatial or tem poral changes occur— the regions char arc
m ost informative.
M utual inh ibitory m echanism s arc responsible for co n ­
trast processes and opponent processes at various levels in
a variety o f sensory systems. O p p on en t m echanism s detect
changes in one stimulus feature in the presence o t changes
in som e other feature (Section 4 .2 .8 ).
Barlow (1 9 9 1 ) referred to mutual inhibitory mechanisms
as anti-H cbbian, because they d etect differences rather than
coincidences. H e suggested that H ebbian and anti-H cbbian
m echanism s work together at successive levels w ithin chc
processing hierarchy o f the visual system— H ebbian m echa­
nisms d etect coincidences betw een inputs, anti-H cbbian
mechanisms sharpen the distinctions between sets ot detected
coincidences.
In the standard account o f L T P it is assumed that pre-
and postsynaptic activities o ccu r simultaneously. However,
tem poral relationships between these events are im portant.
Postsynaptic spikes that follow presynaptic spikes within
2 0 ms induce LTP. Those that precede presynaptic spikes by
up со 2 0 ms induce long-ccrm depression (L T D ) (B i and
Poo 1998). This is known as spike cim ing-dcpendenc
p lasticity ,o r S T D P (see S ection 6.5.2).
Long-term depression induced by advanced postsynap­
tic activity could form the basis for predictive coding in
which postsynaptic accivicy arising from higher cencers
and generated in advance o f stim ulation gates the inputs
according to w hether they conform to what is anticipated
(R ao and Ballard 1999). M odels ol .ST D P and its possible
uses have been reviewed by Bi (2 0 0 2 ) and Kepees ec al.
(2002 ).
H ebbian synapses are imporcant in the development
o f the visual sysccm, particularly in chc developm ent o f
binocular vision (Sections 6 .6 .3 and 6 .7 .2 ). For discussions
o f Hebbian synapses, see Clochiaux ec al. (1 9 9 1 ), Dan
and Poo ( 1 9 9 2 ), M algaroli ec al. (1 9 9 5 ), and Cicri and
M alenka (2 0 0 7 ). Scructural changes underlying m em ory in
adult animals have been reviewed by Bailey and Kandcl
(1 9 9 3 ).
4 .3 .4 g M o d e ls ©( S y n ch ro n iz e d A ctiv ity
Several investigators have developed neural netw orks that
model synchronized activity in the visual cortex (Eckhorn
c t al. 1990; Schuscer and W agner 1990; Grossbcrg and
Som ers 1 9 9 1 ;S p o r n s e t al. 1 9 9 1 ; W ilso n and Bow er 1991;
Niebur et al. 1 9 9 3 ). Som e models are based on known
properties o f excitacory pyramidal cells and inhibitory
interneurons (T ra u b et al. 1 9 9 6 ; W right et al. 2 0 0 0 ). Ghose
and Freeman (1 9 9 7 ) developed a model o f cortical oscilla­
tions that would arise from the integration ot oscillatory
signals in the L G N and from intrinsic oscillations o f cells in
cortical layer 5.
Chawanya et al. (1 9 9 3 ) developed a neural netw ork
model that simulates synchronized oscillations w ithin and
betw een oriencacion colum ns o f chc visual corccx. In che
m odel, che screngch ot che phase correlations between
different colum ns reflects the length and con tin u ity o f
bar-shaped stimuli (see also K onig and Schillen 1991).
Schillen and K onig (1 9 9 4 ) described a netw ork model
that developed synchronized firing after a period ot
tem poral correlation betw een the activation o f distributed
assemblies responding to different features o t an object.
Christakos (1 9 9 4 ) provided a mathematical basis for analy­
sis ot synchrony in neural necs using the co h eren ce fu n c­
tio n , which expresses the extent to which two processes
covary as a function o f frequency. It is the frcqucncy-
dom ain analog o f the squared cross-correlation coefficient.
Ritz et al. (1 9 9 4 ) based a netw ork model o f collective
oscillations in the visual cortex on local inhibition between
single spiking neurons. Parodi ct al. (1 9 9 6 ) developed
a model based on the detection o f differences in arrival
cime o f incegrated visual inpucs as opposed to differences
in spikc-train frequencies (see also Gawne et al. 1996).
M echanism s o f neural synchrony have been reviewed by
Scurm and K onig (2 0 0 1 ).

4 .3 .5 T E M P O R A L C O D IN G O F
S P A T IA L F E A T U R E S
Up to now we have assumed chat che cemporal characteris-
tics o f neural responses code only temporal variations in
stimulus intensity and relative times o f responses. It is gen­
erally assumed that spatial features o f stimuli are coded in
terms o f the location and types o f neurons.
A group at the N ational Institute o f H ealth in Bethesda
proposed the radical idea that tem poral aspects o f the
spike train code spatial features o f a stimulus (R ichm ond
and O pcican 1987, 1990; Richm ond et al. 1 9 9 0 ; Gawne
et al. 1991). They recorded from the L G N and from com ­
plex cells in the visual cortex, as alert monkeys fixated
small patterns o f black and w hite squares and rectangles
(W alsh patterns). The patterns varied along three dim en­
sions— pattern, duration, and contrast. 'I he spike train o f a
cells response to each stimulus was sm oothed to produce a
spike-density profile over the first 2 6 0 ms. C om ponents
that accounted for successively smaller correlations between
stimuli and the response profiles over the set o f stim uli were
determ ined by principal com ponents analysis. A weighted
sum o f rhe com ponents represented the response o f a cell
to a particular stimulus. The first com ponent was corre­
lated w ith mean firing rare. Higher com ponents presum­
ably arose from differential latencies o f subregions o t the
receptive field or differential delays in recurrent inhibition
from different regions o f the receptive field. The effect on
the spike train o f varying one stimulus feature depended on
the value o f the o ther features. Thus, the features inter­
acted nonadditivcly. The response was the same tor many
com binations o f the stimulus o f pattern, duration, and co n ­
trast. I lowever, principal com pon ent analysis o f the spike
train allowed the investigators to extract som e inform ation
about each stimulus feature, and about com binations ot
features.
In another study w ith Walsh patterns, spike trains ot
cells in V I , V 2 , and V 4 were found to contain a temporal
code for color and a distinct tem poral code for pattern
(M cC lu rkin and O ptican 1 996}. They suggested that pat­
tern and color are processed in distinct multiplexed tem po-
ral-code channels, rather than in distinct labeled-line
channels. This would facilitate binding o f spatially related
features.
Gawne (2 0 0 0 ) found that stimulus orientation was
related to spike frequency o f com plex cells in m onkey V I
but that contrast was related to response latency and
spike m odulation. Both features could be reliably recovered
from stimuli that varied in both contrast and orientation
when the responses o f several neighboring neurons were
pooled.
The principal com ponents m ethod reveals independent
com ponents only if the underlying structure o f the spike
train is linear. The approach seems to be justified because a
nonlinear m ethod based o n neural netw orks did not reveal
evidence o f significant nonlinearities in spike trains pro­
duced by cortical neurons, at least to static stimuli
(Fotheringham e and Baddeley 1997).
The approach makes tw o novel claims. First, that
responses o f single neurons contain d istinct tem poral co m ­
ponents that relate to d istin ct stimulus features. Second,
that the nervous system is capable o f decoding this tem po­
ral inlorm ation. The traditional view is that transmission ot
sensory inform ation in the single axon is in terms o f response
frequency, with tem poral m odulation serving to indicate
only tem poral m odulations o f stimulus strength.
Even i f the spike rrain o fsin g le neurons contained infor­
m ation about a variety o f stimulus features, additional
neural processes would be required to extract it. Since there
is n o evidence about what these processes would be, the
approach leaves che problem o f scimulus analysis in the ner­
vous system unsolved. G iitig and Som polinsky (2 0 0 6 )
developed a com putational model o f a neuron chat learns со
respond differentially со dilferent spiking patterns.
Furtherm ore, che analysis was based on only a subset o f
values o f tw o or three stimulus features exposed tor a fixed
duration. G olom b e t al. (1 9 9 4 ) found a well-defined set o f
principal com ponents in the spike train o f cells in the lateral
geniculate nucleus, but only for a stim ulus o f fixed duration.
A typical cell in the L G N or visual co rtex is also influenced
by stimulus m otion, color, flicker, disparity, and size. Thus,
in practice, the jo b o f disentangling the contribution o f
each value o f each feature to the principal com ponents
o f the spike train o f a single neuron becom es difficult to
perform.
Tovcce et al. (1 9 9 3 ) applied a similar analysis to responses
ot cells in the primate tem poral cortex to faces. They tound
that the first principal com ponent o f the spike rrain (mean
spike frequency) accounted tor about 7 0 % o f the variance.
Furtherm ore, they found that about 85% o f chc inform a­
tion about firing rate available d u rin g a400-m s period could
be extracced during chc firsc 5 0 ms o f rhe cells response.
Almosc h a lf o f it was available in the first 2 0 ms.
Signals from the visual cortex to the inferior temporal
cortex pass through four stages. Each stage adds about 2 0
ms to the total latency o f response in the temporal cortex
(R o lls 1992). 'Птis suggests that effective inform ation about
firing frequency is extracted in abouc 2 0 ms ac each scage o f
processing. If we assume a firing race o f 100 H z, chis means
th at firing frequency escimaces in a single neuron are based
on up to five spikes. Tovee et al. found that only about 19%
and 8.5 % o f the inform ation in a spike train was contained
in the second and third principal com ponents, respectively.
Furtherm ore, a good part o f this inform ation was tound to
reflect rhe latency o f rhe cells response. Ihey concluded
that features o f the response train o ther than latency and
mean firing rate are probably nor significant for cortical
processing.
The rapidity o f visual processing is also indicated by
the finding that the cortical potential evoked by a decision
thac a com plcx scene exposed for 2 0 ms did not contain a
specified o b jcct, occurred w ithin 150 ms (Thorpe et al.
1996).
H eller et al. (1 9 9 5 ) applied a neural net analysis to spike
train inputs to m onkey V I . They concludcd that variations
in firing rate could n o t be resolved over intervals shorter
than about 25 ms.
To investigate rhe temporal resolution lim itations o f
principal com ponents analysis V icto r and Purpura (1 9 9 6 )
measured the spike latency, spike coun t, and interspike
interval in 3 5 2 neurons in V I , V 2 , and V 3 ot alert monkeys
during the first 2 5 6 ms o f exposure to gratings varying in
orientation and spatial frequency, and to checkerboards
varying in contrast, elem ent size, and texture type. M ost o f
the cells showed evidence o t stimulus-specific tuning by
spike latency and spike interval, but only about h alf showed
evidence o f tuning by spike count.
O ram c t al. (1 9 9 9 ) found large num bers o f stimulus-
elicited and precisely timed spike patterns in the L G N and
visual co rtcx but concludcd that many o f these patterns
arose bv
4 chance and carried no inform ation that was not
available in the spike count. Reinagel and Reid (2 0 0 0 ) ana­
lyzed the spike-train responses o f L G N cells to defined
random sequences o f flashing light and concludcd that
som e cells use tem poral patterns to encode temporal infor­
m ation. Each cortical cell receives thousands o f excitatory
and inhibitory inputs, each o f which fluctuates over time.
The resulting chaotic activity o f a neural netw ork puts
constraints on the use o f precise tem poral patterns (Van
Vrecswijk and Som polinskv 1 996).
H igher-ordcr com ponents in the temporal waveform
do n o t necessarily have to be analyzed to be useful. Rather
than conveying inform ation abou t stimulus features to
higher levels ot processing, they may be involved only in
low-level detection o f texture boundaries for the following
tour purposes:
1. Identification o f surface discontinuities An evenly
texturcd surface has a consistent texture, color, contrast,
and m otion, so that detectors tor that region respond
with similar and synchronous response trains. This
synchrony would enhance responses ot the cells onto
w hich the detectors converge because synchronous
inputs summate at synapses. H ence, the postsynaptic
cells would resonate to an input from an evenly
textured region. A t the boundary o f two texturcd
regions, there would be a discontinuity in the pattern o f
resonance, which could be used to locate the boundary,
even before any analysis o f particular texture features
had occurred. There is evidence that cells in the visual
cortex with sim ilar responses to stimulus orientation
fire in synchrony (Section 5 .5 .3 ). Evidence o f neuronal
mass activity related to texture segregation, which is
independent o f the visual feature defining the textures,
has been revealed in visual evoked potentials trom the
human scalp (I.am m c c t al. 1 9 9 3 ; Bach and M eigen
1997). Fahlc (1 9 9 3 ) found that a phase difference o f
only 5 ms betw een the tem poral m odulation o f groups
o f spatially hom ogeneous points was sufficient for
perceptual segregation o f one group o f points from the
background.
2. Matching binocular image* The tuning characteristics o f
the com ponent m onocular receptive fields o f a
binocular cell in the visual cortex tend to be similar.
The cross-correlation o f signals arriving at an array o f
binocular cells could indicate w hether the eves are
4
properly converged on a given stimulus (Section
11.10.1). A process th at com pares patterns o f spikes in
tw o or more neurons is known as a co rre la tio n code.
A model o f this has been provided by M urata and
Shim izu (1 9 9 3 ).
3. Detection o f disparity discontinuities T ootcll c t al.
(1 9 8 8 c ) reported enhanced neural activity (as reflected
in the uptake o f dcoxyglucosc) along cortical loci
corresponding to borders between differently texturcd
regions o f a stimulus display. Tins enhanced activity was
evident only when the display was viewed binocularly.
4. Discrimination o f complex temporal stimuli Com plex
temporal stim uli are produced by m oving stimuli.
Reinagel and Reid (2 0 0 0 ) found that a defined random
series o f flashes produced its own characteristic
temporal pattern o t discharges in an individual neuron
in the L G N o fth e cat.
4 .4 C O D IN G P R IM IT IV E S
Signal analysis is concerned with finding a set o f basis
fu n ctio n s that can synthesize any com plex signal, as
described in Section 3.2.6a. For example, sine waves o l d if­
ferent frequencies and phases provide a set o f basis func­
tions, which can approximate any well-behaved function
arbitrarily closely. A good set o f basis functions should be
com plete, m eaning that they must be able to synthesize all
stimuli. They should also be independent, m eaning that
each function captures a stimulus property not captured by
another function.
We can ask w hether the visual system contains a set o f
basis functions by which it analyzes com plcx visual scencs.
The basis functions can be regarded as a set o f filters applied
to the visual input, or wc can talk about a set o f visual chan­
nels o r coding primitives. Physiologically, a set o f basis fu n c­
tions in the space dom ain is the sensitivity profiles o fth e
receptive fields o f a set o f similar cells at a given level o fth e
visual system. For example, at the level o f ganglion cells,
the primitives are the spatial tuning functions o f rcceptive
fields o f ganglion cells (Section 5 .1 .4a). The idea can be gen­
eralized to the spatiotem poral response profiles o f cortical
cells (Section 5 .5 .3 ). The general m ethods of'signal analysis
were discussed in Section 3 .2 .6 . Visual primitives that have
been proposed For the visual system will now be discussed,
starting with Fourier com ponents.
4 .4 .1 F О U R IE R С О M P O N F. N T S
4 .4 .1 a T h e V isu a l Sv stem as F o u rie r A n aly zer
A linear system transm its signals o f different frequencies
w ithout distortions or interactions. For many purposes, it is
convenient to specify the spatial Fourier com ponents o f a
visual display. As we saw in Section 3 .2 .2 , it is a particularly
useful procedure when one is testing the linearity o f a
svstem.
The French m athem atician Duffieux (1 9 4 6 ) was the
first to apply Fourier analysis to optical systems. The lens
o f the eye is a reasonably linear transmission system. The
D utch engineer D eLange (1 9 5 8 ) analyzed the visual
response to flickering light in terms o f temporal frequen­
cies. O tto Schade (1 9 5 6 ) was the first to apply Fourier
analysis to spatial aspects o t vision.
The way an optical system, including that o f the eye,
resolves images ot different spatial frequencies provides an
adequate measure o f its perform ance. But that does not
mean that the eye perform s a Fourier analysis o t the input.
It simply means that we can use Fourier analysis to assess its
perform ance, as explained in Section 9.1.3.
A system that merely transm its different spatial frequen­
cies does not detect the different frequency com ponents in
com plex signals. For detection o f com ponents the different
frequencies must stim ulate distinct detectors. The system
may then carry o u t a Fourier analysis, or redcscription, o f
the input to produce output signals that indicate the am pli­
tude and phase o fe a c h frequency com ponent in the input.
The human ear can be said to produce at least a crude
temporal Fourier analysis o f sound patterns. This is because
the ear has many distinct frequency channels, each respond­
ing to a narrow range o f sound frequencies.
C am pbell and Robson (1 9 6 8 ) proposed that the visual
system has distinct channels, each tuned to a particular
range o f spatial frequencies. C onsequently, they argued that
the system achieves a spatial Fourier analysis o t visual pat­
terns. The idea th at the visual system perform s a Fourier
analysis can be misleading. In theory, any system capable o f
detecting rhe spatial Fourier com ponents o f com plex pat­
terns efficiently must fulfill three requirem ents:
1. It must possess a set o f independent and linear detectors
each o f infinite size and very narrow spatial-frequency
bandwidth. N o t only detectors of low spatial frequency,
but also detectors o f high spatial frequency must be large.
2. It must be spatially homogeneous.
3. It must encode both am plitude and phase.
The first condition is n o t satisfied in the visual system,
since receptive fields are comparatively small and not nar­
rowly tuned to spatial frequency. A lso, there are many non-
linearities in the visual system. The con d ition o f spatial
hom ogeneity is also not achieved, since receptive fields
becom e larger and less dense in the peripheral retina.
Nevertheless, a typical receptive field in the retina is m axi­
mally sensitive to a spatially periodic stimulus o f a given
period, and reccptivc fields vary in size and thus vary in
their preferred spatial periodicity. G anglion cclls with d if­
ferent sizes ot receptive field are often called spatial-
frequency channels. The term “spatial-scale channels” is
better because it does n o t suggest that the visual system per­
forms a Fourier analysis, which would require receptive
fields o t infinite size.
The im portance o f phase can be illustrated by consider­
ing the Fourier transforms o f a thin line and white noise.
They have the same am plitude spectrum since they can both
be decom posed into sets o f equal amplitude sine waves o f
all spatial frequencies. They differ only in their phase spec­
tra. Phase is random tor w hite noise but, tor a line, the peaks
o f the sine waves coincide at one location.
4 .4 .1 b N u m b e r o fS p a tia l-F r e q u e n c y C h a n n e ls
The spatial-frequency tuning o f a visual channcl depends
basically on the size and internal structure o f receptive fields
o f ganglion cells. There is a gradual increase in the size o f
receptive fields w ith increasing retinal eccentricity. I f the
internal structure o f receptive fields scales in the same way,
there must be a continuous gradation o f the bandwidth o f
spatial-frequency channels over the whole retina. The
im portant question is how many channels arc present in
each local region o t visual space.
Four psychophysical procedures have been used to
determ ine the num ber and bandwidth ot spatial-frequency
channels in a local region o f the visual field.
1. Method o f adaptation C hannel bandwidth is indicated
by the range o f spatial frequencies over w hich an
adapting grating elevates the threshold o f a
subsequently exposed test grating (Blakem ore and
C am pbell 1969).
2. Method o f subthreshold summation C hanncl bandwidth
is indicated by the range o f spatial frequencies over
which subthreshold gratings reduce the threshold o f a
superimposed test grating (G raham and Nachmias
1 9 7 1 ; Sachs c t al. 1971).
3 . M ethod o f masking C hanncl bandwidth is indicated by
the frequencies over which suprathreshold masking
gratings elevate the threshold o f a superimposed test
grating (Strom cyer and Julesz 1972; W ilso n c t al.
1983). After allowing for etfccts o f probability
summation and nonlinear interactions, the results are
 reasonably consistent with there being ac least six
spatial-scale channels in the visual system with a
half-am plitude bandwidth o f abou t 2.2 octaves for
die lowest spadal-frequency channel, and about
1.3 octaves for the highest spatial-frequency channel
(W ilson 1991a).
4 . Comparison o f detection an d discrimination In this
m ethod the contrast at which two gratings are detected
is com pared with the contrast at which they are
discrim inated. II they are the same it is assumed that the
tw o gratings stimulate d istin ct spatial-frequency
channels. W ith this m ethod, W atson and Robson
(1 9 8 1 ) concluded that there arc seven distinct spatial-
frequency channels.
4 .4 .1 с D e te c tio n o f S p a tia l F re q u e n c y
an d P o sitio n
Investigators have raised the question o f w hether spatial
frequency and spatial position arc coded by the same or
by distinct m echanism s. At first glance this appears to be­
an empirical issue» requiring an experim ental approach.
However, at least part o f the answer can be obtained from a
theoretical analysis, once the general properties o f a partic­
ular system are know n. G abor (1 9 4 6 ) applied this analysis
to tem poral signals in acoustic systems, rather than to spa­
tial frequency and position in the visual system. However,
the conclusions apply to both domains.
I f the tem poral frequency o f a signal is represented on
the .v-axis and tim e on the у-axis we have a tim c-freq u en cy
d iag ram . C onsider an impulse o f sound occurring at a well-
defined time but with energy distributed evenly over the
whole frequency spectrum (an impulse, or delta function).
An impulse in the tim e-frequency diagram is a horizontal
line (Figure 4 .2 ), I f a systems response to an impulse is
know n, one can calculate its transfer function. This is
because a linear systems response to an impulse is the
Fourier integral o f its transfer function.
C onsider, next, a pure tone with a well-defined fre­
quency but infinite duration. It is represented in the time-
frequency diagram by a vertical line. Any signal o f finite
duration is interm ediate betw een an impulse, w hich is
determ inate in tim e bu t n o t in frequency, and a sine wave,
w hich is determ inate in frequency but indeterm inate in
tim e. A detector can be designed to extract inform ation
about the tim e o f events bu t disregard frequency, or to
d etect frequency and disregard tim e. For instance, an ideal
oscillograph with uniform response over all frequencies and
a very short tim e constant (qu ick decay o f response) is an
instrum ent o f the first type. A set o f narrowly tuned oscilla­
tors, each with a long tim e constant (prolonged resonance),
may be regarded as an example o f the second type o f instru­
m ent. O n e instrum ent can n ot do both jo b s efficiently
because the design characteristics are incom patible.
Im pulse (all frequencies)
С
О
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'(/> 03
a <D
С
03 (Л
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о Q-
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e
T em poral o r spatial frequency
,. 2. The im pulse a n d p u re lin e wave. A tem p oral im pulse (delta
fu n c tio n ) o ccu rs at a specific tim e , w ith en ergy spread evenly over the
w hole tem p oral-freq u en cy sp ectru m . A pure to n e co n ta in s on ly on e
freq u en cy b u t ex ten d * over an in fin ite period o f tim e. Sim ilarly, a spatial
im pulse o ccu rs at a specific lo c a tio n , w ith energy d istribu ted over the
w hole spacial-frequency sp ectru m . A pure spatial sine wave has on ly on e
vpalial frequ ency b u t exten d s over in fin ite space.
The same argum ent applies it we substitute spatial fre­
quency tor tem poral frequency and position for time. The
ideal spatial-frequency detector is narrowly tuned to spatial
frequency and has a long space constant (infinitely large
receptive field). The ideal position detector is broadly tuned
to spatial frequency and has a small receptive field. It is
impossible to design a sensor that can perfectly detect both
types o f inform ation. If both types o f inform ation are
required trom the same detector, there must inevitably be a
com prom ise, which is expressed by the fact that, in any
detector
Tim e constant x bandwidth > 1/2
A consequence o f this relationship in the space dom ain is
that, i f we define the sensitivity o f a detector to differences
in position as Ds, and its sensitivity to spatial frequency as
Df, then the product o f these uncertainties can n ot be less
than one-half, or
Ds x Df> 1/2
This reciprocity between tw o uncertainties is essentially che
same as that expressed in Heisenberg s principle o t uncer­
tainty. This states that it is impossible to know both the
position and frequency characteristics (mass) o f a funda­
m ental particle at the same time. The best com prom ise
betw een detection o f position and spatial frequency is
achieved when Ds X D f is a minim um , which in the ideal
case is 0.5. G abor defined the d etecto r for which this is
true. In the space dom ain, the requirem ents are m et if the
sensitivity profile o f each detector is a Gaussian (norm al)
distribution multiplied by a sine or cosine function. This
is known as a G a b o r fu n ctio n . A Gaussian function has
the unique property that its Fourier transform is also a
Gaussian function. A t each location, there should be pairs
o f detectors with sensitivity profiles in phase quadrature.
These two requirem ents are summarized by the expression:
S (дг) = e zr cos I n F x ( or sin 2 J l F x )
where 5 (x ) is the norm alized sensitivity profile o f a d etec­
tor, s is the standard deviation o f rhe sensitivity profile, F is
the optim al spatial frequency to which the detector is tuned,
and .v is distance along the дг-axis (Kulikowski 1980;
M arcclja 1 980).
Tw o sensitivity profiles are in quadrature when one is
phase-shifted 90° with respect to the other, like sine and
cosine functions. A cosinc function betw een 0° and 180" is
symmetrical, whereas a sine function is asymmetrical.
A Gaussian profile m ultiplied by a cosinc wave produces
an even-sym m etric G abor function and a Gaussian profile-
multiplied by a sine wave produces an odd-symmetric
G abor function. O n e can think o f a G abor function as the
image produced by looking at a sinusoidal grating through
a Gaussian window. The grating is the carrier, and the
window is the envelope. The scale o f a G abor function
varies according to the width o f the envelope. W h en the
envelope is very wide, the G abor function is a sine wave
(narrowband display), and when it is very narrow, the G abor
function becom es a thin line, or delta function (broadband
display). An interm ediate case is shown in Figure 4.3. Thus,
for a given spatial frequency o f the sine wave, the spatial-
frequency bandwidth o fth e patch is inversely proportional
to the size o f the envelope.
There is thus a family o f G abor functions extending
from a sine wave to a line (Graham 1989). At interm ediate
values, the G abor function is a spatially localized patch o f
damped sine or cosine waves, known as a G abor patch. Just
as any visual scene can be decom posed into sine waves it can
Cosine input Gaussian-window Gabor-patch
function function
Gabor patch
F,««rc «.>. A G abor patch. A G abor patch is constructed by m ultiplying a
patch with a sinusoidal lum inancc profile with an aperture with л
Gaussian (norm al) lum inancc profile. (A d ap ted fro m G rah am 1 9 8 9 }
also be decomposed into G abor patches derived from a
Gaussian function o f specified width.
G abor pointed o u t thac there exists a class o f real-valued
functions that are more general than G abor functions and
which also maximize chc joinc dcccccion o f position and
frequency.
4.4.2 G A BO R FU N C T IO N S AND WAVELETS
Elongated G abor patches, as defined above, provide a rea­
sonable fit to the 2 -D response profiles of simple cells in the
visual cortcx o f the cat (Jo n es and Palmer 1 9 8 7 ) and o f the
monkey (Ringach 2 0 0 2 ). Furtherm ore, cortical cells with
even-symmetric (cosine) and odd-sym m etric (sine) sensi­
tivity functions are in quadrature (their sensitivity profiles
arc relatively phase-shifted by 90"). There is evidence that
cells in quadrature occur in pairs in the visual cortex, with
different pairs tuned to different regions o f the spatial-
frequency spectrum (Pollen 1981). This suggests that the
visual system achieves an optim al com prom ise between
detection o f spatial frequency and detection o f stimulus
position. This arrangem ent is also ideally suited for o p ti­
mally deblurring images and reducing noise in the visual
input.
These ideas have been generalized to two spatial dim en­
sions and to the dim ension o f orientation (Daugm an 1984,
1 9 8 5 ). The sensitivity profiles o f the receptive fields o f
simple cells in the visual cortex can be described as 2-D
G abor functions with different spatial periodicities, even-
or odd-sym m etric profiles, and oriented at different angles.
Each detector has an orientation bandwidth o f about 15°,
a half-am plitude spatial-frcquency bandwidth o f about
1.5 octaves, and a lengch-co-widch racio o f abouc 2:1.
A branch o f m athem atics known as w avelet th eo ry has
been applied in vision (Young 1 9 8 7 ; Daugman 1 9 9 0 ,1 9 9 1 ;
Farge ct al. 1 9 9 3 ). Wavelets, are localized, self-similar, undu-
latory functions derived from G abor functions. They differ
with respect to size (dilation), position (translation), and
phase. I f the wavelets are anisotropic, like G abor patches, or
the elongated receptive fields of cortical cells, they also
differ in orientation (rotation ). Even with a sparse sampling
of size and orientation, one can construct any com plex pat­
tern from an appropriate set o f wavelets, with a resolution
lim ited by
*
the smallest wavelets in the set. Wavelets are effi-
cicnt in that the dim ensions o f position, spatial scale, and
orientation arc detected independently with no cross talk
(sec Sakitt and Barlow 1982).
W e shall now see that the receptive fields o f cells in the
visual system can also be fitted by other functions with
other properties.
4.4.3 O T H E R VISUAL PRIM ITIVES
Th e receptive field o f a ganglion cell can be considered to
be an excitatory area with a Gaussian sensitivity profile
 Sensitivity A system conform s cxactly to any one o f them . Spatial filters
__ P o sitiv e
//\\ G a u s s ia n
^ N eg ativ e
G a u s s ia n
A
Figure 4 .4 . D ifferen ce o f G aussian sensitivity profile. (A ) A n idealized
sensitivity profile o l л ganglion cell receptive field depicted as th e sum
o f a narrow positive G aussian d istrib u tion rep resenting the excitato ry
co m p o n e n t o f the c e lls response and a broader negative Gaussian
d istrib u tion rep resenting the in h ib ito ry c o m p o n e n t o f the
response. (B ) A 3 'D sensitivity profile o t a ganglion ccll. I he "volu m es"
o f the ex citato ry and in h ib ito ry regions are equal» so th at w hen the
receptive field is evenly illu m in ated , the firing rate o f the cell is the same
as in th e d ark . (Adapted from Rodicck 1965}
superimposed on an inhibitory area w ith a som ew hat wider
Gaussian sensitivity profile. The com posite sensitivity pro­
file is known as a d ifferen ce o f G au ssian s (D O G ). The
D O G profile o t a ganglion cell is circular symmetric, or iso­
tropic, as in Figure 4 .4 . The receptive field o f a cortical
cell may be represented as an elongated D O G . It is even-
symmetric (cosine) when the excitatory and inhibitory
com ponents are spatially in phase, and odd-symmetric
(sine), when they arc 90° our o f phase.
Assume that the receptive fields o f the basic units o f the
visual system conform to these specifications. In that case it
would be useful to use stim uli w ith these spatial characteris­
tics, since they are m ost easily detected. Hugh W ilson and
others have used D O G s extensively in the study o f contrast
sensitivity and stereoscopic vision, as we will see in later
chapters. A D O G stimulus, unlike a sine-wave grating, has
a well-defined location in space. It also has a peak, or center
spatial frequency, which can be varied by changing the
width of the com pon ent Gaussian distributions.
Since a Gaussian function is not a pure sine wave, it
necessarily has a certain spatial-frequency bandwidth. By
differentiating a Gaussian, one obtains a Gaussian with a
narrower bandwidth. The sixth and tenth derivatives o f a
Gaussian function, known as D 6 and D IO , are often used in
visual experim ents, including those on stereopsis. Stork and
W ilso n (1 9 9 0 ) showed that Gaussian derivatives are real-
valued functions, w hich, like G abor functions, maximize
the jo in t detection o f position and frequency. Being real-
valued they have the advantage that they require only single
detectors rather than the paired dctcctors in quadrature
required by complex-valued G abor functions.
O th er types of mathem atically defined filters have been
borrowed from physics and used to characterize low-level
visual processing. These include zero crossings (M arr 1 9 8 2 ),
Cauchy functions (K lein and Levi 1 9 8 5 ), dipoles (K lein
and Levi 1 9 8 6 ; Klein et al. 1 9 9 0 ), and cepstral filters
(Yeshurun and Schwartz 1 9 9 0 ) (Section 15.2. Id ). Although
each formalism has advantages, it is unlikely that the visual
may improve the efficiency o f low level coding, but visual
processes arc too nonlinear to be described by any set o f
linear filters. Also, linear image transform ations do not
solve the problem o f visual recognition, they simply
postpone it.
4 .4 .4 N O N L IN E A R V IS U A L P R O C E S S E S
Since a linear system can only add or subtract, other forms
o f com putation must depend on nonlincaritics. The basic
nonlinearity in a digital com puter is che tw o-state transis­
tor. C om putations other than addition carried o u t by the
nervous system depend on nonlinearities at synapses. There
are several types o f nonlincarity in the nervous system.
For som e types, che system is approximately linear over
a lim ited range o f amplitude m odulation. An essential
n o n lin earity is one that does n o t approach linearity when
input am plitude is reduced. M ultiplication, division, and
rectification arc essential nonlinear processes. The follow ­
ing is a list o f com m on nonlinearicies encountered in
sensory systems.
1. Thresholds In the region o f the threshold, the rcccptor
potential is a nonlinear funccion o f light incensicy and
the principle o f superposition docs n o t hold. O n e
reason for chis is that additive noise increases in
proportion to the signal as signal strength is reduced
(m ultiplicative noise is a constant fraction o f signal
strength). A nother reason is that stimulus events
becom e quantal near che chreshold. For inscance,
w hether or not light is dctcctcd depends on the
statistical probability o f lighc quanca falling on a
rcccptor plus the probability o f quanta being absorbed
by pigm ent molecules. A third reason is thac sensory
responses may be quantal and therefore subject to
random fluctuations. For instance, a synaptic response
depends on the release o f a threshold num ber o f
neurocransmiccer molecules from synaptic vesicles.
Beyond the receptor level, neurons produce spike
potentials in an all-or-nonc fashion. Thus, stimulated
receptors w ithin che receptive field o f a ganglion cell
produce a neural spike in the ganglion ccll when the
com bined generator potential reaches a threshold value.
In the presence o f uncorrclatcd noise, som e receptors
will be nearer threshold than others at any time. This
produces response variability, w hich smooches the
response o f the ganglion ccll to variations in stimulus
strength in the chreshold region (Anderson et al. 2 0 0 0 ).
Similarly, in the cortcx, spontaneous synaptic accivicy
enhances the probability o f an action potential to weak
stimuli buc reduces the response to a larger stimulus
(Shu Y e t al. 2 0 0 3 a ).
2. Compressive an d accelerating nonlinearities In a
compressive nonlinearicy the response o f a system
saturates as stimulus strength is increased. This is
known as a ceiling effect. The logarithm ic relationship
betw een stimulus intensity and the generator potential
o f retinal receptors is a nonlinear function o f this type.
A system may be linear over its operating range but, as
the intensity o f a stimulus is increased beyond a certain
level, the response levels off to an asym ptotic value.
In an accelerating nonlinearity, the output accelerates
relative to the input. This typically occurs near the
sensory threshold. The output is raised by a power
greater than one. Raising an input by a power greater
than one introduces an accelerating nonlinearity.
Several characteristics o f binocular cells in the visual
co rtex can be accounted lo r i f it is assumed that inputs
are squared (Section 11 .1 0 ).
3. Rectification M any neurons act as half-wave rectifiers o f
the input since they respond only to displacements
in one direction along the stimulus continuum .
R ectification arises when the stim ulus dim ension is
bipolar and extends in both directions with respect to a
norm , but for which the sensory detectors are
m onopolar. For example, retinal bipolar cells arc
half-wave rectifiers because they respond either only to
stimulus onset or only to stimulus offset. Also, many
m otion detectors in the visual cortex respond only to
m otion in one direction. W e will see th at some
detectors o f binocular disparity are also half-wave
rectifiers in that they respond only to crossed or only to
uncrossed disparities (Section 11.4.1}. The com bined
output o f two half-wave rectifiers, with signs ignored,
produces a fully rectified signal. Full-wave rectification
is formally equivalent to squaring the inputs, since
squaring removes signs. For example, if the signals from
O N -cen ter and O F F -cen te r receptive fields were
com bined w ithout regard to sign it would produce a
fully rectified signal that would indicate an edge
whatever the sign o f its contrast. A fully rectified signal
o f binocular disparity would signal the am plitude o f a
disparity w ithout indicating its sign. The com bined
output o f two half-wave rectifiers, with signs intact,
reconstitutes the original signal. Thus the output signal
from two rectifiers may be linear even though each
rcctificr is nonlinear (see W arland et al. 1997).
Advantages o f rectification in sensory systems were
discussed in Section 4 .2 .3 .
4 . Multiplicative nonlinearities M ultiplication o f two
signals is a nonlinearity, since the output is more chan
the sum o f inputs. M any neurons are su bject to
m ultiplicative gain co n tro l, w hich affects the strength
o f their response but not their tuning functions. For
example, the discharge o f neurons in the visual cortex
may be up- or downregulaccd by the direction o f
atten tion or the position o f the eyes (Salinas and Their
2000).
G anglion cells, relay cells in the lateral gcniculatc
nucleus, and sim ple cells in the visual cortex are
reasonably linear, in that their responses to complcx
stim uli can be predicted from the superim position o f
their responses to simpler stimuli. C om plex cclls in the
visual cortex and visually responsive cclls in higher
visual centers, such as the inferior temporal cortex and
parietal cortex, respond in a highly nonlinear way.
D etecto rs at all levels o f the nervous system show
inh ibitory interactions, w hich arc believed to reduce
activity within hom ogeneous regions relative to activity
at boundaries between distinct regions. The result is
that contrast, rather than lum inance, determines
activity ac higher levels o f the visual system.
M any detectors show subthreshold summation in
which a subthreshold stimulus presented to one
d ctccto r is brought above threshold by the
sim ultaneous subthreshold stim ulation o f a second
dctcctor. This type o f nonlinear facilitation occurs in
the response o f binocular cells in the visual cortex to
inputs from the two eyes (S ectio n 11.4.1). The
nonlinearity is extrem e in so-called ANL) cells, which
respond only to sim ultaneous inputs from the two eyes.
Interactions betw een neurons can change the gain o f a
neural system, or change the tim e and space conscancs
o f rcceptive fields o f sensory neurons— both nonlinear
processes. Enhancem ent o f responses со synchronized
inputs relative to nonsynchronized inputs is also a
nonlinear process.
Logical, or Boolean, operators such as A N O -gates and
O R -gatcs involve a type ot m ultiplication based on
threshold processes. An example o f an A N D -gace is
provided by cells in the visual cortex chac respond only
when both eyes are stimulated (Section 5.7.2d ). A set o f
Boolean operators form s che basis o f che p ercep tron
model o f visual processing (R osenblatt 1958). A
perceptron mechanism can carry ouc many types o f
com putation, but cannot com pute distributed
functions such as figure-ground segregation. In general,
any real continuous function can be approximated by a
polynom ial. Polynom ials can be derived by multiplying
inputs from a set o f detectors, and can be used to
com pute a broader set o f functions than can be
com puted by a “perceptron” (K o ch and Poggio
1 9 9 2 ).
D etectio n o f correlation betw een sensory inputs
involves a nonlinear process ot m ultiplication. For
exam ple, chc Pearson correlacion coefficicnc is chc mean
o f che produces o f normalized deviacions from rhe
 mean. The dececcion o f chc direccion o f a moving
stimulus necessarily involves a multiplicative
nonlinearity. For exam ple, in the Reichardc m otion
detector, a linearly filtered output from one detector is
m ultiplied by the delayed output from a neighboring
detector and then averaged over tim e (Rcichardt
1 987). People can detect the degree ot correlation
betw een images presented to rhe tw o eyes
(Section 15.2.2).
Responses ot a H cbbian synapse, which arc responsible
for synaptic plasticity and learning, depend on the
product o f the prcsynaptic potential and the
sim ultaneous postsynaptic potential (Section 6 .5 .1 ).
5. Cross~madulation products The response o f a linear
system to tw o superimposed sine waves is two sine
waves with their frequencies unchanged. The output o f
a nonlinear system to two sine waves consists o f the two
sine waves (the fundam entals) plus harm onics o f each
sine wave, plus sums and differences o f the harm onics o f
the tw o sine waves, such as 3 F I + 2 F2. C ross-
m od u lation p ro d u cts are characteristic o f nonlinear
systems. Each type o f rectifying nonlincariry produces
characteristic cross-m odulation products. Therefore,
one can infer the type o f rectifier in a given system by
measuring its cross-m odulation products, and
consulting a catalog o t rectifiers.
Regan and Regan (1 9 8 8 ) developed a general
m athematical treatm ent involving the zoom fast-Fourier
transtorm . This gives a very high resolution o t the
cross-m odulation products produced by two sine-wave
inputs. W h en applied to the analysis o t evoked
potentials generated in the human visual cortex
by tw o lights flashing at dilferent frequencies,
it produces a sharp separation between stimulus-related
signals and signals arising from noise, as shown in
Figure 13.12.
Z hou and Baker (1 9 9 6 ) recorded trom cells in visual
cortical areas 17 and 18 o f the cat, w hich responded со
m oving cross-m odulation products (spatial beats) ot
superimposed sine-wave gratings, even though the
spatial frequencies o t the gratings were outside the
tuning range o f the cells. Cross-m odulation products
arc n o t detected by a purely linear system, since they arc
n o t represented in che Fourier dom ain. Any syscem
generating cross-m odulation products must thcretorc
involve nonlinear processing.
6. Second-order stimuli Scimuli defined by lum inance are
often referred to as first-order, linear, o r Fourier stimuli.
They arc distinguished from second-ordcr, or non-
Fourier stimuli defined by texture, disparity, or m otion.
They arc callcd non-Fourier stim uli because they arc not
represented in the lum inance Fourier spectrum o f the
stimulus. Buc chis term inology is racher arbitrary since
lum inance-defined edges are not necessarily detected by
linear processes and the visual system docs n o t contain
Fourier m echanism s in the strict meaning o f the term.
Furtherm ore, a second-ordcr stimulus, such as a figure
defined by texture, can be converted into one with
Fourier com ponents if ic is firsc rcccificd. In che visual
syscem, full-wave rectification can be achieved by
pooling the inputs from O N -ccn tcr and O F F -cen tcr
receptive fields. This introduces a spurious doubling o f
the spatial frequency o f the stimulus, which can be
removed by subsequent fileering ac an octave lower chan
chc spurious signals. The resulcing signal can then
activate a detector o f stimuli defined bv lum inance. For
4
example, a Reichardc m otion detector can detect
first-order m otion defined bv m otion o f luminance-
defined edges. However, it cannot detect second-order
m otion o f edges defined by contrast or texture.
However, a Rcichardt detector can detect a second-
ordcr signal after it has been rectified and filtered
(C h u bb and Sperling 1988; W ilso n and Kim 1994).
7 . Adaptation an d hysteresis Sensory adaptation, defined as
short-term m odification o f the response o f a sensory
system exposed to constant stim ulation, is a
nonlinearity because it violates the timc-invariance
assumption o f linear systems. Sensory adaptation
amplifies transient inputs relative to sustained inputs. It
is equivalent to differentiating the input.
The response o f a neuron subject to adaptation is
greater when a given value o f stim ulation is reached
from a low value chan when ic is reached from a high
value. As stim ulus strength is slowly increased and
decreased over a given range, the response-stimulus
function does n o t traverse the same path but traces out
a loop, known as a hysteresis loop. The binocular
fusion m echanism shows hysteresis in that the disparity
at w hich initially fused stim uli becom e diplopic is not
the same as the disparity at which initially diplopic
stimuli fuse. Binocu lar fusion is a bistable system in
which change o f state with changing disparity is
saltatory rather than continuous (Scctio n 12.1.6).
8. Learning The long-term m odification o t a response
to a given stimulus through learning is a nonlinear
process.
9. Bistable percepts Spontaneous changes in the
inrerpreracion o f a visual scimulus, such as those chac
occur in reversible perspcccive and ambiguous figure-
ground displays are nonlinearicies. Ihese nonlinearicies
in high-level control systems are difficult if not
impossible to specify mathematically.
Procedures for analyzing nonlinear systems were
reviewed in Section 3.4.
 4.5 HIGHER-ORDER SENSORY
SYSTEMS
As a basis for discussion, visual primitives will be defined as
those stimulus features that arc channeled at the retinal
level. These include position, brightness, contrast, spatial
periodicity, color, and flicker. M otion will be included as a
visual primitive, although it is channeled in the visual cortex
in some animals. All highcr-order visual features are derived
from these primitives.
4 .5 .1 T Y P E S O F S E N S O R Y P R O C E S S IN G
4 .5 .1 a Serial and Parallel Processing
Sensory inform ation related to space perception is com ­
bined in a great variety o f ways for diverse purposes. W c
often distinguish between serial p ro cessin g and parallel
p ro cessin g o f sensory inform ation in the central nervous
system.
There are three types o f serial processing:
1. Hierarchical processing within a feature system In
hierarchical processing a given stimulus' attribute is
processed sequentially at increasing levels o f complexity.
For example, visual disparity is processed at successively
higher levels in the nervous system to code more
com plex patterns o f disparity.
2. Sequential processing o f distinct features In this type o f
serial processing, d istin ct stimulus attributes are
processed sequentially. For instance, color and
binocular disparity are processed serially since some
color processing occurs in the retina before binocular
disparity is processed in the visual cortex.
3. Serial search In serial search, stimuli in different
locations o r different attributes o f a given o b ject arc-
attended to in sequence.
In a parallel system, different stimuli or different attri­
butes o f a stimulus arc processed simultaneously by neural
m echanism s laid o u t in parallel. For example, rods and
cones operate in parallel, as do O N -ganglion cells and O F F -
ganglion cells. Two types o f sensory input m aybe processed
in parallel initially and then com bined into one processing
stream. For example, inputs from the two eyes are processed
in parallel before they are com bined in the visual cortex.
T h e terms “serial” and “parallel” can also be used to
describe the structural organization of sense organs with
respect to a given task. For example, the sense organs in the
jo in ts o f the arm are structurally in series with respect to
judging the position o f che finger in relation to the torso.
Systems o f this kind are nested. The tw o eyes are structur­
ally in parallel. W h eth er sense organs are structurally nested
or in parallel has n othing to do with w hether inform ation
from the sense organs is processed serially or simultaneously
(in parallel). For example, the join ts o f a lim b are structur­
ally in series bu t inputs from jo in t receptors are processed
simultaneously.
4 .5 .1 b T y p es o f Ju d g m e n t an d S tim u li
A relation al ju d g m en t requires inform ation from two or
more sensory inputs. For example, che task ot judging che
position o f the unseen hand relative to the torso is rela­
tional, since one can n ot perform it i f inform ation from any
o f the join ts is missing. A m u lticu e ju d g m en t, like that o f
judging depth trom each ot several depth cues, is not rela­
tional since each cue can operate alone. However, a cue may
be ambiguous, or u n d erd eterm in ed . For example, a ju d g­
m ent o f a change in o b ject size based on a change in image
size is ambiguous because a change in image size can be due
to a change in o b jcct size or o b je ct distance. An am biguity
in one cue may be resolved by another cue. For example, the
am biguity o f image size as a cue to distance may be resolved
by binocular disparity.
Sensory inputs are d isso ciab le when judgm ents can be
made on the basis o f each one, at the same tim e as a judg­
m ent about the relationship betw een them. For example,
one can judge the orientation o f each o f two lines as well as
the angle betw een them . In binocular fusion, fused images
are n o n d isso ciab le because the visual system has no access
to the separate locations ot fused images, only to the dispar­
ity between them. The images are dissociable when the
disparity is beyond the range o t fusion.
Sensory inputs are in d ep en d en t when a jud gm ent based
on one input does n o t affect a judgm ent based on che
other. Ashby and Townsend (1 9 8 6 ) discuss types o f percep­
tual independence. G arner (1 9 7 4 ) distinguished between
in tegral and sep arable stimulus dim ensions. Integral
dimensions necessarily coexist, like hue and saturation,
while separable dim ensions may occur independently o f
one another, like shape and flicker.
For purposes such as com paring colors or chc orienta­
tions o f lines, the visual system seeks to isolate specific stim ­
ulus features. For other purposes, it is an advantage to have
cells that respond to a particular com bination o f stimuli.
A stimulus attribute that is defined in terms o f two or more
stimuli is a h ig h cr-o rd er feature. Sensory systems that
proccss highcr-order features fall into six classes.
1. Systems that detect relationships within a feature system
The visual system forms a hierarchy in which neural
signals within a given feature system com bine to form
detectors for increasingly com plex patterns. For
example, at a higher level o f processing, spatially
distinct stimulus elem ents are grouped into figures
according to the G estalt laws of proxim ity, continuity,
and similarity. D isconnected but aligned line elements
tend to be grouped to form a figure, especially when
 there is evidence that the elem ents appear disconnected
because o f occlusion. A t a still higher level the
conju nction o f line elem ents can define a corner,
a T -ju n ctio n , or a surface.
The visual system also constructs a hierarchy o f
spatiotem poral patterns progressing through simple
m otion and relative m otion to com plex Row fields. In a
sim ilar way the auditory system detects tones, chords,
d J 4
and melodies.
2. Systems jointly tuned to two or more features Many
cortical cells respond to more than one stimulus feature.
Responses are said to be sep arable when the tuning
function lor one feature is not affected by the value o f
another feature. Separable tuning simplifies the
detection o f variations in single features in a population
o f cells. Responses arc in sep arable when a cell is
responsive to particular com binations o f different
features (see Section 5 .6 .5 ). Such cells d etect high-level
features. For example, some cells in the m edial temporal
cortex ( M T ) respond to specific com binations o f
disparity and m otion (Section 11.5.2a).
3. Learned feature associations A t a higher level o f
processing we learn recurring associations between
features. For example, different con ju n ction o f color
and shape can be used to distinguish different objects.
M u ltid im en sio n al sca lin g deals with how we compare
and classify stimulus o b jects chat differ with respect to
cwo or m ore features (see Davison 1983). The differenc
features o f an o b je ct are processed by distinct
m echanism s buc muse be recognized as belonging со che
same o bject. This is the problem o f feature binding.
Associative learning involves Boolean operations o f
class inclusion and exclusion.
4 . Systems that detect stimulus covariance Judgm ents
based on detection o f covarying features o f rhe world
are referred to as percep tu al co n stan cies. The
constancies allow us со dececc invariant properties o f
the world in spite o f changes in the proximal stimulus.
A covariance can be a constant ratio, product, or
correlation becween stimulus elem ents or between
stim ulus features.
5. Nested sensory systems In a nested sensory system a set o f
sense organs is embedded in a series o f jointed body
parts. For example, the position o f che hand with
respect to the corso is indicated by the vector sum o f the
arm -joinc angles scaled by the lengths of the arm
segmencs. Similarly, che posicion o f a poinc o f lighc with
respect to the unseen torso is indicated by the vector
sum o f che retinal location o f rhe image, the direction o f
gaze, and the position o f the head on the body.
D etection w ithin a nested system involves vector
4
addition.
6. Multicue systems In many cases a given stimulus
attribute may be detected by distinct sensory
mechanisms. For example there are several distinct
sources o f inform ation about the relative distances o f
cwo objects. D etection w ithin a m ulticue system
typically involves weighted averaging o f inform ation
(Section 3 0 .1 ).
Each o f these types o f processing will now be consid­
ered in m ore detail.
4 .5 .2 R E L A T IO N S H IP S W IT H IN
A FEA TU R E SYSTEM
4 .5 .2 a C o n s tr u c tio n o f Low-Level
Feature D e te cto rs
At the retinal level, responses o f receptors are com bined to
form the receptive fields o f the various types o f ganglion
cells. Aligned ganglion cells form che orientated receptive
fields o f cells in che visual cortex. N eighboring ganglion
cells feed into cortical m otion detectors. These processes
are discussed in Section 5.6.2.
The processing o f sim ilar inputs from paired sense
organs provides the basis for some o f the m ost precise sen­
sory mechanisms known. D etection of binocular disparities
form s the basis for stereoscopic vision, as we will see in
Chapters 11 and 19. The deccccion o f incensicy and time
differences betw een sounds in the two ears forms the basis
for auditory localization, as we will see in C hapter 35.
4 .5 .2 b D e te c tio n o f Figural G rou p in gs
The ability to perceive coherent o b jects is basic to visual
perception. The G estalt psychologist M ax W ertheim er
(1 9 2 3 ) proposed several principles o f figural organization,
or visual grouping, to explain how a set o f isolated stimuli is
perceived as a coherent pattern (see KofTka 1935). These
principles are spatial or tem poral proxim ity, continuity,
sim ilarity o f form , com m unality o f m otion, and good figure
(Pragnanz), as discusscd in Section 4 .5 .1 0 a . We are more
sensitive to stimulus elem ents chac are pare o f a figure chan
to elem ents that arc part o f a background (Section 2 2 .1 .2 ).
We are parcicularly sensicive со collinear visual stimuli.
For example, collinear secs o f docs stand out w ithin an irreg­
ular array o f dots, as shown in Figure 4 .5 Л . People are also
sensitive to collincar points chat traverse a 3-D random
array o f points, when disparicy provides che only inform a­
tion about their collinearity (U tta l 1983; Hess c t al. 1997a).
However, people are more sensitive to collinear points lying
in one depth plane than to points that traverse several depth
planes. The stereoscopic im plications o f these effects are
discussed in S ection 16.6.
M organ and H o to p f (1 9 8 9 ) suggested that diagonal
lines seen running betw een che intersections o f regular grid
pacccrns are due со che activation o f collinearity detectors.
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F.j;urc «.5- D ela tio n ofA lign ed dots a n d lines. (A ) A ran d om p attern plus a
radially expanded copy form a radial Gla&s p attern . {G la ss a n d P erez
1 9 7 3 ) ( B ) A ligned elem en t* arc d etected m ore easily than elem ents
o rth o g o n a l to th e line throu g h the sec. T h e sets o f elem en ts arc shown
o n th e right. (RcdfAsvn from FicMcc.il. 19V?)

W c arc also particularly sensitive to aligned line clc-

m ents (Polar and Sagi 1994). Thus, aligned line elements
arc easy to d etect as a coherent figural grouping am ong ran­
dom ly oriented line elem ents, as can be seen in Figure 4.5 В
(Field et al. 1993). The line elem ents need n o t Ы1 on a
straight line b u t can form tangents to a curve. Furthermore,
the line elem ents may be a few degrees o u t o f alignm ent and
still be interpreted as belonging to the same figure. An array
of- line elem ents is m ost difficult to d etect when the lines arc
at 4 5 ° to the axis o f the array (Ledgeway et al. 2 0 0 5 ).
People can also detect aligned G abor patches in a
stereoscopic random array in w hich alternate patches lie in
different depth planes (H ess and Field 1995).
Sim ple recurring patterns, such as corners, T-ju nction s,
and intersections have specialized detection systems in
higher visual centers o f the brain (Section 5.8.3b ).
The perceived orientation o f an array of line elem ents is
distorted when the line elem ents are not aligned, as can be
seen in the well-known “crazy letters" illusion shown in
4
Figure 4 .6 A , or the Fraser spiral shown in Figure 4 .5 В
(Fraser 1 9 0 8 ). Pattern perception is subject to error arising
from nonlinear interactions, as in geom etrical illusions,
tilt con trast, and figural aftereffects. It is also su bject to
ambiguity, as discussed in Section 4.5.9.
C ells in the primary visual cortex that are tuned to the
same orientation are linked bvi excitatoryJ lateral conncc-
tions (Section 5.5.6a). Linkages are particularly strong for
»’i*ur< •.6. C on flict b etw een lo c a l a n d g lo b a l orien ta tio n . (Л ) Th с Ic t tc rs appear
tilted in the d irectio n o l the line elem ents. ( B ) T h e co n c e n tric rings
appear to form a spiral. (Adapted from Fraser 1908)
orientation detectors that not onlv* have the same o rien u -
rion tuning but also have aligned receptive fields (N elson
and Frost 1 9 8 5 ). These linked orientation detectors could
form alignm entdetectors responsible for modal and amodal
con tou r com pletion, as described in the next section.
H igher levels o f neural processing arc also involved in link­
ing the output o f these cells (Sheth et al. 1996; M attingley
ct al. 1997).
Human cortical areas V 3 , V 4, V 7 , and V 8 showed f M R I
responses to illusory contours (M endola ct al. 1 9 9 9 ). C ells
in V 2 and V 3 of alert monkeys responded selectively to the
figure-ground depth order indicated by line term inations in
overlapping rectangles (Baum ann et al. 1997).
M organ and H o to p f (1 9 8 9 ) referred to sets o f co n ­
nected orientation detectors with sim ilar orientation tuning
as c o lle c to r u nits. Field et al. (1 9 9 3 ) called them asso cia­
tio n fields. A m ore specific nam e for an association field
concerned with orientation is alig n m en t d e te cto r. One-
C angeneralize the idea to cover associations betw een other
feature-detectors. An association field o f collincar points
would be a c o llin e a rity d e tecto r. A n association field based
on the size or color o t texture elements could allow one to
perceive figures defined by these scimulus feacures. An
association field ot m otion detectors with sim ilar direction
sensitivities could underlie the perception o f shape defined
by m otion (the Cicstalt phenom enon o f com m on fate).
A set o f d etectors o f this type would form a m o tio n c o h e r­
en ce d e te cto r. D etectors o f binocular disparity could unite
points on a surface to form a co p la n a r d e te cto r (see Hess
c t al. 19 9 7 a ). The existence o f dececcors for differenc cypes
o f stimulus coherence makes the visual system particularly
sensitive to spatial and tem poral discontinuities, such as
discontinuities of contrast, m otion, texture, and binocular
disparity. A t a discontinuity, different coherence detectors
are stimulated or a region o f stimulus coherence is detected
against a region o f random stimulus elements.
4 .5 .2 c M o d a l and A m o d al C o m p le tio n
W e readily perceive an o b ject as com plete when parts are
occluded by o ther objects o r by parts o t the same o bject.
This is known as am od al co m p letio n . An o b ject with parts
occluded by another o b ject is more rapidly recognized
than the same o b ject with the same parts simply depleted
( Joh n son and Ohshauscn 2 0 0 5 ). The role o f am odal com ­
pletion in depth perception is discussed in Section 22.2.4.
C ells in che inferior tem poral cortex o f che monkey,
which responded when the animal recognized a shape, also
responded when the shape was partially occluded. Therefore,
these cells respond to amodal com pletion o f partially
occluded o b jects (К о vies et al. 1 995).
W e also sec an o b ject as com plete when parts ot it arc
invisible because the o b je ct has the same lum inance and
texture as the background. In ocher words, we sec a com -
plcte o b ject when part o f it is cam ouflaged. This is know n as
m odal co m p letio n . The apparently com plete contour is
know n as an illu sory co n to u r. Som e cells in area Vr2 o f the
visual cortex o f the monkey respond со illusory contours
(v o n d er H eyd tan d Pecerhans 1989).
4 .5 .2 d C o m p a rin g Spatially Separaced O b je cc s
We can readily discrim inace differences in a given feacure
bccween spatially separated stim uli. For example, we can
d etect differences in the relative positions, lengths, or orien­
tations o f two spatially separated stim uli presented at the
same tim e. There is evidence that discrim ination o f such
differences depends on specialized sensory systems thac reg­
ister sim ultaneous responses in cortical cells some distance
apart (M organ and Regan 19 8 7 ; K ohly and Regan 2 0 0 0 ).
These svstcms
t involve lateral connections betw een cortical
cells (Section 5 .5.6).
4 . 5 .2e Perception o f D y n a m ic Relationships
There arc dynam ic relationships between stim uli w ithin a
given feature. For example, the parts o t the human body
move in characteristic patterns (Johansson 1973). The
perception ot patterns o t m otion is subject to error. For
example, in induced m o tion , a stationary o b ject appears to
move when seen against a moving background (Section 22.7).
Patterns o f m otion may also be ambiguous. For example,
oblique, orthogonal gratings moving in opposite directions
past an aperture can be seen as a coherent plaid moving in a
direction and at a velocity that represent the vector sum o f
the com ponenc m otions, or they can be seen sliding over
each other (Section 2 2 .3 .3 ).
4.5.3 J O I N T I. Y T U N E D D E T E С T O R S
Responses o f cells in che visual corccx vary as a funccion o f
the location, orientation,spatial frequency, and direction o f
m otion o t a stimulus wichin chc reccpcivc field. Responses
со differenc feacures arc said со be sep arable when che
tuning function for one feature is noc affected by changes in
che value o f anocher feacure. The response o f chc ccll ac any
instant is the simple sum o f ics response to che values o f
che cwo feacures. The responses o f a ccll are in sep arable
when che cells tuning function to one feature is modified
bv che value o f a second feacure. This involves nonlinear
processing.
For example, morion dececcors in chc visual corccx show
space-time inseparability because there is a spatial shift o f
activity w ithin chc receptive field over tim e (Section 5.6.4).
C ells in the medial temporal cortex ( M T ) are disparicy-
m otion inseparable because chey arc tuned со particular
com binations o f disparity and direction o f m otion. For
example, they may be selectively responsive to m otion in a
particular depch plane relative to che plane in which the
eyes arc converged. There are cclls in V I and M T thac
respond to an o b ject approaching che head along a parti­
cular crajeccory (Seccion 3 1 .8 .2 ). Ic has been claimed
chac some cells in the visual cortex are sensitive to parti­
cular com binations o f temporal disparicy and spatial
disparicy. However, there is con flictin g evidence on chis
issue (S ectio n 2 3 .3 ).
4.5.4 AS SО С IAT I O N S В ET W EEN
D IS T IN C T FEATURES
4 .5 .4 a B in d in g th e F eatu res o f an O b je c t
Many objects have com binations o f characteristic features.
For exam ple, bees have a characteristic size, shape, noise,
and color. T ax o n o m ic featu res can be very com plex, as in
faces and in animal and plant species. W e have to discover
them and they often defy precise analysis.
The presence o f many visual areas, each devoted to spe­
cific features or parts o f a visual stimulus, raises the problem
o f how this distributed activity is synthesized into the per­
cept o f a single o bject. This has been dubbed the ‘ bin d in g
p ro b lem ” (H in to n et al. 1986). D ifferent visual objects are
juxtaposed and may overlap and move. Thus, a given pat­
tern o f neural activity is only fleetingly related to a given
stimulus o b je c t— che same cells may code features o f several
com plex objects in rapid succession.
The binding problem has tw o aspects. In the first place,
parts o f an o b ject occurring over many receptive fields must
be recognized as belonging to a single o b ject. This is spatial
b in d in g . For insrance, the boundary o f a large objecr stim u­
lates many orientation detectors, and their outputs must be
related to form a coherent percept o f che o b je c ts shape. The
role ot spatial interactions betw een cortical neurons in this
process was discussed in Section 4 .2 .6 c. In the second place,
objects possess concatenations ot visual features that must
be recognized as belonging to the same o bject. This is
featu re bin d in g.
It has been suggested chat feature binding involves chc
convergence ot diverse neural activities evoked by a given
ob ject o n to a single cell devoccd to recognicion o f chac
particular objecr. Such cells have been called g ran d m o th er
cells. Such a mapping process requires an impossibly large
number ot dedicated cells and connections. A t any instant,
only a tew o f the high-order cells would be active (the
coding would be extremely sparse).
A nother suggestion is that responses offeature-extracc-
ing systems in ditferent processing streams and at several
levels o f processing becom e bound into a particular spa-
tiotem poral pattern o f activity (Z ek i and Shipp 1988).
Each neuron participates in many ditferenc patterns, and
only che spatiotem poral response o f a particular cell assem­
bly is unique to a particular o bject. This is known as a
d istrib u ted rep resen tation . A distributed system can score
many m ore o b jects than there are neurons in the netw ork.
It has been proposed chac responses o f widely dispersed
neurons responding со che same objccc are bound by cheir
synchrony o f firing. However, che evidence for chc role o f
synchrony in stimulus binding is equivocal. It is difficult to
understand how synchrony arising from processing differ­
ent parts or features ot a given o b ject could be distinguished
from that arising from responses to unrelated objects that
are presenc a che same tim e (see Section 4.3 .4 c).
Proponents o f fea tu re -in teg ra tio n th eo ry suggest that
visual features and location are initially processed indepen­
dently and arc bound by an act o f accencion. For example,
chc accuracy in reporcing the colors o f objeccs was found to
be independent o f che accuracy o f reporcing their shapes
(Trcism an and Clelade 1 980).
O th er invcstigacors have produced evidence chac the
above eifect is due to difficulties in registering or recalling
the locacion o f stim uli chac are presenced for only a b rief
period. Joh n ston and Pashlcr (1 9 9 0 ) obtained only weak
evidence that identification o f an o b ject feature is indepen­
dent o f localization o f che objecc. Also, contingen t afteref­
fects (Section 4 .2 .9 c ) arising from inspection o f two
con join ed features are not affected by m anipulations o f
attention (H ouck and Hoffm an 1 986).
Feature-integration theory is supported by confusions,
called illu sory c o n ju n ctio n s, which occur when attention
is overloaded (Trcism an and Sch m id t 1 9 8 2 ). C onsider chc
follow ing examples.
First, when subjects arc asked to describe the color o f
briefly exposed letters they som etim es confidently report
seeing the letters in the wrong color. Evidence from patients
with a unilateral attention deficit has been equivocal, but
some studies seem to confirm that illusory conjunctions
occur in the hemifield affected by a unilateral attention
deficit (Arguin et al. 1994). Fricdm an-H ill ec al. (1 9 9 5 )
described a 58-year-old man with bilateral parieco-occipical
lesions who contused the colors o f simultaneously pre­
sented letters and objeccs, even when they were presenced
tor several seconds. He was also unable со report the relative
spacial posicions o f cwo o b jects displayed on a screen.
In the second example ot illusory conju nctions, a 12°
wide display o f red dots fianked by green docs moved
upward while a superimposed 12° wide display o f green
docs flanked by red docs moved downward. W h en looking
ac chc center o f the com bined display, subjects erroneously
reported that all che red docs moved upward and all chc
green docs moved downward. In ocher words, che conjuga-
cion o f color and mocion in che ccnccr o f chc visual field
decermined che perceived conjunccion o f features in the
periphery (W u et al. 2 0 0 4 ).
There has been some dispute abou t the interpretation o f
experim ents on illusory con ju n ctions (Tsai 1989; Green
1991). G reen (1 9 9 2 ) argued that a distributed process that
docs n o t require an act o f attention binds visual features
and copographic location directly and locally. The follow ­
ing arc som e factors, o ther than failure o f early feature
integration, chac may cause illusory conjunctions.
1. Som e illusory conjunccions could be due со unusual
persistence o f vision, so chac afterimages are carried
from one objccc со anocher as che eyes scan chc scene.
P alin o p sia is a clinical con d ition in which a visual
perception recurs after the o b ject has been removed.
Illu sory visual spread is an illusory spacial extension ot
a seen objccc (sec C ricchley 1955).
2. Som e illusory conjunccions could result from
inadequate visual resolution o f the stimuli. This may
have been a factor in the effect reported by Wu et al.
described in che previous paragraph. The stimuli that
showed the illusory conjugation were more than 6°
away from the fovea.
3. Som e illusory conju nction s could result from
confusions ac che level o f recall racher than at the level
o f perceptual registration.
The problem o f binding different features o f an o b je ct is
m ost severe if one adopts a strictly hierarchical model of
visual processing (W olfe and Cave 1999). A ccording to this
m odel, outputs o f distinct feature processing streams arc
united to reconstruct the visual scene, and only this recon­
structed scene is available to consciousness. The binding
problem is cased i f the visual system can access inform ation
from each o f the various processing stages and streams
according to the type and level o f analysis the perceiver is
perform ing. It is reasonable to assume that the spatial layout
o f the scene, simple feature d etection, and o b ject segrega­
tion are achieved in V I . Area V I is consulted when these
simple aspects o f the scene are being attended to.
High-level processing streams are engaged when atten­
tion is directed to specific features, o bjects, or events for the
recognition o f o b jects or events. Dam age to high-level cen­
ters may impair o b ject recognition while leaving visual
acuity and figure-ground segregation intact. Also, high-
level processing may be needed to disam biguate ambiguous
figure-ground relationships. For example, contours due to
shadows must be distinguished from those due to o b ject
boundaries, and o b ject boundaries may be partially occluded
o r cam ouflaged. Such problem s require high-level process­
ing because they usually require inform ation to be inte­
grated over wide areas o f the visual scene o r over a temporal
sequence o l scenes. The results o l attention driven high-
level processing feed back to and modulate the activity o f
cells in V I (Section 5 .6 .7 ). To-and-fro activity betw een all
levels o f cortical processing continues until the perceiver is
satisfied that objects have been recognized (Lee et al. 1998;
M oradi and Sh im ojo 2 0 0 4 ).
4 .5 .4 b Intersensory R elation sh ip s
A person may respond to relationships between stim uli in
different sensory modalities. The task o f judging som e attri­
bute o f a stimulus in one m odality with respect to the same
attribute in another m odality is referred to as cross-m od al
m atch in g. For example, we can set the length ot a seen rod
to match the length o f a rod estimated by touch.
The sense organs involved in an intersensory relational
task arc structurally in parallel with respect to a com m on
reference frame. The frame may be part o f the body, such as
the г body axis; an external reference frame, such as gravity;
o r a com m on internalized m etric, such as centim eters,
degrees o f angle, or straightness. O n e can think o f the speci­
fied stimulus attribute o f an object generating distributions
o f neural activity in the feature-detector systems o f each o f
the two sensorvi modalities. Each distribution will have a
mean and a variance. Intersensory discrim ination depends
on the least difference betw een the m eans o f the two distri­
butions that can be detected. Intersensory scaling depends
o n com paring tw o suprathreshold stimuli. Ideally, the vari­
ance o f an intersensory com parison task should equal the
sum o f rhe variances o f the tasks performed separately in the
two m odalities. C o n stan t errors should add algebraically.
In measuring intersensory discrim ination, subjects
should believe that the stimuli in the tw o sense organs arise
from different objects. O therw ise the stimuli will be per­
ceived as linked, and spatial offsets will n o t be detected. For
example, ifo n e hears a bell ringing and sees a bell, the sound
seems to com e trom the seen bell, even when the heard and
seen bells are up to 30 " apart. The ventriloquist effect does
n o t occur when the sound is not one that the seen object
would em it (Section 3 5 .6 .1 ).
In measuring intersensory discrim ination, the task
should be performed w ithout error feedback. O therw ise,
perform ance will improve with practice.
4.5.5 STIM U LU S COVA RIA N CE
Som e stimuli covarv systematically. As one stim uluschangcs,
one or more other stim uli change in characteristic ways. The
covariation may be defined by a correlation, a product, a
ratio, or by a more com plex relationship, such as m ultiplica­
tion after squaring. Judgm ents o f stimulus covariance are
relational because they cannot be performed unless both
sensory inputs are present. The following types o f stimulus
covariance may be distinguished.
4 .5 .5 a In cid en tal C o v a ria n c c w ithin
a Sen sory Svstem
The perceived features o f a stimulus can covary because o f
som e characteristic o f the visual system. For exam ple, the
chrom atic aberration o f the eye creates color fringes o f co m ­
plementary color on opposite edges o f an o b ject. We do not
normally n otice these color fringes. However, after lenses
that correct the chrom atic aberrations o f the eye have been
worn for som e tim e, color fringes becom e visible when che
lenses arc removed. Thus, there must be som e mechanism in
the visual system that com pensates for chrom atic aberration
(see Section 9 .1 .3 ). C hrom atic aberration varies with the
distance ot a stimulus trom the plane ot fixation and
therefore provides inform ation about relative depth
(Section 9 .6 .2 ).
4 .5 .5 b C o v a ria n c c B e tw e e n M o to r E ffc r c n c c
an d A ffe re n ce
We can regard the m otor command, or cffcren cc copy associ­
ated with a voluntary movement as a type o f sensory input.
A voluntary movement also produces stimulation o f sense
organs. For example, when we move our eyes, the image o f a
stationary object sweeps across the retina. Von H olst and
M ittelsraedt (1 9 5 0 ) called these forms o f sensory stimulation
reafference to distinguish them trom exaffcrencc, which is
sensory stimulation that does not arise from voluntary move­
ment. Eflcrence copy scaled by reafference expresses the invari­
ant relationship between voluntary m otor commands and
consequent sensory stimulation. Over many repetitions o f
voluntary movement, animals learn how cffcrencc and reaffer­
ence are related (von Holst 1954). The sight o f self-produced
movements o f the limbs plays a crucial role in infant develop­
ment (H eld and Bauer 1967; Bahrick and Watson 1985).
P rop rio cep tiv e reafferen ce consists o f stimuli from
jo in t receptors, muscle spindles, o r the vestibular system
that are correlated with voluntary m otor efference. Over
tim e we learn the relationships betw een efference and prop­
rioceptive reafference. A mism atch betw een the current
efference-rcafference relationship and rhe learned relation­
ship signifies the presence o f an external stimulus or force.
live m ovem ents generate proprioceptive reafference,
which provides an error signal for long-term calibration ot
the o cu lo m oto r system. K itten s wich section o f afferents
4
from the extraocular eye muscles suffer perm anent deficits
in visual-m otor coordination and depth discrim ination
(Section 3 2 .5 ).
E x tero cep tiv e reafferen ce consists o f tactile, visual, or
auditorv* stim uli that are correlated with m otor efference
arising from voluntary m otion o f some part o f che body.
We also learn whac stim ulation to expect trom a given self­
produced m otion. Л mism atch betw een expected and
actual stim ulation signifies that part o f the reafierent signal
is due to external events rather than to self-m otion. A per­
sistent m ism atch in either proprioceptive or exteroceptive
reafference signifies that the system is in need o f recalibra­
tion. This happens as the body grows during infancy or
is injured. Even a short period o f m ism atch between self­
produced m otion and reafierent visual or auditory signals
can lead to recalibration o f the system. For example, we
readily learn to adapt pointing responses со visual targets
viewed through displacing prisms (H ow ard 1 9 8 2 ).
An example o f stim ulus covariance based on exterocep­
tive reafference is as follows. T h e depch between tw o objects
equals che ratio o f che velocicy o f parallaccic m ocion between
the images o f the objects to the velocity o f sideways head
movem ent, scaled by the distance o f the nearer objccc
(Section 2 8 .3 ).
4 .5 .5 c Stim u lu s C o v a ria n cc and
Perceptual C o n sta n cie s
Many stimulus features covary in a characteristic way as a
tunction o f the position, orientation, or m otion ot an object
relative to che observer. Judgm ents based on such covarying
features are referred to as percep tu al co n stan cies. They
allow us со detect invariant properties o f the world as we
move about or as the stimulus o b ject moves. The basic prob­
lem o f perceptual constancy is to define the invariant fea­
tures in stim uli viewed from different vantage points and in
different sizes and locations (see Riesenhubcr and Poggio
1999). An experim enter must define these invariances before
asking whether observers use them , and that is not always
easy. 'I he following are examples o f covariance functions:
1. The size o f an o b je c ts retinal image is inversely
proportional to the distance o t the o b ject from an
observer. Size constancy refers to the ability to use this
relationship to estimate the linear size o f an o b ject at
different distances (Section 2 9 .2 .2 ).
2. For a small spherical o b ject moving toward an eye at a
constant speed, the rate at which its image increases in
size is proportional to the velocity o f its approach
and inversely proportional to the tim e to impact
(Section 3 1 .1 ).
3 . The binocular disparity produced by tw o objects
separated in depth by a fixed distance is inversely
proportional to the square o f the distance o f the
nearer o b ject from the observer (Section 14.2.3).
4 .5 .4 d C o v a ria n c e o f O b s e rv e r-In d e p e n d e n t
S tim u li
Som e features o f the world covary independently o f their
relation to the observer. A stimulus covariance may involve
a simple association w ithin a given feature system. For
exam ple, the direction and speed at which a ball moves
varies with the direction and speed o f an o b ject that impacts
it. A covariance may be betw een different sensory systems.
For example, the hotter it gets, the higher the m ercury in a
therm om eter. Som e covariance relationships are very co m ­
plex. For example, an em bryo changes in com plex interre­
lated ways as it develops.
W hen two or more stimulus features vary in a consis­
tent way one can define a function chac specifies che covaria-
cion.
The percepcion o f scimulus covariance is discussed fur-
cher in Section 4 .6 .3 .
4 .5 .6 N E S T E D S E N S O R Y S Y S T E M S
A nested sensory system consists o f sense organs embedded
in a series, or chain, o f join ted body pares. For example,
inputs from proprioceptors associated with che shoulder,
elbow, and wrist form an in trasen so ry nested system ,
which enables us to judge the 3 -D position o f the unseen
finger in relation to the torso (see M atthew s 1988). The
efference copy associated w ith active m ovem ent ac each
jo in t can also be regarded as a sensory input. The position o f
che hand wich respecc со che corso is indicaced by chc sum o f
che arm -joint vectors, with each vector scaled by the length
o f the segment o f the arm distal со che joinc (lm am izu ec al.
1 9 9 5 ; Pagano and Turvcy 1995). The lengchs o f limb
segmencs form part o f che body schema, or incernal repre­
sentation o f the body. This schema operates largely at a
preconscious level. Phantom limbs experienced by ampu­
tees illustrate that the body scheme is independent o f the
somesthccic-proprioccpcive syscem.
The nested sensory and m otor com ponents o f the arm-
jo in t system and eye-head system arc depicted in Figure 4 .7
 WRIST* EL BOW- SкKMJLDER EYE-HEAO-NECK
NfcSlfcU SYSTEM NESTED SYSTEM
4 Visual targe:
ExUaoeuta»
S m u sctes
^ * / т V V
V I • Torso
/ / I ••
SPATIAL / / V V V
CODERS "*V _
у !;
'F ^ b o R D I N ^ R ^ T ' ‘
Eyro-hard Hand-eye Sensory-sensory
A-------------------- ,
H1GHER-ORDER CONTROL
Figure 4.7. The eye-band I'oordinatioH system. Structural com ponents (b o ld )
arc linked by jo in ts with muscles and sense organs. Dashed lines arc
sensory or m otor nerves and short bars are neural centers. Spatial coders
process sensory input* and m otor cffcrcncc. Integrators process
inform ation from in-scrics sense organs or to in-series musclcs.
C oord inators relate sensory inform ation from the arm with that from
the eye-head system or relate sensory inputs w ith m otor outputs.
Examples o f cffcrcncc-copy and rcatlcrcncc signals arc shown.
together with coding processes responsible for relating the
tw o svstems
* in the control o f movement o f the hand to a
visual target.
A hand reaching for an o b ject moves in nearly a straight
path. This suggests that arm m ovements arc initially p ro ­
grammed in extrinsic coordinates that map the trajectory o f
the hand relative to the body, rather than in intrinsic jo in t
coordinates (Haggard et al. 1 995). Moreover, arm trajecto ­
ries involve intersensory co d in g , since they are planned in
terms o f their visually perceived straightness rather than in
terms o f their actual straightness (W olpert c t al. 1995).
M ovem ents must finally be coded into contractions o f mus­
cles. This is not a simple task, since the same arm position
can be achieved in many ways (So cch tin g and Terzuolo
1988).
Som e cells in the posterior parietal co rtcx o f the monkey
are influenced by proprioceptive inputs from two or more
arm joints (M ountcastlc c t al. 1 9 7 5 ). Som e cells respond
when the lim b is in a particular posture (C ostan o and
Gardner 1 981). These cells could serve as sensory integra­
tors (see Section 5 .8 .4 e ). Som e cells in the prem otor cortex
and basal ganglia respond to the direction o l an arm move­
m ent irrespective o f the muscle pattern used to im plem ent
the movement. These arc m otor integrators. The transforma­
tion into a pattern o f muscular contractions at the level o f
m otor coders depends on both the direction o f movement
and the load opposing the m otion. The transformation is
probably achieved by other colls in the prcm otor cortex,
basal ganglia, and cerebellum (see Georgopoulos 1991).
An example o f an in tersen sory nested task is that o f
judging the direction o f a visual object with respect to the
torso by vector addition o f the local sign ot the retinal
image, and the sensed positions o f eyes in head and o f head
on body (see Figure 4 .7 ). The system is subject to constant
errors, especially when the eyes are in an eccentric position
(R ossetti e t al. 1994). The position and m ovem ent o f the
/
eyes is registered by cfference copy, or corollary discharge
(Som m er and W urtz 2 0 0 2 ). Proprioception may also be
involved (Steinbach c t al. 1988). The position o f head on
body is coded mainly by proprioception, bu t etference
could be involved. Th e spatial coders process inform ation
trom each sense organ or generate the m otor com m ands to
muscles at each jo in t. Integrators process inform ation from
a set o t nested receptors or generate coordinated m otor
outputs to the neck muscles and extraocular muscles.
Spatial inform ation from the eyes and other sense organs
is integrated at several levels in the nervous system. Sonic
cells in the posterior parietal cortex (areas 5 and 7 ) o fth e
m onkey are influenced by proprioceptive signals from both
the eyes and the neck, and seem to be concerned with
coding the bodycentric direction o f gaze (B ro tch ic c t al.
1995). Visual inputs and eye-position inform ation interact
at various subcortical and cortical sites (Section 18.10).
Such cells could serve as spatial integrators for rhe headcen-
tric direction o f visual stimuli (Andersen and Zipser 1988).
Som e cells in the parietal lobe and prem otor cortex respond
to visual and tactile stimuli that arise from the same
location (Section 5.8.4g ).
Nested systems adapt to the growth o f the body, and to
unusual sensory inputs. For example, people readily adapt
their pointing to visual targets seen through a displacing
prism (Howard 1982). A P E T scan o f the human parietal
cortex has revealed changes associated with such learning
(Glower c t al. 1996). W h en an optical system gradually dis­
torted the visual trajectory ot the hand into a curve, subjects
unconsciously adapted the reaching m ovem ent to maintain
an apparently straight path (Flanagan and Rao 1995;
W olpert c t al. 1995), although the path that visually appeared
straight was not actually straight (W olpert ct al. 1994).
A nested system is com m utative if the tem poral order o f
operations does n o t affect the outcom e, as for rotations ot
the eyes, head, and torso on vertical axes. R otations o f an
eye about three hypothetical gimballed axes o f horizontal
gaze, vertical gaze, and torsion are noncom m utative, since
the final position o fth e eye depends on rhe order in which
the movements occur. Eye movements are com m utative
if they occur only about axes in a plane fixed to the head—
L istings plane (Section 10.1.2d).
 Tasks performed by vector addition w ithin a nested sen­
sory system are relational and dissociable. For example, the
task o f judging chc position o f the hand relative to the torso
is relational since inform ation trom all the join ts is required,
and ic is dissociable because a person can judge chc angle ac
any jo in t as well as the position o f the hand relative to the
body. The com ponents o f nested syscems are typically inde­
pendent in the sense th at a judgm ent o f rhe scace o f one
com ponent does n o t affect that o f another.
C o n stan t errors o f judgm ents based on che com ponencs
o f a nested syscem should sum algebraically to produce the
constant error o f a judgm ent o f che relationship between
com ponents. For example, directional errors in the local-
sign system o f the retina, in che sense o f position o f the eye,
and in the sense ot position ot the head on the torso should
add to produce che overall error in judging the direction o f
a visual o b je ct relative to the unseen body (Section 16.7).
The variance o f judgm ents based on the separate co m p o ­
nents should sum to produce the variance o f the relational
judgm ent. This is che addicive v arian ce hypothesis.
4 .5 .7 M U L T 1С U E S Y S T E M S
4 .5 .7 a T h e N ature o f C u es
Som etim es, the same percept is generated by different
sources o f sensory inform ation. For example, a percept ot
self-rotation is produced by stim ulation o f the semicircular
canals o f the vestibular sysccm or by m otion o f the visual
scene. The m ultiple cues that indicate depth are the main
concern o f Volume 3.
Perceptually equivalent sources o f in form ation are often
referred со as cu cs. But the term “cue” is ambiguous. It can
refer to a property o f the distal stimulus or o f the proximal
stimulus, or it can refer со one o f the sensory processes that
code the proximal stimulus. For exam ple, a cue can be an
approaching o b ject, a change in the size o f the objeccs
image, or one o f the sensory processes that code changing
image size. O n e o f these sensory processes involves registra­
tion o f changing area, and another involves registration of
m otion. These processes are independent. O n e can change
area w ithout stim ulating m otion dececcors by using discrete
increm ents or equilum inant stim uli. Also, one can create an
impression o f increasing area in a m otion aftereffect from a
rotating spiral w ithout changing the area o f the image. The
m otion syscem icsclf may consist o f several morc-or-lcss
independent sensory channels, such as short-range and
long-range m otion detectors. W c could call these m otion
channels different cues to m otion.
4 .5 .7 b Types o f M u lticu e System
In a m ulticue system, there are tw o or more relatively inde­
pendent types o f sensory inform ation for a response to or a
judgm ent abouc a specified scimulus accribute. For example,
judgm ents o f the relative depth betw een tw o objects may
be based on binocular disparity, perspective, accom m oda­
tion, and o b ject overlap. The sensory systems involved are
structurally in parallel rather than nested.
M ulticue judgm ents are n o t relational, since chey may
be based on any one o f the cues in isolation. M ulticue sys­
tems can be incrascnsory or incersensory. Incrasensory mul-
cicuc judgm ents are typically nondissociable. For example,
we do noc have separate access to depth impressions gener­
ated by each cue to depth when they arc presented together,
bu t only to a single impression o f depth. The com bination
o f the cues is obligatory. D ifferent com binations o f cues can
give rise to the same percept. Thus one cue may be traded
against another. The difference cucs arc therefore com bined
metamerically. C o m bin in gcu es this way improves discrim i­
nation. H illiset al. (2 0 0 2 ) produced evidence th at intrasen-
sory shape judgm ents, such as judgm ents o f the shape ot an
o b ject by binocular disparity and perspective, arc nondis­
sociable. However, they tound that intersensory shape
judgm ents, such as judgm ents o f the shape o f an o b ject by
vision and by touch at the same tim e, are dissociable. The
com bination o f intersensory inform ation is n o t obligatory.
This makes sense, because an o b ject we are feeling may not
be the o b ject that we are looking at.
Three broad types o f m ulticue system may be
distinguished.
Type J Convergence o f low-level signals
Relatively simple signals from distinct sense organs
som etim es converge at an early stage o f processing со pro­
duce a signal chac controls a relatively simple response or
judgm ent. For example, the accom m odative response o f the
eye is jointly controlled by blur o f the retinal image and che
state of vergence o f the eyes (Section 10.4). Visual signals
arising from m otion o f the w hole visual scene generate
optokinetic nystagmus and inputs trom the sem icircular
canalsgenerace vestibular nystagmus. Visual m otion signals
and vestibular signals converge on cells in the vestibular
nucleus so as to join tly control nystagmus. W e will see in
Section 22.6.1 that signals from the stereoscopic system
also feed into chiseyc-m ovem enc sysccm. Anocher example
o f low-level convergence is chc convergence o f interaural
intcnsity-differcnce signals and interaural tim e-of-arrival
signals in the olivary nucleus for detection o f the direction
o f a sound source (see C h ap ter 3 5 ).
Type 2 Convergence of high-level signals
D istin ct complex signals from the same sense organ or
from different sense organs may provide inform ation about
the same feature o f a distal stimulus, such as its three-
dim ensional structure. Although the different signals p ro ­
vide inform ation about the same distal stimulus, they are
processed in different locations and may differ in their sta-
bilicy, ambiguity, and range. Therefore, high-level neural
processing is required to com bine these diverse sources o f
inform ation into a single percept. Cells that respond in the
same way to diverse signals associated with a single percept
are said to be featu re invariant.
Type Systems involving categorical judgm ents
In the lirsft tw o types it was assumed that the judgment
o r response varied continuously over a range o f values.
However, many judgm ents are categorical in that they fall
into tw o or more discrete values. For example, phonemes
can vary continuously, but a speaker o f a given language
perceives discrete categories. Similarly, strokes in written
letters can vary continuously bur readers see distinct letters.
W h en a phonem e or letter stroke falls on the decision
boundary between tw o categories there is categ o ry a m b i­
guity. For example, when a sound is interm ediate between
a “b” and a “d,” listeners hear one or other phonem e accord­
ing to the context.
Systems involving discrete stimulus values necessarily
involve categorical decisions. For example, which o t two
objects overlaps the other is a discrete variable and gives rise
to a categorical response o t the occluding o b ject being in
fron t o f the occluded o b je ct (Section 2 7 .2 ).
Studies o f m ulticue systems have been concerned with
the follow ing issues:
1. Early convergence o f sensory signals (Section 4 .5 .7 d ).
2. Sensory summation an d masking O n e issue is whether
the detection threshold is lower for a stimulus seen by
both eyes than tor a stimulus seen by only one eye, after
making allowance for the increased statistical
probability o f detection with two eyes (Section 13.1).
Л second issue concerns the circum stances under
which different stimuli interfere with each other
(Section 13.2).
3. Multistable percepts The issue under this heading is
w hether rhe stability o f o n e interpretation o f an
ambiguous stimulus is influenced by the addition ot
other inform ation. The stability o f a percept is indicated
by three factors, (a) its latency, (b) its probability ot
occurrence on different occasions, and (c) its resistance
to spontaneous change (Section 4 .5 .9 ).
4. Creation o fa commonframe o f reference O b jects may be
detected by tw o o r m ore sense organs that operate in
distinct fram es o f reference. For example, sound sources
are coded in a hcadccntric fram e o f reference, whereas
the seen o b ject making the sound is initially coded in a
retinal fram e o f reference. These d istin ct frames o f
reference are reconciled in the superior colliculus and
posterior parietal co rtex for the purpose o f directing the
eyes or hands to an o b ject (Section 5.8 .4 c). There is
evidence that tactile and visual stimuli are transformed
into a com m on frame o f reference in the prem otor
cortex (G raziano and G ross 1998).
5. Multisensoryjudgments o f stimulus magnitude The issue
is how dilferent sources o f inform ation com bine to
determ ine the perceived m agnitude o f a stimulus
attribute. D o they com bine additively, by averaging, by
a m ultiplicative process, by use o f the m ost reliable
in fo rm atio n ,o r in some other way? This issue is
discussed in the next section.
4 .5 .7 c M u lticu e Averaging
According to the central tendency theorem , the best esti­
m ate o f a quantity is the mean o f independent sources o f
inform ation. If one source is more reliable than another, the
best estimate is a weighted mean. In assigning weights to
sensory cues it is im portant to define the judgm ent. A cue
with high weight for ordinal judgm ents may contribute
nothing to quantitative judgm ents. For example, the over­
lap cue to depth has high reliability for judgm ents o f depth
order but provides no inform ation about the m agnitude o f
relative depth. O n the other hand, relative m otion betw een
the front and back o f a transparent rotating o b ject provides
reliable inform ation abou t relative depth but is ambiguous
with respect to which is the fron t and which is the back o f
the o b ject (Section 2 6 .7 ).
The defining characteristic o f an averaging system is
that sensory inform ation is summed and divided by the
num ber o f inputs. If the strengths o f tw o cues are л, and s,
and their weights arc w and u\, cue averaging can be
represented by
+U'lS2
w , 4- H'2
Division by the sum o f che weights converts them into
relative values, w hich sum to unity. Any constant error in
one cue system will distort the judgm ent in proportion to
the num ber o f cues involved and the weight given to each.
W eights assigned to cues may vary with their m agnitude or
with changes in features such as spatial and tem poral fre­
quency. In that case, cue averaging is nonlinear (Anderson
1974).'
I f tw o sources o f inform ation that code the same quan­
tity are com bined in the m ost efficient way, the reciprocal o f
the total variance should equal the sum o f the reciprocals o f
the com ponent variances (Fisher 1966). Thus the reciprocal
o f the variance o f a judgm ent based on averaging cues Л and
R ( K . ) should equal the sum o f the reciprocals o f che
variances o f judgm ents based on each cue separately, or:
1 _ 1 J_
Ум ~ У АЛ У»
This means that judgm ents based on several cues should
be more precise than those based on one cue.
In a cue-averaging system, two or more cues provide
independent estim ates o f the same continuously variable
stimulus feature. Lack o f agreem ent betw een the estimates
constitutes a mutual error signal. In the absence o f other
inform ation, the observer can n ot know which estim ate is
correct. For small discrepancies, the best strategy may be to
use a weighted average. However, even in statistics, averag­
ing may not be the best strategy when tw o estim ates differ
widely. It is usually better to question the validity o f one ot
the estim ates. Large discrepancies betw een cues are resolved
either by cue averaging or in one o f the other ways discussed
below.
C onsider first som e examples ot cue averaging.
Images in the tw o eyes that have a binocular disparity
appear in an interm ediate direction that depends on their
relative luminances. The same images appear in distinct
directions when they are seen one at a time (Section 16.7.3).
The apparent brightness o f an evenly illum inated
surface viewed with both eyes is a weighted mean ot
the brightness o f the images seen by each eye separately
(S ectio n 13.1.4).
These examples are Type 1 m ulticue systems (low-level
convergence), since stimuli are ncurally com bined at an
early stage. They are nondissociable. In other words, we do
n o t have access to the tw o sources o f inform ation, which
may be regarded as repeated measures o f the same quantity.
Averaging ot inputs occurs m ost clearly in such cases and
shows evidence o f being reasonably linear.
In more com plex cases, cue averaging is likely to be n o n ­
linear. For example, the location or m otion o f a visual co n ­
tour may be defined in terms o f the visual attributes o f
lum inance, color, m otion, texture, or binocular disparity.
Th e literature on how precisely wc discrim inate shapes
defined by different features is reviewed in Regan (1 9 9 1 b ,
1999). Rivest and Cavanagh (1 9 9 6 ) found that the preci­
sion o t localization o f a contour improved as more
attributes were added. Rivest c t al. (1 9 9 7 ) found that
im provem ent ot orientation discrim ination with practice
transferred betw een bars defined by color, by lum inance,
and by m otion. These findings support the idea ot a pooling
o f inform ation from the different featurc-detcction systems
w ithin the same sensory m odality, but the pooling is highly
nonlinear.
The relative distances o f objects in depth may be derived
from any one or any mixture o f a variety o f depth cucs
including binocular disparity, visual parallax, and perspec­
tive. It has been claimed that depth cues either add or aver­
age. For example, Bruno and C u ttin g (1 9 8 8 ) reported that
perceived relative depth between simple squares is based on
the sum o f the m onocular cues o f size, relative height, occlu ­
sion, and m otion parallax. However, M assaro (1 9 8 8 ) inter­
preted the data according to a model in which perceived
depth is based on che m ost reliable cue. See Section 2 8 .1 .2
for m ore discussion o f this issue.
Experim enters som etim es assume that a given cue is
absent when it is held at a value o f zero while o ther cues are
varied. But this is a false assumption. For example, the
cue o f changing image size to m otion in depth is not
absent when image size is held con stan t, because constant
image size is a cue that a stimulus is n o t m oving in depth
(S ectio n 3 1 .3 .1 ).
Nonlinearity in cue averaging may arise for the following
reasons:
1. The strength o f a cue may vary in a nonlinear fashion
with respect to the judged feature. For example,
vcrgcncc increases with decreasing viewing distance
according to a tangent function. This means that
vcrgcncc can be a cue to distance only over short
distances. The relative binocular disparity between the
images o f tw o o b jects decreases as a function o f distance
squared.
2 . Cues may be affected in different ways by changes in
associated sensory features such as spatial frequency,
contrast, or color. For example, depth cues such as
overlap and disparity operate in both the lum inance
and chrom atic dom ains, while others, such as shading,
operate in only the lum inance domain (Cavanagh
1987).
3 . Tlie weighting function for cue averaging may vary with
the level o f agreem ent betw een cues. The cue-averaging
system may be switched o ff when cues are highly
discrepant. For example, Zacharias and Young (1 9 8 1 )
suggested that vestibular and visual cues to self-rotation
arc averaged when they arc consistent, but that one cue
is ignored when they are highly inconsistent.
4 .5 .7 d M u lticu e T rad in g
W hen distinct stimuli generate the same perceptual effect,
changing one stimulus can som etim es null the effect o f
changing the other. For exam ple, the sensation o f a sound
source in a particular direction relative to the body midline
can be generated by a difference in tim e o t arrival o f sounds
at the two ears or by an interaural difference in sound inten­
sity. An apparent displacem ent o f a sound source produced
by an interaural tim e difference can nulled (titrated ) by a
displacement produced by an intensity difference and vice
versa (H arris I9 6 0 ). The set o f null points for different
values o f each sensory cue defines a trad in g fu n ctio n
in m icroseconds per decibel. Examples o f a trading fu nc­
tion in stereoscopic vision are titration o f binocular dispar­
ity against m onocular parallax (Section 3 0 .2 .5 ) or against
perspective (Section 3 0 .3 ).
C u e trading is convincing only when the two cucs inter­
act in a continuous fashion. Titration o f one cue against
another allows one to investigate the degree o f equivalence
betw een cues and their relative efficiency. The existence o f a
cuc-trading function is evidence that inputs from two cue
systems converge to produce a signal com m on to both.
 C u e trading is m ost evident in Type 1 (low-level conver­
gence) m ulticue systems. For exam ple, interaural intensity
differences are converted in to tim e differences because the
m ore intense sound is processed with shorter latency. This
tim e difference and the tim e-of-arrival difference arc then
converted in to the same position-dependent signal by a
delay line in the olivary nucleus (Van Bcrgeijk 1962).
In o ther cases, cue trading may occur in the integration
o f discrepant signals from different cue systems at a higher
level o f processing. For example, m otion-in-depth produced
by image expansion can be traded against m otion-in-depth
produced by changing disparity (G ray and Regan 1996).
This topic is discussed in Section 3 1.3.4.
C u e averaging and cue trading occur convincingly only
betw een cue systems that generate sim ilar signals at a rela­
tively early stage o f processing. O th er m ulticue systems
resolve large discrepancies by one o r other o t the following
processes.
4 .5 .7 e C u e C o n firm a tio n and Percept Stab ility
Som e m ulticue systems do not average but simply confirm
o r supplem ent one another. C ue confirm ation operates
m ost clearly in Type 3 (categorical) m ulticue systems in
which the task is that of interpreting b ista b le p ercep ts or
recognizing discrete stim ulus categ o ries. Cue confirm a­
tion operates like voting, where weighted values o f the vari­
ous cues are summed to determ ine the strength o f a given
interpretation o f the stimulus. Since the alternative inter­
pretations are discrete, the pooled voting strength o t the
different cues determ ines the sta b ility o f a given interpreta­
tion, n o t its m agnitude. An interpretation is stable when it
has a high probability o f recurring under similar circum ­
stances, has low latency, and does n o t change as the stimulus
is m aintained.
The reversible perspective ot a 3 -D skeletal cube pro­
vides an example o f cue confirm ation for a bistable percept.
Perspective reversals occur m ore frequently when the cube
is viewed m onocularly rather than binocularly (Howard
1 9 6 1 ). The stability o f a particular depth interpretation o f a
bistable 3 -D cube depended on the additive contributions
o t disparity and the relative contrasts o f tar and near sides.
The m agnitude o f perceived depth was noc affected, only ics
sign (Sperling and D osher 1 9 9 5 ).
A n example o f cue confirm acion for a cacegorical judg­
m ent is the increased certainty about what word is spoken
when we can both hear the speaker and see the lips moving.
Th e tw o sources o f inform ation do n o t average since they
arc n o t com posed o f continuous variables. U nder normal
circum stances, they simply confirm each other, and supple­
m ent each o ther if one or the other source is weak.
Perform ance on this type o f cask involves high-level stim u­
lus categories stored in memory. It the word heard does not
prom pt recall o f the same word as that prom pted by sight o f
the speaker s m outh, as in a badly dubbed movie, the system
accepts the least noisy stimulus w ith a bias toward the word
that best fits in to the con text o f other words spoken.
It iseasy to confuse acue-confirm acion mechanism with
cue averaging in a Type 3 (categorical) m ulticue system. For
example Trueswell and Hayhoe (1 9 9 3 ) concluded that the
magnitude o f perceived depth betw een tw o squares is an
average o f inform ation from disparity and overlap (Section
3 0 .4 ). However, they measured the probabilities o f seeing
each interpretation averaged over trials, not the magnitude
o f perceived depch. The averaging was done by che experi­
menters, not by the subjects.
Thus, in depth perception, we may accept the m ost
highly weighted cue and the one m ost consistent with other
inform ation and then seek for confirm ation in ocher cues.
If the other cues to depth do n o t agree, they may be reinter­
preted or ignored rather than averaged wich che m ost
reliable cue.
4 .5 .7 f C u e R c in c c r p rc ta tio n
A co n flict between cues to a particular stimulus feature may
be resolved by a reincerprecacion o f the stimulus situation.
This happens in a Type 2 (high-level convergence) multicue
syscem when a change in a stimulus feature is ambiguous, or
u n d erd eterm in ed . For example, a change in the size o t the
image o f an o b ject could arise from m otion o f chc o bjecc in
depch, buc ic could also arise because che objecc is changing
in size. Thus, a change in image size is an elem ent in two
in tersectin g co v arian ce fu n ctio n s; the invariant relation
between image size and distance for a given o bject, and the
invariant relation betw een image size and o b ject size for a
given distance.
The following rule could operate. W h e n there is a severe
co n flict betw een tw o cues to a stimulus feature, the more
ambiguous cue will be reincerpreced. If neither cue is am big­
uous, a con flict causes a recalibration ot the cue systems
rather chan a reincerprecacion. C u e recalibracion is discussed
below. Cue reinterpretation can be continuous or saltatory,
as che follow ing examples will show.
W h en a change in the size o t the images ot an object
m atches the changing disparity between the images, we see
an o b ject o f fixed size moving in depth. But i f the images
change in size w ithout an equivalent change in relative dis­
parity, then the o b ject appears to change in size by an
am ount that accounts for that discrepancy. This reinterpre-
tation resolves the con flict betw een cues to depth because
the com pon ent o f changing size that is noc com m ensurate
with changing disparity is no longer accepted as a cue to
depth. There would be a residual perceptual co n flict only if
che o b ject were noc expecced со change in size, or if ocher
sensory inform acion, such as taccilc inform ation, signified
chac ic was nor changing in size. The residual discrepancy
may be resolved in another way. For instance, the object
may be perceived as nearer chan ic is because a given change
in disparity produces a smaller change in image size tor a
nearer objccc chan for a far objccc. The general principle is
thac enunciated by H elm holtz (1 9 1 0 , vol. 3, p. 2 ), “such
o b jects arc always imagined as being present in the field o f
view as would be there in order to produce the same impres­
sion on the nervous m echanism , the eves being used under
ordinary normal conditions." This proposition is given
quantitative expression in Bayesian analysis described in
Scction 3.6.
In the above example, cue reinterpretation involves
reassigning a change in a particular scimulus feacure from
one covariance function to another, where both functions
em body distinct continuous variables (Type 2 high-level
systems). In the following example, cue reinterprctation
involves a change o f state o f a two-valued feature (Type 3
categorical system).
Л wire cube spontaneously reverses in apparent depth
when viewed for some time. After it reverses, the cu b e’s per­
spective is reinterpreted to conform to its new depth. If the
cube is rotating, each reversal o f perspective changes the
percept from that o f a rigid cube rotating in its actual direc­
tion to that ot a nonrigid trapczoid rotating in the opposite
direction (Howard 1 9 6 1 ; Sperling and D o sh cr 1995).
4 .5 .7 g C o m p le m e n ta ry M u lticu e System s
D ifferent sources o f informacion may com plem enc each
other, each providing som ething lacking in the other. The
following are som e o t the ways in w hich this can happen:
1. Disambiguation o f cue attribution The ambiguity in one
sensory cue can be resolved by a second cue. For
example, a given o to lith input may be produced by head
acceleration or by head tilt. This am biguity manifescs
itself in the inability o f pilots flying in clouds to detect
w hether the aircraft is accelerating or clim bing. The
am biguity may be resolved by sight o f the ground or by
inputs from the sem icircular canals, which register head
rotation bu t n o t linear acceleration.
Prior exposure to an unambiguous stimulus may bias
the interpretation o f an ambiguous stimulus. For
exam ple, prior exposure to a corrugated surface
defined by the unambiguous cue o f binocular disparity
biases the perceived depth o l a corrugated surface
defined by the ambiguous cue o f m otion parallax
(S ectio n 2 1 .6 .2 b ).
2. Disambiguation o f stimulus sign Som e cues are
ambiguous with regard to sign but n o t w ith regard to
m agnitude. H ie am biguity o f sign may be resolved by a
second cue, w hich is often a two-valued stimulus
lacking quantitative inform ation. For example, image
blur is an am biguous cue to lens accom m odation,
because an o b je ct nearer than the focal point produces
the same blur as one beyond the focal point. The sign o f
chrom atic aberration o f the lens resolves the ambiguity
(Scctio n 9 .8 ). In a second example, the am biguity o f the
sign o f depth perspective is resolved by the two-valued
cue o f stimulus overlap (Section 3 0 .4 ).
3. Complementary ranges Mu Itiple cues typically extend
the stimulus range o f a feature-detecrion system. This is
because one cue may be more effective at one end o fth e
stimulus range, and a second may be more effective at
the other end. For example, binocular disparity is most
effective for near viewing, while perspective remains
effective for distant viewing. Also, the effectiveness o f a
cue tor a given stimulus feature may differ as a function
o f some other stimulus feature. For example,
accom m odation becom es an ineffective cue to distance
for stim uli with low spatial frequency, while perspective
is relatively immune to a lowering o f spatial frequency.
4. Filling in O n e cue may fill in for a second cue that is
hidden or not attended to. For exam ple, sight o f
som eone speaking may help us to recognize a word that
is difficult to hear. M ultiple cues p ro tect against loss or
pathology o f one cue system.
5. Provision o f an error signal O n e cue may provide an
error signal that is absent in another cue. For example,
the cxtraocular muscles provide little or no feedback to
indicate the adequacy o f the vestibulo-ocular response
induced by head rotation in the dark. If the eyes arc-
open there is an error signal in che form o f recinal slip
velocity.
4 . 5 .7 h C u e D o m in a n ce
M ore reliable cues arc m ore heavily weighted in a con flict
situation. This is known as cue dom inance. In extrem e cases,
one source o f inform ation com pletely overrides conflicting
inform ation. For exam ple, when a bell is seen in one place
and heard in a place less than 30° o f subtense away it seems
to be located where it is seen rather than where it is heard.
This is the basis o f ventriloquism . W hen a felt o b ject is o p ti­
cally m inified it feels smaller than when viewed normally
(R o c k 1965).
4 .5 .7 i C u e D issociation and A lternation
W hen the co n flict betw een two cues is severe, the cues may
dissociate and create an impression o f two objects. This can
happen in one sensory modality. For example, when the
interaural delay cue and the interaural intensity cue to the
direction o f a sound source are widely different, one hears
two sounds. C u e dissociation also occurs for cues in differ­
ent modalities. For example, a seen bell more than 30° away
from a heard bell dissociates into two, a seen bell in one
location and a heard bell in a second location.
Instead o f becom ing dissociated, discrepant cues may
alternate. For example. Van F.e et al. (2 0 0 2 ) found that.
when chc cucs o f disparicy and perspective со chc slant o f a
surface in depth were highly discordant, many subjects
alternated bccwccn seeing slanc appropriace со disparicy and
slanc appropriate со perspective.
4 .5 .7 j C u e R e c a lib r a tio n
C u e con flicts may lead со long-cerm recalibracion o f m u lti'
cue syscems. This is mosc likely со occur when both cues are
unambiguously related со a given percepcual incerprecacion.
For example, an unusual relationship betw een convergence
and fam iliar size affects che scaling o f perceived dcpch
( O ’Leary and W allach 1 980). Л change in perceived dis-
cances o f objeccs, as revealed by pointing wich unseen hand,
was produced in subjects who inspected cheir own feet tor
3 m inutes chrough base-out prisms (C raske and Crawshaw
1974) (see Section 2 5 .2 .6 b ).
4 .5 .7 k R e c r u itm e n t o f N ew C u c s
In early developm ent, animals learn to use sensory inform a­
tion. Evidence reviewed in Section 33.8.1 indicates chac
animals can learn C o use novel sensory inform ation. But
w hat evidence is there that human adults can learn to rccruic
novel cues chat affect che way chey perceive. H aijiang ec al.
(2 0 0 6 ) exposed subjects to a rotating wire cube with
all depth cues present. W hen the objective direction o f
rotation was reversed che locacion o f che cube o r ics direc­
tion o f cranslacion was changed. After 45 m inutes, each
o f these added cues to che direction o f rocacion affected
the apparent reversal in direction in a cube lacking depth
inform ation.
4 .5 .7 k S u m m ary*
This section provided a classification o f che ways in which
sensory inform ation is com bined within and bccwccn sense
organs. Roughly speaking, inpucs from nested systems com ­
bine by vector addition,com parative judgmencs are derived
by subtraction, the detection o t invariants and scaling o f
one inpuc by another are achieved by division or m ultiplica­
tion, and multiple cues to the same judgm ent may be com ­
bined by averaging. However, cue averaging occurs only for
signals that signify continuous changes in the same stimulus
variable. Signals that indicate discrete values, such as depth
order, com plem ent each other, strengthen a given interpre­
tation o f a stimulus, o r reduce am biguity, rather than engage
in averaging. C u e conflicts are resolved in cerms o fc u e trad­
ing (averaging), by reintcrpretation o f covariancc functions,
by cue dom inance, or by dissociation. The ways in which
sensory inform ation and cffcrencc are com bined, whether
by addition, subtraction, m ultiplicative scaling, or averag­
ing, depends on the physical organization ot the sensorim o­
tor systems but also on the purposes for which the
inform ation is being used. In any case, sensory inform ation
is often com bined in a highly nonlinear fashion, which
defies simple analysis. A fuller account o f intersensory sys­
tems is provided in Howard (1 9 9 7 a ). Interactions between
different sources o f inform ation for the perception o f
relative depth are discussed in C hapter 3 0 .
4 .5 .8 T H E S IT E AN D O R D E R O F
V IS U A L P R O C E S S E S
4 .5 .8 a L o ca tin g Visual Processes
Psycho physically
The following tests have been used to reveal w hether an
effect occurs in the recina or the cortex.
1. Interocular transfer An induction stimulus is presented
to one eye for some tim e followed by a test stimulus
presented со che ocher eye. It is argued thac any
interocular transfer o f the effect produced by the
induction stimulus must arise in binocular cclls in the
visual cortex. Tins argum ent is n o t always valid. An
afterimage shows intcrocular transfer, in the sense that
an afterimage impressed on one eye is visible when chac
eye is closed and the other eye is open. This does not
prove that afterimages are cortical. It simply means that
activity arising in a closed eve still reaches the visual
cortex and can appear superimposed on whatever the
open eye is seeing. This interpretation is confirm ed by
the fact chac an afterimage is no longer visible when the
eye containing it is paralyzed by the application o f
pressure to che eyeball (Oswald 1957). To prove that an
aftereffect is cortical, one must show that it survives
paralysis o f the eye. Interocular transfer is discussed in
S ection 13.3.
2. Monocular independence In this procedure, opposite
induction stimuli arc presented to each eye and the
aftereffect is tested in each eye separately. For instance, a
leftward-moving tcxtured display is presented to the
right eye and a rightward-moving display is presented at
che sam e tim e to the corresponding area o f the left eve.
A stationary cesc pattern is chen presenced со each eye in
curn со reveal w hether the direction o f the aftereffect in
each eye is appropriate to that eye’s induction stimulus.
If it is, then at least some aftereffect must have been
generated in pathways specific со each eye. I f che
aftcrcrtccc in each eye is just as scrong as when chac eye
alone is exposed to an induction stimulus, chen che
processes responsible for the aftcreffecc are independcnc
in the cwo eyes. I f che aftereffect were generated wholly
in a pathway com m on to both eyes, induction stim uli o f
equal magnitude but opposite sign should cancel when
presented со opposite eyes. Experim ents involving this
procedure are reviewed in Section 13.3.
3 . Cyclopean procedures Enable a stimulus to be
presenced со che visual corcex w ithout a corresponding
 stimulus on the retina. There are three basic ways to
do this:
Л . Paralysis o f an eye For instance, i f an afterimage
formed in one eye is still visible after that eye has
been pressure paralyzed, one must conclude that
afterimages can be generated at a central site.
B. Direct stimulation o f the visual cortex D irect
stim ulation o f the visual cortex by an electric current
creates visual phosphenes. Fortification illusions o f
migraine are a naturally occurring cyclopean
stimulus, since they arise from a direct disturbance
o f the visual cortex (W ilk in son 2 0 0 4 ).
C . Use ofdichop tic stimuli In this procedure, distinct
stimuli are presented to the two eyes in a stereoscope
(dichoptically) to create an effect not evident in
either m onocular stimulus. A dichop ticcom p osite
stimulus is one in w hich the effect produced by
com bining images from two eyes is sim ilar to the
effect produced by com bining the same images in
the same eye. For instance, a display o f lines
presented to one eye can be com bined dichoptically
with a different display o f lines in the other eye so
that they form the same com posite shape that would
be produced by com bining the lines in one eye, as in
Figure 4 .8 . The literature on dichoptic com posite
stimuli is reviewed in Section 16.3.
A purely dichoptic stimulus is one that is uniquely pro­
duced by com bining the images from the tw o eyes. For
example binocularly disparate stim uli create an impression
o f depth. D ichop tic stimuli interact to produce binocular
rivalry, binocular disparity, or dichopcic m otion or flicker.
Each o f these effects may be used to synthesize a cyclopean
shape. O n ce synthesized, a cyclopean shape may be moved
by simply m oving the dichoptic boundaries that define it.
к.диг. 1 ..V J didw ptic composite stimulus. Fusion o f the two upper displays
product* the lower thapc.
Cyclopean procedures are described in more detail in
C hapters 13 and 16.
4 .5 .8 b D e te rm in in g th e O rd e r of
V isual Processes
It is difficult, if n o t impossible, to establish the precise site
o f postrecinal visual processes by psychophysical procedures
alone. However, psychophysical procedures allow one to
make inferences about che order in w hich distinct processes
o ccu r in the nervous system. These are known as psycho-
an ato m ical p ro ced u res (Julesz 1 9 7 1 ). It is argued chac
because one percept depends on anocher, ic muse be p ro ­
cessed ac a later stage. Buc che logic may be flawed. For
example, from che fact that the perceived direction ot
m otion o f a grating in an aperture depends on the way line
ends are interpreted, it has been concluded that line p ro ­
cessing precedes the processing o f m otion (Section 2 2 .3 .1).
But a mocion signal could be excracced firsc and then rein-
cerpreted after line ends are assessed. In other words, a given
visual feature can be processed in several stages; some ot
which precede and others follow the processing o f another
feature. Also, the outcom e o f a perceptual process could
feed back to an earlier stage or to a parallel stage and affect
what is occurring there. W ith o u t supporting anacomical or
physiological evidence, one may n o t be able to draw firm
conclusions about the order in which sensory features are
processed merely from the way one perceptual phenomenon
depends on another.
The logic is firm in ocher cases. For example, the d etec­
tion o f a disparity-defined shape in a random -dot stereo­
gram must occur after binocular disparities are processed.
The shape is not present in the input from either eye.
It a perceptual process occurs more rapidly than it would
take neural feedback to occur, one may conclude chac ic
involves feedforward processes.
I f an effect in scimulus feature A occurs only for cercain
values o f scimulus feature B, then it is reasonable to co n ­
clude that feature В is processed before feature A. For
instance, certain effects, such as perspeccive illusions, occur
wich stimuli defined by luminance buc noc wich chromacic
4
stimuli. Thev therefore occur after chromatic and achromatic
channels arc partitioned.
If tw o sensory inputs produce the same perceptual effect
we can infer th at they feed in to a com m on neural process.
For example, binocular disparity and m onocular m otion
parallax produce similar impressions o f depth. O th e r psy­
chophysical evidence supports the idea that they feed into a
com m on m echanism (Section 3 0 .2 .5 ).
Psychophysical procedures can allow one to character­
ize nonlinearities, such as signal rectification, ceiling effects
(compressive nonlinearity), and spatiotem poral interac­
tions betw een stimuli. They can also reveal whether distinct
visual features, such as d istinct cues to depth, interact in a
linear or nonlinear fashion (C hapter 30 ).
 4 .5 .9 M U L T IS T A B L E P E R C E P T S

4 .5 .9 a Types o f M u ltistability

W h en a stimulus allows m ore chan one interpretation, the

pcrccpt is said со be undcrdecermincd. D ifferent intcrpreta-
tions may com pete for attention and alternate as one co n ­
tinues to view the stimulus. Such figures are said со be
ambiguous, and the percepts are said to be n iu ltistable.
Am biguous figures fall into two broad classes.
(a) S ectored discs.

A. Figures with m ultistable structuralfeatures

In the first class o f am biguous figures the alternative
percepts consist o f different ways in which simple structural
feacures o f a stimulus are organized. The following scimuli
produce mulcistable percepts.

Figure-ground relationships An example is the M altese

cross and its derivatives shown in Figure 4.9a. Figures
ot this kind occurred in Rom an mosaics and were
(b) The N e cke r cube. (c) T h e S chroder staircase.
popular in European art in the 18th and 19th centuries
(P iccolin o and Wade 2 0 0 6 ).

Depth orderfrom overlap This topic is discussed in

Sections 2 2 .1 .2 and 2 7.2.

Reversible perspective Examples arc shown in

Figures 4 .9 b and c. This topic is discussed in
S ection 2 6.7.

Depth from shading This topic is discussed in

(d) A rotating textured sphere (e) Interchanging the w hite
Section 27.3.2.
a lternates betw een leftw ard and and black sectors creates
rightw ard rotation. a m biguous a pparent m otion.
Direction o f real motion An example is shown
in Figure 4.9d . This topic is discussed in *.», E xam ples o f am bigu ity based on sim plefeatures.
Section 28.5.

Patterns o f apparent motion For example, four flashing

lights arranged in a square create various patterns o f
apparent m otion that change during a period ot
inspection (Ram achandran and Anstis 1983). Also, an
interchanging patcern o t black and whice scccors, as
shown in Figure 4 .9 e , creares ambiguous apparenc
mocion.
IS. Figures that produce two or m orefam iliar objects
In che second class o f ambiguous figures the alternative
percepts consist o f d istin ct fam iliar objects, each o f which
represents a different way in which the figural elem ents o f a
com plcx stimulus arc organized. Figure 4 .1 0 contains three
examples that have been used in many studies o f multistable
perception. They arc the “My wife and m y-m othcr-in-law ”
figure (B orin g 1 9 3 0 ), Jastro w s duck-rabbit figure, and
R u bins tacc-vasc figure. Since both interpretations arc
fam iliar o bjects, a person must be fam iliar w ith them in
order to experience figural reversal.
The following processes contribute to the way in which
ambiguous stim uli are interpreted.
4 .5 .9 b W e ig h tin g o f C u e s
W ith a com plcccly ambiguous scimulus, ditferenc intcrprc-
cacions occur wich equal frequency. The scimulus is said со
be unbiased. If stimulus informacion favoring one intcrprc-
cacion is more evidenc chan chac favoring ocher interpreta-
cions, wc have biased ambiguity. For example a 2 -D N cckcr
cube is just as likely to be seen in one depth order as in
the other, but a 3-D outline cube is seen for longer in its
true depth order. The relative durations o f different inter­
pretations of an ambiguous stimulus provide a measure
o f che weighting attached to various types o f stimulus
inform ation.
W e can think o f the relative probabilities o f different
interpretations o t an ambiguous stimulus as torm ingdips in
a probability landscape. The deeper the dip, the m ore stable
the percept. The perceptual system may becom e locked in
an interpretation that docs n o t represent the cruc scacc o f
che world. This could be avoided if che syscem were subjecc
со inscabilicy or jicccr thac shakes it out o f a shallow dip
in to a deeper dip. This would be equivalent to random ,

(a) B o rin g 's w ife -m o th e r.
(b) Ja stro w 's d u c k -ra b b it.
(c) R u b in 's face-vase.
!'•;•»< t.io Exam ples o f am biguity b ated on fam iliarity .
or stochastic, fluctuations in the depth o f a dip in the prob­
ability landscape (Taylor and Aldridge 1974). TJiis type o f
proccss is described in Section 15.2.1 in con nection with
the task o f finding the best match between binocular
images.
4 .5 .9 c A d ap tation o f Specific Processing C h an n els
Prolonged exposure to one alternative o f a reversible figure
increases the probability that the o ther alternative will be
seen. For example, inspection o f a stereogram o f the
Schroder staircase, in which disparity caused it to be seen as
if from above, increased the probability that an ambiguous
zero-disparity staircase was seen as i f from below (Virsu
1 9 7 5 ). After 1 m inute o t adaptation, the effect lasted about
2 0 s. Harris (1 9 8 0 ) obtained the same effect when disparity
aftereffects were elim inated by presenting the test staircase
monocularly. The adaptation process must occur at a high
level where depth order is assessed independently o f specific
depth cues. Adaptation effects in reversible perspective
o f dynamic displays arc discussed in Sections 26.7.1
and 30.5.1.
K ohler 1,1940) proposed that ambiguous figure-ground
stimuli, such as R u bins cross, reverse when rhe neural pro­
cesses underlying one interpretation becom e satiated. Kohler
did not have a clear idea o f how neural systems satiate. But
we now have physiological evidence that visual channels
adapt during continued stim ulation (Section 4 .2 .9 ).
Adaptation o f the neural processes responsible tor a
particular interpretation o f an ambiguous stimulus should
facilitate the emergence o t another interpretation. This
would be equivalent to the dip in the probability landscape
becom ing less deep over time. For example, the rate o f rever­
sal o f the Neckcr cube increases over a period o f observa­
tion. The increase in reversal rate occurred with interm ittent
viewing as long as the intervals between stimulus presenta­
tions were not longer than about 0.5 s (O rbach et al. 1963).
Thus, with continuous or briefly interrupted viewing, the
processes responsible tor both interpretations became
simultaneously adapted. W ith interruptions longer than
about 1 s the adaptation process recovered so th at the same
interpretation persisted from o n e exposure to chc ncxc.
Leopold ec al. (2 0 0 2 ) measured che race o f alcernation
o f several ambiguous figures including a rotating cube,
and che race o f rivalry o f orchogonal gratings. The rate
was greatly reduced when chc stimuli were presented tor
3-second periods interrupted by 5-second blank periods.
They argued thac an adaptation process couldn’t explain
chis effect. Buc one could argue that the dom inant interpre­
tation would recover from adaptation during the 5-s blank
interval and therefore reappear when the stimulus returned.
In o ther words, interruption o f an ambiguous stimulus
forestalls adaptation o f che dom inant stimulus, which is
then preserved over interrupcions. However, when an
ambiguous rotating cylinder was interrupted and made to
reappear in a different location the previous interpretation
did n o t reappear above chance level (C h en and He 2 0 0 4 ).
Thus, whatever is preserved over interruptions is location
specific.
For a N eckcr cube, a rotating sphere, and an ambiguous
m otion pattern a given interpretation was preserved over
4-s interruptions when a distinct stimulus was inserted into
the interruption period. Also, particular interpretations o f
each o f two interleaved ambiguous patterns tended со be
preserved (M a ic r c t al. 2 0 0 3 ).
4 .5 .9 d A ctive Scarch
There has been som e debate about whecher particular types
o f eye m ovem ent cause reversals o f perspective in simple
reversing figures or occur after a reversal. Pheifier et al. (1 9 5 6 )
found chac characteristic eye movements followed rather
than preceded perspective reversals o f the Schroder
staircase.
Л related question is whether perspective reversals are
determ ined by the part o f the figure chat the observer fix-
ates. Am biguous figures, such as the N ecker cube, reverse
whichever part is fixated. However, o f the two central co r­
ners o f the N ecker cube, the one thac is fixaced is more fre­
quently seen as the nearer corner than is the corner chat is
noc fixated (Ellis and Stark 1 9 7 8 ; Kawabata e t al. 1978).
The effects o f eye fixation are particularly evident in
figures such as rhe duck-rabbit figure or B o rin g s young
w om an -old woman (Tsai and K olbet 1985). Fixation on
the upper part o f Boring’s figure brings the salienc feacures
o t the young woman onco the fovea, while fixation on the
lower pare brings che salienc feacures o f che old woman onco
the fovea (G arda-Perez 1 989).
W e can actively seek a given incerprccacion o f some
ambiguous stim uli, by searching in specific locations or for
specific features, w ith or w ithout m ovements o f the eyes.
4 .5 .9 e A ssu m p tion s and C o n te x t
In traditional experim ents on ambiguous figures, subjects
were instructed that there were tw o interpretations. Girgus,
R ock, and Egatz ( 1 9 7 7 ) found that about h a lfo fa g ro u p o f
adult subjects did not report reversal o f a Rubin vase-face or
a N ecker cube during a viewing period of 6 0 s, buc did so
when inform ed chat there were tw o interpretations. In a
later study R ock and M iteh cn cr (1 9 9 2 ) used less familiar
ambiguous figures, namely a M altese cross, the M ach book
figure, and a figure that could be either a ch ef or a dog. O n ly
seven o f 18 subjects saw reversals in less than 3 0 s, but saw
reversals readily when told what to look for. R ock et al.
(1 9 9 4 ) found that none o f a group o f 2 5 children between
the ag esof 3 and 5 years experienced reversals ot the Rubin
vase or o f an ambiguous duck-rabbit drawing. Four o f the
children did not experience reversals even when told what
to look for.
Som e assumptions that determ ine the way we interpret
am biguous stim uli may be learned at an early age and
function w ithout conscious awareness. They are implicit
descriptive rules, or schemata. These rules express very
general assumptions about properties o f real world scenes,
and place constraints on the interpretation o f potentially
am biguous stim uli (Howard 1974).
O n e example o f an implicit rule is that stimuli that could
have been produced by either a convex or concave surface
arc usually seen as convex, presumably because we see more
convex surfaces chan concave surfaces (Section 2 7 .3 .2 ).
The generic view point assumption provides another
example o f an im plicit descriptive rule. A given o b ject can
be viewed from different positions, in different orientations,
o r under different lighting conditions. These arc generic
variables. For certain viewpoints, the proximal stimulus
may assume a peculiar form . For example, a cube viewed
along a diagonal appears as a hexagon. This is known as an
accidental viewpoint. Also, in an accidental view point, the
images o f certain disconnected edges may appear to be co n ­
nected, and other edges may be hidden. A small change
from an accidental view point produces a sudden change in
the proximal image. The accidentally connected lines may
suddenly becom e disconnected and hidden edges visible.
V iew points for w hich the image docs n o t change abruptly
arc called generic viewpoints. In general, the m ost likely
o b ject is one that would produce a gradual change in the
proximal stimulus over a change in view point (Freeman
1994).
The general principle is that we prefer interpretations o f
ambiguous stimuli that arise trom a generic viewpoint
rather than those that arise from a particular vantage point.
The same rule operates in the perception o t the three-
dimensional motion o fo b jects (Kitazaki and Shim ojo 1996).
There is behavioral evidence that monkeys perceive am big­
uous displays according to the same rule (U k a ct al. 1999).
The gestalt notion o f "figural goodness” is related to
that o f generic view point (K offka 1935). For example, a
cube viewed along a diagonal appears as a 2-D hexagon
rather than a cube because a hexagon has good symmetry
and has fewer edges than a cube (H ochberg and Brooks
1960).
The interpretation o t an ambiguous figure can be influ­
enced by its direction o f m otion. For example, the o b ject in
Figure 4.11 was seen as a swan when it moved to the right
and as a cat when it moved to the left (Bernstein and C ooper
1997).
The way an ambiguous stimulus is interpreted can be
affected by context. For example, Bruner and M inturn
(1 9 5 5 ) showed that:
4 . 5 . 9 f C o n s c io u s C o n c ro l o f A m b ig u o u s F ig u res
To some exten t one can control the rate at w hich an am big­
uous figure alternates betw een its cwo interpretations.
O n e would expect people to have more control over the
reversal o f ambiguous figures th at denote m eaningful
objects than over the reversal o f abstract figures. In co n fo r­
m ity with this expectation, Striiber and Stadler (1 9 9 9 )
4.1 1. Effect of'm ovem ent on figu ra l am biguity. The ob jee t lookc d
like a cat w hen m oved to th e left and like a sw an w hen m oved to
the right.
Ъь \а
found chat subjects could bold a particular interpretation o f
Jastrow s duck-rabbit figure or R u bins vase for longer than
a particular interpretation o f the N ecker cube, o r the
M altese cross.
Long and T oppino (2 0 0 4 ) reviewed che topic o f percep­
tual ambiguity.
4 .5 .9 g Neural C h a n g es Related to
M u ltistable Percepts
In any ambiguous figure, the interpretation changes
although rhe stimulus rem ains the same. Any change in the
way a stimulus is interpreted must be accom panied by some
change in the nervous syscem. In human subjects, fM R I
recordings have been used to locate such changes in the
cerebral cortex.
Kleinschmidc et al. (1 9 9 8 ) recorded fM R I responses
from five human subjects as they observed R u b in s vase or
B o rin g s young w om an -old woman figures. Each change in
interpretation was accom panied by transient activity in the
ventral occipital cortex (m iddle fusiform gyrus), posterior
intraparietal cortex, and some frontal areas, including the
frontal eye fields. A t the same tim e, there was a transient
depression o f activation in the visual cortex. However, the
same transient changes occurred whichever interpretation
becam e dom inant. This means that these neural events were
related to perceptual changes rather than to the percepts
themselves. Responses in the frontal eye fields could have
been due to saccades occurring during the transitions.
However, eye m ovem ent recordings revealed that subjects
remained fixated on che fixacion spot.
Sakata et al. ^1994) tound the response o f many cells in
area 7a in the parietal lobe showed periodic changes when
the monkey viewed an am biguous rotating trapezoid (Am es
window).
Sterzer et al. (2 0 0 2 ) recorded fM R I brain activity while
human subjects viewed a bistable spinning segmented ring,
as shown in Figure 4.9e. Reported reversals ot the direction
o f mocion were accom panied by cransienc changes in the
parietal and frontal areas. In particular, changes occurred in
V 5, an area known to be associated with processing visual
m otion (Section 5.8.4b ). There was no activation w ithin the
ventral stream o f neural processing, the stream concerned
with pattern perception (Section 5 .8.3). These results show
that the parts o f the brain activated by bistable stimuli
depend on the perceptual category o f the percepts. However,
the fM R I m ethod was noc sensitive enough to detect
whether the location o f neural activity in V5 depended on
the perceived direction o f m otion. Single-cell recordings
from that area in monkeys have shown that different cells are
tuned to different directions o f m otion (Section 5.8.4b).
The human fM R I reveals that the fusiform gyrus and
superior tem poral sulcus are particularly active when people
view faces, while rhe lateral occipital lobe is active when
nonface objects are viewed. Andrews et al. (2 0 0 2 ) found
that the fusiform gyrus was activated, as revealed by the
fM R I, when people reported seeing the face interpretation
o f R ubins vase but not when they reported seeing the vase
interpretation.
4 .5 .1 0 R U L E S O F V IS U A L S T R U C T U R E S
We live in a highly structured world. O b jects in natural
scenes tend to have certain characteristics and tend to
be arranged in certain ways. These characteristics can be
classified as o b ject structure, scene structure, and scene
semantics.
4 .5 .1 0 a Principles o f O b j e c t S tru ctu re
M ost natural scenes contain objects disposed on surfaces.
O n e o f the basic tasks ot visual perception is to segregate
objects and register their structure.
Figural regions have certain characteristics. For exam ­
ple, in the Rubin cross, the region seen as figure appears
bounded and in the foreground while the nonfigure region
appears to be continuous and extend behind the figure
region.
The G estalt psychologist M ax W ertheim er (1 9 2 3 ) p ro ­
posed several p rin cip les o f figural o rg an izatio n , or visual
grouping, to explain how sets o f stim ulus elem ents are per­
ceived as a coherent pattern (see K oflka 1 9 3 5 ). Som e o f
these principles are illustrated in Figure 4 .1 2 .
The principles are:
Proximity In a mixed set o f similar scimulus elements,
those that are closer together form perceptual groups.
Kubovy et al. (1 9 9 8 ) varied the relative spacing o f
colum ns and rows in a regular dot m atrix and asked
subjects to report whechcr chey saw colum ns or rows.
The probability o f a given grouping decreased
exponentially as the distance betw een the dots for that
grouping was increased relative to the distance between
the dots tor the alternative grouping.
Similarity Elem ents that are sim ilar in shape,
orientation, or color tend to be seen as grouped, as in
Figure 4.12b .
Continuity Originally, the principle o f continuity
referred to how we segment intersecting lines. In Figure
4 .1 2 c continuous sm ooth lines arc seen in preference to
lines that contain sharp angles. However, when lines
form a closed shape, as in Figure 4 .1 2 d , the principle o f
line continuity may be overridden. The principle has
also been used to explain how we link disconnected
elements. For example, aligned line elements are readily
detected w ithin a display o f randomly oriented line
elements. This topic was discussed in Section 4.5.2b .
The principle has also been applied to how we perceive
an o b ject as com plete when parts are occluded by

(a) G rouping by proxim ity.
o o * * o o * * o o *
(b) G rouping by sim ilarity.
(c) G rouping by continuity.
(e) G ro up in g by sym m etry.
Figure*. I J . Рг-inciptesojjiguralgrouping.
another o b ject (am odal com pletion) or rendered
invisible bccausc the o b ject is camouflaged against the
background (m odal com pletion). These topics are
discussed in Section 2 7.2.
Good figure In G erm an, chis is known as the principle
o f Pragnanz. The principle states that we have a
preference tor seeing shapes that arc closed, sm ooth,
sym m etrical, and contain che least num ber o fsid es
4
(Barrow and Tcncnbaum 1 981).
Common motion This principle is vividly illustrated by
moving a subset o f a display o f random dots coherently
with respect to the other dots. The moving dots
suddenly form a pattern, which disappears as soon as
the dots stop moving. The effect is known as shape
fro m m o tio n .
For any 3 -D o b jcct, the arrangem ent o f edges, corners,
and surfaces obeys certain rules, which can be called stru c­
tu ral rules fo r o b je c ts (M ackw orth 1973). These rules will
be discussed in Section 27.1.
A t a higher level, solid objects arc perceived as
com posed o f sim ple g eo m etric co m p o n e n ts such as
cylinders, blocks, wedges, and cones, which the perceptual
system uses со conscruct im plicit descriptions (M arr 1977;
Bicderm an 1987).
A t a higher level still, fam iliar com plex o bjects, such
as chairs, houses, autom obiles, and com puters, are per­
ceived in terms o f fu n ctio n a l co m p o n en ts (Tversky and
Hcm cnway 1 984).
Many natural o b jects deform in characteristic ways. An
o b ject may consist ol articulated rigid com ponents, like the
parts o f a human body. Plastic o b jects may undergo co n ­
tinuous and reversible deform ations, like a human face or a
crcc blow ing in chc wind. These objects preserve topological
properties o f continuity and connectedness. O th er objects
undergo continuous but nonrcvcrsiblc deform ation, like a
growing anim al, a wave on the ocean, or a cloud blowing
in the wind. Still other objects undergo discontinuous
deform ation, such as a wave breaking on the shore, a tree
breaking in che wind, or ccll division.
All chese rules arise because o f che way our norm al envi­
ronm ent is constructed. Tlievi are evident in the second-
order statistics o f natural scenes. However, second-order
statistics do not distinguish between structure arising trom
regular textures and that arising from che scructure o f
objects. Elder and G oldberg (2 0 0 2 ) developed a way ot
characterizing chc G estalt laws o f grouping in terms o f chc
sequence o t cangencs chat define connected contours. Rules
o f o b ject structure have little or no application in a snow­
storm or tog. In the deep ocean the only visible things arc
patterns o f light em itted by fluorescent creatures.
People can apply these rules with objects they have not
seen before. Knowledge o f an o b je c ts shape helps when
only part o f it is visible. Also, knowledge o f an o b ject s size
helps in judging its distance.
A well-defined fam iliar o b ject can be perceived in an
unspecifiably large num ber o f ways, according to the
descriptive dom ain w ithin which che perceiver is operating.
For exam ple, in looking at a face, o n e may attend со its age,
sex, race, expression, or any o f a num ber o f ocher features.
For each feature there arc rules that govern the way faces are
classified, although che rules may be difficult со specify.
The knowledge and incerests o f the perceiver determ ine the
dom ain w ithin which o b jects are identified or classified (see
Section 4 .6 .3 ).
4 . 5 . 1 Ob P rin cip le s o f S c c n c S tru c tu re
The above rules apply to images o f simple objects seen in
isolation. Their application to the images o f natural scenes
becom es very uncertain because edges are often obscured by
texture and shadows.
The relationships between objects in natural scenes gen­
erally obey some very general structural ru Ics. The following
are som e examples.
1. Support M ost o b jects resc on a surface chat is
gravitationally beneath them.
2. Orientation to gravit y M ost o b jects have a
distinguishable top and b o tto m , and chc axis join in g
the top and bottom is usually an axis o f bilateral
symmccry and vcrcical.
3. Opacity M osc objeccs are opaque and occlude more
distant objects along the same line ot sight.
4. Shading a n d shadows Rules governing shading and
shadows arc described in Section 2 7 .3 .
5. Relative motion M oving objects produce characteristic
patterns o f relative m otion w ith respect to other
objects.
4 .5 .1 0 c Principles o f S c e n e Sem an tics
C onstraints can be imposed on the interpretation o f a 2-D
image if the perceivcr has knowledge about particular scenes
or objects, which Biederinan (1 9 8 1 ) called scen e sem antics.
Here are a few examples o f scene semantics:
1. Object probability The probability that a given o b ject is
in a scene varies with the scene. For example, in a living
room the head o f a tiger is likely to be part o f a rug, but
in a forest it is likely to be part o f a living tiger.
2. Fam iliar arrangements For example, if the scene is a
room , then floor, ceiling, windows, and doors can be
identified by their relative positions (Tenenbaum and
Barrow 1 977). A schem a, or frame (M insky 1 9 7 5 ) is a
structural description o f an o b ject or scene, or a nested
sec o f descriptions.
3. Inferencesfrom localfeatures Partial inform ation from an
image or from som e ocher source may evoke a particular
stored frame from am ong a sec o i possible frames.
Further exploration o f the image will reveal whether
this is the mosc appropriate interpretation (see
M cA rthu r 1982). For exam ple, a cartoon ist can use a
few simple lines to evoke the idea o f a com plex scene.
4 . Effect o f context on interpretation o f local features
D epending o n chc conccxc, a given o b ject can be
perceived in an unspecifiably large num ber o f ways. For
example, in different contexts, a cube can be a box. a
dice, a lump o f sugar, a building, a stool, a brick, a
compucer, or many other things.
5- Patterns o f motion an d events Natural objcccs move and
inceracc according to chc rules o f physics. C ollid in g and
falling objects rebound at specified velocicies and in
specified directions. W ater and traffic flow in
characteristic paccerns, and foocball players move in
characccristic ways. F.pisodcs such as the day-night cycle
and storm s produce characteristics sequences o t events.
4 .6 TYPES OF PERCEPTU A L
JU D G M E N T
A visual stim u lu s dom ain is a sec o f objects or events with
defined visible features and values o f those features, plus the
rules o f com position and transform ation o f those features
and values. A stimulus domain mav * be a set o f stimuli in a
laboratory o r a set o f naturally occurring objects. The set o f
possible responses to the defined stim uli defines che
response dom ain (Section 3 .1 ). This book is mainly co n ­
cerned with responses involving some kind ol judgm ent.
Judgm ents may be classified into d etection, resolution, dis­
crim ination, categorization, recognition, identification, and
description. They form a task hierarchy. This ordered sec o f
casks involves a hierarchical sequence o f processes in che
nervous system. Successful perform ance at a given level o f
the hierarchy requires successful perform ance at all lower
levels buc n o t ac any higher level. However, perform ance ac
a higher level may improve perform ance at a lower level.
For example, it is easier to detect a fam iliar o b ject than an
unfam iliar objccc.
4 .6 .1 D E T E C T IO N , R E S O L U T IO N .
AND DISCRIM IN A TIO N
The basic casks o t d etection , resolution, and discrim ination
were described in Section 3 .1 . All sensory systems transduce
specific torins o f energy falling on an array ot detectors into
neural responses so thac spatiotem poral variations in stim u­
lus energy may be detected and discrim inated. The co m ­
plexity o f subsequent neural processing depends on the use
to which the inform ation is put.
For the visual system, we can think o f these uses form ing
an evolutionary sequence, involving increasing com plexity
o f neural processing in a hierarchy ot neural centers. For
exam ple, lens accom m odation uses simple attributes o f
the visual input, such as image blur and chrom atic aberra­
tion, and is controlled by subcortical centers (S ectio n 9 .6 ).
A m ore recently evolved level o f concrol allows accom m o­
dation to be coupled to vergence cvc movements.
O p to kin etic nystagmus (O K N ), in its prim itive form , is
evoked by retinal m otion signals chat arc extracted over a
wide area and processed in the accessory optic system and
vestibular nuclei. In higher mammals, O K N is supple­
m ented by more highly processed signals from the visual
cortcx (Section 2 2 .6 .1 ).
Neural processing tor simple responses such as accom ­
m odation, eye movements, and postural control can involve
fairly com plex relationships betw een dilierent sensory
inputs, bu t this processing is stereotyped and occurs with
m inim al conscious awareness o r control. Sensory-m otor
learningcan be involved, as when a child learns to walk, but
the learning does n o t involve conscious knowledge o f che
decailed scruccure or contents o f the visual world. For these
types o f response, stimulus am biguities in one sensory
system are usually resolved by another sensory system. The
processes are those o f detection and discrim ination only.
M ore com plex inputs are required for the conscious
perception o f the three-dim ensional layout o f the visual
world for guiding movements and tor navigation. For
these purposes, elaborate neural processes occur in several
hierarchical and parallel visual centers (Section 5.8.4).
These processes allow us со perceive objeccs and features o f
objeccs «is rem aining chc same under incidental transform a­
tions o f size, distance, oriencation, m otion, and lighting.
These are chc basic p erce p tu a l co n sta n cies described in
C h ap ter 2 9 . These higher visual processes also allow us со
perceive objects as d istin ct entities even when they are par­
tially occluded, as described in C hapter 2 7 . Finally, they
allow us to perceive che m ovements o f arciculaced or plastic
objects, as described in Section 2 8.4.
4 .6 .2 C A T E G O R IZ A T IO N , S C A L IN G ,
A N D I D E N T I F I С AT I О N
In simple ca te g o riz a tio n , subjects group, or classify, a set o f
stim uli according to defined criteria. In the simplest case,
subjects arrange stim uli in to feature-defined secs wich no
order within or betw een the sets. For example, colored
o b jects in one set, round o b jects in a second set, and moving
objects in a third set. A simple categorical schema is assumed
to exist when som e aspect o f behavior is contingen t on the
presence o t a relatively simple scimulus feature o r set o t fea­
tures. For instance, the aggressive posture o f the robin red
breast is contingent on its seeing a patch o t red on a birdlike
o bject. Signs o f this kind are known as releasers. M ost
releasers described by the ethologists are o f this simple kind.
M ore com plex taxonom ic schem ata underlie che ability со
categorize things in terms ot several feacures.
In simple sensory scalin g, subjects categorize stimuli
in term s o f their value on a defined dim ension. It can be
simply rank ordering, equal-interval ordering, or equal-
racio ordering. The ordering can be on a one-dim ensional
continuum such as size, velocity, o r distance, or in a m ulti­
dim ensional feature space. Thus, in addition codiscrim inac-
ing becween stim uli, observers arrange them in bins o r in
order. Readers are referred to Torgerson ( 1 9 5 8 ), G arner
(1 9 6 2 ), and Falmagne (1 9 8 6 ).
Ac a more com plex level, people classify stim uli accord­
ing to a com plex set o t rules. Subjects need have no prior
knowledge o f the categories if they are shown a representa­
tive sample ot stim uli in each category. Even tor categories
that have been learned, people may have no explicit under­
standing o t the criteria that determ ine class membership.
For instance, we classify faces by sex, age, and race but are
not necessarily aware o f the features that we use.
R eco g n itio n involves even m ore com plex neural pro­
cesses. In a simple recognition task, subjects state whether
they have or have n o t seen a stimulus on a previous
occasion.
In an id e n tifica tio n task, subjects em it a distinct learned
response to all stim uli in a defined category and different
responses to stimuli in each ot the other defined categories.
Th e response may be an action that is specific to that class o f
o bjects. For example we may be said to have recognized a
spade when we select it to dig a hole. O cherw ise, che
response may be a convencional name o r a novel name chac
an experimencer has assigned со a given objecc. Thus, in
addicion со cacegorizingstim uli, subjects must learn specific
responses to different stimulus categories. Subjects can
identify a single stimulus only when they have prior know l­
edge o f the relevant categories. A good deal o f perceptual
learning consists o f isolating salient features or partial cues
as aids to rapid identification (G ibson 1967).
The interior tem poral cortex and prefrontal lobes are
the regions o f the brain devoted to o b je ct categorization,
recognition, and identification (Section 5 .8 .3 ). C ells in
these regions in the alert m onkey have been found to
respond to particular objects chac the animal has been
trained to recognize, the im plication being that the cells
respond to parcicular concatenations o f stim ulus feacures.
However, Freedman et al. (2 0 0 2 ) found chat cells in che
froncal corcex respond to stimulus categories that che
monkey has been crained to construct, even after the stimu-
в
lus features defining the category boundaries have been
changed.
It has yet to be shown that the response o f an “o b ject
recognition” cell depends on how an animal regards an
o b ject (what descriptive dom ain ic is using). For example,
an animal could be trained to use a box as a seat, or as an
o b ject to throw, or as an o b ject to open. W ould the response
o f a cell varv
* with the wav
* that the animal intends to use
the box ?
M odels o f perception o f the ‘'perceptron” type, such as
“Pandem onium " (Selfridge 1 9 5 9 ), essentially embody che
caxonom ic level o f perform ance. That is, percepts are
defined in terms o f the presence or absence o f weighted
elem entary stim ulus features. Also, m ost studies o f con cept
form ation have involved the study o f conjunctive or dis­
junctive categorical concepts such as large green objects
versus small red objects. It is as it zoology never got beyond
Linnaeus. The m athem atics underlying categorical behavior
is set th eo ry . A set is a collection o f item s belonging to a
defined class, but having no internal structure. Perhaps the
belief that categorical percepts are primary arose out ot the
b elief that set theory is basic to logic and mathematics.
M any aspects ot perception require analysis in terms o t a
richer sec o f m athem atical ideas, such as group theory, pro­
jective geometry, and che calculus o f variations (G clfand
and Fom in ( 2 0 0 0 ). These mathematical tools add the
notion o f structure to that o f class membership.
4 .6 .3 P E R C E P T U A L D E S C R IP T IV E
PR O C ESSES
4 .6 .3 a D escriptive D o m a in s
A rep resentation is som ething that is accepted as resembling
some defined aspects o f a specified thing (objecc, event, or
idea) o r s e to f things, tor some specified purpose. A d e scrip ­
tion is a representation involving com position rules within
a d escrip tive d o m ain . A described o b ject is seen as a
m em ber o f a see o f items with which it is equivalent in some
respect. This process involves memory ot the equivalence
relation. W hen operating at the descriptive level wc can:
1. A ttend to one or other aspect o f an o b jcct in response
to centrally determ ined requirem ents or criteria, such as
perform ance o f a task or the search tor an answer to a
problem.
2. C o m bin e subroutines in a novel fashion to suit the
demands o f a com plex task. This enables us to define
new equivalence relations w ithin an existing set o f
discrim inated stimuli and thus derive ever more
com plcx descriptive functions or dusters o f such
functions.
3. Perform som e function that is specifically related to the
descriptive structure o f an o b ject or event.
Presymbolic descriptive rules are implicit descriptive
rules, or schemata. They may be perceptual descriptive
functions that allow us to recognize com plex stim uli or
events or they may be perceptual-m otor functions that
allow us to perform com plex skills such as riding a bicycle
or juggling. They may be learned at an early age and func­
tion w ithout conscious awareness. For example we soon
learn to recognize people w ithout conscious awareness ot
rhe processes we use. Presymbolic schem ata involve an
internal analog representation o f rules and structures. At
rhe sym bolic level we describe objects and events in terms
o f arbitrary symbols, such as words or pictures. These
descriptive systems are learned deliberately and w ith co n ­
scious effort, although they operate with little conscious
effort when thev are well learned.
H elm holtz ( 1 9 1 0 ), in revolting against Germ an idealist
philosophers, stated that sensations do not resemble the
o b jects they symbolize, any more than letters resemble the
sounds they represent (Section 2 .8 .1 ). For H elm holtz,
sensations were “signs that we have learned to decipher”
But this idea ignores the fact that neural events, and the
sensations they produce, are lawful transductions o f
stimuli arising from external o bjects, while stim uli such
as words, are totally arbitrary signs o f the o b jects they
denote. In the form er case, the external o b je ct can be recon­
structed from knowledge o f the eyes optics and the filter
characteristics o f neural processing. If there is any am bigu­
ity, at least a range o f possible stimuli can be recovered.
The development o t sensory and perceptual mechanisms
involves learning, but not learning o f arbitrary signs. In
the case o f language, purely perceptual processes can
indicate the shape or sound o f a word. However, recovery o f
the o b ject denoted by the word requires knowledge o f the
arbitrary symbols o f the language. I Iclm holtz’s view also
ignores the possibility that the visual system is genetically
programmed to interpret certain stimulus features in
certain wavs.
Even at the prelinguistic level, wc classify o b jects into
hierarchies o t su pcrord in atc and subordinate categories.
For exam ple, at the supcrordinatc level we distinguish
betw een living and nonliving objects. At an interm ediate
level wc distinguish betw een cats, dogs, and humans. A t a
subordinate level we distinguish between difterent breeds
o f dog or between our own dog and other dogs. M em bers o f
a supcrordinatc class share only very general properties.
For example, all animals share the general property o f self-
generated motility. M em bers o f a subordinate class may be
similar in all but one small feature. Semantic nets may be
used to simulate these processes (Findler 1979).
These perceptual descriptive categories reflect the struc­
ture o f the world and our interactions with the world ( Rosch
et al. 1 9 7 6 ). Natural scenes contain a variety o f distinct
objects that fall in to natural classes determ ined by related
features that persist over tim e. For example, m ost land ani­
mals have fur and legs, while most birds have feathers and
fly. Im plicit descriptive rules express general properties ot
real scenes, and place constraints on the interpretation o f
potentially ambiguous stim uli (H ow ard 1974).
Through learning, wc develop hierarchical descriptive
structures. These structures do not require language since
they are evident in nonhum an specics. Experts in a task,
such as recognizing makes ot car or interpreting X-ray
images, develop refined descriptive structures. For example,
see Tanaka and Taylor (1 9 9 1 ) and Schyns and Rodet
(1 9 9 7 ).
At the symbolic level wc con stru ct elaborate classifica­
tion schem es, such as the Linnaeus classification o f animals
and plants, which can be passed to person to person. By
com parison, perceptual descriptive systems are loose co n ­
glomerates o f locally uniform systems w ithin which there is
com putational power over local descriptive domains. But
there is no com m on syntax or grammar, and no com m on
set o f axioms or rules beyond the local domain. H ence, pre­
linguistic descriptive processes do n o t have the descriptive
power ot a sym bolic language although, in practice, they
usually outperform sym bolic systems. For example m ost
people can recognize when the rules o f perspective have
been broken even though they have no explicit knowledge
o f those rules. W e normally perceive things or behave with
respect to them quite adequately w ithout being able to say
how we do it. O nly when we can express adequately what
we are doing arc wc able to outstrip our own prelinguistic
performance.
The piecemeal specific schematic structures typical o f
perception are adaptive for an evolving creature, where the
first priority is to develop the capability to deal with many
diverse and local contingencies in a complex environment.
General computational power is a luxury that can evolve later.
Perception is not language-like in the sense o f using symbols,
but it is language-likc in the sense o f having some uniform ity
o f representational structure within local schemata (Ncisser
1967; Newell and Sim on 1972; Bryant 1974).
 A lthough we arc generally conscious of* the things we
perceive we are not conscious o f im plicit descriptive pro­
cesses. For exam ple, we may recognize people while noc
being aware o f che facial features that we use. W e also behave
appropriately in com plex skills and social inceraccions w ith­
o u t explicit knowledge o f the rules that guide us. The struc­
ture o f im plicit knowledge can be inferred only from
behavior. For exam ple, we can infer from che way a child
speaks chac the child has acquired som e knowledge o f the
rules o f grammar. But the child is noc consciously aware o f
chose rules.
4 .6 .3 b Feature D e te c to r s and
Perceptual Sch em a ta
Dedicated neural units seleccively tuned to a composice
feature code higher-order features, such as the direction ot
approach o f a visual o b ject. A system o f dedicated hardware
o f this cvpe is che mosc efficient and rapid way o f coding
vital types o f inform ation that recur frequently. The exten­
sion o f this idea to more com plex features has given rise to
che concepc of' che p o n tifical c ell, or grandm other cell—
a cell specifically dedicated to the recognition o f features as
com plex as o n e s grandm other. The notion o f dedicated
hardware at this level o f com plexity has severe lim itations,
since it would require an explosively large num ber o f
dedicated cells, each o f w hich would be dorm ant most
o f the time.
A more efficient cod in g process for com plex features is
d istrib u ted co d in g . This is analogous to com puter pro­
gram m ing, in w hich com plex forms are stored as general
descriptions o t com ponents and rules o f com position (algo­
rithm s). Language works this way, and rhe higher processes
o f perception have language-like properties. For instance,
when we recognize a face we construct a type o f description
by com bining features from different parts o f the face, an
ability reflected in the way a portrait is built up by police
sketch artists (see Rolls 1 9 9 4 ; Rolls and Tovee 1995).
W hereas che num ber ofscim uli that can be encoded by local
pontifical cells increases linearly with che num ber o f cells,
the num ber o f stim uli that can be encoded by distributed
descriptive processes increases exponentially with the
number o f cells. Rolls ec al. (1 9 9 7 ) produced physiological
evidence thac faces are coded by a distributed process in the
temporal lobe o f the monkey. We will see in Section 5.8.3b
thac neural processes in che inferior temporal cortex are
involved in coding perceptual descriptions o f objeccs.
4 .6 .3 c The Ideal Pcrceiver
An ideal descriptive domain is one thac can be fully
described, that is, one about which all answerable questions
can be asked and answered. The finite groups o t machemac-
ics are prototypes o f perfect descriptive dom ains. For
exam ple, the 17-space group o f crystallography and the
group that generates che sec o f five Platonic solids (regular­
sided polygons) are ideal descriptive dom ains. Linear per­
spective is also an ideal dom ain, for it is possible to fully
describe linear projection trom three to tw o dimensions
(Section 2 6 .1 ). An ideal descriptive system is one that has
com plete knowledge o f an ideal descriptive dom ain. It may
construct descriptions that a less adequate system does not
understand. Also, only a p erfect system can com pletely
assess the adequacy o f another system.
There can n ot be an ideal perceiver for a natural objecr,
tor nobody can know all there is to know about a natural
o bject. A theory o f perception maps the descriptive struc­
tures ot a perceiver— n o t into the world— but into a verbal
or mathematical description o f some abstracted aspect of'
the world that che investigator creates. The em pirical study
o f perception and cognition is essentially che study o f che
constraints o t natural pcrceivers and thinkers and o t the
ways in w hich such constraints change with experience.
Such an enterprise is always lim ited by the adequacy o f the
explicit descriptive functions that investigators possess, chac
is, by the adequacy o f the descriptive structures ot science
and mathematics.
The description o t an ideal perceiver tor a given domain
is essentially che prescription o f what must be done to suc­
ceed in a specified task that faces a perceiver with defined
discriminacion capacicy. Such a prescription can also be
regarded as a feasibility test— it establishes chat the speci­
fied task is solvable. It defines chose aspects o t the task that
are attributable ro rhe requirem ents o f the task (given the
discrim ination constraints ot the perceiver).
M ost, if nor all, com puter sim ulations o f perceptual
processes attempc со con stru ct an ideal perceiver for a
defined task performed in the co n text o f a defined set o f
environm ental constraints. Psychologists, studying natural
pcrceivers, need to define the stim uli, the task, and the envi­
ronm ental constraints in as perfect a form as possible. O nly
then can they determ ine che descriptive structures that
people use, with all their contrad ictions, contusions, and
omissions. W e need sim u latio n so f interesting ways in which
perception fails and o f systems that learn by failing.
There is an unspecifiably large num ber o f ways to
describe any natural object. For example, consider the per­
ceptual and conceptual descriptive dom ains that relate to
the human bodv.
/
1. К i>iesthetic body Th is refers to the sensory and
perceptual processes th at underlie our ability to judge
che relative spatial dispositions and movements o f
unseen body parts.
2. Seen body This refers our ability to visually recognize
parts o f our own body o r direcc che gaze Co a particular
part o f the body.
3. Body schema This is the set o f descriptive rules and
scored daca responsible tor che sense o f familiaricy wich
 our own body. Ic is responsible For che phancom limbs when presented with an incom plete stimulus. For example,
chat people report after am putation. This schem atic they can be asked to interpolate che pach followed by an
structure is probably intim ately connected wich che objccc when ic moves behind an occludcr. In whac may
m ocor com m and centers that direcc movements and be called the “w hcn-does-it-look-right” technique subjects
body parts. pick out the corrcct stimulus from am ong several displays.
Finally, one can measure a person’s ability to adapc to anom ­
4 . Body image This is the set o f descriptive rules chac
alous cxpcricnccs. The behavioral methods for teasing out
enables us to imagine our own body.
the structure o f perceptual schem ata need enlarging and
5. Conceptual body This is chc knowledge scruccurc chac systematizing.
allows a person to make such statem ents as “I have two The following are som e examples o f descriptive dom ains
arms, one nose, and ten fingers.” for which there is good cvidcncc that they arc represented
ac chc perccpcual prelinguiscic level.
6. Pictorial body This enables us to recognize ourselves in
drawings and pictures.
4 .6 .3 d T ra n s fo rm a tio n s
7. Anatomical body This is that set o f data and rules thac
enables chc surgeon со navigate the body o f a patient or This section deals wich chose scruccural feacures o fcla sse so f
pass an anatomy exam ination. It is a collective product objects that are invariant under contorm al transform ations.
o t human perccpcion and intellect. These are point-for-point cransformacions chac preserve
angles buc noc lengths, straightness ot lines, or parallels.
Think o f the variety o f descriptive dom ains chac we can These transform ations occur in the evolution and growch o f
use when we look ac a face. We can recognize it as a face biological forms. The classic discussion o t the invariant
racher chan noc a face. W ichin chc dom ain o f faces chere are properties o f natural objects is contained in D ’Arcy
discincc feacures chat allow us to recognize the species, sex, W entw orth Thom pson’s book On Growth an d Form , first
family, and individual. O th er feacures allow us со recognize published in 1916. Figure 4 .1 3 shows three primate skulls.
changes that can occur in a given facc, such as aging or O n casual inspection, they do not seem to have a similar
changes o f mood or health. Finally, there arc sicuational fea­ shape. However, if one o f chcm is plocccd on Carccsian
tures that allow us to recognize chc orientation, vantage coord inaces, che ocher skulls can be derived by applying a
poinc, and m orion o f a facc. All these features arise from the contorm al transform ation со chc coordinates.
same basic anatom ical structures and ways o f m oving that Carcooniscs have developed similar mechods for produc­
define a facc. W c perceive faccs in all these ways wichouc ing cartoons, which scrcss certain essential features o f chc
necessarily being aware o f whac feacures wc are using. We
recognize fam ily rcscm blanccs and carcoon drawings o f
fam iliar people (D od w cll 1983).
The cask o f analyzing perceptual syscems is furchcr com -
plicaced by che facc chac, for any defined cask, a person may
call on m ore than one dcscriptivc system for an answer. But
the answers may noc agree, in w hich case we say chat the
person has an illusion. For instance, chc amputee wich a
phancom arm will decide he has tw o arms when lie relcrs со
his body schem a, buc chac he has only one arm when he
refers to his seen body. In the M iiller-Lyer illusion, die lines
appear unequal in Icngch when “cycballcd” but arc reported
as equal when end-to-end m atching is applied. It is som e­
times not possible со decide which description to trust.
C him panzee
The science o f perceptual systems consists o f studying
the structure, growth, and adequacy o f such rule systems and
relationships between chcm. Ic is a matccr o f empirical inves­
tigation, just how che various syscems relate, and the safest
initial assumption is that they funccion indcpcndcncly.
Bayesian analysis has been used со investigate the ade­
quacy o f observers’ prior knowledge o f a stimulus domain
on their ability to discriminace or identify stim uli (see
Scction 3 .6 ). In a broader co n tcxt, chc adequacy o f pcrccp-
cual schem acacan be studied by the following procedures. In Figure \. 1 3. TriiftsJannAlions tn the evolution o f dculls. (Adapted from D'Arcjr
the production m ethod, subjects extrapolate or interpolate Wcmworih Ihompson 1952)

t agurс 4 . 1 1. Transfirm atU m s used by caricaturists. (From Rulesf i r Draming
C a rica tu res b y Гтдгки G ro se 1 7 8 8 )
original. Artists also use such m ethods to explore the rela­
tionships between faces of' different types so as to improve
their graphic descriptive powers. Figure 4 .1 4 is from an
18th-century text on the techniques ot* drawing, which
employed the same m ethod used by Thom pson (1 9 5 2 ).
There are two descriptive dom ains in any transform a­
tion. O n e is the transform ation rule, and the o ther consists
o f the invariants that survive the transform ation.
W e can ask what transform ations and invariants o f
visual stimuli people can norm ally recognize or can be
taught to recognize. The perceptual constancies, such as size
and shape constancy, involve the appreciation o f simple
rules o f transform ation (C h ap ter 2 9 ). A ttem pts have been
made to reveal whether people use more complex transfor­
mation rules, such as the cross ratio o f projective geom etry
(Section 2 6 .3 .3 b ). There is a large literature on the ability o f
people to recognize objects from different viewpoints.
There have been many studies ot biological m otion, involv-
ingsuch things as che ability to recognize the sex o f a person
trom the m otion ot points ot lights attached to the body
(T r o je e ta l. 2 0 0 5 ).
4 .6 .3 e Sym m etry•
•
L et each point in a given pattern be mapped o n to a distinct
point in a second pattern. For all pairs ot points, let the
mapping involve the same isom etric transform ation o f
translation, rotation, reflectio n ,o r glidc-reflection. The two
patterns are said to have translation, rotation, reflection, or
glide-reflection symmetry about a defined axis o f sym m e­
try, as shown in Figure 4 .1 5 . A translational o r rotational
m apping may be repeated about the same axis o f symmetry
to form a series o f connected or separated symmetrical pat­
terns. A pattern may have cwo or m ore axes o f symmetry o f
the same or different types. For example, a square has tour
axes o f m irror symmetry and one axis o f i oration symmecry.
Mosc com m on objects have ac least one axis o f mirror
symmetry. For a fascinating introduction to the su bject o f
symmecry see Shubnikov and Kopcsik (1 9 7 4 ).
(a) Translation sym m etry
(b) Rotation, o r point sym m etry (c) R eflection sym m etry
(d) G lide-reflection sym m etry
li(«> 1.1 v T he fo u r basic types o f sym m etry.
The visual system is particularly sensitive со symmetries
o f all kinds (Kahn and Foscer 1981; Fisher and Bornscein
1982). Mosc invescigacors have concencrated on m irror
symmetry (C orballis and Beale 1970; Barlow and Reeves
1 9 7 9 ; Barret ec al. 1999; Tyler 1999). See Howard (1 9 8 2 ,
Chapcer 14) tor a review o f studies on the perception o f
symmecry in shape recognicion. Lee us look ac one inceresc-
ing case involving symmetry in three dim ensions, which
illuscraces che im porcance o f che concept o f chc group in
perception and cognition.
Mosc people say chac cheir image in a m irror is reversed
trom left to right but not reversed top to b o ttom . But they
cannoc understand how a symmetrical m irror can produce
a seemingly asymmetrical effect. C rou p theory solves the
problem.
Take an asymmetrical o bject, such as a hand. Let the
дг-axis be bccween little finger and rhumb, the Y-axis be
between finger tips (top) and wrist (b o tto m ), and the г -axis
be between palm (fro n t) and back. C all che opposite ends
o f an axis its poles. L et a 180°-rocacion abouc the л -axis be
picch (/>), that abouc the jy-axis be yaw (y), and that abouc
the г -axis be roll (r). D cnoce congruence betw een the poles
o f an axis o f one hand and che poles o f che same axis o f
another hand by 1, and denote noncongruence o f poles by
0. Start with two identical hands in the same orientation
and allow ISO0 o f rotation about each o f the three axes.
If we take the axes in the order xyz, all relative orientations
o f rhe identical hands are represented in the group
Table 4 .1 . Ic is a group because it is closed, associative, and
contains an identity elem ent (no location) and an inverse
elem ent (opposite rotacion) (Section 3 .7 .1 ). The symmetry
o f che group cable indicaces chat the group is commucacive.
This means thac che order o f rocacions does noc make
T a b le I . ! . T H E G R O U P T A B L E F O R M A T C H IN G T W O T a b le 1 .2 . T H E G R O U P T A B L E F O R M A T C H I N G
I D E N T IC A L O B J E C T S . O N E O B J E C T IS R O T A T E D 180* E N A N T IO M O R P H S . O N E O B J E C T IS R O T A T E D 180"
A B O U T E A C H A X I S F R O M F .A C H O F A S F .T O F A B O U T E A C H A X IS F R O M E A C H O F A S E T O F
S T A R T IN G P O S IT IO N S . E A C H S E T O F T H R E E N U M B E R S S T A R T IN G P O S IT IO N S .
I N D I C A T E S M A T C H E S A L O N G T H F X - , Y -, A N D Z - A X E S
AXIS O F ROTATION
R E S P E C T IV E L Y , W IT H 1 IN D IC A T IN G C O N G R U E N C E
A N D O IN D IC A T IN G N O N C O N G R U E N C E . STARTING PO SITIO N PITCH YAW ROLL

A X I S OK R O T A T I O N 011 000 1 10 101

ООО O il 101 110
STARTING POSITION PITCH YAW ROLL 110 101 011 000
101 110 000 011
010 001 1 11 100
001 010 100 III
III 100 010 001
I0U 1)01
The group table is shown in Table 4.2. No entry in Table 4 .2
111 010
is the same as any entry in Table 4 .1 , because one can go
from Table 4.1 to T ib le 4 .2 only by reflection, w hich changes
any difference. The group may also be represented by а the m atch on only one axis. H ie two groups arc said to be
Cayley diagram. In this ease, the Cayley diagram is the blue coscts o f the larger group formed by com bining them.
tetrahedron in Figure 4 .16. Each apex o f the diagram is a The tw o groups can be com bined to form one com m u ­
state o f relative orientation o f two identical objects, and tative group by adding the operation o f reflection, as shown
each side denotes a 180" pitch, vaw, or roll rotation o f one by the green lines in Figure 4 .1 6 .
o b ject relative to the other. The answers to all m eaningful questions about m atch­
Now take tw o hands o f the same person or a hand and ing an o b ject and its m irror reflection are contained in che
its m irror reflection. They cannot be made congruent along group table. All arguments betw een people with incom plete
all three axes. O b je cts o f this sort are cnantiom orphs. knowledge o f the group are spurious, like those between
two blind men who feel different parts o f an elephant.
Paradoxes stem from misrepresentations o f the group.
010 The statement that o n e s m irror image is reversed left-
right but not up-down is misleading. It can be seen in Table
4 .2 that an o b ject and its cnantiom orph can be m atched on
any pair o f axes o r on none, depending on w hether the
operation o f translation, pitch, yaw, or roll is applied before
the o b jects are com pared. Thus we can walk into own reflec­
tion and m atch all but the front-back. O r we can imagine
ourselves rotated about the body’s x-axis (p itch ) and match
all but the head and feet. O r we can rotate about the Y-axis
(yaw) and match all but the hands. Finally, we can rotate
about the Z-axis (roll) and leave all axes unmatched. There
is no logical priority for any one o f these operations.
W hen we wish to identify the left and right hands o f a
person facing us, we naturally rotate or imagine ourselves
rotated about the Y axis to bring the head-feet and back-
fron t axes in to congruence. W e intuitively realize that the
left and right hands are congruent only when the o ther two
body axes are congruent. W e do n o t need a rotation to iden­
tify the head and feet or the front and back o f another
person because these features have distinct shapes. I f all
Hj.mc4.i6. A 3 -D C aU y diagram form irror-reflectu m . The blue tetrah ed ron people had blue left hands and red right hands we would
ind icates how th e X - , Y -, and Z -a x cs o t tw o id en tical 3 -D o b je c ts can be n o t need to apply a rotation to identify left and right
m atched by 1 8 0 ° ro ta tio n o f on e o t th e o b je c ts a b o u t each o f three
hands.
o rth o g o n a l axes. T h e red tetra h ed ro n in d icates all ways in w h ich an
o b je c t and it m irro r reflection (cn a n tio m o rp h ) can be m atched . Each Youngchildren behave differently. Even i f they can iden­
set o f th ree n u m b ers in d icates w h eth er the o b je c ts m atch ( I ) or d o n o t tify their own left and right hands they get confused when
m a tch (0 ) alo n g th e X * . Y -, and Z -a x c s respectively. E ach red and blue asked to identify the hands o f a person facing them and are
line represents a ISO 1' rotation ab ou t the roll (r ), p itch (p ), o r yaw (y)
more likely to say that the hand directly facing their left
ax is o f o n e o b je c t relative to the other. E ach green lin e represents
reflection o t o n e o b je c t relative to the o th e r a b o u t an axis in d icated by hand is a left hand. The answer is correct with the mirror
w hich o f th e th ree num bers changes. image, but not with another person.
 The m irror problem arises because we confuse the
enantiom orphic m irror image of ourselves with the body of
another person and apply the same rotation test. W ith the
m irror image, the test reveals that left and right do not
match when the ocher two body axes arc congruent. W e say
the m irror has produced a left-right reversed image. W c find
it difficult to imagine m atching ourselves with our m irror
image by a tran slation ,or a rotation abouc chc .v-axis (p itch )
o r the г -axis (ro ll) because wc intuitively realize that these
operations bring one or both o f rhe o ther body axes into
noncongruence. However, i f we apply chcm, wc see chat it is
just as valid to conclude thac our mirror image is reversed
fronc-to-back, head to toe or along all three axes as it is to
say that it is reversed left со righc.
People also puzzle over why the m irror image o f print is
left-right reversed, bu t noc upside dow n. C onsider a printed
word on a transparent plate o t glass. The print and ies reflec-
cion arc boch normally orienccd wich rcspecc со a viewer.
Thus, a m irror does n o t reverse or invert print. We see the
o ther side o f the print in the m irror but, since the cwo sides
are the same, this has no effect. W ith print on opaque paper
we must either rotate the paper vertically o r horizontally to
see ics reflection. A ccording to which rocation we apply we
see the print either reversed or inverted. It is n o t the mirror
that causes che reversal or inversion buc the rotacion applied
to the sheet o f paper (G regory 1999).
The m irror problem dem onstrates that our descriptive
structures arc often an incom plete subset o f more valid and
com plete group structures, w hich it is often possible со
define abstractly. A well-defined group is che theory o f
the ideal perceiver (and thinker) for that descriptive
task. The theory ot the ideal perceiver can be com plete
w ithin chc dom ain o f a specified group, buc there arc always
more general group structures (theories) to be discovered.
M athem atical descriptions allow us to define groups thac
are m ore complece, more com prehensive, and more certain
than those chat our percepcual syscem exhibics. Machcmacics
thus provides an abstract theory o f perception or intelli­
gence in terms o f w hich we can assess natural perception or
intelligence.
A ny theory o f natural perform ance in a given dom ain is
an account o f how rhe assumptive structures that are
inferred from behavior relate to the ideal perceiver for that
dom ain. The ideal perceiver is a system that knows the com ­
plete structure o f a defined descriptive dom ain, and is both
an account o t what is perceived and of "how " it is perceived.
It docs noc prescribe the hardware (neurons, cransiscors,
etc.) needed to realize a perceiver, but it can specify the
operations (program ) th at the perceiver could carry out, as
fully as one wishes.
A bstract groups have always fascinated people. This fas­
cination is apparent in the way che G reeks, Kepler, and arr­
ises such as Escher have pondered the group o t five Platonic
solids. These are che only possible regular-sided solids. Such
groups are fascinating because chey are derived by ehoughe
and yec inform us abouc che world. W c know m orecercainly
chat there cannot be an o b ject in the world that fits the
description “sixth regular solid” than wc know any fact
derived from observation. It was this that led Plato to dispar­
age perception and idealize geometry. Thus we know things
about the world by referring to group structures within
abstract descriptive syscems as well as by observacion.
The m ost powerful scientific theories are those that
describe grouplike structures, such as M en d cleef s table o f
chem ical elem ents, crystals, or fundam ental particles,
because these group structures tell us what to look tor, and
what kinds o f things can n ot be found. There seem to be no
psychological studies o f group concepts, although Piaget
used the con cept o f groups inform ally in his theory o f co g ­
nitive development. Por an introduction to group theory
see Budden (1 9 7 2 ).
4 . 6 . 3 f E q u ilib riu m Stru ctu res
The forms o f natural objects have a regularity that results
from the interplay o f com peting forces. A snow crystal
has a six-fold symmetrical branching structure because
o f the interplay betw een che forces acting during its
growth and certain constraints in the system. D ’Arcy
W entw orth Thom pson (1 9 5 2 ) showed how the forms o f
many animals are determ ined by similar principles. For
instance, Figure 4.17a shows the skeleton o f a radiolarian,
and Figure 4 .1 7 b shows the same form constructed by dip­
ping a tetrahedral frame in a soap solution. The principle
that determ ines these shapes is referred to as the principle
o f least effort, or the principle o f equilibration. The shortest
route on the surface o f a sphere (geodesic), the brachisto-
chrone problem (the curve o f m ost rapid fall in a diagonal
d irection ), and che shapes ot honeycom b and living cells are
other examples o f equilibrium systems, w hich can be under­
stood with the help o fth e calculus ot variations (see C ourant
and Robbins 1 9 5 6 ). These structures arc essentially eq u ilib ­
rium states that maximize or m inim ize the values ot certain
variables.
The layout o f the cerebral cortex seems to be governed
by these principles (Section 6 .4 .2 ). The principle o f least
effort also applies to certain form s ot behavior. For example,
the principle is represented in the path we follow when we
run round obstacles. This is determ ined bv
J the inertial
forces accing on che m oving body and by reflexes and skills
that we are not aware o f exercising.
The principle also operates in perception when we per­
ceive the apparent path o f an o b ject as it moves behind an
occluder o r when wc resolve ambiguous stimuli. The way
we interpret ambiguous stereoscopic displays seems to be
guided more by a preference for flat surfaces rather than for
geodesic surfaces (Section 2 2 .2 .1 ).
A nother related set o t structures is the spirals, as repre­
sented in the shapes o f shells, horns, whirlpools, and in
the flight o f m oths round a flame or ot diving talcons

(a ) S ke le to n o f a ra d io la ria n
(b ) Soap film o n w ir e fra m e . T h e in n e r sh ap e v a rie s in size.
f * . rc 4.17. Equilibrium structures. (From D ’A rc y W en tw o rth T h o m p son 1 9 5 2 )
(Callimitria agnesae)
spatially, and causal relationships may be represented as
intersections, pointers and the like, as in flow charts, family
trees, sw itchingcircuits, state diagrams, and Cayley diagrams
(abstract state diagrams o f groups).
There have been relatively few studies o f the perception
o f causal structures. M ich o tte (1 9 6 3 ) investigated the phe­
nom enology o f causal impressions. H e set out to prove that
impressions o f causality are direct and unlearned rather
than interred trom a sequence of events, as proposed by
British em piricists such as Hume. However, M ich o tte did
n o t study young children (see O lum 1 9 5 6 ), nor did he
study the ways in w hich adults change their descriptions as
a result o f experience. Therefore, his results, interesting
though they are, tell us n oth in g about w hether impressions
ot causality are innate or learned. Furtherm ore, M ich o ttes
experim ental procedures have been called into question
(Joynson 1971).
Paradoxically, the technique th at M ich o tte used is ideal
tor investigating the role o t experience in the perception ot
events, the thing that M ich o tte him self did not study.
G ruber et al. (1 9 5 7 ) investigated this question. They
showed th at delaying the tim e betw een rhe removal o f a
support and the collapse o f a bridge modified the impression
o f what caused the bridge to fall.
Implicit physics is a branch of psychophysics concerned
with how accurately and precisely people make judgm ents
or perform tasks thac embody some natural property o f
physical objects. There are four psychophysical procedures
for revealing the assumptions that underlie the perception
of events.

(Section 3 3 .6 .2 ). The appeal ot spirals in art suggests that
we appreciate the underlying orderliness o f these structures,
but behavioral studies seem to be lacking.
Branching structures are also well represented in nature.
The perceptual recognition o f different species o t tree
involves the building o f a descriptive domain that operates
over the relevant variables, such as the num ber and spatial
disposition o t branching patterns at each node and the dis­
tance betw een nodes. Botanists have developed formal
descriptive systems tor this purpose. The theory o t the ideal
perceiver o f spirals and trees is the m athem atical theory o f
spirals and trees (phyllotaxis). It is the jo b o t experimental
psychology to determ ine to what exten t a human observer
is or can becom e such an ideal perceiver tor defined
structural domains.
1. Extrapolation In this procedure the subject observes
an event sequence, such as an o b ject moving in
a spiral. The m otion is interrupted, and the subject
extrapolates the m otion by moving a point o f light,
or by selecting one o f several m otion paths. This
procedure has revealed that m ost people expect a ball
will move in a curved path when released from moving
in a circular path. It actually moves in a straight
tangential path.
2. The “when-does-it-look-right method In this procedure
the su bject is shown a sequence o f simulated physical
events and is asked to select the one this is physically
correct. For exam ple, the su bject may be shown a movie
o f two balls colliding and then separating, only one o f
which is a true depiction o f tw o actual balls.

3. The "cognitive prism m ethod The subject is exposed for

4 .6 .3 g Causal S eq u e n ces— S tru ctu res o f Events
W h en we ask “w hat caused ‘X,’” we seek a description o f a
structure o t events in which " X " plays the role o t a neces­
sary consequent event. In theory, there is always an infinite
num ber o f such descriptions, but the con text in which the
question is asked usually prescribes the type o f answer
required. Sequences o t events over time may be represented
som e time to an event sequence that is distorted by
som e means hidden from the subject. For example,
subjects may be trained to catch a ball that moves in
an unnatural trajectory. O n e can measure how long it
takes to adapt and to what extent the adaptation affects
their perception o f the true trajectories o f moving
objects.
4. V)e method o f confrontation M ost people maintain
grossly distorted assum ptions about the natural world.
For exam ple, many people believe that o b jects that
differ in weight fall at different velocities, that a moving
ball rebounds from an identical stationary ball, and that
a thrown o b ject falls straight down alter reaching its
peak height. In the m ethod o f confrontation one asks
what people do when confronted with a display that
contradicts their assumptions.
For example, m ost people believe that liquid in a tilted
jug slants up toward the spout in proportion to the angle o f
tilt (Howard 1 978). In chis case, people assume a propor­
tional relationship betw een two sensory features that does
n o t exist— liquid remains horizontal as a jug is tilted.
An amusing example o f naive understanding o f spatial
relationships was provided by H in to n (1 9 8 7 ). L et a large
collection o f pins be released at random . As the pins fall in
a vacuum, will there be more vertical o r m ore horizontal
pins? There will be many m ore horizontal pins becausc
there is only one way a pin can be vertical but many ways in
which it can be horizontal. W h a t about falling pennies?
M ost people have a very inadequate understanding o f
natural dynamics, such as falling o b jects, bouncing balls,
and objects released from circular m otion. People’s under­
standing o f natural dynamics is discussed by Proffitt and
Gilden (1 9 8 9 ). Nevertheless, artisans with no formal edu­
cation built elaborate devices through a process o f creative
im agination and trial and error (Ferguson 1977).
In some cases, people believe two features are noc related
when they are. For exam ple, m ost people say that a loop o f
string held in the shape of a square encloses the same area
when it is pulled in to a rectangle. They becom e confused
when the string is pulled out until the area is zero. They
assume that deform ing a loop o f string is the same as cu tting
a shape and reassembling the pieces. The isoperim etric prin­
ciple states that the area o f a rectangle enclosed by a perim ­
eter o f constant length is the product o fle n g th and width,
which is greatest when the tw o dim ensions are equal.
The history o t science is replete with examples ot how
progress was held up because people had an inappropriate
assumption about how objects and events are related. For
exam ple, before G alileo, everyone believed th at heavy
objects fall faster than light objects. They also had an inap­
propriate m ental picture o f the path of' a projectile, and
believed that if the world rotated an o b ject would fall at an
angle when dropped from a tower. M ost people still have
the same erroneous m ental structures.
W hen invalid assumptive structures are found, we can
apply the confrontation procedure described above. This is
just what G alileo him self did when he becam e the first
person to realize that the mass o f an o b ject does nor affect
the tim e it takes to fall a given distance. H e imagined two
weights linked together by a fine thread. 'Ihey now becom e
a heavy weight and should, by the assumptions made at the
tim e, have fallen faster than if they were n o t join ed by the
thread. But, i f this were so, one would have to say that one
o f the weights was pulling the other, which is impossible.
The onlv• wav
в to avoid this contradiction is to assume that
heavy and light weights fall in equal tim e (air resistance
apart).
Perhaps at the root o f all theoretical scientific advances,
there is a confrontation experience— a realization that the
old form ulation leads to a con trad iction . C o n fron tatio n
experiences are at the root o f perceptual learning, that is,
the acquisition o f more adequate and valid perceptual struc­
tures. C on fron tation s are also fundam ental to the scientific
enterprise o f constru cting adequate models ot perceptual
processes.
The perceptual system also em bodies im plicit rules
about how m otion, occlusion, depth, transparency, and
shadingare related in real world scenes (Stoner and Albright
1993). Im plicit perceptual schemata involving stereoscopic
depth are discussed in Sections 22.1 and 2 2 .2 .
4 . 6 . 3 h S y m b o lic D e s c rip tio n s
An ex p licit d escrip tive p ro cess is represented at the co n ­
scious level and is built on the use o f symbols. Symbols
allow things to be named and described in arbitrary abbre­
viated representations that form the basis for an econom ical
m nem onic system. Sym bols enable us ro define new equiva­
lence relations w ithin an existing descriptive dom ain and
thus derive ever more com plex descriptive functions or clus­
ters of such functions. Sym bolic descriptive processes can
have great com putational depth, generality, and economy,
as in the descriptive structures of science or when a person
derives a m athem atical theorem from a set o f axioms or
learns the distinctive features o f different makes o f au tom o­
bile. W e can recursively apply a symbolic system to itself.
For example we use language to describe the grammatical
structure o f a language. Im plicit descriptive functions
underlying perception are not used recursively in this way.
The perceptual system does n o t describe itself.
To describe an o b ject verbally one m ust identify rele­
vant features and their spatial or tem poral relationships.
However, we may not be able to describe an o b ject that we
can recognize. For example, people are generally poor at
describing faces from memory. Also, we may not recognize
an o b ject that we can describe. Patients with agnosia can
describe fam iliar objects w ithout being able to recognize
them . W e can describe unfam iliar or imaginary objects.
There is an unspecifiably large num ber o f ways to describe
any natural o b ject because an o b ject has an unspecifiably
large num ber o f features— ic can be perceived as belonging
со any o f a large num ber o f scimulus domains.
Natural languages do noc achieve the sam e degree
o f uniform ity o f symbolic expression that is achieved by
the formal systems o f logic and m athem atics. Languages
are relatively loose conglom erates o f specific descriptive
dom ains, unified by a com m on grammar (phonem ics,
syntax, and inflection) bu t n o t by a com m on set ot axioms
or function rules. There is com putational power within
local dom ains but often verv little between them . This is
why people tolerate so many contrad ictions and fail to
appreciate what may appear to others as obvious relation­
ships. Humans invent and enlarge the scope ot sym bolic
descriptive systems in historical rime.
An explicit description o f an o b ject may include the
nature o f its parts and the way they are organized, rhe
way the item changes over tim e, and what it does when han­
dled in some way. M insky (1 9 6 1 ) called these descriptions
“articular” descriptions to distinguish them from simple
class assignm ent descriptions (see also Clowes 1971). Such
descriptions are potentially infinite tor any o bject, tor they
may be applied recursively; that is, each product o f analysis
can be an item ot further analysis.
The descriptions that we trust the m ost are used to
define and construct what we call reality. W e then use this
con stru ct to test the validity o f other descriptive systems.
Generally speaking, today s scientific descriptions are based
on identity m atching operations such as are involved in
using rulers and reading a vernier scale, or m atching D N A
sequences. These highly valid and often highly sophisticated
modes o f perceiving and describing the world were devel­
oped in historical tim e. The less developed they are, the less
adequate are the means o t resolving contradictory experi­
ences, and humans invent the co n cep t o f “magic.” That is,
they deliberately tolerate contrad ictions by saying that they
exist in the world and not just in their own imaginary
descriptive domains.
Even when techniques and knowledge are generally
available for resolving con flictin g experiences many people,
who should know better, accept magical explanations ot
illusory effects, such as the conjuring tricks o f m ediums and
stage mystics.
We can discover new descriptive dom ains by observing
objects and events in the natural world. For exam ple, we
may walk around an o bject, or fly around the m oon to
discover its 3 -D structure. We invent m icroscopes and
telescopes to reveal new worlds.
We can use the world .is an analog com puter. For
example, the correct shape o f an arch (a catenary) can
be determ ined by hanging a rope. W e can determ ine the
gravitational con stan t by observing a swinging pendulum.
In each case, we get a “readout” ot a natural process in
the form o f a stimulus display. W c need sense organs, knowl­
edge, and a perceptual schema or an explicit theory
with which to interpret the display in relation to the task
we are perform ing or the question we are asking. We
can also use the world as a memory/ store in the torm ot
objects or events that can be displayed or attended to at
will. Hum ans are m ore intelligent than digital com puters
mainly because they have a two-way interface with rhe
natural world. O n e task ot any theory ot perception is to
understand how perceivers acquire the ability to “con su lt”
the natural world.
Instead o f observing a real o b ject wc can observe an
analog o f the object. The analog is isom orphic with some
aspect o f the o b ject. A photograph or retinal image is spa­
tially isom orphic w ith an o b ject as seen irom a particular
vantage point and is said to be an “image” o fth e o b jcct. If
an image is blurred, faded, enlarged, projected at an angle,
rotated, or stretched, it may be possible to restore or
“norm alize” it to congruence with the o b ject and apply a
superim position o r “tem plate-m atching” test to check its
identity.
M ost com puter pattern-recognition devices operate in
this way. M ental images can be rhought o f as analogs o f
objects in this sense, but many good arguments have been
put forward tor doubting that the tem plate-m atching pro­
cedure plays a dom inant role in human pattern recognition
(N cisscr 1967; Pylyshyn 1973). There is no need to repeat
those arguments here.
The medium in which an analog o f an o b ject is repre­
sented can be arbitrarily related to the o b ject or event.
Temporal events can be represented as spatial analogs and
vice versa. For example, a phonograph record is a spatial
a n a lo g o f a piece o f music, and a radio signal is isom orphic
with a televised picture. The frequency o f nerve impulses
can be described by an experimenter as an analog o f the
intensity o f a stimulus. For any system to recognize that
som ething is isom orphic with som ething else it is necessary
lo r the system to express the structure o f the two things in a
com m on medium o f representation. O n e can n o t com pute
over incom patible data.
In an analog com puter, variables in a uniform analog
medium, namely voltages in an electrical netw ork, are set
up to be isom orphic with a defined physical system, such as
an aerodynamic system used for designing aircraft. The
sense organs achieve a general uniform ity o f expression by
transducing all stim uli in to patterns o f nervous activity
(see Rushton 1 9 6 1 ). Such a uniform medium o f expression
provides the basic “hardware” com patibility that any natu­
ral or artificial com puter requires. However, in spite ot this
underlying uniform ity in the nervous system, any given
stimulus o b ject may com e to be represented in the nervous
system in a variety o f ways. For instance, an o b ject is coded
very differently by the eyes than by the sense o f touch. If the
perceiver is to recognize that a seen o b je ct is the same as a
felt o b ject it must converge the two coded representations
into a com m on com putable form .
W hen we use an analogcom pu ter we do essentially the
same thing as observing natural objects or events but speed
the process up and bring it within a smaller spatial and tem ­
poral compass by sim ulating the feature o f the world we are
interested in. W h en we use a digital com puter, we eco n o ­
mize further by having a single m achine that can simulate
any well-defined feature o fth e world within a uniform and
4
econom ical medium o f expression (digital symbols).
 The mosc powerful representational and descriptive sys­
tems are more sym bolic than analogical. A syscem is sym­
bolic to the extent that units o f expression are arbitrarily
related to the items represented. All sym bolic systems retain
som e analogical features. For instance, expressing the fo r­
mula for a circle in term s o f noncom plcx, positive, rational
numbers implies som e isom orphism between the selected
properties o f the number space and chc spatial properties o f
circles. M athem atics is the isom orphic mapping o f aspects
o f real or imaginary things inco a structured symbol system
with rigorously defined axiom s and syntax.
Sym bolic systems often involve che conversion o f
descriptions inco linear scrings o f symbols. Thus, whac may
be an underlying n-dim cnsional descriptive scruccure is
reduced to an n-1 dim ensional expression. As in the projec­
tion o f objects into a picturc plane, this reduction o f dim en­
sions leads to am biguity. Thus, rules of syntax are needed to
disambiguate the symbol string and parse it back in to a
higher dim ensional structure, what psycholinguists call a
syntax-free expression or deep structure.
4 .7 G E O M E T R Y A P P L IE D T O
V IS U A L S P A C E
4 .7 .1 IM P L IC IT P R IN C IP L E S OF
V IS U A L G E O M E T R Y
'lb rhe excenc chac we use perspective со make judgmencs
abouc relative distances, the visual system must embody
the rules o f projective geom etry that were described in
Section 3 .7.2c. However, people are not aware o f these
rules. This issue is discussed in C hapter 26.
The generic view point described in S ection 4 .5 .9 c is a
general example o f how che visual syscem em bodies some
general rules about the spatial structure o t objects.
An o b je ct may appear com plete when only part o f it is
in view. The perceptual system em bodies a set ot structural
rules about how corners, edges, and surfaces are connected
in 3 -D o b jects, and how a changing image can signify a solid
rotating o b ject (see Section 2 8 .5 ). O b jects that do not co n ­
form to these rules, such as the o b ject in Figure 3 .2 2 are
imm ediately recognized as impossible. However, we are
usually unable to state why the o b ject is impossible. These
perceptual abilities mean that the visual system muse
em body some o f the principles o f topology that were
described in Section 3.7.2d . This issue is discussed in
Section 2 7.2.
Basic transform ations ot visual stim uli, such as the
changing size or shape o f the retinal image as an object
moves in 3-D space, or patterns o f optic flow produced by
self-m otion can be described in terms o f Lie operators
(Section 3 .7 .1 ). It has been proposed that these operators
are embedded in the visual system (H offm an 1 9 6 6 ; Dodwell
1 9 8 3 ). Inspection o f one m em ber o f any pair o f Lie orbits
for som e m inutes induces an aftereffect that resembles the
other m em ber ot the pair. For exam ple, inspection ot a
radial pattern creates an aftereffect o f concentric rings and
vice versa (M acKay 1961). G allant et al. (1 9 9 3 ) found some
cclls in area V 4 o f the m onkey that responded selectively to
stim uli resembling one or another o f the Lie orbits. Lie
operators are related to the operators o f differential geom ­
etry that have been used to describe patterns o f binocular
disparity (Section 19.5).
Although geom etrical operations arc em bodied in che
visual system, we are not consciously aware o f them.
W ith o u t specific training, im plicit rules do not provide a
basis tor explicit knowledge. Nevertheless, we are aware
when a visual scene does not conform to the usual geom et­
rical principles. For example, we can usually tell when a
drawing does not have the correct perspective and wc are
puzzled by drawings, such as those by the artist Escher, that
violate the principles o f topology.
4 .7 .2 T H F. G E O M E T RY О F V IS U A L SPA С E
For ordinary purposes we use Euclidean geom etry to record
the positions o f objects in the world. O n a cosm ic scale,
Einstein used non-Euclidean geom etry to describe the
intrinsic curvature o f space-time in the neighborhood ot
massive objects. O n e can ask w hether the visual system has
an intrinsic geom etry in terms o f w hich the positions o f
o b jects are perceived. I f so, this geom etry should manifest
itself in the way people perform psychophysical tasks, and
we should be able to derive the basic parameters ot the
intrinsic geom etry o f visual space.
The axes o f Euclidean geom etry are straight, and
Euclidean space has zero curvature. In Riem annian hyper­
bolic geometry, space is curved. A space o f positive curva­
ture is elliptical, and the axes o f a Riem annian elliptical
geom etry lie on the surface ot a sphere or ellipsoid. A space
o f negative curvature is hyperbolic, and the axes o f a
Riemannian geom etry lie on a hyperbolic cone. In Euclidean
geom etry, the angles o f a triangle sum to 180°, but in
Riem annian geom etry they sum to more or less than 180°.
For example, on the surface o f a sphere, the angles o f a
triangle sum to more than 180c.
In Euclidean space, the shortest distance betw een two
points (a geodesic) is a straight line but, in Riemannian
geom etry, geodesics are curved. For example, the shortest
distance betw een two points on the surface o t a sphere lies
along the equatorial circle, o r great circlc, through the
points. Since all great circles intersect, like lines o t longi­
tude on the Earth, geodesies in elliptical geom etry cannot
be parallel in the sense o f never m eeting. I f we assume that
the space o f visual perception is Riemannian with constant
curvature, then the main task is to determ ine the constant
that determ ines that curvature.
W h ile visiting the D artm outh Institute in New
Hampshire in 1 9 4 5 , R ud olf Luncburg was shown some
data on spacc perception chat did noc conform со Euclidean
geometry. H e also considered the puzzling results in the
Blum enfcld alley experim ents (Blum cnfeld 1913). In the
d ista n ce alley, subjects are shown a pair ot fixed lights on
the horizon, one on each side o f the median plane. A pair o f
test lights is then presented at dilferent distances on the
horizon plane and the subject adjusts their separation until
it appears the same as that o f che fixed lights. In che parallel
alley, subjects adjust two receding lines ot lights term inat­
ing in the fixed lights until they appear parallel. In Euclidean
space the settings in the two tasks should m atch. In fact, the
lights in the parallel alley arc usually placed nearer rhe
median plane than are those in the distance alley.
I.u n eb u rg (1 9 4 7 , 1 9 5 0 ) concluded that settings in alley
experim ents correspond to a non-Euclidean hyperbolic
geom etry— a geom etry o f constant negative curvature. In
the mapping trom Euclidean o b ject space to visual space,
egocentric directions arc preserved, bu t near distances arc
expanded and far distances are contracted. This conclusion
has general validity only if the perceptual geom etry remains
the same across various tasks. But we will now see that this
is noc so.
A parallel array o f lights probably provides more infor­
mation abouc absolucc and rclacivc discances chan do chc
two pairs ot lights in the distance alley. For example, sup­
pose thac the distances o f the lights in the distance-alley are
underestimated relative to the distances o f the lights in the
parallel alley. Because o f size-distance scaling, observers
would perceive the distance-alley lights as closer together
than the parallel-alley lights.
Luneburgdied in 1 9 4 9 ,but Blank and others continued
to work on che cheory in che Knapp Laboratory at Columbia
University until 1 9 5 2 (B la n k 1953, 1958). Relevant experi-
mencs were also performed by Zajaczkowska (1 9 5 6 ),
Shipley (1 9 5 7 a , 19 5 7 b ), Foley ( 19 6 4 ), Indow and W atanabe
(1 9 8 4 ), Rosar ( 1 9 8 5 ), and W agner (1 9 8 5 ).
This work was mocivaced by a desire со find a consiscent
im plicit geom etry ot visual space that underlies all visual
experience, analogous to geom etries used in physics to
describe the structure o f space-tim e. But the formal theory
is based on a restricted set o f assumptions and viewing co n ­
ditions and tells us n othing about visual mechanisms. The
experim ents are highly artificial and chc geomecry chcy
reveal varies widely/ between individuals and betw een tasks.
The results o f a given experim ent may have little to do w ith
how we perceive spatial relations in com plex visual scenes
(H e ch t et al. 1 9 9 9 ). In any case, human space perception is
subject to adaptation, contrast, figural interactions, cue
interactions, and long-term recalibration. Furthermore, d if­
ferent visual subsystems may conform со different geom e­
tries, because different cues are affected in different ways by
changes in stimulus conditions.
There is also the problem o f instructions and scoring cri­
teria. A person viewing railway lines extending into che dis­
tance may adopt a realistic criterion and report that the
lines appear parallel. O n the other hand, they may adopt an
analytic criterion and report that the images converge
(C arlson 1962). Even i f subjects are carefully instructed,
one cannot be sure about the criterion they use because they
themselves may not be fully aware o f what they arc doing.
Also, judgm ents o f the size and distance o f objects vary with
the psychophysical method (Ehrenstcin 1 9 7 7 ). The quest
tor a unified geom etry ol binocular visual space based on
judgm ents made under conditions o f reduced depth in for­
m ation is doom ed to failure.
Koenderink and van D o om (2 0 0 0 ) used a different
procedure. O bservers stood in one spot on a large meadow
with knee-high grass and distant trees and buildings. By
rem ote con trol, they set a horizontal pointer supported in a
cu be to align with a sphere, w ith both pointer and sphere at
eye level. The pointer and sphere were at chc same distance
and 120° apart. D istance varied up to 2 5 meters. Thus, the
pointer, sphere, and subject formed a triangle and the co r­
rect setting o f the arrow was 30°. The curvature o f
Ricm annian geom etry can be derived from the exten t to
which the sum o f the angles o f a triangle departs from 180°.
The triangle derived from pointer settings indicated a space
of positive (elliptic) curvature tor near distances and a space
o f negative (hyperbolic) curvature for far distances. The
transition occurred at about 2 meters. O n e crucial factor is
the accuracy o f che angular seccing o f che pointer and sup­
porting cube to the required angle o f 30° as a function o f
distance. Binocu lar disparity would probably becom e inef­
fective at about 2 meters, leaving only perspective. If the
results arise from a changing bias in the local setting o f the
arrow to 30° they tell us little about the global geometrical
structure o f visual spacc.
In a later experim ent, rhe locations o f the pointer, target,
and observer formed a right-angled triangle. Settings o f the
pointer to the target were noc che same after chc positions o f
the target and pointer were interchanged. The results rule
out the existence o f a consistent subjective scale o f straight-
ness becween two points. They therefore rule out the notion
o f a simple hom ogeneous spacc underlying visual percep­
tion (K oend erink et al. 2 0 0 8 ).
An array o f vertical rods in a froncal plane appears со lie
on a convex surface at near distances and on a concave sur­
facc at far distances. This is known as che H cring-H illebrand
deviacion. This is noc due со an inherent curvature o t b in ­
ocular visual space but rather to a lack o f relevanc discancc
inform ation. W h en more inform ation is added, the distri­
bution o f the lines is perceived correctly (Section s 14.6.2
and 20.6.5a).
Koenderink et al. (2 0 0 2 ) had subjects set a vertical pole
to the same frontal plane as two ilanking poles with all cues
to depth present. The Hanking poles were 2 or 10 m from
the subject and 3 0 , 6 0 , or 120° apart. Tw o o f the four sub­
jects performed almost perfectly, bur there was a general
tendency for the rods to appear frontal when they fell on a
surfacc concave toward the subject. Thus, an array o t frontal
poles would appear convex (negative curvature). This is
opposite to the result obtained by K ocndcrink and van
D o o m with the pointing task, which indicates that the
“curvature” o f visual space is task-specific.
C uijpers c t al. (2 0 0 0 ) asked subjects to rotate a test bar
on a vertical axis until it appeared parallel to a com parison
bar. Both bars were horizontal, at eye height, and seen
against wrinkled black plastic. Errors increased linearly
with increasing separation o f the bars, and were up to 4 0 u.
Errors did nor vary with viewing distance. C uijpers e t al.
(2 0 0 2 ) used the same apparatus, but changed the task to
that o f setting the bars into collinearity. However, these
deviations were m uch smaller than the parallel-setting
errors in the earlier experim ent. These results confirm that
the intrinsic geom etry of visual space varies w ith the type
o f task.
W e must discard the notion o f that the m etric o t visual
space conform s to a consistent geometry.
The geom etry ot binocular visual space is discussed
further in Section 2 6.1.
4.8 MECHANISMS OF ATTENTION
4 .8 .1 T H E N A T U R E O F A T T E N T IO N
A ttention is the process o f concentrating lim ited percep­
tual, m nem onic, and response resources on the task o f
im m ediate im portance. All stim uli are initially processed in
parallel in the sense organs, thalamus, and primary cortical
areas. But the initial processing is carried o u t only to a cer­
tain level, which has been called the prcattcntivc level
(Neisser 1 967). Itw ould require an impossibly large am ount
o f neural m achinery to analyze all sensory inputs in
detail. In any case, there is a response bottleneck in rhe
response system. We can move a lim b or the body in only
one direction at a time.
Visual items ot particular interest are fovcatcd, attended
to, and processed in greater detail at the level o f focal atten­
tion. Typically an act o f visual attention involves the follow­
ing stages.
4.8 .1 a Task and S tim u lu s Selection
Som e simple stimuli have an innate salicncy, which impels
us to attend to them and respond to them whatever we arc-
doing. For example, a sudden m ovem ent in peripheral
vision triggers a startle response and autom atically causes
the gaze to shift in that direction. A loom ing o b ject on a
collision course generates an avoidance response, while an
o b je c t noc on a collision course does not. A sudden move­
m ent o f rhe ground generares an autom atic postural
response. A loud noise or an unexpected tactile stimulus
generates a startle response. These responses involve only
bottom -up processing of stimuli.
Even com plex stim uli autom atically accracc our atcen-
tion. For example, we react autom atically to potentially
dangerous objects and to sexually attractive people. W'c
respond more rapidly to a peripheral stimulus when it is
one that we sec anocher person looking at (Friesen et al.
2 0 0 5 ). W c rapidly notice objects that suddenly appear in
the center o f a visual scene, especially when wc do n o t expect
to see them in that co n text (Biederm an 1 9 8 1 ). In all these
cases the stimuli have a built-in salicncy and are said to
exhibit attentional capture.
W h en we deliberately plan a course ot action we first
search for relevant stimuli or memories. This involves refer­
ring to informacion stored in memory. Relevant stimuli gain
accencional salicncy. Usually, we arc in a familiar environ-
menc and our behavior involves a continuous sequence ot
more-or-less familiar actions. W e therefore know where to
look for relevant stimuli. For example, when driving we
know where to look for road signs. The relevance o f stimuli
in che visual field is sec by the demands o f the task and by our
fam iliarity with che environm ent and the task. In an unfa-
4
miliar environment we search tor relevant stimuli and may
be bewildered when we do not find any familiar objects.
For any natural scene there is an unspecifiably large
number o f stimuli that may be relevant to a given task. For
example, when a person drives a car, salient stimuli include
red lights, stop signs, approaching pedestrians, and optic
tlow. The same stim uli may have no salicncy for a passenger
who, instead, may be interested in the con ten ts o f a shop
window. Also, for any stim ulus o b je ct there is an unlim ited
num ber o f tasks that could be performed. These tacts are
easily ignored in studies involving a restricted set o f stimuli
and well-defined responses.
A distinction is drawn between stimulus features that
arc processed in parallel that immediately “pop o u t” in
mixed displays, and features that arc identified only after a
serial search (Beck 1967, 1 9 7 2 ). A feature is said to be pro­
cessed in parallel when the time taken to find a single o b ject
with one value o f the feature is independent o t the num ber
o f surrounding o b jects that have a different value o f chc fea­
ture. For instance, the tim e taken со find a vertical line set
am ong horizontal lines is independent o f che num ber o f
horizontal lines in the display. Features processed in parallel
are described as being processed preattentively because one
does noc need to perform a serial search to find them.
A feature is said to require a serial search when the time
taken to find an o b ject with a given value o f the feature
increases with che num ber o f ocher objcccs in chc display
(Trcism an 1988).
Visual features that are processed preattentively include
orientation ,color, curvature, flicker, m otion, size, and depth
(Julcsz and Bergen 1983). Each o f chese features is served
bv dedicated feature detectors, either in the retina or in the
4
primary visual cortex. However, we will see that m ore co m ­
plex stimulus features served by dedicated detectors at a
higher level may also be detected preattentively.
 Features thac are processed preattentively arc noc
immune to the effects o f attention. For exam ple, an oddly
oriented elem ent was identified in a briefly exposed array
less accurately when subjects had to identify a letter pre­
sented at the same tim e (Joseph et al. 1 9 9 7 ). This type o f
attcntional blockage was found not to operate betw een a
visual stimulus and an auditory stimulus (D uncan et al.
1997).
4 .8 .1 b Sw itch o f A tten tion
W h en a stim ulus relevant to a given task has been found,
attention must be disengaged from the o b ject that is pres­
ently fixated and reengaged on the task-relevant o b ject
(Posner 1 980). The disengagemcnc process is revealed by
che fact chat a saccadic eye movement to a newly attended
o b je ct has a shorter latency when the gaze is not initially
centered on another o b ject (M ackebcn and Nakayama
1993).
Typically, we shift our gaze to bring the image o f a salient
o b je ct o n to the fovea, where it can be processed in detail.
We can attend to an o b je ct in the visual periphery while
fixating a central o bject, but the low resolution o f the
peripheral retina allows us to process only its coarse fea­
tures. A change o f gaze may n o t be required when attention
shifts from one feature to another feature o f the same
object.
4 .8 .1 c Sen sorv/ E n h a n ce m e n t
There is behavioral evidence that the effective contrast
o f an attended visual o b ject is enhanced and that o f sur­
rounding nonattended objects is reduced (C ap u to and
Guerra 19 9 8 ; C utzu and Tsotsos 2 0 0 3 ). Physiological evi­
dence suggests that these etfccts are due to feedback
from higher centers (Vandutfel et al. 2 0 0 0 ). Tsotsos e t al.
(1 9 9 5 ) modeled these processes. Reynolds and Chelazzi
(2 0 0 4 ) reviewed the evidence that top-dow n attcntional
modulation o f neural activity is due to increased contrast
sensitivity.
4.8.1 d E n g ag em en t of Relevant
H ig h -O r d e r Processes
The real w ork o f visual attention starts only after we have
foveatcd a selected o bject. We must then decide which parts
o r which features o t the o b ject we are interested in and what
responses to make. For any real o b ject there is an unspecifi-
ably large num ber ot parts or features that can be attended
to anil an unspecifiably large num ber o f responses that can
be made. For example, when wc look at a face we can attend
to its sex, age, expression, race, spatial attitude, m otion,
o r to any num ber o f other general features. We may also
attend to any local feature o f the face, such as the nose or a
dim ple in the chin. In an am biguous figure, such as Rubin s
vase-profile figure or B o rin g s w ife-m other-in-law figure,
the perceived identity o f the figure may change w ithout any
change in the stimulus. Even w ithout a stimulus, we can use
our attention processes to recall a particular memory, imag­
ine a real o r con cocted o bject, or execute a particular
action.
The basic purpose o f attention is to engage those per­
ceptual, memory, and overt response processes appropriate
to the perform ance ot a given task. Signals in the visual
cortex from an attended o b ject or feature are passed to rel­
evant high-order processors. Signals from nonattended
objects are simply n o t passed on to higher centers. They
continue to be processed at lower levels, but the objects
remain unidentified and not remembered (Everling et al.
2 0 0 2 ; Pinsk et al. 2 0 0 4 ).
4 .8 .2 S T I M U L U S F A C T O R S IN A T T E N T I O N
There has been a debate about whether we attend to loca­
tions, to o bjects, or to stimulus features. These alternatives
are som etim es treated as distinct theories o t attention.
However, each factor is involved in determ ining the span o f
attention and the ease o f visual search. W h ich factor is
d om inant depends on the stimulus and the task. The fol­
lowing is a b rie f review o l the voluminous literature on this
topic.
4 .8 .2 a L o catio n -B ased A tte n tio n
According to the spotlight theory ot attention, at any
m om ent wc assimilate inform ation only w ithin a particular
area o f visual space. In one sense, this theory is trivially true.
We can detect fine detail only w ithin a radius o f about Г
round the fovea. But the other claim o f the theory is that
the spatial resolution o f chc accencion mechanism is much
coarser than the basic spatial resolution o f the visual system.
This issue com es under the heading o f visual crow ding,
which is discussed in the next section.
4 .8 .2 b O b je c t-B a s e d A tten tio n
O bject-based theories o f attention stipulate that perception
takes place in tw o stages. Ac the preactentivc stage che
visual scene is scgmcnccd into d istin ct objects on the basis
o f con tou r continuity and proximity, and sim ilarity o f
texture, color, and m otion. At the focal a tte n tio n stage a
particular o b je ct is sclccced for detailed processing (Neisser
1967).
This theory is clearly true when we are presented with a
display o f well-separated simple objects. For example, it is
easier to d etect two distinct features ot an o b ject than to
detect che same two features discributed betw een two
objects (D u n can 1984).
But m ost o b jects consist o f many parts. For example,
the Jacquard silk-weaving loom shown in Figure 4 .1 8 has

F.Rurc « .is . 7b ejd cifu a rd stlk tvcA tingU om . The w hole loom is an o b jccc but
so to o arc all o f its m any p arts and saibparts.
hundreds o f pares, each o f w hich can be regarded as a dis­
tin ct o b ject. W h en we attend to the whole o b ject we recog­
nize it as a loom and can give it a name. W e can also attend
to and name each m ajor com pon ent, such as the fram e,
the shuttle, or the cloth. We can also attend to su bcom p o­
nents. For example, we can attend to the belt that contains
the weaving code, to one horizontal elem ent o f the belt,
or to one hole in one elem ent. M any parts o f the loom
lose their distinct identity as parts o f a loom when seen in
isolation.
4 .8 .2 c Feature-Based A tten tion
The time taken to find an object that differs from other
objects is independent o f the num ber o f objects in the dis­
play when the target o b ject and the distracters differ in
terms o f a simple feature such as color, line orientation, or
m otion. However, it has been reported that detection o f an
o b ject defined by the con ju n ction o f two or more simple
features is serial (Trcism an and G cladc 1980). For example,
a line that is both red and vertical does not pop out when
em bedded in a display o f lines that can be either red and
horizontal or blue and vertical. A ccording to this evidence,
visual processing at the prcattcntivc level operates on
separate simple features but not on com binations o f
features. This is called the featu re-in teg ratio n th eory
(Trcisman 1988). O n e problem in applying the theory is
that ol defining a simple feature. There are at least three
ways to define a simple feature.
1. Sim ple features may be defined as those that are
processed in parallel. This definition renders the
feature-integration theory circular.
2. A second approach is to define a simple feature as one
involving only one sensory dim ension, such as position,
color, m ovem ent, or orientation. There is then the
problem o f defining what is m eant by one sensory
dim ension. For instance, all the so-called single features
studied by Treisman (1 9 8 2 ) are really conjunctive
because the stim uli differed in retinal position as well as
in the feature being studied.
Treisman and Gelade (1 9 8 0 ) argued that stimulus
identification precedes localization while Sagi andju lesz
(1 9 8 4 ) and G reen (1 9 9 2 ) showed that identification
and localization can proceed in parallel. The answer one
gets depends on the nature o f the task (Saarinen 1996).
An identification task can be simple, such as saying
which is the odd stimulus, o r it can be com plex, such as
describing the stimulus. Similarly, a localization task can
be that o f reporting the position o f a stimulus, saying
how many odd stimuli there are, or saying where an odd
stimulus is with reference to other stimuli.
3. Finally, one can define a simple feature as one processed
by a dedicated feature detector at an early stage in visual
processing. O n this basis, a conjunctive feature would
lie detected preattentivelv i f it had a detector
specifically tuned to specific feature conjunctions.
A moving target letter X was rapidly detected when set
in an array o f stationary X s and moving O s. Thus a
con ju n ction o f form and m otion was detected
preattentively (M cL eod et al. 1988). A conju nction ot
color and form was also detected preattentively (W olfe
et al. 1989). Treisman has agreed that certain
conjunctive features are processed in parallel and
discussed various theories to account tor this type ot
processing ( Treisman and Sato 1990).
A related issue is whether one can acquire, through
learning, a dedicated d etecto r for a given feature. W ang
et al. (1 9 9 4 ) found that a letter S is easily seen am ong m irror
reversed S s but only when the shapes arc vertical, that is,
when the S looks like a letter.
People can conduct a parallel search in a 2-D display
for a feature such as color for which there are d etectors at
each location ot the display. We will see in Section 2 2 .8 .2
that the same is true for the detection o f visual features in
disparity-defined 3 -D space.
 4 .8 .3 A T T E N T IO N A N D S T IM U L U S
C R O W D IN G
4 .8 .3 a The Basic Features o f C ro w d in g
Spatial attention has been likened to a spotlight that selects
stimuli from w ithin a given area o fth e visual field. The pro­
cess works best when a person is required to respond in а
well-defined way to a fam iliar isolated o bject. For example,
we readily identify a letter presented on a blank background.
Bur the attentional m echanism may have difficulty isolating
a relevant o b ject when it is set am ong other objects. For
example, a letter flanked by other letters takes longer to
recognize than an isolated letter. This effect is known as
crowding. Crow ding weakens as the distance betw een the
target letter and the distractcr letters increases (Friksen and
F.rikscn 1 974). B u t crow ding increases as the stim uli are
moved into the retinal periphery. Boum a (1 9 7 0 ) summed
up these effects by stating that the critical spacing for
identification o t neighboring stimuli is roughly halt the
eccentricity. The critical spacing is independent o f die stim ­
ulus objects or their size. This has becom e known as
Bourn a’s law.
A grating is not detectable when its spatial frequency
exceeds about 6 0 cpd. This is not crowding. It is due to the
lim ited resolution o f eye optics and the spacing o f retinal
receptors.
Crow ding differs from masking that occurs when super­
imposed stim uli are presented simultaneously or succes­
sively (Section 13.2.1). A masked stimulus is noc visible,
whereas a crowded stimulus is visible but not recognizable.
M asking is explained in term s o f inh ibitory interactions
between excitatory and inhibitory regions ot the receptive
fields o f ganglion cells o f co rtical cells. It occurs at a low-
level o f visual processing where stim uli com pete tor access
to further processing. In crow ding, all the stim uli are
detected but interfere with each other at the level where
spatial features arc integrated into distinct objects (Pelli
et al. 2 0 0 4 a ; Pelli and Tillm an 2 0 0 8 ).
The follow ing sections describe three ways to think
about crow ding:
4 .8 .3 b C ro w d in g E ffc c ts in H ypcracu itics
Vernier acuity and other hyperacuities can be a few seconds
o f arc. They reflect the capacity o f the visual system to regis­
ter the relative positions o f two stimuli in distinct locations.
Vernier acuity is degraded when the test lines are flanked by
parallel lines several m inutes ot arc away (W cstheim cr and
Hauskc 1 975). Stereoscopic acuity is also degraded by
flanking lines (Section 18.6.2a). In boch cases, crow ding is
evident when the test stimuli and flanking stimuli are pre­
sented to different eyes (see Section 13.2.5). This proves
that the etfects are cortical.
He et al. (1 9 9 6 ) showed that crow ding in orientation
discrim ination is a high-level process. Subjects inspected
for some tim e a patch o f grating, either alone or flanked by
patches in o ther orientations. The tw o stim uli produced the
same elevation o f the contrast-detection threshold in a sub­
sequently presented isolated test patch ol the same orienta­
tion. In other words, the crowded patch produced the same
orientation-specific adaptation as che isolated patch, even
though the orientation o fth e crowded patch could n o t be
detected. 'Ihus, signals confused at a high level were resolved
at a low-level. He ec al. concluded chat crowding is due to
the low spatial resolution o fth e attention m echanism .
C row ding in hyperacuities could be m ediated by lateral
cortical con nection s (see Scction 5 .5 .6 ). The spatial range
ot crow ding is similar to the spatial range ot these co n n ec­
tions, and both processes show a sim ilar dependence on
stimulus eccentricity (Tripathy and Levi 1994). Also, che
range o f crow ding in vernier acuicy corresponded со che
spacing ot ocular dom inance colum ns in che visual cortex
(Levi D M et al. 1 9 8 5 ). Registration o f position involves
integrating inform ation over a relatively large area in the
visual cortex. Levi e t al. referred to this cortical integration
area as a "perceptive hypercolumn. '
4 .8 .3 c Low Spatial R eso lu tio n o f A tte n tio n
It has been argued that the atten tion spotlight has low spa­
tial resolution so that the identification o f an o b ject is
degraded by nearby similar objects. But »r is difficult to
understand why the spatial resolution o f high-level visual
processes should be any worse than that o f rhe basic resolu­
tion o f the visual system. W e have no difficulty attending to
a particular doc in a random -dot display, as long as doc den-
sicy does n o t exceed the basic resolution ot the visual system.
If the attention mechanism had low spatial resolution,
crowding would occur for all simple stimulus features. But
the color o f a patch becom es m ore evident when the patch
is surrounded by patches in other colors. The color o t an
isolated spoc cends со fade wich sceady fixacion. Similarly,
the m otion o f an isolated spot is difficult to detect but is
easy to detect when seen in the con text o f spots m oving in
ditterent directions (H oward and Howard 1 9 9 4 ). These
etfects arc the opposite o f those predicted from low resolu­
tion o f the attentional spotlight. Tightly packed colored
dots engage in m etam eric color m ixing, as in co lo r printing.
Also, closely packed dots m oving in different directions
metamerize to an interm ediate m otion direction. But
metamerism occurs onlvJ when the stimuli fall within
the resolution lim its o f the low-level feature-detection
mechanism. M etamerism is noc crowding.
4 .8 .3 d Effects o f C o m p e titiv e Figural G rouping
Crow ding with com plex stim uli is due principally to am bi­
guities in figural grouping. For that reason it is evident only
for stim uli consisting o f spatially organized elements.
Stim ulus elem ents ot neighboring objects becom e grouped
F^urc «. 19. C row ding d u e to com peting grouping o f tines. The square is d i tliciilc
to d c tc c t w hen n o t shaded.

with elem ents o f the target o bject. This grouping is most

likely to occur .it high levels o f visual processing, where
com plex structures arc segregated and detected. The follow­
ing evidence supports this conclusion.

1. Overlapping shapes with multiple groupings It is not easy

to see the square in Figure 4 .1 9 when it is n o t shaded.
This is because chc lines com prising the square also form
shapes with other lines. This is the principle o f
cam ou flage. A m biguity o f figure-ground organization
or o f figural interpretation are special cases that were
discussed in Section 4.5.9.
Fig«rc 4.20. Perception o f in teg ral $ -D structure. (A ) Each o b jc c t has many
2. Overlapping shapes with unambiguous grouping W c
parts seen as fo rm in g to o n e o b je c t. ( B ) W h e n superim posed, th e tw o
readily recognize a com plex 3 -D o b ject as one object
o b je c ts can still be seen. ( C ) A d ifferen ce in c o lo r helps to segregate chc
even though it consists o f many overlapping parts, as in o b jects. ( D ) Sep aration in d ep th produced by fusing th e tw o im ages
the two objeccs in Figure 4 .2 0 A . In each o b ject, che helps to segregate the o b jects.

pares form a coherent structure because lines jo in in

consistent ways that conform to a 3 -D structure. O b je ct
shapes. Thus, the letter v in Figure 4.21 is difficult to
coherence is also fostered by the bilateral symmetry o f
detect when embedded in cursive script. But a vertical
each o bject. W c still rccognizc the two objects when
offset or the addition o f vertical lines betw een the
they are superimposed, as in Figure 4 .2 0 B . They remain
letters helps со segregace che letters. These effects cannot
distinct objects bccausc the lines in one drawing do not
be explained by lateral inhibition or by low spatial
coincide with or abut those in the other. A t any
ф
instant
resolution. The vertically shifted lecters occupy a smaller
wc can acccnd to one o f the overlapping drawings and
area than the letters in a linear string. A ccording to the
ignore the other. This is easier when the shapes differ
spatial resolution accounc chis should make ic more
in color or arc separated in depth, as in Figure 4 .2 0 C
difficult со resolve the offset leccers. Also, the vertical
and D.
lines should increase the effect o f lateral inhibicion.
T ip p er (1 9 8 5 ) briefly presented superimposed drawings
o f two objects, one in red and the other in green.
Subjects were asked to attend to the red o b ject and
ignore the green o b jcct. O n e second later they were
asked со name che red o b ject in a second pair o f
superimposed drawings. They responded more quickly
when che two red objeccs were same com pared wich
when che second red objccc was chc one chcv had
previously ignored. This atten cional p rim in g effect
illuscratcs thac it takes tim e to disengage actention from
one ob ject and sw itch it to a second o bject.
Figure 1.21 . A m biguous grou pin g o f neighborin g shapes. T h e letter v is difficu lt
3. Ambiguous grouping o f neighboring shapes A to d c tcc t when jo in ed to O ther letters. T h e v is easier to see when
becom e difficult со dceecc when joined to vertically staggered o r w hen vertical m arkers segregate the letters.
 T h e effects in Figure 4 .1 9 arise because there arc several
ways со group che stimulus elem ents. This problem
would scill arise even if chc atccncion mechanism had
high spacial resolution.
Spatially defined stimuli, such as leccers, chat differ in
color or morion do noc show crow ding. They “pop our”
racher chan being grouped with neighboring scimuli. For
example, D river and Bayliss (1 9 8 9 ) found that moving
discraccer leccers had lictle effect on chc accuracy or
speed o f recognition o f a stationary letter. The adverse
effects o f flanking lines on vernier acuicv were removed
when the vernier lines and the flanking lines differed in
color, concrasc sign, or disparity (Sayim ec al. 2 0 0 8 ).
Also, che concrasc or tile of a (la b o r patch becam e more
difficult to detect when surrounding patches were made
similar in orientation or length (Saarela e t al. 2 0 0 9 ).
Thus, visual stimuli with similar simple spatial features
are passed on to a high-order mechanism, where they
becom e subject to ambiguous grouping. Hue chc
am biguity ofgrou p in g is resolved if the stim uli differ,
especially if they differ in a nonspatial feature, such as
color or m otion. Also, there is less crow ding between
scimuli separated in depch (Section 13.2.4b).
4. Effect o f supporting context M ost natural objects consist o f
many parts, some o f which may be perceived as parts o f
very different objects, as illustrated in Figure 4.22.
In such cases, an o b je ct’s perceived identity is revealed by
ics conccxc. This is che reverse o f crowding.
N /
# w ithin the display on some trials. Reaction tim es were
V longest when the doc was adjacent со chc cargec. This sug­
i investigators have shown that o b jects adjacent to a stimulus
i .*.!« «.22 Ih e effect o f con text on object recognition. T h e dark o b jc c t could be
a sproutin g seed, b eetle, absent nose ( its tru e id en tity ), o r spear,
d ep en d in g on co n tex t.
The basic problem arises because neurons ac higher
levels o f che visual system have large receptive fields. The
receptive fields must be large because the neurons integrate
inform ation from a given region so as to d etect stimulus
configurations such as curvcd lines, angles, or various types
o f contour junctions. But this means that the receptive field
o f a given neuron may contain elem ents from two o r more
distinct figures that happen to be contiguous or superim­
posed. Suppose chac by the cooperative processing o f several
neighboring neurons or by prior knowledge o fth e stimuli,
one figure is recognized. It would then be beneficial it other
interpretations or figural groupings o f che scimulus complex
were suppressed. This has been termed the n eig h b o rin g
in h ib itio n hypothesis. A ccording to this hypothesis, once
a given figure has been attended to and recognized,
overlapping or neighboring figures that fall w ithin the same
receptive field should be suppressed. Physiological evidence
showing that attention increases sensitivity со chc attended
o b ject was presented in Section 5.9.2. L et us look at the
behavioral evidence for this hypothesis.
A spot placed on one region o t a reversible figure-ground
display, such as a M altese cross, is detected at a lower lum i­
nancc when that region is seen as a figure than when the
same region is seen as ground (Frank 1 9 2 3 ; W eitzman
1963; W ong and W eisstein 1982). Also, neurons in V I of
the monkey respond m ore vigorously to texture elements
belonging to a figure than to che same elem ents belonging
to aground region (Lam m c 1995).
Cave and Zim m erm an (1 9 9 7 ) trained subjects to
recognize a target letter in an array o f letters. After
subjects were proficienc ac chis task they were asked to
respond to the presence o t a small dot that appeared
shortest tor a d ot superimposed on the target letter but were
gests that there is an inhibitory zone round an attended
object.
O th er evidence tor the neighboring inhibition hypoth­
esis com es from the phenom enon o f atten tio n a l capture.
The attention is captured by a stimulus with abrupt onset or
one that is discincc from ocher objects in an array. Several
that has captured the attention have a heightened detection
threshold or a longer response latency com pared with stim ­
uli more distant from the attended stimulus (sec M ounts
2000 ).
The effects o f figural grouping on stereoscopic vision arc
discussed in Section 22.1. D ie hop tic crow ding is discussed
in Scction 13.2.5. Crow ding in stereopsis is discussed in
Section 2 2 .5 . le. Stereoscopic depth as an attention-getting
stimulus is discussed in S ection 22.8.
M echanism s o f visual attention are reviewed in Koch
and U llm an (1 9 8 5 ), D esim one and D uncan (1 9 9 5 ), Kastner
and Ungerleider (2 0 0 0 ), and C orbetca and Shulman
(2 0 0 2 ).

4 .8 .4 A T T E N T IO N AND C O N S C IO U S N E S S
Consciousness is difficult to define. W e know very little
abouc chc mechanism o f consciousness and arc unable со
chink o f what would be involved in designing a machine
chac would be conscious.
In general, we are conscious o f those sensory events and
responses thac recur in different forms and abouc which wc
have to make decisions based on past experience. Thus, we
arc not conscious o f the sensory and response processes
involved in digestion because, although different foods
must be processed in different ways at different stages, the
processes are fundamentally the same throughout life. The
internal m ilieu of the bodv• is reasonably• stable so that its
regulation can b e assigned to routine processes abou t which
we need n o t be conscious. The external world is changeable,
and novel circum stances constantly arise. Sim ple animals
that live in local and restricted environm ents rely on a
repertoire o f relatively constant response mechanisms. But
animals that move over large distances betw een diverse
environm ents must possess com p lex behavioral repertoires.
They must learn the characteristics o f many different
situations so as to recognize when a learned pattern o f
responding needs to be adjusted to novel circumstances.
W e can say som ething about w hich parts o f the nervous
system are required for the conscious perception o f visual
stimuli. All consciousness, visual o r otherw ise, ceases after
damage to the upper brainstem in the region o f the hypo­
thalamus. All consciousness o f visual stim uli ceases when
the primary visual cortex ( V I ) is removed. Som e visual
areas beyond V I operate in p arallel. Each area processes
distinct types o f inform ation that can be processed inde­
pendently o f processing in other parallel pathways. Damage
to such an area can produce a lack o f awareness o f a particu­
lar stimulus feature. O th er areas operate in sequence to
form a processing hierarchy. In this case, processing in each
area depends on inform ation supplied by areas earlier in the
hierarchy. Inform ation from areas that operate in parallel
may be com bined at a higher stage. Also, processing o f
inform ation in earlier stages may be modified by feedback
from higher stages.
A t higher levels o f the hierarchy the stimuli that cclls
respond to becom e m ore com plex. Each higher stage need
take only th at inform ation from preceding stages that it
requires for the processing it performs. For example, a center
devoted to the recognition o f faces need not be concerned
with inform ation that specifies the location or size o f the
facc. But that docs not mean th at inform ation n o t passed
o n to higher stages is lost to consciousness. Each hierarchi­
cal stage provides a different level o f inform ation and that
processed at each stage is available to consciousness when
needed. If a higher center is lost, wc may not be able to rec­
ognize particular o b jects bu t we can still perceive the
detailed structure o f the visual world and perform basic
tasks such as stimulus detection and discrim ination o f
simple features. Thus, conscious perception is not the end
product o f a hierarchical process. Rather, different types o f
perceiving are possible from the outputs o f each stage o f
processing from V I to the highest levels.
C rick and K och (1 9 9 5 ) argued that visual conscious­
ness does n o t occur unless a visual area projects directly to
the prefrontal lobe, which they understood to be the high­
est point in the visual hierarchy. They argued that, since the
prim ary visual cortex ( V I ) docs not project directly to chc
frontal cortex, we are n o t aware o f the processing that occurs
in V I . A ccording to chis view, visual consciousness should
cease when the frontal lobes are removed. Hut this is n o t so.
Visual consciousness ceases when V I is removed, but that
does not prove that V I is the sole site o f visual conscious­
ness. It simply means that all visual inform ation passes
through V I . Visual consciousness is not lost after removal
ot any other visual area. Removal ot specific areas produces
losses in one or m ore specific visual abilities. For example,
damage in V 4 produces an inability to recognize colors
(Section 5.8.3a) and damage to a region in the temporal lobe
produces an inability to recognize faces (S ectio n 5.8 .3 c). In
such cases there is no loss in basic visual abilities such as
acuity or the ability to perceive the locations o f objects.
Consciousness operates at four levels:
1. Perception W e can be aware o f or n o t aware o f a given
stimulus at each o f various levels o f cortical
processing— namely d etection, discrim ination,
recognition, and description.
2. Decisions W e can be aware o t deciding to make a given
response or the response can be autom atic.
3 . Responses W e can be aware o f or not aware o f a response
we have made.
4 . Thought processes We can attend to and be conscious o f a
memorized or imaginary o b ject or event.
There is some evidence for each o f the following
statements.
1. W e can be aware only o f things that involve neural
events in the cerebral cortex. W e are n o t aware o f simple
responses, such as pupil dilation and vestibular
nystagmus, w hich involve only subcortical processing.
Sahraie c t al. (1 9 9 7 ) described a patient with damage to
the visual cortex who could indicate the direction in
which a stimulus was moving if forced to make a
decision. He was usually not aware o f the moving
stimulus, and fM R I revealed activity* mainly
/ in
subcortical centers. O n occasions when he was aware o f
stimulus m ovem ent, fM R I activity was evident in the
prestriate cortex and prefrontal area 4 6 .
2. We can be aware o f things that involve neural events in
any part o f the cerebral cortex.
3. W c are aware only o f dhings chat wc attend to or o f things
that force themselves into our attention. The
phenomenon o f change blindness demonstrates that we
are n o t aware ot visual things that wc arc not attending to,
even though they generate activity in V I and elsewhere.
A stimulus that we arc not attending to may suddenly
intrude into consciousness. For example, we become
aware o f making a startle response to a loud sound or to a
loom ing object in peripheral vision. Also, we arc aware ot
making corrective postural responses evoked by a sudden
movement ot the surface we are standing on.
As we practice skills such as driving, typing, or playing
the piano, we becom e less aware ot the stimuli that guide
our actions and o fth e decisions we make. We begin to
respond automatically. There is physiological evidence
that as we becom e proficient at a skill the centers o f
neural activity shift from higher centers, such as the
prefrontal cortex and cingulate sulcus, to subcortical
centers, such as the cerebellum and putamcn (Della-
Maggiore and M cIntosh 2 0 0 5 ; Putter mans et al. 2 0 0 5 ).
In general, wc arc m ost aware o f stimuli about which we
must make decisions, and o f responses in novel situations.
4. O u r attention can be directed to a stimulus even though
we are not aware o t the nature o t that stimulus. A ttention
was found to be automatically allocated to a loom ing
stimuli on a collision trajectory even when subjects were
n o t aware o f the difference between such a stimulus and
one that was on a near-miss trajectory (L in c t al. 2 0 0 9 ).
5. C enters th at code the location or stimulus feature that
wc arc actcnding to are distinct trom cortical areas
where decisions are made about what we attend to. This
issue is discussed in Scction 5.9.
It would require an impossibly large am ount o f neural
m achinery to process all sensory inform ation beyond a
simple level. Hut this is not necessary because there is
a physical lim it on the responses that we can execute at a
given tim e. For exam ple, a lim b can move in only one direc­
tion at a time. We must therefore select those stimulus
objccts o r events that arc relevant to the actions we arc plan­
ning at a given tim e. Also, we must process relevant features
o fth e selected stim uli, at the level o f discrim ination, recog­
nition, or description that is required. W c allow other
o b jects and o ther features th at are n o t relevant to the task
to tade from consciousness.
The selective effects o f attention on awareness arc
dramatically revealed by the phenom enon ot change b lin d ­
ness. W hen a com plex scene is m om entarily interrupted,
people do not notice large changes in unattended parts ol
the scene. For example, in a picture o f a street scene, people
do nor notice that a large building has been removed while
the scene is flashed off and on again (R cnsink et al. 1997;
Sim ons and Levin 1 9 9 8 ). The change is noticed only when
the subject was paying attention to that part ot the scene
before the interruption. W hen a blank rcctanglc suddenly
covers a nonattended o b ject, leaving the rest o f the scene
visible, subjects sec the rectangle but can n ot report rhe
identity o f the o b je ct that has been covered (O ’Regan c t al.
1 9 9 9 ). C hange blindness dem onstrates that nonattended
objects do not enter awareness.
Merely looking at som ething docs n o t ensure that wc
are aware o f it. To be aware of an o b ject wc must have
attended to it and processed it. But there is an unspecifiably
large num ber of ways of processing a given o b ject. By an act
o f attention wc can access the inform ation processed by V I
or by any other cortical visual area according to the task wc
are perform ing.
W atanabe c t al. (1 9 9 8 ) provided one piece o f evidence
in support ot this idea. They found that V I o f humans
showed enhanced activity, as revealed by magnetic response
imaging (t M R l), when subjects attended to an array ot dots
executing simple translatory m otion but not when the dors
executed expansion m otion. But both types o f m otion
enhanced activity in area V 5 , an area devoted to che d etec­
tion o f patterns o f m otion (Section 5.8.4b ).
A nother piecc o f evidence was provided by C o rb etta
e ta l. (1 9 9 1 ). The region o f extrastriate co rtex showing m ost
activity in a PF.T scan varied according to which feature was
being attended to in a discrim ination task. A ttention to
shape accivaced chc ventrom edial occipital region, and
attention to movement activated area V 5 , a region corre­
sponding to m onkey M T (C o rb etta et al. 1991).
Som e people experience vivid hallucinations, especially
when half-awake. However, m ost people do not expcriencc
hallucinations when fully• awake. H allucinations would
interfere with the perception o f the real world. Visual cen ­
ters have evolved to be silent when not stim ulated. Patients
with the C h a rles B o n n e t sy n d rom e have weak vision but
experience strong hallucinations. The co n ten t o f the illu­
sions experienced by a group o f these patients was related to
the areas o f the brain showing enhanced fM R I (ffytchc
et al. 1998). For example, patients who hallucinated faces
showed enhanced activity in che middle fusiform gyrus, an
area known to be involved in facial recognition. Patients
who hallucinated in color showed activity in V 4 , an area
involved in color processing.
There must be a mechanism for selecting the neural p ro ­
cesses that we arc attending to. It seems that the parietal
lobes and subcortical areas such as the pulvinar and thal­
am ic reticular form ation arc involved in d irecting attention,
and hencc awareness, to visual stim uli and to stimuli in
other senses.
The attentional system, in con ju n ction with stored
memories, creates and controls a stream o f co n sciou sn ess.
Tliis involves four com ponents:
1. Consciousness o f self-idcntitv.
2. Consciousness o f self-location in space.
3. Consciousness o f the general 3 -D structure o f the
environm ent and o f the identity* and structure o f
o b jects o f particular interest.
4 . Consciousness ot progression through tim e, past and
present, and consciousness o f anticipated events and
plans tor future actions.
Thus, one o f the m ajor functions ot attention is to direct
the con ten ts o f the stream o f consciousness. W e are aware o f
our continuous existence as the same person. The spatial
inform ation that we receive at a given m om ent is set within
the co n text o f the learned structure o f the local environ­
m ent and o f whatever knowledge we have o f the extended
environm ent. We also maintain a continuous ordered
record o f events over our lifetime.
U nder ordinary circum stances, we do these things so
well that we take the process for granted. Hue we can som e­
times be abruptly reminded o f the im portance o f an intact
stream ot consciousness. W hen we awake in an unfam iliar
place it can take several seconds before we recover a sense o f
self-location. Also, we can lose all sense o f self, location, and
tim e when com ing our o f an anesthetic. People with dem en­
tia associated with parietal-lobe damage may suffer a perma­
nent loss o f self-identity. In extrem e cases, patients deny
their own existence, a symptom known as depersonaliza­
tion. In o ther cases, patients lose all sense o f location even in
their own house. They may also lose their sense o t tim e, and
feel that events that occurred long ago occurred recently
(C ritchley 1 955).
4 .8 .5 S T IM U L U S E X T E R N A L IZ A T IO N
The ancient G reeks wondered how we perceive an external
visual world. This is the problem o f stimulus externaliza-
tion. There was no problem in touch because the fingers
touch an external o b ject and the impression formed on
the skin has the same size as the o bject. D istance is
indicated by the extension o f the arm. So it was believed
that, in vision, som ething had to leave the eyes to touch an
o b je ct so as to detect its shape and size. The extromission
theory was designed to solve the problem o f how visual
objects are externalized and seen in their proper size
(Section 2 .1 .4 ).
W e now understand that the crucial factor in external-
ization in any sensory m odality is the interplay between
m otion o f stim uli and the activity o f the perceiver. For
exam ple, auditory stim uli seem to be inside the head when
they delivered through headphones so that they m ove with
the head (Section 3 5 .1 .1 ).
Presumably, infants soon learn to externalize the
visual world as they move their eyes, head, and body.
However, there are reports o f patients with head injuries for
whom the world appeared tw o-dim ensional, like a picture
(Section 3 2 .3 .1 ).
An afterimage is not clearly externalized when viewed
with m oving eyes. Also, the pressure phosphcne created by
pressing on the side o f the eye appears inside the head.
Bach-y-Rita et al. (1 9 6 9 ) transform ed signals from a
video camera into tactile stim uli on the skin o f the back.
W ith practice, blind subjects recognized simple objects and
detected their relative positions. They spontaneously
reported that the stim uli seemed ro com e from in fron t o f
the camera rather than trom the vibrators on the back.
However, W h ite (1 9 7 0 ) showed chat blind subjects learned
to externalize tactile stimuli onlv# when thev/ controlled the
m otion o f rhe cam era (see Secrion 3 4 .5 ).
4 .9 P L A S T I C I T Y O F B A S IC V IS U A L
F U N C T IO N S
4 .9 .1 B A S IC F I N D I N G S
It seems that practice does not improve grating resolution in
either the central or peripheral retina (B en n ett and
Westheimer 1991; W estheim er 2 0 0 1 ). Sim ple grating reso­
lution depends on the spacing o f detectors, and it is difficult
to see how practice could affect it. However, Fiorcntini and
Berardi (1 9 8 1 ) found that subjects improved in discrim inat­
ing the waveforms o f com plex gratings over 1 0 0 - 2 0 0 trials.
Hyperacuities, such as vernier acuity, depend on more
complex neural processes that m ight well change with prac­
tice, especially for stimuli presented in the peripheral retina.
In earlier studies, practice was tound to have little effect
on the hyperacuity task o f gap bisection (K lein and Levi
1985) or three-point alignm ent (B en n ett and W estheim er
1991). However, in a more recent study, practice over sev­
eral weeks improved the ability to center a line between two
other parallel lines presented 5° away from the fovea (C rist
et al. 1997). The im provem ent was largely specific to the
location and orientation o f the lines and showed little
transfer to a vernier alignment task.
Several investigators have reported an im provem ent o f
vernier acuity with practice, but there were wide individual
differences. M cK ee and W estheim er (1 9 7 8 ) found that
improvements in vernier acuity after 2 0 0 0 practice trials
ranged from 2% to 70 % , even w ithout error feedback.
Saarinen and Levi (1 9 9 5 ) exposed four subjects to 8 0 0 0
vernier acuity trials spread over several days. O n e subject
showed no im provem ent while one showed a six-fold
improvement. Subjects who improved also showed a nar­
rowing o f orientation tuning around the orientation o f the
test lines, as assessed by the masking effects o f noise ele-
menrs at various orientations. This is in line with other evi­
dence that vernier acuity is closely linked to orientation
discrim ination.
Improvement on vernier acuity with vertical test lines did
not transfer to test lines rotated by as little as 10° or to test
lines in another retinal location (Fahle 2 0 0 4 ). Also, there
was no transfer to other casks, such as curvature discrimi­
nation, oriencacion discrim ination, or sccrcoscopic acuicy
(Fahlc and F.delman 19 9 3 ; F ah leec al. 1 9 9 5 ; Fahle 1997).
Practice produced some im provem ent in Snellen acuity
(see Bennecc and W estheim er 1991).
Practice has been found to improve discrimination o f dif­
ferences in line oriencacion. For example, Vogels and Orban
(1 9 8 5 ) asked subjects со reporc whether a luminous bar
was clockwise or anticlockwise with respect to a previously
presenced scandard. Performance improved for oblique orien-
cacions o f che scandard buc not tor the two principal orienta­
tions. Presumably, the subjects discrimination o f orientations
around che vertical and horizontal was already well practiced.
The well-known oblique effect indicates chac oblique orienta­
tions are less well discriminated than principal orientations.
Schoups et al. (1 9 9 5 ) found thac practice greatly
improved the ability to detect whether a 2.5° patch o f grat­
ing wasclockw isc or anticlockwise with respect to an oblique
grating. The improvement did n o t transfer to a gracing in a
new location or in a new orientation. It did transfer between
eyes. This suggests that the training affected specific orienta­
tion detectors early in the visual system. However, Zhang
ct al. (2 0 1 0 ) obtained transfer o f improvement in orienta­
tion discrim ination o f G abor parches from the fovea to a 5°
peripheral location. But transfer occurred only when sub-
jeccs had received preliminary cescing ac che peripheral loca­
tion. The prelim inary testing must have somehow produced
a high level improvement in the decision process.
The orientation tuning o f cells in V I takes 3 0 to 4 5 ms
to develop (sec Section 5 .6 .2 c). Ic therefore takes tim e for
the oblique effecc со manifesc icself (Macchews ec al. 2 0 0 5 ).
Scrong ec al. (2 0 0 6 ) found that practice reduced the time
chac subjeccs required со discrim inace che oriencacions o f
successively presenced C ab o r pacches. The improvement
was the same for principal and oblique orientations o f rhe
standard. Thus, practice improved dccection ot principal
oriencacions in the initial period o f uncertainty.
D iscrim ination ot direction o t m otion showed some
im provem ent for stim uli in rhe same retinal location and
m oving in the same general direction as the training stimuli
(Ball and Sekuler 1 9 8 7 ).
The fact that che effeccs o f practice on simple discrim i­
nation casks are limiced со the retinal location and spatial
features o f the training stimuli suggests that they occur at an
early level in the visual system. The fact that training trans-
fers bccween the eyes (Section 13 .4 .1) suggests that changes
occur after inputs from the two eyes have been com bined
in V I . W e will see in S ection 18.14 that stereoacuity
improves with practice.
Practice has much m ore effect in more com plex tasks
involving many stimulus features than in simple discrim ina­
tion tasks involving one stimulus feature. We learn to recog­
nize novel o b jects or fam iliar objeccs in novel oriencacions.
We also learn to search for a shape am ong discraccers
(Fine and Jacobs (2 0 0 2 ). The ability со sec a shape defined
by relacive m otion o f line elements improved with practice.
In this case, the learning was not specific to che oricncation
o f line elements or to the direction o f m otion (Vidyasagar
and Stuart 1993).
It had been assumed chac percepcual learning occurs only
when arcention is direcced со che relevant stimulus. However,
some recenc evidence has challenged chis view (see Sasaki
et al. 2 0 1 0 ). The physiological basis o f the effects o f learning
and attention are discussed in Sections 5.6.8 and 5.9.1.
4 .9 .2 C A U SE S O F E X P E R IE N C E -D E P E N D E N T
PLA STIC ITY
4 .9 .2 a G ro w th Factors
In che infanc, visual resolution and acuicy improve because
the optical structures o f che eye develop. The growth o f che
eye is guided by signals arising from che blur o f the image, a
process known as emmetropizacion (see Section 6.3 .1 c).
Also, the sensitivity and cuning specificity o f cortical cclls
to stimulus features such as m otion, orientation, and dispar­
ity improve with age (C hapter 7).
4 .9 .2 b E ffects o f E rro r Feedback
There is con flictin g evidence about the role o f error feed­
back in the im provem ent o f vernier acuity with practice.
Fahlc and Edelman (1 9 9 3 ) reported improved vernier
acuity after prolonged practice w ith no knowledge o f
results. Im provem ent was specific to the orientation o f che
stimulus. However, H erzog and Fahlc (1 9 9 7 ) found chac,
w ithout error feedback, 10 subjects showed no mean
improvement o f vernier acuity. All subjects showed
im provem ent (m ean 14.7% ) when the experim enter p ro ­
vided a direction error signal on each trial. I.carningdid not
o ccu r when che feedback was uncorrelaced wich responses.
Poggio et al. (1 9 9 2 ) proposed that che nervous syscem
sets up task-specific neural modules that improve in sensi­
tivity when the task is repeated. They illustraced chis idea by
a com puter sim ulation o f a neural netw ork th at manifested
improved perform ance in a vernier acuity cask when p ro ­
vided wich appropriace feedback. NaTvc observers showed a
similar cask-specific im provem ent in vernier acuity over a
few tens o f trials when given knowledge o f results. The
model replicated several features o f human perform ance,
such as chc dependence o f vernier acuicy on chc length and
relacive orientation o f the test lines.
In a rcal-lifc sicuacion ic is noc clear whac consticuccs
visual feedback for resolution or acuity. There are no
obvious error signals.
4 .9 .2 c R e c ru itm e n t o f Resources
Im provem ent may also occur because o f an increase in the
efficiency with which a particular configuration o f cortical
ceils processes sensory signals. Learning, as ordinarily
understood, need n o t be involved. It could simply be a
m atter o f t h e nervous system recruiting its local resources
tor the perform ance o f a repeated specific task.
Im provem ent in a discrim ination task could be due to
increased tra n sd u ctio n efficien cy . This is the efficiency
with which the stimulus is transformed into neural signals.
Improved efficiency could arise from a narrowing o f the
tuning functions o f cortical detectors for the features
involved in the task. It could also involve recruitm ent o f
detectors with neighboring tuning functions, to provide a
better sampling o f stim ulus features.
Improvement in a discrim ination task could also be due
to increased ca lcu la tio n efficien cy . This is the efficiency o f
the visual system’s ability to make correct decisions on the
basis o f noisy neural signals. In Section 5.1.5 it is explained
that intrinsic noise in the visual system determ ines trans-
duction efficiency. It was also explained that the level o f
intrinsic noise is indicated bv
ф
the knee in the function that
relates the threshold to the level o f external noise applied to
the stimulus. Any im provement in transduction efficiency
shifts the knee o f the function down and to the left,
as shown in Figure 4 .2 3 . Any im provem ent in calculation
efficiency shirts the curve down but leaves the position o f
the knee on the x-axis unchanged.
I.i e t al. ( 2 0 0 4 ) obtained im provem ent in the detection
o f a vertical m isalignm ent betw een tw o side-by-sidc rows o f
dots. The position o f each d ot was randomly perturbed,
keeping the m ean vertical position o f each row constant.
They measured the change in threshold as a function of the
level o f position noise added to the stimulus. 'Ih e results
indicated that im provem ent was due more to increased cal­
culation efficiency than to improved transduction efficiency.
The visual system improved in its ability to extract the mean
position o f each row o f dots in the presence o f the applied
perturbation.
D oshcr and Lu (1 9 9 9 ) applied similar m ethods to
determ ine the source ot im provem ent in an orientation
discrim ination task. They concluded that, for this task,
learning involves an im provement in noise suppression
(transduction efficiency). They also concluded th at there
was no change in the tuning functions o f orientation detec­
tors nor any change in decision strategies. Instead, they
С
£
У
<TJ
"O
о
SI
40 1 ■ Im proved calculation
®
SI efficiency
Im proved transduction
efficiency
J
0.1 1
E xternal noise (arcm in)
Tran lAuctin n an d catiu latu m cjfkim cy . P rcd ictcd learning-
induced ch an g cs in tran sd u ctio n and calcu lation ciR cicn cy as a
fu n ctio n s th e level o f n oise applied to th e stim ulus. (Adapted from
l.i ct at. 20CI4)
concluded that there was a change at an interm ediate
level where inputs from different orientation detectors
are weighted in m aking a decision. O n e can n ot assume
that all forms o f perceptual learning involve the same
mechanisms.
4 .9 .2 d A tte n tio n C o n tr o lle d R e c ru itm e n t
o f Resources
R ecruitm ent o f resources to a particular task would pro­
duce a perform ance decrem ent on tasks that use the m echa­
nisms that have been diverted to the specific task. I Iowevcr,
this problem would be overcome i f the system temporarily
modified local neural netw orks according to the demands
o f a given task. In this case, signals from higher centers
would direct local network in V I to be modified in one way
for one task and in another way for another task.
We will see in Section 5.6.8 that local netw orks in the
primary visual cortex ( V I ) adjust themselves to the demands
o t different tasks. Changes in V 1 could conceivably be stim ­
ulus induced. But they are more likely to be induced by sig­
nals from higher centers triggered by attention to a
particular stimulus and a particular task. In other words,
the processes involved in generating neural changes arising
from practice may not be the same as those responsible for
storing the required changes.
 5
P H Y S I O L O G Y OF T H E VISUAL SYSTEM

5.1 The eye 206 5.5.5 C o r t i c a l la y e rs 25/

5.1.1 G e n e r a l s t r u c tu r e o f c h c e y e 206 5.5.6 L a te ra l c o r tic a l c o n n e c tio n s 252
5.1.2 R e c e p to r s 207 5.5.7 B lin d s ig h t 2$6
5.1.3 B ip o la r , h o r iz o n t a l, a n d a m a c r in e c e lls 209 5.6 Stimulus tuning o f cells in V I 25<5
5.1.4 G a n g l io n t e ll s 24 5.6.1 C o n t r a s t s e n s itiv ity o f c o r t i c a l c c lls 256
5.1.5 L ig h t d e t e c t i o n 2/5 5.6.2 O r i e n t a t i o n t u n in g 257
5.2 Lateral gcniculate nucleus 216 5.6.3 S p a t ia l- p c r io d ic it y t u n in g 260
5.2.1 S tru c tu re o f rh e I.GN 2 16 5.6.4 S p a tio r c m p o r .il t u n in g o f c o r t i c a l c e lls 261
5.2.2 P r o p e r tie s o f LGN re la y c e lls 2 1S 5.6.5 Cells tuned to multiple features 2 6 3
5.2.3 B in o c u la r re s p o n s e s in L G N 220 5.6.6 Cytochrome oxidase areas o f V I 2 6 4
5.3 Visual pathways 221 5.6.7 C o n t e x t u a l and fig u ra l r c p o n s e s in V I 266
5.3.1 V is u a l in p u r s ro s u b c o r t ic a l c e n t e r s 221 5.6.8 Effects o f learning on runing functions in V 1 26$
5.3.2 The c h ia s m a n d o p t i c t r a c t s 222 5.7 Columnar organization o f the cortex 2 7 0
5.3.3 Hcmidecussarion 222 5.7.1 C o lu m n t o p o l o g y 270
5.3.4 P a r t it io n in g o f h e in ir e t in a s 224 5.7.2 O c u l a r d o m i n a n c e c o lu m n s 274
5.3.5 Corpus callosum 226 5.8 O ther visual areas 278
5.4 Ncurophysiologieal procedures 229 5.8.1 I n t r o d u c t io n 278
5.4.1 Histological procedures 229 5.8.2 Areas V2 a n d V3 2 S I
5.4.2 U s e o f in v irro tis s u e s lic e s 231 5.8.3 The ventral pathway 2S3
5.4.3 Methods applied ro the living brain 232 5.8.4 The dorsal pathway 2 S 7
5.4.4 C o n t r o l l i n g n e u r a l a c tiv ity 236 5.8.5 E v id e n c e f o r d isri n c r p ath w ay 's 296
5.5 The visual cortex 237 5.8.6 M u lt im o d a l re s p o n s e s 297
5.5.1 C o r t i c a l c e lls 237 5.9 Physiology o f visual attention 298
5.5.2 Cortical synapses and ncurotransmittcrs 240 5.9.1 G e n e r a l a t t e n t i o n m e c h a n is m s 29$
5.5.3 R e c e p tiv e fie ld s o f c c ll s in th e v isu a l c o r t e x 246 5.9.2 Location-specific cortical effects o f actencion 299
5.5.4 V is u a l c o r t ic a l p r o je c t i o n s 24S 5.9.3 Stimulus-specific effects o f attention 3 0 0

5 .1 T H E EVE
5.1.1 G E N E R A L S T R U G T U R K О F T H E EVE
The cross section o f the human eye is illustrated in Figure 5.1.
Th e human eye is approximately spherical with a diameter
o f about 2 4 mm. Larger animals have larger eyes, except
that birds rend to have unusually large eyes in proportion to
their body size. A nim als with larger eyes have an advantage
because the size o f the image increases with eye size and
a large eye can house more receptors, which increases
sensitivity.
The cornea has a width o f abou t 12 mm and a radius o f
curvature o f about 8 mm. Its refractive index is about 1.38
and its power is about 4 3 diopters, which is about 70 % o f
the eye’s total refraction. The cornea is continuous with the
sclera, w hich form s the w hite outer structure o f the eye.
The inner surface o f the sclera is lined with the choroid,
w hich is lined w ith the retina. The optic nerve leaves the eye
from the optic disk. This is known as the blind spot because
it contains no receptors.
The pupil and associated iris muscles arc just in front o f
the lens. They form an aperture that controls the am ount o f
light entering the eye. Changes in the size o f the pupil also
affect the optical quality o f the image and the eye’s depth o f
focus, as explained in C hapter 9 . For a given viewing dis­
tance and level o f illum ination, the pupil automatically
adjusts in size to achieve the best com prom ise betw een
these optical factors. The ocular m edia transm it about 75%
o f incom ing light at a wavelength o f 5 0 0 nm and about 80%
at 5 6 0 nm (N orren and Vos 1974).
The human lens has a diam eter o f about 9 mm and a
thickness o f about 4 mm. It is supported by the ciliary m us­
cles and ligaments. The fluid-filled cham ber in front o f the

Figure i. I . H orizontal section through th e right hum an eye.
I>57)
lens is the aqueous cham ber and thac behind the lens is the
vitreous chamber.
The refractive index o f the lens increases m onotonically
from 1.38 in the surface regions to about 1.4 in the core
region. This gradient o f refraction (G R IN ) increases the
refractive power o f the lens and reduces its spherical aberra­
tion. The visual axis is the line join in g the point on which
the eye is fixated and the center o f the fovea. The o p tic axis
is the best-fitting line through the optic ccntcrs o f the four
refractive surfaces o f the eye. These are the outer and inner
surfaces o f the cornea and o f the lens. The optic axis inter­
sects the retina about 1.5 mm from the fovea on the nasal
side and about 0.5 mm above the fovea. It thus makes an
angle o f about 5° to the visual axis. This is known as the
an gle alpha. The optical dcccntration o f the image o f a fix­
ated point causes the image to be asym m etrical, an effect
known as co m a. C om a is partially compensated for by an
opposite decentration o f the pupil.
See Section 14.1 for the geom etry o f the visual fields
and Section 9.1 for a discussion o f optical aberrations o f the
human eve
« and lens accom m odation.
The retina is a multilayered
Ф m em brane with an area o f
about 1,000 square mm. It is about 2 5 0 /mi thick at the
fovea, dim inishing to about 100 /mi in th e periphery.
The fine structure o f the retina is depicted in Figure 5.2.
This structure was first revealed by Ram on у C ajal using the
G olgi staining m ethod, and was described in a series o f
papers betw een 1888 and 1933 (sec Polyak 1941).
The retina is separated from the choroid hv a pigmented
epithelium , which absorbs light and prevents light that has
passed through the retina from being reflected back onto
the rcccptors. In nocturnal animals this epithelium reflects
light and thus improves sensitivity at the expense o f image
quality.
Outer
segments
Rod Inner
segments
Cone
Soma
Outer
plexiform
Horizontal cell layer
Bipolar
A m acrine
cells Inner
p tex tfcrm
layer
Ganglion cells
Axons to
optic nerve
of light
(R « Jr » n fro m Fv-hjJk.
I'ig v r c s . 2 . th e gen eral structure o f the retina. (A J-ip ic J from D < m ltng j » J B u n u i i 1 9 6 6 )
For details o f the structure o f the eye, see Polyak (1 9 5 7 ),
Davson (1 9 6 2 ), Charm an ( 1 9 9 1 ), and O yster (1 9 9 9 ).
Section 6.3.1 deals with the developm ent o f the eye.
5.1.2 R F.C F.PTO RS
5 .1 .2 a S tru c tu r e o f R e c e p to rs
The retinal receptors are densely packed in the outer layer o f
the retina— the layer furthest removed from the source o f
light. There are tw o main types o f receptor— rods and
concs. R o d s have high sensitivity, an exclusively peripheral
distribution, and broad spectral tuning. C o n e s have
lower sensitivity, and high concentration in the fovea with
decreasing concentration in the peripheral retina.
There arc chrcc types of cone, each with a distinct spec­
tral tuning, peaking at around 4 5 0 nm (Blue or S -c o n e s),
535 nm (G reen or M -co n cs),a n d 5 6 5 nm (Red or L -co n cs).
To identify different types o f con e, the optical aberrations
o f the eye are first measured and corrected by adaptive
optics (see Section 9 .6 .5 a ). Photographs o f the human
retina are then taken after each o f the different photopig­
ments has been bleached by an appropriate m onochrom atic
light (R oord a and W illiam s 1999; H ofcr et al. 2 0 0 5 ). This
procedure has revealed that S-cones (blue cones) constitute
6% o f all cones, w ith little variability betw een people. O n
the other hand, the ratio o f I. concs to M concs (the L:M
cone ratio) in eight males with normal color vision varied
between 5 2 .7 % and 9 4 .3 % , w ith a mean o f about 71% .
Figure 5.3 shows an example in w hich the different types o f
co n c have been artificially colorcd. Generally, the distribu­
tion o f L and M cones was found to be random . But a
random distribution necessarily produces patches that co n ­
tain only one type o f cone. These patches could explain why

Figure s .i D istribution o f (on e types in rise hum an retin a. T lic photograph
o f the retina was taken a t 1.5“ on the nasal side o f the fovea. C o lo rs
in d icate the S (b lu e ), M (g ree n ), and L (red ) con es. In this exam ple the
ratio o t L co n es to M c o n c s was 6 5 .5 % . (From I .«I 2005)
gracing acuity measured wich gratings illum inated by light
thac stim ulates only L or only M cones is no worse than that
measured with w hite light (C avonius and Estevez 1975).
Blue cones are sparse and occur singly, so that the blue-cone
system has lower sensitivity and lower resolving power. The
patchiness o f L and M cones may also explain why an array
o f small w hite abutting disks on a dark ground appears in
different pastel colors (Skinner 1932).
The retin al m ag n ificatio n fa c to r is the linear distance
on the retina corresponding to one degree o f visual angle. In
the human fovea it is about 0 .2 9 mm/dcg (W illiam s 1988).
The adult human retina has betw een 4 and 6 m illion cones
with a peak density ot betw een 1 0 0 ,0 0 0 and 3 2 0 ,0 0 0 per
m m 2 at the fovea declining to about 6 ,0 0 0 per m n r at an
eccentricity o f 10° (C u rcio et al. 1 9 9 0 ). The primate fovea
is a centrally placed pic abouc 1.5 mm in diameter, which
contains a regular hexagonal mosaic o f cones with a mean
spacing o f betw een 2 and 3//m (M iller 1979) (Figure 5.4).
The central fovea, which is about 0 .2 7 mm in diam eter and
subtends about 1", contains at least 6 ,0 0 0 cones. I he human
retina has 100 m illion or m ore rods, which are absent in the
fovea and reach a peak density o f about 1 6 0 ,0 0 0 per m n r at
an eccentricity o f about 20° (O sterberg 1935). Retinal
receptors constitute about 7 0 % o f all sensory receptors in
the human body.
A fine meshwork o f blood vessels lines the inside o t the
retin a,so that light must pass through them before reaching
the receptors. The shadows o f the blood vessels becom e vis­
ible when one looks through an illum inated pinhole. As the
pinhole is moved from side to side, the shadows undergo
parallactic m otion because they are som e distance in front
r.*u.< У4. V)c сочс m osaic o fth e ccu m tljivca. P ic m osaic o f in n e r conc
Segment* at th e center o f (be fovea o f th e m acaque m onkey. The conc
d e n s ity is about 151 ,0 0 0 /m m ', and the mean in tc rc o n c distance is
2 .8 / J i l l . (From Miller 1979 with kin Jp < rro iw .n o f Spnn£<r SeHnc«48ii*incw M«du)
o fth e receptors. M iiller (1 8 5 4 ) measured the m agnitude o f
this parallactic m otion, and, by applying his results to reti­
nal anatomy, deduced that light is absorbed in the outer
segments o f rods and cones.
F.ach receptor has an elongated outer segm ent, an inner
segment, a cell body, a short axon (5 0 to 5 0 0 /nn), and a
single synaptic term inal, as shown in Figure 5.2. The outer
segment is about 5 0 ftm long and consists o f a m em brane
folded into about 7 5 0 lavers
a
to form a stack o f disks. A bout
10” m olecules o f photopigm ent are packed along the mem­
brane so that light passing through the layers stands a good
chance o f being absorbed. From tim e to tim e, disks arc shed
from the outer segment and absorbed by the pigm ent epi­
thelium that lies betw een the retina and chc choroid layer o f
the eyeball (Young 1971).
The image plane o f the eye is at the level o f the inner
segments, but all the photopigm ents are in the outer seg­
ment. l.ight entering the inner segment o f a receptor at the
correct angle is guided in to and along the outer segment by
internal reflection. The two segments therefore act as a
waveguide, which concentrates light quanta in to the outer
segm ent and prevents light scatter beyond the image plane
o f the inner segments. Their efficiency as waveguides is
enhanced by the fact that their diam eter is similar to the
wavelength o f light. I f the diam eter o f receptors were less
than about 2 //m, light would leak from one to the other
(Snyder and M iller 1977). Because o f these design require­
m ents, the diam eter o f cones is remarkably con stan t over
the animal kingdom and is the ultim ate factor lim iting
visual acuity.
M ost light enters the inner segm ent o f cones at the co r­
rect angle because the outer segm ent is aligned with the
center o f the pupil. This is the direction from w hich most
light rays com e. Rods are less well aligned with the pupil.
C laudet (1 8 5 8 , p. 2 2 5 ) reported that a Dr. Scrrc had
proposed thac receptors are aligned wich che nodal point o f
the eye. M odern optical procedures can reveal the align­
m ent o f individual cones in the living eye. The alignm ent
is very precise, with very little disarray over a set o f recep­
tors (R oorda and W illiam s 2 0 0 2 ). This explains why wc
are m ore sensitive to light passing through the center o f
the pupil than to light passing through its margin. This
fact is know n as che S tiles-C ra w fo rd effect {Stiles and
Craw ford 1 9 3 3 ). This m echanism reduces che effects o f
light scatccr and o f aberrations in the lighc that passes
through the margins of the eye's optical syscem (see Enoch
and Tobey 1 9 8 1 ).
Som e alignm ent of receptors is present in the retina o f
che neonate, and is presumably determ ined by the way
receptors are packed together. However, an active process
must control the fine alignm ent o f the receptors bccau.se ic
recovers in an area that has been disturbed by retinal detach­
m ent (C am pos et al. 1 978). Also, receptors becom e less
well aligned after an eye has been occluded for several days,
but becom e aligned again after the occluder is removed
(F.noch et al. 1 979). A person whose pupil in one eye had
been displaced 3 mm for 2 5 years showed maxim um sensi­
tivity for light entering from the center o f the displaced
pupil (Honds and M acl.cod 1 978). A man who had bilat­
eral cataracts removed showed a shift in the direction o f the
Stiles-Craw ford effect from the preoperadonal region o f
the pupil o f m axim um brightness to the postoperacional
region o f maximum brightness (Sm allm an et al. 2 0 0 1 ).
5 .1 .2 b T h e R e c e p to r P o te n tia l
Light is absorbed in the outer segment ot rods by the
photopigm enr rh o d o p sin , which consists o f che procein
opsin bound to the chrom atophore 11 -f/V-retinal. Light
causes 1 1-w -retinal ro isomerize (change its shape) into
11 -/rv7W>retinal and becom e unbound from opsin. This
initiates an am plifying cascade o f chem ical events chac
results in hydrolysis ot guanosine m onophosphate (G M P )
molecules. In the dark, unhydrolyzed G M P molecules
bind to the cell m em brane and open che channels chrough
which sodium and calcium ions en ter the outer segment.
Hydrolyzed (IM P m olecules allow the channels to close,
resulting in a fall in the concentration o f sodium and cal­
cium ions w ithin che cell and hyperpolarizacion o f che cell
membrane.
The m em brane o f rhe inner segment o f a retinal recep­
tor contains a sodium-potassium ionic pump that modifies
rhe voltage changes induced in the outer segm ent and in iti­
ates the release o f che ncurotransm itter glutamate into the
synaptic clefr on the co n e term inal (see Yau and Baylor
1 9 8 9 ). These events take abouc 0 .2 s, which is similar to the
integration tim e for rod vision measured psychophysically.
A com plex series o f chem ical reactions in the pigment epi­
thelium , known as the retin oid cycle, restores 11 -trans*
retinal to the cis torm and reunites the chrom atophore with
opsin in the receptor. The restoration process takes about
1.5 m inutes in cones and about 5 minutes in rods.
The visual transduction process is studied by placing a
piece o l living excised retina under a m icroscope and draw­
ing the outer segm ent o f a single receptor into a m icropi­
pette 2 //m in diameter. In the dark, positive sodium and
calcium ions flow into the outer segm ent and o u t from the
inner segment. This creates a resting potential difference o f
abouc - 4 0 millivolcs. W hen chc receptor is illuminated with
a spot o f light, the flow o f ions is reversed and the electrode
picks up the resulting m em brane current.
A single response o f a rod is influenced by the num ber
ot photons absorbed over a period o f about 2 0 0 ms. Vision
is still possible when only one photon arrives in the rod
integration tim e (Baylor et al. 1 9 8 4 ). This represents an
enorm ous degree o f am plification (Baylor cr al. 1 9 8 7 ). The
2 0 0 ms integration time means that rods have high sensitiv­
ity but low temporal resolution. The spectral sensitivity
function o f rods determ ined physiologically is sim ilar to
the function relating psychophysically determ ined scotopic
visibility to wavelength.
A recep to r p o ten tial is a noisy, continuously graded
electrical signal (analog signal). Graded potentials also
occur locally at synapses and w ithin dendrites throughout
the nervous system, where they are known as p o stsy n ap tic
p o ten tials.
The norm al range o f lum inance sensitivity o f che human
eye extends about 3 log units from roughly 10” cd/m2 to
10* ' cd/m2. The lum inance o f stim uli varies about 10 log
units. Specialized m echanism s com pensate for the limited
dynamic range o f the eye (Section 4 .2 .3 ).
5 .1 .3 B IP O L A R , H O R IZ O N T A L .
A N D A M A C R IN E C E L L S
The second main layer ot the retina consists o t bipolar cells.
The region containing synapses betw een the receptors and
the bipolar cells is the o u ter p lexiform layer. Each bipolar
ccll receives inputs from only con es or only rods conveyed
by the ncurotransm itter glutamate. However, the two types
o f bipolar cell converge onto ganglion cells. There is only
one type o f rod bipolar cell but many types o f cone bipolar
ccll, defined by the shape and stratification o f their axon
terminals in the in n er p lexiform layer. M id g et b ip o lars
in the central retina are fed by only one cone. They serve
the red-green com ponent o t color vision and high visual
acuity. M idget bipolar cells are turthcr divided into
O N -b ip o la r cells, w hich respond ro light increase, and
O F F -b ip o la r cells, which respond to light decrease. Axons
o f O N -bipolars term inate in rhe inner h alf o f rhe inner
plexiform layer, while axons ot the otf bipolars term inate in
the ourer half. D iffu se co n e b ip o la rs are fed by several
neighboring red and green cones and are either O N -bipolars
or O FF-bipoIars, each subdivided into six types, which differ
in their tem poral characteristics. Som e exhibit a sustained
response and some a more transient response, depending
on the rate o f recovery o f glutam ate neurotransm itter.
Diffuse bipolars carry a lum inosity signal and have high
sensitivity, but may have som e chrom atic specificity. Rods
and blue concs feed exclusively inco specialized O N -bipolar
cells (Kouyam a and M arshak 1 992).
Each cone o f che central retina contacts all six types o f
diffuse bipolar cells and ac lease cwo types o f midgec bipolar
cells. Furchermore, che dendritic trees o f each cype o f bip o ­
lar cell form a complece and independenc coverage o f rhe
recina. Thus, any spot ot light on the retina stim ulates at Telodondria

lease one o f each type o f bipolar ccll (Hoycocc and W assle

S ynaptic ribbon
1999). This means chac the separation o f visual inputs into
S ynaptic vesicles
at least 10 parallel filters, or channels, begins in chc outer invagination
plexiform layer ot che retina. horizontal cells
Each rod cerminaces in a spherical synapcic struccure, bipolar cells
about 2 //m in diameter, called a spherule. Each rod co n ­
tacts horizontal cclls and betw een 2 and 5 bipolar cells, and
each bipolar cell is ted by up to 4 5 rods (K olb 1 9 7 0 ). Each C o n e tria d
cone term inates in a flat synaptic p ed icle. There are three 1 /ЛП
—I
types o f synapse at the receptor level.
S ynaptic ribbon
1. Gap junctions These occur on fine radiating processes S ynaptic vesicles
(telodendria) and make electrical co n tact with similar
invagination
processes on neighboring cells. Transm ission across the
gap is m ediated by co n n cx in s contained on the From horizontal cells
m em branes o f boch cells. Gap junctions connecc rods
From bipolar cells
wich rods and cones wich cones (D eans ec al. 2 0 0 2 ). Rod spherule

They also connecc am acrine cells with bipolar cells. R o d tria d

M ice lacking the relevant connexin show abnormal

Fipir* S-5. Term inals a n d synapses o f rods a n d cones. (R«kawn from0>wr
responses in O N -typ e bipolar cells (Giildenagel e t al. ТЪ<Нш*лмЕу 1999)
2 0 0 1 ). Gap junctions also co n n ect horizontal cells and
probably contribute to che cencer-surround
organization o f che receptive fields o f ganglion cells. In the dark, the neurotransm itter L-glutam ate or a
sim ilar substance is continuously released from recepcors
2. Synaptic invaginations Rod spherules have up со three
inco bipolar cells (D ow ling 1 9 8 7 ). W hen a receptor
synapcic invaginacions and cone pedicles have 4 0 or
absorbs lighc, less neurocransmiccer is released. This causes
m ore, each o f w hich contacts one type o f bipolar cell.
O N -bip olar cells со becom e hyperpolarized and O F F -
Thus, a single cone can contribute to many types o f
bipolar cclls, w hich form flac synapcic conneccions, со
bipolar cells. Each invagination typically contains a
becom e depolarized. The difference is due to the fact that
single dendritic bouton from an O N -bip o lar ccll and
O N -bip olar cclls express a m etabotropic glutamate recep­
two boutons from horizontal cells, known collectivelvi
to r while O FF -bip olar cells express ionotropic glutamate
as a triad synapse. The m em brane in each synaptic
receptors as defined in Section 5 .5 .2 ). Bipolar cclls, like
invagination contains a synaptic ribbon, about 1 //m
receptors, respond in a graded (analog) fashion to changes
long, surrounded by syn ap tic vesicles containing
in stimulus strength.
neurotransm itter (glutam ate), as shown in Figure 5.5.
H o rizo n tal cells run laterally in the outer plexiform
The synaptic ribbon helps to m aintain the release o f
layer over a distance o f about 1 mm. They respond in a
vesicles during periods o f prolonged visual stim ulation
graded fashion to release o f glutamate from rods or cones,
and to coordinate the sim ultaneous release o f vesicles
using ionotropic glutamate receptors. H orizontal cells
required for precise tim ing (M atthew s and Fuchs
release rhe inhibitory neurotransm itter G A B A . O n e type
2 0 1 0 ).
o f horizontal cell receives inputs from green cones or red
3. Fat synaptic boutons These occur only on cone pedicles. cones w ithin its dendritic field, and makes inhibitory co n ­
The boutons near a synaptic invagination contact tacts with several cone bipolar cells. For example, some
dendrites of O N -bip olar cells. Those away from an horizontal cells receive inputs from red cones and send
invagination co n tact dendrites o f O F F -b ip o lar cclls. inhibitory inputs to synapses co n n ectin g green cones to
bipolar cells, while other horizontal cells operate in reverse
fashion. A second type o f horizontal cell receives inputs
primarily from rods or blue cones.
These reciprocal con n ection s betw een different types ol
cone were believed to form the basis for the first stage o f
color opponency. However, it now seems that this is not the
case (D acey et al. 1 9 9 6 ). H orizontal cells also make direct
synapses with neighboring horizontal cells o f the same type
so that, collectively, they form a resistive netw ork. Signals in
horizontal cells are also believed to feed back to cones in
the form o f a delayed depolarization, but the extent and
significance o f this process has been a subject o f debate
(Burkhardt 1993).
A m acrin e cclls occur in the in n er plexiform layer
betw een bipolar cells and ganglion cells. In this layer, ama­
crine cells form in h ibitory con nection s with bipolar cells
and ganglion cells. Their dendritic fields extend up to 1 mm
in diameter.
A m acrine cells generate the first all-or-none actio n
p o ten tia ls. An action potential is all-or-none because it has
con stan t am plitude for that nerve cell (see Section 4 .2 .1 ).
W hereas a receptor potential is local, an action potential is
a b rief event that travels along an axon, sometimes for co n ­
siderable distances. The speed o f propagation o f an action
potential is proportional to axon diameter, which varies
betw een 0.1 and 2 0 ftm in vertebrates. In large axons,
condu ction speed reaches 120 m/s.
Thirty types o f amacrine cclls have been described. They
differ in rhe type o f bipolar cells they receive inputs from ,
which is related to their depth w ithin the inner plexiform
layer. 'I hey also differ in the lateral spread o f their dendritic
fields and in the ncurotransm itter they use (see Rowe 1991).
Each type seems to fulfill a d istin ct function, although rhe
functions served by m ost of them remain obscure. The
dendritic fields o f the different types o f am acrine cell may
overlap, but in m ost cases the fields o f each type tile the
retina w ithout overlap (M acN eil and M asland 1998).
5 .1 .4 G A N G L IO N C E L L S
5 .1 .4 a R e c e p tiv e F ield s o f G a n g lio n C e lls
G anglion cclls form the third and final outer layer o f the
retina. Their axons form the optic nerve, which extends to
the lateral geniculate nucleus.
D ischarges o f the whole optic nerve were first recorded
by Adrian and M atthew s (1 9 2 7 ) in the eel. The firsc
responses from single ganglion cells were recorded by
H artline and Graham (1 9 3 2 ) in che arrhropod L i m ulus,
and by H airline (1 9 3 8 ) in rhe frog. The receptors that
direcdy or indirectly atfect the firing o f a given ganglion cell
is the receptive field o f che ganglion cell, a cerm incroduced
by H artline.
Kuffler (1 9 5 3 ) showed that ganglion-cell receptive fields
in che cac recina are circular, wich a concentric organization
o f excitatory and inh ibitory regions. Receptive fields with a
central excitatory region and inhibitory surround arc
known as O N -c e n tc r recep tive fields. They cause the gan­
glion cell to fire preferentially to the onset o f a stimulus in
che recepcive-field center. Ganglion cclls w ith chis type o f
receptive field are known «is O N cells. Those with an in h ib ­
itory central region and excitatory surround arc known as
O F F -c e n te r recep tive fields. They cause the cell to fire to
stimulus offset. Ganglion cells with this type o f receptive
field arc known as O F F cells. O N cells tend to have larger
receptive fields, and their responses are m ore rapid and
more linear than those o f O F F cells (C hichilnisky and
Kalm ar 2 0 0 2 ).
G anglion cclls have overlapping receptive fields because
receptors supply inputs to several ganglion cells (see
C hichilnisky and Baylor 1999). Those with overlapping
receptive fields that are either both O N -ccn ter o r both
O F F -cen ter tend to fire at the same tim e, w hile those with
opposite-sign centers tend n o t to fire at the same time
(M astronarde 1 9 8 3 ). O N -ccn ter and O F F -cen te r receptive
fields feed into pathways that remain d istinct as far as the
visual cortex (Schiller 1992).
The center o f an O N -cen tcr ganglion cell receives direct
signals from several receptors through O N -bip o lar cclls,
and indirect signals trom horizontal cells that originate in
O F F bipolar cells. The center o f an O F F -cen te r ganglion
cell receives direct signals from O F F -b ip o lar cells, and
indirect signals from horizontal cells that originate in O N
bipolar cells. Thus, bipolar cells act on ganglion cells in a
“p u sh-pu ir mode. We will see in Section 5 .1 .4 f that the
push-pull m ode increases the dynamic range o f ganglion
cells to luminance and ensures that the strongest signals
com e from where lum inance changes spatially or over time.
These are the signals containing useful intorm ation.
5 .1 .4 b T y p es o f G a n g lio n C c lls in C a ts
The retinas o f cats contain at least 10 types o f ganglion cells,
each o fw h ich is believed to tile the retina. A b o u t h alf are X
cells or Y cells (R o ck h ill et al. 2 0 0 2 ) , which arc subdivided
into O N -typ es and O FF -typ es according to w hether che
ccnccr ot che receptive field is excitatory or inhibitory
(F.nroth-Cugcll and Robson 1 9 6 6 ). Type X cclls (/?cclls)
are m ost dense in the central retina. They have small recep­
tive fields with segregated excitatory and inhibitory regions
trom which signals are summed in a linear fashion. Their
axons conduct ac a velocicy becween 15 and 2 3 m/s and
project m ainly to cortical area 17. They are m ost sensitive
со high spaCial-frcqucncy and low tcm poral-frequcncy
Stimuli.
Type Y cells a cells) are m ore evenly distributed over
the retina. They have larger receptive fields thac are not
segregated into clearly defined regions, and show n o n ­
linear summation o f lum inance distributions. Their axons
conduct at between 2 0 and 3 0 m/s and project mainly to
corcic.il area 18. They respond bcsc to low spatial-frequency
and high tem poral-frequency stim uli (Pasternak et al.
1995).
O th er ganglion cells are known as W cells. They have
large receptive fields concentrated in the central retina.
They have thin axons that conduct at a velocity o l between
2 and 18 m/s, and project to cortical areas 17, 18, and 19
and to rhe pulvinar in the thalamus. The functional proper­
ties ot other types o f ganglion cell are n o t know n. Som e are
photosensitive (Section 5 .1 .4 e) and som e seem to he sensi­
tive to the Earth’s m agnetic field (Section 3 7 .5 ).
The retinas o f primates arc tiled by at least 13 types o f
ganglion cells. The tw o m ost com m on types are broadly
classified into c o lo r-o p p o n e n t cells and ach ro m a tic cells
rather than X and Y cells.
5 .1 .4 c C o lo r - O p p o n e n t G a n g lio n C e lls
C olor-op p on en t ganglion cells have small cell bodies, thin
axons, and small, dense dendritic trees. They are known as
m idget g an g lion cells, parvocellular cells, or simply P cells.
“Parvo” is Latin tor “small." They project to the p arv o cel-
lular lam in ae o f the L G N and then to layer 4 C B in the
visual cortex. They constitute about 7 0 % o f ganglion cells.
Each cone contributes, directly or indirectly, to at least
two m idget bipolar cells, o n e O N -cen tcr and one O F F -
center (K o lb 1 9 7 0 ). Red cones (L cones) and green cones
(M cones) feed inco the cellular netw ork o f the retina to
create four types o f color-opp onent ganglion cells. 'Iheir
receptive fields are (1 ) red O N -ccnter/grecn O FF-surround,
(2 ) green O N -center/red O FF-surround , (3 ) red O F F -
center/green O N -surround, and (4 ) green O FF-ccnter/red
O N -surround. T h e firsc tw o types correspond to inner
m idget ganglion cells and the latter two types to oucer
m idget ganglion cells. The receptive fields o f inner and
outer midget cells torm distinct mosaic coverings ot the
retina. Sim ilar opponent structures are created from yellow
(red plus green) and blue cones (S cones) teeding into a dis­
tin ct class o f ganglions cells known as bistratified ganglion
cells.
The firing rate o f a color-opponent ganglion cell
increases above the baseline when the excitatory region is
stim ulated m ost and decreases below the baseline rate when
the inhibitory region is stim ulated most. For example, a cell
with a red-excitatory center and green inhibitory surround
produces an increased response to a long-wavelength stim u­
lus and a decreased response to a medium-wavelength stim ­
ulus. N ote that single opponent cells do not respond to
chrom atic boundaries. We shall see later that che tour types
o f red-green ganglion cells converge on so-called double-
opponcnc cells in che visual cortex thac produce signed dif­
ference signals related ro local color contrast.
A ccording to che tradicional view, che receptive field ot
a color-opp onent ganglion cell contains cones o f one type
in che cencer and o f anocher single cypc in che surround
(Reid and Shapley 1 9 9 2 ). Lennie et al. (1 9 9 1 ) suggested
that, at least for eccentricities up to 10°, the recepcive-field
center consists o f a single S, M ,o r L e o n e , and the surround
contains a random m ix o f cone types, which feed into b ip o ­
lar cells through horizontal cells. This type o f recepcive
field organizacion creates at least som e color opponency.
However, recenc evidence suggests that, in the macaque
monkey, ganglion cells receiving inputs from either L (red)
cones or M (green) cones do not receive any input from
S (blue) cones (Lee 1 9 9 6 ; Sun et al. 2 0 0 6 ). This means that
the capacity o f the parvocellular syscem to resolve high spa­
tial frequencies is not degraded by rhe chrom atic aberration
produced by shorc-wavelength light.
It had been assumed that horizontal cells in che outer
plexiform layer co n n ect cones o t opponent types, buc there
is evidence that chey co n n ect all types o f cones (D acey et al.
1 9 9 6 ). Am acrine cells form ing inhibitory links between
m idget ganglion cells in the inner plexiform layer arc also
indiscrim inate with respect to che spectral specificity o f che
cells chey co n n ect (C alk in s and Sterling 1996).
C olor-op p onen t ganglion cells have small receptive
fields, low sensitivity to lum inance, but high sensitivity to
chrom atic m odulation. They conduct nerve impulses at
medium velocity. They produce a sustained response to
continued stim ulation wich a high degree o f linearicy in
their temporal response. Their small receptive fields enhance
spatial resolution and enable them to respond со stimuli
with high spatial frequencies. Their sustained characteristic
reduces their tem poral resolution. Thus, parvocellular cells
in the m onkey can resolve gratings up to 4 0 cpd buc are
m ost sensitive to temporal frequencies o f only 10 Hz
(D errin gton and Lennie 1 9 8 4 ). C o lo r opponency is
reduced at scocopic lum inance levels.
5 . 1 .4 d A c h r o m a tic G a n g lio n C e lls
A ch ro m atic gan glion cells are called parasol gan glion
cells, or m agnocellular cells (M cells). They have large
receptive fields and project to the m ag n o cellu lar lam inae
o f the L G N and then to layer 4 С a in the visual cortex.
They con stitu te abou t 10% o f ganglion cells. They have
recepcive-field centers and receptive-field surrounds made
up o f rods o r M (green) cones and L (red ) cones. There has
been dispute about w hether the m agnocellular pathway
receives inputs from S (blue) cones, but recenc evidence
suggests that they do not (Sun et al. 2 0 0 6 ).
Achromatic ganglion cells have high contrast sensitivity,
are broadly tuned to wavelength, and do n o t show color
opponency. They are referred to as b ro ad b an d cells.
However, for some o f them , rhe receptive field center and
surround are not in spectral balance, and color opponency
is revealed under certain conditions o f stim ulation (Shapley
1 9 9 1 ) (Portraic Figure 5 .6 ). Som e have O N -cencer recep­
cive fields and others have O F F -cen te r receptive fields.
Their large receptive fields enhance their lighc-colleccing

Figure5-6 R obert ShapUy. B o rn in N ew York 1 9 4 4 . H e graduated in
ch em istry and physics from H arvard in 1 9 6 5 and ob tain ed a P h .D . in
neu roph ysiology from the R ock efeller U n iv ersity w ith H . K . H artlin e
in 1 9 7 0 . A fter p o std o cto ra l w ork at C am brid ge U niversity he becam e
an assistant professor at R ock efeller U niversity in 1 9 7 2 . In 1 9 8 7 m oved
to the C e n te r for N eural Scien ce at N ew York U niversity, where he is
N atalie C lew s Sp en cer Professor. H e w on the N Y U Sokol award in
1997.
efficiency and render chem sensitive ac lower lum inance.
C ells with large receptive fields have higher sensitivity also
because they have a higher signal-co-noise racio. Noise is
due to fluctuations in photon distribution and to spontane­
ous events at che photopigm ent and synapcic levels. W hen
N receptors feed into one receptive field, the total noise is
proportional со \(N.
M agnocellular ganglion cells have large-diam cter axons
and consequently con d u ct nerve impulses rapidly. They
show a transient response to continued stim ulation. Their
large receptive fields reduce cheir spacial resolution, buc
cheir transicnc characteristic improves their cemporal reso­
lution so chac chey are able to respond to higher races o f
flicker and higher velocities o l m otion than the sustained
color-opp onent cclls. In the monkey, broadband cclls can
resolve gratings up to a spatial frequency o f only about
10 cpd but are m ost sensitive to tem poral frequencies o f
2 0 Hz (D errin gton and Lennie 1984).
Selective staining has revealed that about 6% o f gan­
glion cells serving the foveal cen ter are parasol cells and that
each cell receives inputs Irom 3 0 to 50 cones (G ru n ert et al.
1 9 9 3 ). This means chat chey have a spacial resolution o f
about 4 arcm in. Foveal acuity, w hich is about 1 arcm in,
must therefore depend on m idget ganglion cells.
G anglion cells are classified in other ways according to
che organizacion o f cheir receptive fields, but this goes
beyond the scope o l this book. In the retinal periphery
there arc at least 10 types o f ganglion cclls that arc neither
m idget cells n or parasol cells, but little is known about the
functional properties o f these cclls. For more details on
the structure and function o f the retina see Dow ling
(1 9 8 7 ), W assle and B o yco tt ( 1 9 9 1 ), Lee ( 1 9 9 6 ), and
R odieck (1 9 9 8 ).
5 . 1 .4e C o n n e c tio n s an d R esp o n se s o f
G a n g lio n C c lls
In humans, the total num ber ot ganglion cells varies between
0 .7 and 1.5 m illion. In che central retina, ganglion-cell
densities vary betw een 3 2 ,0 0 0 to 38,000/ m m 2. D ensities in
che nasal retina are 3 0 0 % higher than those at correspond­
ing positions in the temporal retina. D ensities in the supe­
rior retina are 60 % higher than those in the inferior retina
(C urcio and Allen 1990). Visual consequences o l retinal
asymmetry are discussed in Section 14.6.2a.
For each cone in the central fovea of che monkey retina
there arc three to four ganglion cclls. Each ganglion cell
receives inputs trom more than one cone and each cone
influences several ganglion cells. A t an eccentricity o f about
15° there is one ganglion cell per cone. In the peripheral
retina there arc many more concs than ganglion cells. In the
m onkey retina ganglion-cell density decreases from abouc
50,0 0 0 / m n r near chc fovea to about 800/m m 2 in the nasal
periphery and to about 100/m m 2 in che cemporal periphery
(W assle et al. 1 9 9 0 ). Thus, the precision with which the
retina samples the distribution o f lighc in che image declines
syseematically with increasing eccentricity.
A single recepcor, even in che fovea, cypically co n trib ­
utes to the center and surround o t several ganglion-cell
receptive fields. In other words, neighboring receptive fields
of ganglion cells overlap. Overlap improves the signal-to-
noise ratio by averaging responses over several receptors.
It also produces uniform ity ot contrast sensitivity over
che retina. O ptim al uniform ity is achieved by separating
recepcive-field centers by twice the standard deviation of
the reccptive-field profile. However, overlapping receptive
fields are less econom ical and increase response redundancy.
See Borghuis c t al. (2 0 0 8 ) for a discussion o f this issue.
For reccptive-field centers arranged in a square lattice
and separated by distance a, as in Figure 5 .7 Л , the m ini­
mum radius of the receptive fields required for com plete
coverage is a/\'2. For receptive fields arranged in a hexago­
nal lattice, as in Figure 5.7B , the m inim um radius for co m ­
plete coverage is a/ \'3. For a given type o f ganglion ccll, the
ratio of recepcive-field spacing to reccptive-field diam eter is
close to that predicted trom the m ost efficient coverage tor
a hexagonal lattice ( W assle et al. 1981). Thus, at every point,
the retinal image is efficiently sampled for che differenc
visual feacures chac each o f che differenc cypes o f receptive
field dcccccs.
The areas o f cencer and surround regions o f che recep­
tive fields ot boch opponenc and achrom atic ganglion cells

а tyrate (A P B ) to an anim als recina. This impairs the anim als
Я
В
К*аг«$.7. C overage of'gangfion’ceU rcceftivefields. (A ) F o r a square lattice- o f
receptive Helds, a u nits a p art, (he m in im u m radius o f coverage is a f \!2
(B ) F<ir a hexagonal la ttice, th e m in im u m radius is a / J J . (Ad^Kitrom
W i t J c c i iL 1 9 8 1 )
increase in proportion ro eccentricity. A t all eccentricities
the receptive fields o f achrom atic cells have about twice
rhe area o f those o f opponent cells. Peak sensitivities o f
center and surround regions are inversely proportional to
receptive-field area, and hence ro eccentricity, so that spa­
tially integrated contrast sensitivities (contrast gains) are
constant over the visual field (C ron er and Kaplan 1995).
M ost ganglion cells m aintain an irregular discharge in
the absence o f stim ulation. The irregularity o f the m ain­
tained discharge, especially in the low-frequency range, is
also evident in the power spectrum o f the responses o f gan­
glion cells to stim uli. The irregularity in dim light arises
from chc stochastic quantal nacurc o f lighc and from random
variations in the initiation o f neural spikes (R obson and
Troy 1 987). The form ation o f che recinal image and visual
resolution are discussed in Section 9.1.
Nerve impulses in ganglion-cell axons take longer со
reach the optic nerve the greater their distance from the
optic disk. However, at least for X cells o f the cat, chis dif­
ferencial delay is com pensated for by the increase in axon
diam eter with increasing ccccntricicy. Axons with greacer
diam eter con d u ct m ore rapidly (Stanford 1987).
5 . 1 . 4 f A d a p tiv e C o d in g in G a n g lio n C e lls
It was explained in Section 5 .1 .4 a that ganglion-cell recep­
tive fields contain excitatory and inhibitory regions thac
receive inputs from O N bipolar cells and O F F bipolar cells
respectively. Thus, ganglion cells show spacial antagonism
between the center and surround o f their receptive fields
and a biphasic tem poral antagonism . This push-pull mode
o f operation increases che dynamic range o f ganglion cclls
to changes in lum inance (Sterling 1990). The O N -chan nel
can be selectively blocked by applying am inophosphonobu-
ability to detect lighc increm ents and reduces contrast sen­
sitivity. However, responses to shape, color, and movement
are impaired only mildly (Schiller et al. 1986).
'Ihe partition o f receptive fields into excitatory and
inhibitory regions and the tem poral biphasic response
ensures that the strongest signals com e from regions where
lum inance changes spatially or over tim e. These are che sig­
nals rhat contain useful inform ation. Ganglion cells are
insensitive to areas o f even anti unchanging lum inance.
Local regions in natural scenes rend со have che same lum i­
nance chac persiscs over time. Ganglion cells can be said to
reduce the redundancy present in the inform ation provided
by natural scenes, and thus economize on neural transmission
(Barlow 1961).
Several investigators have reported that, as lum inance is
reduced, ganglion cells lose their inhibitory surround
responses (Barlow et al. 1 9 5 7 ; M uller and D acheux 1997).
However, other investigators have n o t confirm ed chis effect,
at least atsuprathrcshold scotopic levels o f lum inance (Troy
ec al. 1999). Loss o f inhibicion would improve light sensi-
tivicv bu t degrade sensitivity to stimuli o f high spatial fre­
quency or high rates o f interm ittence. W ith decreasing
lum inance, the frequency o f response o f O F F -ce n te r gan­
glion cells falls more rapidly than chac o f O N -ccn ter cells
(R a m o a e ta l. 1 9 8 5 ).
Adapcacion со che mean level o f illuminacion occurs
entirely in che recina. G anglion cells and cells in V I adapt ro
the mean level o f contrast. Thus, contrast adaptation is due
to both retinal and corrical processes (see Kohn 2 0 0 7 ).
Inspection o f a high-contrast grating for some tim e reduces
concrasc sensicivicy, so chat a low-conorasc gracing may be
invisible for some cime. Concrasc adapcation is specific to
the spatial frequency and orientation o f rhe adaptation
grating.
Following onset o f high-contrasc scimuli, ganglion cclls
of the salamander showed three changes, starting in less
than 0.1 s and developed over 10 s.
1. Reduction in integration time, which reduced
sensitivity to low spatial frequencies.
2. Reduction in contrast gain, w hich protected against
response saturacion.
3. An initial increase in spike frequency followed by a slow
reduction. The initial increase indicated chat a change
o f contrast had occurred, and che subscqucnc rcduccion
protected against saturation (Baccus and M eiscer 2 0 0 2 ).
Ganglion cells also adapt to the local spacial and temporal
features o f the stimulus. Hosoya et al. (2 0 0 5 ) exposed a rab­
b its retina со a flickering checkerboard for several seconds.
Л tier adaptation, responses o f ganglion cells to a flickering
checkerboard became about 50% weaker and responses to a
flickering uniform field increased by about 40% . The reverse
changes occurred after adaptation to a uniform flickering
field. Exposure to a flickering horizontal grating decreased
ganglion-cell responses to a horizontal grating and increased
responses to л vertical grating. Thus, ganglion cells adapt to
the predom inant local spatial structure so as to becom e less
responsive to more predictable (redundant) stimuli.
5 . l . 4 g P h o to se n s itiv e G a n g lio n C e lls
In rodents, and probably in all mammals, about 1% ot gan­
glion cells contain photosensitive m elanopsin. These cells
torm an electrically coupled network in the inner retina
that acts as a ph otod etector rather than an im agc-detector
(Berson et al. 2 0 0 2 ). The cells respond with spikes in mice
lacking rods and cones (Freedm an et al. 1999). They depo­
larize in response to light, like rods and cones o f inverte­
brates, but unlike those o f vertebrates. They have very low
tem poral resolution (D o et al. 2 0 0 9 ). The cells p roject to
the su p rach iasm atic nucleus via the suprachiasmatic tract.
This nucleus controls the circadian rhythm , as explained in
Section 5.3.1. It is also involved in the pupillary light
response. This whole system matures before the system
serving image detection.
M igratory birds possess a distinct class o f ganglion cells
known as displaced ganglion cells (Britto et al. 1988). There
is evidence that they contain light sensitive cryptochrom es
that detect the earth s magnetic field (Section 3 7 .5 .6 ).
5 .1 .5 L IG H T D E T E C T IO N
It has been estim ated that between 15 and 50 % o flig h t
quanta striking the cornea o f rhe cat are absorbed by rods.
Under dark-adapted conditions, cat retinal ganglion cells
respond on average with one or more nerve impulses per
photon absorbed by the visual pigm ent ( Barlow e t al. 1971).
Thus, at the absolute threshold, ganglion cells can transm it
inform ation on quantal absorptions very efficiently and
w ithout a threshold nonlinearity. Psychophysical experi­
ments have shown that the human visual system
Ш
has a similar
efficiency ( H e c h te ta l. 1942).
A cone integrates photons over about 50 ms. W ith in
the lum inancc range o f a cone the num ber o f photons arriv­
ing in the integration tim e varies between about 100 and
1 0 ' (Sch n ap f e t al. 1990). W ith in the linear range o f the
visual system, the num ber o f quanta absorbed is propor­
tional to the lum inance o t the light (Barlow and Lcvick
1 9 6 9 ). The hyperpolarization o f the cell m em brane is
proportional to the rate o t absorption o f light quanta by
photopigm ent.
Light sensitivity is reduced after exposure to bright
light (ligh t adaptation) and increased afier exposure to dim
light (dark adaptation). C ontin u ed exposure to bright light
depletes the stock o f unbleached pigm ent molecules and
depletes neurotransm itter vesicles trom the prcsynaptic
m em brane o f ganglion cells. These processes allow a system
with lim ited dynam ic range to cope with changes in light
intensity o f ten orders o f magnitude.
In an ideal detector (one free ol internal noise), sensitiv­
ity to a change in lum inance should depend only on random
fluctuations in rhe number o fq u an ta absorbed by the detec­
tor (DeVries 1 9 4 3 ; Rose 1 9 4 3 ). I f we assume that these fluc­
tuations follow a Poisson distribution, the detectability o f a
luminance increm ent should be proportional to the size ot
the change. Also, detectability should increase as the square
root ot the pedestal lum inance, a relationship known as the
d cV ries-R o se law (C oh n c t al. 1 9 7 5 ). These predictions
held tor frog ganglion cells only over a small range ot low
pedestal lum inance. At higher levels, the increm ent thresh­
old is proportional to pedestal lum inance (W eber’s law).
A signal-detection measure o f the sensitivity o f ganglion
cells in the cat s eye to a change in lum inance could be m od­
eled quantitatively only when noise in the receptors was
taken into account (Levick et al. 1 9 8 3 ).
Rose (1 9 4 8 ) introduced the con cept o f the qu antal
efficien cy o f any system that detects a stimulus at low light
levels. If the average num ber o fq u a n ta absorbed in a given
tim e by a given detector is N, with a deviation ol >/]V , then
the smallest change in N that can be detected, д N is:
ДЛ’ = JN (i)
where is the sig n al-to -n o ise ratio. It can be shown diat:
l \ = L C '( X ' (2)
W h ere /r, is a constant that depends on the optical param­
eters, quantal efficiency, and integration tim e o f the detec­
tor, L is the lum inance o f the stimulus, С is the threshold
contrast, and a is rhe angular subtense o f the stimulus.
Thus, for optical or visual systems with sim ilar optical prop­
erties and integration times, quantal efficiency is propor­
tional to che square o f the threshold contrast. Rose estimated
the quantal efficiency of' the human eye as 5% for a small
b rief spot on a low lum inance background at threshold
lum inance (see also van M eeteren 1 9 7 8 ). Receptors in the
eye are subject to noise arising from random fluctuations in
the num ber o flig h t quanta arriving at a given location in a
given tim e, and from variations in absorption o f light
quanta. But, in addition, there is noise due to random fluc­
tuations in the biochem ical processes w ithin the retina,
including thermal instability ot the visual pigments and o f
the neural transduction processes (Lam b 1987). Visual
inputs arising from spontaneous events in the retina art-
known as “dark lig h t” (Barlow 1957). ЛИ these sources o f
noise are known as the in trin sic n oise ot the visual system.
t
N eighboring retinal cones arc interconnected by
gap junctions, through which electrical signals can pass.
Strong signals spreading over a wide area o f the retina would
wash o u t differences in visually evoked potentials and
thereby degrade visual resolution. However, it has been
shown that the signals carried by gap ju n ction s spread no
further than the radius o f image blur arising from the eye’s
optics (S ectio n 9 .1 .1 ). These local signals tend to even out
the uncorrelated random noise across neighboring cones
leaving correlated activity due to the stimulus relatively
unchanged. In this way, gap ju n ctio n s betw een cones
improve the signal-to-noise ratio (DeVries ct al. 2 0 0 2 ).
E xtern al n oise is a perturbation ot that feature o f a
visual stimulus that is being investigated. For example, lum i­
nance jitter can be added to a stimulus patch or random
spatial fluctuations o f am plitude or contrast can be added
to a sinusoidal grating.
In the absence o f external noise, the threshold in a
psychophysical experim ent measures how well the visual
system transform s a given stimulus into a decision. This
transform ation involves tw o stages— the form ation o f a
neural signal and a decision stage. T ran sd u ctio n efficien cy
indicates how well the stimulus is converted into neural
signals. Intrinsic noise reduces this efficiency below a value
o f 1. C a lcu la tio n efficien cy¥ indicates how well the visual
system makes correct decisions on the basis o f noisy neural
signals. It the input is specified in term s o f light quanta, the
luminance threshold specifies the quantal efficiency o f
the visual system for that stimulus, which includes trans­
duction efficiency and calculation efficiency. Thus, quantal
efficiency equals the product o f transduction efficiency and
calculation efficiency.
Visual scientists have attem pted to obtain separate mea­
sures ot transduction efficiency (intrinsic noise) and calcu­
lation efficiency. Engineers specify the intrinsic noise o f an
amplifier by measuring the noise level o f the outpuc at each
o f several frequencies as a function o f the level o f an input
o f white noise. At low levels o f external noise, output noise
is dom inated by intrinsic noise and remains relatively co n ­
stant. W h en the external noise begins to exceed the intrin­
sic noise, the output noise as a proportion o f input noise
begins to rise more steeply. The noise level at which this
begins to happen is known as the eq u iv alen t in p u t noise.
Thus, the position o t the "knee" in the output function is
taken as a measure o f the intrinsic noise o f the system.
A similar procedure has been used to determ ine the
intrinsic noise o f the visual system with respect to specified
detection tasks. For example in a tw o-interval forced choice
lum inance detection task, the square o f the contrast thresh­
old in decibels specifies the output noise level. This is plot­
ted as a function o f the level o f external noise in decibels
that has been added to the stimulus. The level o f external
noise where the slope o f the threshold function begins to
change is taken as a measure o f the intrinsic noise o f rhe
visual system tor chat task (P clli 1 990). The intrinsic noise
includes fluctuations in absorption o f light and neural insta­
bility and indicates the transduction efficiency o f the
system. The calculation efficiency can then be derived
by dividing the quantal efficiency by the transduction
efficiency.
This procedure has been used to determ ine whether
practice in a psychophysical task improves transduction
efficiency or calculation efficiency (see S ection 4.9 .2 c).
The form ation o f the retinal image and visual resolution
are discussed in Section 9.1.
5 .2 L A T E R A L G E N IC U L A T E N U C L E I
5 .2 .1 S T R U C T U R E O F T H E LG N
The thalamus is a subcortical structure through which
alm ost all sensory nerves pass on their way to higher cen ­
ters. The two lateral g en icu late n u clei (LC iN ) are the part
o f the thalamus through which visual inputs pass on their
way to the visual cortex.
The axons o f ganglion cells leave the eye in the optic
nerve. Alter passing through the optic chiasm , the axons
form the optic tract. In higher mammals, m ost o f the axons
in each optic tract go to the ipsilateral lateral geniculate
nucleus. In each L G N the axons segregate into distinct
layers, or lam inae, where they synapse with relay cells
(Perry et al. 1 9 8 4 ). The axons o f relay cells go to the prim ary
visual cortex.
The projection ot the visual field o n to the primate LG N ,
shown in Figure 5.8, has been revealed by use o f retinal
lesions (Brouw er and Zeem an 1926; ('la rk and Penman
1 9 3 4 ) anil, in m ore detail, by m icroelectrode recording
(M alpeli and Baker 1 9 7 5 ). The horizontal retinal meridian
divides rhe LG N along its axis o f symmetry. The lower
Lateral
L o w e r field
M e d ia l
Retina LGN
Figure s-я. P rojection o f th e visualfie ld auto the LG X . S ch e m a tic view o f the
right hem ificld o f th e m o n k e y s recina and its p ro jectio n o n to the dorsal
surface o f layer 6 o f the left L G N . N u m bers represent degrees, ’the
blue lines are azim u ths, and th e black lines arc elevations. T h e red lines
represent th e lim its o f chc visual field. Quforwn fom м fekcr 1975)
visu.il field is represented in the medial superior h alf and the
upper field in the lateral inferior half. The vertical meridian
o f the visual field divides the L G N in the orthogonal direc­
tion. The fovea is represented at the posterior, or caudal
pole, and peripheral regions arc represented at the anterior,
or rostral pole. In the macaque L G N , 10,000 times more
parvocellular neurons are devoted to each unit area ot
the fovea than to each unit area o f the far periphery
(M a lp c licc a l. 1996).
The LG N o f the ca t contains four principal laminae des­
ignated A , A 1, C , and С 1, and two others known as C 2 and
C 3 . C ells in laminae A and С receive their inputs from the
contralateral eye and those in laminae A l and C l from the
ipsilateral eye. The tw o A laminae con tain sim ilar types o f
cells but the cells in lam ina C , which originate in the nasal
hem iretina, are considerably larger than those in layer C l ,
which originate in the tem poral hem iretina. The axons o f
m ost X and Y cells term inate in laminae A and A l with
about 6 2 % o f all Y cells term inating in lamina A l. The
С lam ina receives a few X and Y cells but mainly W cells.
W cells are a heterogeneous group o f slowly conducting
ganglion cells. Their large receptive fields have poorly
defined excitatory and inh ibitory regions and poor spatial
and tem poral resolution. Also, the ca ts L G N has tw o asso­
ciated nuclei— the medial interlam inar nucleus and the
geniculate wing (Kaas et al. 1972).
The retinogeniculate pathways o f monkeys have been
investigated by tracing the retrograde transport o f horse­
radish peroxidase from specific layers o f the L G N to spe­
cific types ot ganglion cell in the retina (Perry et al. 1984).
The pathways have also been investigated electrophysiologi-
callv bv recording trom cells in the living L G N (K aplan and
Shapley 1 986).
The axons o t color-opponent ganglion cells (P cells)
term inate in the four dorsal laminae in the primate L G N ,
where they synapse with relay cells (Figure 5.9). These are
the parvocellular lam inae, or P lam inae. Inputs from the
ipsilateral eye go to laminae 3 and 5. and those trom the
contralateral eye go to laminae 4 and 6. The whole visual
channel, including color-opponent ganglion cells, the
P laminae o f the L G N , and the cortical pathways to
which they lead, form s the p arv o cellu lar system .
The axons o f achrom atic ganglion cells term inate in the
two ventral laminae o f the L G N , known as the m agnocel-
lular laminae, or M lam inae. Inputs from the ipsilateral eye
go to lamina 2, and those trom the contralateral eye go to
lamina 1, as shown in Figure 5.9. A chrom atic M ganglion
cells, the m agnocellular laminae, and the cortical pathways
into which they feed form the m ag n o cellu lar system.
In the part o f the L G N devoted to the central retina
there arc four P laminae and tw o M laminae. In parts
devoted to the peripheral binocular visual field, there are
onlvs tour lam inae— tw o P and two M laminae. The blind
spot is represented in che transition zone betw een the six-
layered and four-layered regions (Lee and M alpeli 1994).
V entral
Fi**rc$.9. I b e la tera lg en h u la te nucleus. L am in atio n and p ro jectio n
co lu m n s in a co ro n a l se ctio n o t the L G N o f a m onkey. A co lu m n is
defined as having 9 0 % o f the cclls w ith a single visual d ire ctio n . Inputs
from the ipsilateral eye term in ate in L am in ae 2 , 3 . and 5 , w hile those
from the con tralateral eye term in ate in lam inae 1 ,4 , and 6 . (From
S x c n U g o t i u i 1 9 7 3 «»*tli k i n J p c n o i w i o e o f S f n a ^ c r S i * c m c * B u u n c » * M e d ia )
The region devoted to the m onocular temporal crescent ot
the visual field receives only crossed inputs and therefore
contains only tw o lam inae— one P and one M lam ina (Kaas
et al. 1 9 7 2 ). Inputs to each lam ina in the L G N arc projected
in systematic retinotopic order. Inputs from corresponding
areas o t the two eyes lie in p ro je c tio n colu m n s running at
right angles to the laminae, as shown in Figure 5.9. In each
lam ina, ganglion cells with O N -cen tcr receptive fields and
those w ith O F F -cen te r fields term inate on distinct cells.
A ccording to one estim ate, magnocellular inputs reach
the LG N o f the monkey, on average, 17 ms before parvocel­
lular inputs (Schm olcsky et al. 1 9 9 8 ). But, it has been
claim ed that this temporal advantage is elim inated by rhe
time inputs reach the visual cortex, because the more num er­
ous parvocellular inputs converge on cortical cells more
than do magnocellular inputs (M au n sellet al. 1999).
The primate LG N also has so-called k o n io cellu lar cells,
or К cells, which have physiological properties sim ilar to
those o f W cells in cats. They occur m ainly in three ipsilat­
eral and three contralateral lavers in the L G N but some are
scattered in M ccll and P cell layers (H endry and Yoshioka
1994). They torin fewer and smaller synaptic term inals than
do P and M cells and have larger receptive fields (Shostak
et al. 2 0 0 3 ). They relay inputs from blue cones to c y to ­
chrom e oxidase blobs in layers 1 and 3 ot the visual cortex,
to the superior colliculus, and M T . G roups o f large neurons
that tend to occur in К-cell layers, with properties similar to
К cells, project to V 2 , V 4 (Section 5.8.3a), the inferior tem ­
poral cortex (Section 5.8 .3 b ), and M T (S ectio n 5.8.4b ).
These pathways may be responsible for blindsight (see
Section 5 .5 .7 ). In the L G N , К cells receive substantial
inputs from V I and arc the only I.G N cells to receivc inputs
from the superior colliculus (H endry and Reid 2 0 0 0 ).
The neuroanatom v o f the L G N is reviewed in Garey
c t al. (1 9 9 1 ).
5.2.2 PROPERTIES OP LGN RELAY CELLS
5 .2 .2 a In p u ts to L G N R elay C e lls
Th e receptivc'field o f each relay cell in rhe L G N is funda­
mentally the same as that o f the ganglion cell with which it
is connected. Furtherm ore, there arc as many relay cells as
ganglion cells, although there may be some divergence and
convergence o f optic nerve fibers o n to L G N relay cells
(Schein and M onasterio 1 9 8 7 ).
Each neuron in the L G N receives a direct excitatory
input from only one eye. However, there are inputs trom
places o ther than the retina. Also, there are extensive in h ib ­
itory and excitatory interactions between cells in the L G N
(M arrocco and M cC lurkin 19 7 9 ; K ato et al. 1981; Ahlscn
et al. 1985). All inhibitory interactions involve interneurons,
which produce the neurotransm itter gam m a-am inobutyric
acid (G A B A ) (see M ize and M arc 1992).
O n ly about 12% o f synaptic ju n ctio n s found on genicu-
late relay neurons o f the cat originate in the retina. A bout
50% derive from layer 6 o f the visual cortex. The other
30 % are com posed o f inhibitory (G A B A crgic) inputs
from intcrncurons and cholinergic, noradrenergic, and
serotonergic inputs from rhe perigeniculate nucleus, brain­
stem reticular form ation, tegm entum , superior colliculus,
pretectum , and locus coeruleus (Sherm an and Koch 1986;
M ontero 1 992). Inputs to the monkey L G N are similar
except that chey do not include noradrenergic synapses
(Bickford et al. 2 0 0 0 ).
M any inputs to the I.G N from sources o ther than rhe
eye term inate in interlam inar spaces, where they synapse
with dendritic extensions o f cells in the main laminae (see
Casagrande and Brunso-Bechtold 1988).
All direct cortical inputs to I.G N relay cells arc excit­
atory and originate from layer 6 o f the visual cortex. They
innervate corresponding retinotopic regions in the L G N ,
and the orientation selectivity and O N -O F F zones o f the
cortical cells m atch those o f t h e I.G N cells. However, it
seems that the feedback and recipient cells are reversed in
spatial phase (W a n g e t al. 2 0 0 6 ). Also, each axon innervates
several L G N relay cells (see C udeiro and Sillito 2 0 0 6 ). The
cortex also exhibits indirect inh ibitory influences on I.G N
relay cells through G A B A ergic L G N interneurons or the
thalam ic reticular nucleus.
Injection o f tracers has revealed that parvocellular layers
o f the L G N receive m ost o f their inputs from che upper halt
o f cortical layer 6, which is connected to cortical layers
4C /2 and 4 A — the layers receiving inputs from parvocel­
lular layers o f the L G N . M agnocellular layers o f the I.G N
receive all cheir inputs trom cells in the lower halt ot layer 6,
which is connected to layer 4 C 0 f — the layer receiving
inputs from m agnocellular layers o f the L G N (Lund and
B o o th e 1 9 7 5 ; Fitzpatrick e t al. 1994).
R etinogeniculate synapses involve the A M PA recep­
tor subunit G lu R l on rhe postsynaptic mem brane (see
S ection 5.5.2c). This receptor generates slow responses with
the high amplitude and precise tim ing required for trans­
mission o f visual inform ation. Visual activity is involved
in the buildup o f G lu R l receptors in retinogeniculate syn­
apses (K ielland c t al. 2 0 0 9 ). C orticogenicu late synapses
involve che receptor subunit G lu R 4, w hich generates tasc
responses o f much smaller amplitude, appropriate to their
role as m odulators ot visual inputs (Sherm an and Guillcrv
2002 ).
C orticofugal inputs to the L G N do n o t produce
responses in I.G N cells in the absence o f visual inputs.
However, these feedback circuits enable the cortex to influ­
ence the responses o f L G N relay cells. In particular, feed­
back can change the firing o f L G N cells between burst
mode and tonic mode (sustained mode) (sec Sherman
2 0 0 1 ). We will now see that they m odulate the spatial and
temporal properties o fth e center-sur round organization o f
L G N relay cells.
5 .2 .2 b S p a tio te m p o ra l R esp o n se s o f L G N C e lls
In the dark, m ost relay cells in the L G N m aintain a low rate
o f neural discharge o f betw een 10 and 2 0 impulses/s (see
Snodderly and Gur 1995). This is considerably lower than
the spontaneous firing rate o f ganglion cells (Kaplan c t al.
1987). O n ly som e cortical cells into which the L G N feeds
have a m aintained discharge— the rest are silent in the dark.
Inhibitory circuits in the I.G N and cortex muse be respon­
sible tor this progressive reduction o t spontaneous activity
betw een retina and cortex.
The response rate o f ganglion cells and ot L G N relay
cells increases with increasing stimulus contrast. C ontrast
gain is the increase in firing rate per unit increase in contrast
in the linear range. The contrast gain o f ganglion cells is
higher than that o f relay cells. Kaplan et al. (1 9 8 7 ) co n ­
cluded that the L G N contains a nonlinear gain control
m echanism that attenuates transmission as stimulus co n ­
trast increases. This m echanism could be due to inhibitory
interneurons in the L G N or to inhibitory influences arising
from other subcortical centers or the visual cortex. This
response com pression could prevent response saturation
in cortical cells. Each cortical cell receives inputs from sev­
eral L G N cells. If these inputs were summed linearly, the
response o fc o r deal cells would soon saturate. Thus, response
com pression in the L G N extends the dynamic range o f co r­
tical cells and enables them to code contrast and perform a
spatial and tem poral analysis o f the visual stimulus.
The response o f a relay cell in the cat L G N increases
as a grating stimulus reaches an optim al size, after
which the response decreases, as shown in Figure 5.Ю Л
(B o n in ct al. 2 0 0 5 ). This is know n as size tu n ing. The o p ti­
mal size is determ ined by the size o f the excitatory part o f
the receptive field and by the strength o f the in h ibitory sur­
round. A low -contrast grating docs n o t show size tuning
because it docs nor activate the in h ibitory surround.
The response o f a relay ccll saturates as the contrast o f an
optim al grating stimulus increases. This is c o n tra st satu ra­
tion. However, saturation did n o t show for a small stimulus
that did not encroach on the inhibitoryi surround o t the
cells receptive field, as shown in Figure 5 . ЮН.
Bonin et al. (2 0 0 5 ) accounted tor size tuning and co n ­
trast saturation in the cat L G N mainly in terms o f the orga­
nization o f receptive fields o f ganglion cells. They agreed
with previous investigators that inhibition in chc L G N
arises trom stimuli beyond the receptive fields ot ganglion
cells, as defined by classical m ethods (Solom on ct al. 2 0 0 2 ;
W ebb e t al. 2 0 0 5 ). However, they claimed that the standard
mcchods grossly underestim ate the size o f the reccptive-
field surround o f L G N ganglion cells. O th er investigators
have confirm ed that size tuning in the L G N results from
changes in receptive fields o f ganglion cells (N o lt ct al.
2 0 0 4 ). However, Bonin et al. did n o t excludc a contribu ­
tion from inhibitory interneurons in the L G N or from
feedback from the perigeniculate nuclcus.
B o n in c t al. argued that feedback from the visual cortex
is not a m ajor factor in inhibitory effects in the L G N
because the effects were not orientation specific and were
less extensive than cortical receptive fields. Also, ablation ot
the visual cortex in the marm oset m onkey did not abolish
surround inhibition in the L G N (W ebb et al. 2 0 0 2 ).
However, stimuli confined to rhe classical receprive field
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Fi£Uf с 5.Ю. S h e tuning a n d contrast uU uraticn in th e LOW. ( A ) R esponses o f L G N cclls as a fu n ctio n o f stim ulus d iam eter for each o f fou r con trasts.
( B ) Responses a s a fu n ctio n o t co n tra st fo r each o f three stim ulus diam eters. T h e solid lines arc p red ictio n s from a m odel. T h e stim uli were gratings
presented a t th e op tim al values o t 0 .2 4 cpd and 7 .8 H z. (.vbpecd fr.™ *ш п
clicitcd a stronger response when the visual cortex was
intact (Przybyszcwski et al. 2 0 0 0 ).
C ai c t al. (1 9 9 7 ) recorded from L G N relay cells in cats
.is bright and dark bars were Hashed for 13 ms on different
parts o f the receptive fields. M ost cclls had a ccntcr-sur-
round organization and responded with a 3 0 ms burst above
the resting level followed by a sim ilar period o f activity
below resting level. The response o f the receptive-ficld sur­
round was typically delayed relative to that o t the center.
C ells in the m agnocellular lam inae o f rhe L G N have
longer latencies to stim ulation than cells in parvoccllular
layers. This reduces differences in latency arising at the reti­
nal level. Also, cclls in magnocellular laminae have larger
receptive fields, greater sensitivity to lum inance contrast,
and better temporal resolution than cclls in parvoccllular
lam inae (L evitt c t al. 2 0 0 1 ).
Relay cells in the L G N respond either tonically wich a
discharge that persists as long as the stimulus persists or
phasically with a rapid burst ot 2 to 10 spikes. Transition
betw een these modes depends on the initial hyperpolariza-
tion o f the cell m em brane, which depends on inputs from
the visual cortex and subcortex. Sherm an (1 9 9 6 ) suggested
that relay cclls fire in tonic mode when specific objects arc
being inspected and in arrhythm ic bursts when chc animal
is searching tor an o bject. Feedback from the cortex m odu­
lates pattern-specific center-surround interactions in the
receptive fields o f L G N cells (C udeiro and Sillito 1996).
C o rtical feedback also alters the tem poral response
properties o f L G N cells (M arrocco et al. 1996). It induces
correlated firing o f L G N relay cclls in response to moving
oriented stimuli (Sillito e t al. 1994). Also, feedback from
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chc cortcx through the reticular com plex and perigeniculate
nucleus may enhance the response o f active sites in the LG N .
This could be an attentional mechanism (C rick 1984).
5 .2 .2 c O r ie n ta tio n S e n sitiv ity o f L G N C e lls
The dendritic fields o f retinal ganglion cells in the L G N are
organized radially (Schall et al. 1 9 8 6 ). M ost relay cells in
the cat and m onkey L G N are sensitive to the orientation ot
stimuli, especially stim uli w ith high spatial frequency
(D aniels et al. 19 7 7 ; Soodak c t al. 1 9 8 7 ; Shou and LevcnthaJ
19 8 9 ; Sm ith et al. 1 9 9 0 ). Relay cells tend to respond prefer­
entially to stimuli arranged radially with respect to the
fovea. A bout one-third o f the L G N relay cells o f rhe cat
were found to be sensitive to direction o f m otion. Like co r­
tical cells, they arc especially sensitive to m otion o f stimuli
with low spatial frequency (Thom pson et al. 1994a). In the
cat, som e tuning o f L G N cells to orientation and m otion
seems to arise in the retina since ic survives removal o t the
visual cortex (Thom pson et al. 1994a). However, removal
o f inputs from areas 17 and 18 reduced the num ber o f L G N
cells tuned to oblique orientations, which suggests th a tco r-
ticofugal projections have an influence on orientation
tuning in the L G N (Vidyasagar and U rbas 1 9 8 2 ). C o rtical
cells are m ore strongly tuned to orientation and direction o f
m otion than are L G N cells. C o rtical cells show differential
tuning to orientation over the whole range o f spatial fre­
quencies to which they respond, rather than со only a pare
o f that range (Thom pson et al. 19 9 4 b ).
Synaptic boutons o f individual corticofugal axons are
sparsely distributed over a wide region o f the LG N .
However, within this region, there is an elongated region ot
high synaptic density with an axis that is either parallel to or
orthogonal to the receptive field ot the parent cell in the
visual cortcx (M urphy c t al. 1 9 9 9 ). The parallel feedback
could serve to enhance the orientacion specificicy o f cortical
cells by synchronizing the response o f inputs from the
L G N . The orthogonal feedback could enhance the m otion-
direction sensitivity o f cortical cells.
5 .2 .2 d A ro u sa l R esp o n se s in th e L G N
In cats, responses o f L G N cells to light were facilitated by
concurrent stimulation o f the skin (H o tta and Kameda
1963). In alert monkeys, rapid eye movements, blinks, and
auditory and som csthctic stimuli produced nonspecific
responses in the L G N , even in the dark (Feldman and C ohen
1968). These responses may he related to attention (Sherman
and Koch 1 9 8 6 ), but their nonspecificity suggests a general
arousal function rather than attention to specific locations or
stimuli. Electrical stimulation o f the mesencephalic tegmen­
tum, an arousal mechanism in the brainstem, increased the
response o f relay cells in the L G N (Livingstone and Hubei
1981). This increase was particularly evident for stim uli in
the centers o f the receptive fields (H artveit et al. 1993).
5.2.3 B I N O C U L A R R E S P O N S E S IN LGN
5 .2 .3 a B in o c u la r R esp o n se s in C a t L G N
Relay cells o f the L G N o f the cat give brisk excitatory
responses to stimuli presented to the dom inant eye for that
cell. They respond weakly or not at all to stim uli presented
to the other eve.
4
However, stim ulation o f the nondom inant
eye may enhance or in h ibit responses to stim ulation o f the
d om inant eye (N oda et al. 1972). For exam ple, a weak co n ­
ditioning shock applied to one optic nerve facilitated the
response o f L G N neurons to a test shock applied to the
other optic nerve (M arshall and T albot 1940; Bishop and
Davis 1 9 5 3 ). Also, the response o f many relay cells was
inhibited by a con d ition in g stimulus applied to the non-
d om inant eye (Suzuki and K ato 1 9 6 6 ). The direct excit­
atory and indirect inhibitory inputs to relay cells arise from
corresponding regions in the tw o eyes (M archiafava 1966;
Sanderson et al. 1969, 1971; Singer 1 9 7 0 ).
G uido et al. (1 9 8 9 ) measured the responses o f L G N
relay cells in the eat to a drifting grating presented to the
nondom inant eye for those cells. Stim ulation reduced the
spontaneous discharge in 29 % o f the cells and produced
weak excitatory responses in 25% . Som e cells showed both
types o f response, according to the spatial frequency o f che
stimulus. These responses were stim ulus-tuned with respect
to orientation and spatial frequency, and occurred in X , Y,
and W cells in all L G N layers (b u t see C . W an g ct al. 1994).
M urphy and Sillito (1 9 8 9 ) obtained sim ilar results.
Binocular inhibition was more com m on in cells receiving a
d om inant input from the ipsilateral eye than in those receiv­
ing a dom inant input from the contralateral eye (Suzuki
and Takahashi 1970). A pplication o f bicucullinc, an antag­
onist to the inh ibitory neurotransm itter G A B A , blocked
the inhibitory responses but revealed excitatory responses
in cells previously unresponsive to the nondom inant eye
(Pape and Eyscl 1986; Murphy and Sillito 1989). Binocular
interactions in the L G N o f the cat are n o t disparity tuned
( X u c c t a l. 1987).
Indirect influences in the L G N are postsynaptic and
may be m ediated by intrageniculatc connections, by projec­
tions from other subcortical nuclei, such as the nucleus o f
the optic tract, o r by corticofugal inputs from the visual
cortcx. A bou t 25 % o f cells in the cat visual cortex project to
the I.G N . Som e arc com plcx cortical cells serving binocular
or m onocular segments o f the visual field. O th ers are simple
cells, serving only binocular regions. Thus, at least some
corticofugal influences are involved in binocular vision
(Tsum oto and Suda 1980).
There is some dispute about the role o f cortical inputs to
the L G N . Som e investigators found that binocular interac­
tions in the cat LG N require an in tact visual cortex. Reports
that interocular influences are greatest when stim uli pre­
sented to the two eyes differ in position, orientation, co n ­
trast, and m ovem ent prompted the suggestion that cortical
influences on L G N cells facilitate transmission o f signals
J r h e b e r r e c h t lic h g e s c h i i t z t e s M ate
from stim uli lying on the horopter, and arc involved in
binocular fusion and rivalry (S ectio n 12.3) (Schm ielau and
Singer 1 9 7 7 ; Varela and Singer 1987; Grunew ald and
Grossberg 1 9 9 8 ). O th er investigators reported that binocu­
lar interactions in the I.G N do not require corticofugal
inputs (Sanderson et al. 19 7 1 ; Murphy and Sillito 1989;
T u m o sa cta l. 1 9 8 9 a ; Tong ot al. 1 992).
In the cat, responses o f I.G N cells to stim ulation o f the
dom inant eye were n o t m uch affected by changes in the ori­
entation or direction o f m otion o f stimuli presented ro the
nond om inant eye. However, responses o f L G N cells were
affected by changes in the spatial frequency o f those stimuli
(M oore et al. 1 992). This suggests that corticothalam ic p ro ­
cesses balance the responses to small interocular differences
in stimulus contrast, by adjusting the relative contrast gains
o f inputs from the tw o eyes (Section 18.5.4). Perhaps b in ­
ocular rivalry and gain control are served by different pro­
cesses in the L G N . M cC Iurkin et al. (1 9 9 4 ) suggested that
cortical feedback to the L G N m odulates the number and
temporal waveform o f spikes in parvocellular neurons so .is
to enhance differences in response to distinct stimuli.
C o rtical feedback in the m onkey has been found to be also
responsible tor m odulation o t the response o f L G N cells to
a Hashing spot by a grating presented outside the receptive
fields o f the cells (M arrocco et al. 1996).
5 .2 .3 b B in o c u la r R esp o n se s in P rim a te L G N
There has been con flictin g evidence on binocular responses
in the prim ate L G N . Rodieck and Dreher (1 9 7 9 ) reported
that rhe response o f cells in rhe L G N o f the m onkey to
stim ulation o f the cells’ dom inant eye was partially sup­
pressed when the non d om in an t eye was stimulated ar the
same time. But this occurred only in magnocellular lam i­
nae. M arrocco and M cC Iurkin (1 9 7 9 ) found that about
13% of cells in both the parvo- and magnocellular laminae
o f the L G N o f the m onkey responded only ro binocular
stim ulation. These studies were conducted on anesthetized
and paralyzed monkeys.
M ultiple electrodes applied to the L G N o f alert m on­
keys revealed four types o f binocular interaction to light
flashes in both the parvocellular and magnocellular laminae
(Schroeder et al. 1 9 9 0 ). Stim ulation o f the nondom inant
eye reduced the response below the spontaneous level for
one type o fc e ll and increased it above this level for a second
type o f cell. For a third type o f cell, the response was less
vigorous to binocular stim ulation than to stim ulation o f
only the dom inant eye. For a fourth type o f cell, rhe response
was more vigorous to binocular stim ulation than to m on­
ocular stim ulation. Since rhe researchers used m ultiple elec­
trodes, they could not estim ate the proportion o f cells
showing rhese different responses. The latency o f interac­
tions was to o short to involve corticofugal influences.
However, rhe later response com ponents could have been
due to cortical influences. It is unfortunate that only
featureless flashes were used, since binocular interactions
revealed by psychophysical procedures depend on the pres­
ence o f contours (Section 12.3.3).
5 .3 V IS U A L P A T H W A Y S
5. 3. 1 VISUAL INPUTS TO SU B C O R T IC A L
CEN TERS
In the monkey, about 90 % ot axons in the optic tracts go to
the I G N and on ro the visual co rtex, as described in Section
5.2.1. In the cat, only 7 7 % o f ganglion cells project to the
I.G N (Illin g an d Wiisslc 1 9 8 1 ). In rod en ts,on ly about 37 %
o f ganglion cells p roject to the L G N . A bout 95% o f gan­
glion cells in rodents p roject ro the superior colliculus, and
many o t the axons reaching the L G N are branches o t these
axons (M artin 1986). In each case,ganglion-cell axons that
do not project to the L G N project to other subcortical
structures.
Thus, subcortical nuclei receive visual inputs from
op tic-tract axons that do n o t p roject to the L G N or from
collateral branches o f axons that do project to the LG N .
The su p erio r co llicu lu s is a m ajor recipient o f to p o ­
graphic visual inputs. In primitive vertebrates it is the m ajor
recipient area for visual inputs. In some mammals, such as
the rat and tree shrew, it seems that both visual hemifields
are represented in each superior colliculus (K aaset al. 1974).
In mammals, the superior colliculus is mainly concerned
with the control ot saccadic eye movements (G u itton
1991).
The p retectu m also receives topographic visual inputs
by way o f the accessory optic tract. The pretectum is co n ­
cerned with the co n tro l o t pupil diam eter and optokinetic
eye movements, as described in Section 22.6.1.
The su p rach iasm atic nu clei in the hypothalamus
receive visual inputs through rhe retinohypothalam ic tract
(Schein and M onasterio 1 9 8 7 ). The projection involves
only a small num ber o f ganglion-cell axons and is not
topographic. The suprachiasmatic nuclei contain the master
clock that controls the day-night circadian rhythm . In
humans, this rhythm involves a day-night fluctuation o f
body temperature and nocturnal secretion o f m elatonin by
the pineal gland.
Regulation o f the circadian clock and the pupillary light
response depends only on the am ount o t light. These
responses require the eye to act only as a photom eter. They
survive in m ice with genetic degeneration o t the rods and
cones but n o t in m ice lacking ganglion cells (Freedman
et al. 1 9 9 9 ). D ye tracing has revealed that ganglion cells
projecting to the suprachiasmatic nuclei contain photosen­
sitive m olecules o f n ielan op sin (Berson er al. 2 0 0 2 ). The
pupillary response can be driven cither by the rods and
cones con taining regular photopigm ents or by ganglion
cells containing mclanopsin. The pupillary response does
not occur in rnicc lacking both melanopsin and rods and
cones (van G elder 2 0 0 3 ).
The h ippocam pu s in the old cortex also receives direct
visual inputs. The hippocampus and the neighboring
amygdala have reciprocal con nection s with visual areas in
the neocortex and also con nect with the pulvinar region ol
the thalamus.

5.3.2 THE CHIASM AND O P T IC T R A C T S

The axons o f ganglion cells leave the eye to form the o p tic
nerve. Each optic nerve has a diameter o f 3 to 4 mm and
contains over a m illion axons. Alter passing out o l the retina
at the optic disk, che optic nerve travels about 5 cm to end in
the o p tic chiasm , named after the Greek letter chi because
it is shaped like an X . In m ost vertebrates, m ost o f the
axons Irom each eye cross over to the contralateral side in
the chiasm. This is known as decussation from the Latin
decussate, meaning to divide crosswise. In primates and some
other mammals, axons from the nasal hemiretinas decussate
at the chiasm , but those trom the temporal hemiretinas
remain on the same side. This is known as hem idccussation.
The nerves that emerge from the chiasm form the o p tic
tracts. In primates, axons from the tem poral h alf o f the left
eye jo in decussated axons from the nasal h alf o f the right
eye to form the left optic tract. Axons from the temporal
h a lf o f the right eye join decussated axons from the nasal
h a lf o f chc left eye to torm the right optic tract. In this way,
inputs from corresponding locations in the two eyes com e
into close proxim ity in the optic tract.
Each optic tract leaves the chiasm and term inates in the
ipsilateral L G N , where the incom ing axons synapse with
relay cells. A xons o f rhe relay cclls leave the LG N on
each side and fan out to torm the o p tic ra d ia tio n s, which
course backward and upward to term inate in rhe visual
cortex in the ipsilatcral occipital lobe ot the cerebral cortex i. V u visu alpathw ay/. A xon s trom th e rig h t h a lf o f ca ch eye (left

(Figure 5 .1 1 ).
In submammalian vertebrates, the o p tic nerves almost
fully decussate in the chiasm , so that each L G N receives
inputs mainly trom the contralateral eye. Ramon у Cajal
(191 1) proposed that this prim itive condition evolved to
preserve the spatial integrity ot the central neural map ot
the images from the two eyes. Because o f the optical inver­
sion o f each retinal image, the continuity o f the central
mapping is disrupted across the hemispheres when the
pathways are undccussatcd, as in Figure 5 .1 2 A . The central
map is continuous when the pathways decussate, as in
Figure 5 .1 2 B . The spatial integrity o f the internal map is not
im portant as such, since spatial location is coded in cerms ot
fiber con nection s and patterns o f firing, noc in terms o f spa­
tial maps. However, transcallosal fibers co n n ect spatially
adjacent regions from opposite sides o f rhe m idline, so that
visual stimuli in the m idline region can be processed. These
con n ection s for decussated pathways are shorter than for
undccussatcd pathways.
h em ificld ) p ro ject to the right o ccip ital lo b e, and th o se from the left
h a lf o f cach eye (rig h t h em ificld ) p ro ject to the left o c cip ita l lobe.
It is believed th at the crossing over o f visual inputs to
the opposite visual cortices led to che crossing over o f che
m otor pathways. 'Ih is ensured that visual inputs from a
given h alf o t space control chc limbs on the same side o f che
body. N obody has proposed a better explanation o f visual
and m otor decussation.
5 .3 .3 H EM ID E C U S S AT I О N
In animals w ith full hem idccussation, axons from the right
h alf o f cach eye project to the right L G N , and those from
the left h alf o f each eye project to the left L G N . W ith in
cach L G N , inputs from the two eyes remain in distinct lam ­
inae, where they synapse with relay cells. Relay cells from
cach LG N project through the optic radiations to chc ipsi-
lateral visual cortex. Because o f the reversal o f each retinal
 visual field, which depends on the extent to which the eyes
are in a lrontal position. This relationship is known as
the iN cw ton-M ullcr-G u dd cn law. Thus, the proportion o f
uncrossed fibers is alm ost zero in the rabbit, about one-
eighth in the horse, one-fourth in the dog, one-third in the
cat, and h alf in primates, including humans (W alls 1963,
p. 3 2 1 ). In m ost submammalian species the weak ipsilateral
projection o f the visual pathways is not related to the degree
o f overlap o f the visual fields (H ergueta et al. 1992). This
question is discussed in more detail in Section 3 3 .8 .2 .
In mammals, the N ew ton-M iiller-G udden law applies
only to the retinogeniculate pathway. Retinal projections to
the hypothalamus are n o t topographically organized. They
seem to be concerned with synchronization o f m etabolic
activity with the day-night and seasonal cycles. The prim i­
tive condition o f t h e rednohypothalam ic pathway in n on ­
mammalian vertebrates is one o f equal ipsi-and contralateral
inputs. This condition is also present in primitive mammals,
such as anteaters, sloths, and bats. O th er nonprim ate spe­
O p tic a l in v e rs io n
cies, such as the cat and tree shrew, have a predom inance o f
contralateral inputs to the hypothalamus. Primates have a
predom inance o f ipsilateral inputs (M agnin e ta l. 1989).
The boundary in the retina between decussating and
D e c u s s a tio n
nondecussating ganglion cells is known as the nasotem poral
division. In primates, it falls approximately along the
m idvertical meridian o f the retina (Fukuda et al. 1989).
C o h e re n t im a g e
In nonprim ate mammals, the position of the nasotem ­
В poral boundary varies according to the type o f ganglion
cell. Som e types o f cell remain fully decussated, whether
they arise in the nasal or in the tem poral retina (Lcventhal
et al. 1988). In the rat, uncrossed axons arise from a periph­
eral region in each temporal hemifield. These regions
у serve the 40° binocular field straight ahead o f the animal.
У
у However, even in these regions, m ost ganglion cells p roject
O p tic a l in v e rs io n
contralateraliy (C ow ev and Franzini 1979; Cow ey and
Perry 1 9 7 9 ). Som e axons bifurcate and p roject to both
hemispheres.
H e m id e c u s s a tio n
In birds such as pigeons, hemidecussation occurs beyond
the thalamus (C hap ter 3 3 ). The nasotem poral division is
discussed in more detail in Section 5.3.4.
C o h e r e n t a n d
O n e im portant function o f hem idecussation is to bring
s u p e r im p o s e d
im a g e s
inputs from corresponding regions in each retina to the
same location in the brain, as illustrated in Figure 5 .1 2 C .
This allows the visual system to com pare inputs from
Ftgurr 5- J *• Ушла!pathw ays. (A ) U n d ccu ssatcd pathways form а roughly corresponding regions o f the two retinas with a
d isjoin ted m ap. ( B ) Full d ccussarion form s a co n rin u o u s map.
m inim um length o f connections. This process provides the
( С ) I lem idecussacion fo rm s superim posed im ages in fron tal-cycd
an im als. (A f i« R ^ « n « » « i у С ф ! 1 9 1 1) basis for detecting binocular disparities and hence for bin­
ocular stereoscopic vision. The other function o f hem ide­
cussation is in the control o f binocular eye movements.
image, the left h a lf o f the visual field (left hem ifield) is rep­ W hen the gaze moves over the visual scene, the eyes o f ani­
resented in the right cerebral hemisphere, and the right mals with stereoscopic vision must move together to ensure
hemifield is represented in the left hemisphere. that light from rhe same points in the visual scene projects
In m ost, but not all mammals, the optic nerves hem idc- to corresponding points in the tw o retinas.
cussate. W h en they do hemidecussate, the ratio o f uncrossed Binocular inputs are not essential for coordinated
to crossed fibers is proportional to the size o f the binocular version eye movements, since the eyes move through equal
angles when one eye is closed (Section 10.1.3). Even ver-
gence eye m ovements, which converge the visual axes on a
selected o b ject at a particular distance, occur when one
eye is closed. However, both version and vergence eye
movements arc m ore precise when both eyes arc open
(S ectio n 10.5).
Stereoscopic vision is well developed in mammals with
frontal eyes, such as cats and primates. In these animals, visual
inputs trom corresponding regions in the tw o eyes converge
on binocular cells in rhe visual cortex, which are tuned to
binocular disparity (see C hapter 11). There are also some
disparity-tuned binocular cells in some mammals with later­
ally placed eyes and small binocular fields, such as rabbits,
sheep, and goats. Som e nonmammalian species, such as cer­
tain insects, amphibians, and birds, have frontal vision and
perhaps some binocular depth perception (C hapter 33 ).
The binocular field and the associated mechanism ot
corresponding points are n o t necessary for the perception
o f a unified visual field. A nim als with a large binocular field
suffer diplopia when the m echanism s responsible for co n ­
junctive and disjunctive eye m ovements are damaged, as in
strabismus. A nim als with laterally placed eyes have only a
small binocular field, and are therefore less affected by stra­
bismus. They no dou bt experience a unified panoramic
visual field, which may extend 360°. Birds with strongly lat­
eral eyes have a region o f high acuity in each eye. W hen
they inspect an object they can use one or the other eye.
They presumably have a m echanism that allows them to
attend to detailed inform ation arising from one eye or the
other (Voss and Bischof 2 0 0 3 ).
W e experience a unified visual field when the nasal h alf
o f each ey es visual field is occluded. A simple way to dem ­
onstrate this is to hold up against the nose an occluder just
wide enough to make the nasal lim it o f vision for onc-
eve coincide w ith the nasal lim it for the other eye. Three
fingers are about the correct width. The visual field seen
with such an occluder looks com plete, although it is com ­
posed of only abutting monocular temporal hemifields. The
inputs from the two hemifields are processed in opposite
cerebral hemispheres. W e can attend to any location in the
com bined field.
Section 5.5 .4 provides m ore details about the visual
pathways.
5 .3 .4 P A R T IT IO N IN G O F H E M IR E T IN A S
In the higher mammals, inputs from the nasal hemiretinas
decussate in the chiasm and those from the temporal
hem iretinas remain undecussated. For objects to the left of
both visual axes (Figure 5 .1 3 ) both images project to the
right visual cortex. For objects to the right o f both visual
axes both images project to the left visual cortex. Images are
said to have uncrossed disparity when the o b ject is beyond
the horopter and crossed disparity when they are nearer
than the horopter, or locus o f single vision (S ectio n 14.2).
Disparate images to
opposite hemispheres
I
All im ages to
\uncrossed imaaes
7 All im ages to
Figwc у 13. D ivisions o f / b e visti<ilfield. Im ages in b o th eyes from the light
b in o cu lar regions p ro je c t to o n ly the left or to on ly the right cerebral
hem isphere. Im ages from the dark b in o cu lar region s p ro ject to opp osite
hem ispheres. R eg io n s nearer than the h o ro p te r produce crossed im ages.
R eg ion s beyond the h oro p ter produce uncrossed images.
Consider an o b ject lying between the visual axes. The
images o f an object beyond the fixation point fall on the
nasal halves o f each retina and those o f an o b je ct nearer
than the fixation point fall on the tem poral halves.
In both cases, the images project to opposite cerebral
hemispheres. If the nasal and temporal inputs are perfectly
partitioned in the chiasm , no binocular cells in the visual
cortex would receive direct inputs from these disparate
images, and stereopsis based on direct inputs would be
impossible for such objects. In fact, stereoscopic acuity is
particularly good for objects on the m idsagittal plane near
the fixation point. Therefore, there must be cortical cells
serving the m idline region that have receptive fields in
either the two nasal hem iretinas or the two temporal
hemiretinas.
Evidence for this convergence o t inputs has been p ro ­
vided from the cat. A strip o f cortex at the boundary
betw een areas 17 and 18 o t each hemisphere contains
binocular cells with receptive fields that overlap in the
vertical midline o t the visual field (Ston e 1966; Leicester
1 9 6 8 ; Blakem ore 1969). C o rtical cells serving the midline
region near the foveas have receptive fields with centers up
to 3° on opposite sides o f the m idvertical meridians o f the
tw o eyes. C ells serving more eccentric regions above and
below the retinal equator have receptive field centers that
extend up to 10° into opposite hemifields (Payne 1990)
(P ortrait Figure 5 .1 4 ). These types o f cell in the cat are
driven by Y cells, are broadly tuned tor orientation, and are
strongly dom inated by the contralateral eye (D iao et al.
1 9 9 0 ).

F>£urc5.i4< B ertram Payne, B o m in tg v p t in 1 9 5 3 . H e ob tain ed л B .S c. in
1 9 7 4 and a P h .D . in 1 9 7 7 in z o o lo g y Irom the U n iv ersity o f D u rh am ,
England. H e co n d u ctcd p o std o cto ra l w ork a t the M ed ical C o lleg e o^
Pennsylvania. In 1 9 8 4 lie m oved to B o sto n U niversity S c h o o l o f
M ed icin e, w here he becam e professor in the D e p a rtm e n t o f A n atom y
and N cu rob io logy . H e d ied in 2 0 0 4 .
Two m echanism s could underlie bilateral projection
to cclls in rhe m idline region. The firsc is im perfect parti­
tioning ot inputs at the chiasm . The second involves
intcrhcm ispheric con nection s projected through the corpus
callosum.
Linksz (1 9 5 2 ) suggested that the nasal and temporal
hem iretinas are not perfectly partitioned. Im perfect
partitioning could be due to the following three factors.
1. Large receptivefields G anglion cells with large receptive
fields in the m idline region receive inputs from
receptors in both halves o t the retina. Kirk ec al. ( 1976a,
1976b) recorded from ganglion cell axons that crossed
in the chiasm in cats. They found that, although the
receptive fields o f X cells did not encroach m ore than
0.5° across che retinal m idline, those of Y cells and
slowly conducting W cells encroached 15° or more over
che m idline.
2. Incomplete segregation In cats and primates, axons from
the m idline region o f the retina are incompletely
segregated in the chiasm . Thus, in a region extending
about 1 to 2° on either side o f chc vertical retinal
m eridian some ganglion cells in the cat project to the
ipsilatcral I.G N and som e to the contralateral I.G N
(Sto n e 19 6 6 ; N ik a ra et al. 1 9 6 8 ; Sanderson and
Sherm an 1971; C ooper and Pettigrew 1979; I.cvick
et al. 1 9 8 1 ). From each L G N these incompletely
segregated inputs project to the border region between
cortical areas 17 and 18 in cats or betw een areas V I and
V 2 in primates. This cortical region is called the
tran sitio n zone. The transition zone in cach
hemisphere receives inputs from the contralateral
temporal retina and from che ipsilatcral nasal recina
intermixed with inpucs chac are segregated at the
chiasm . The transition zone o f the cat is about
1.5 mm wide.
W h ile few if any X cells in the nasal hem iretina o f the
cat project ipsilatcrally, 5% o f Y cclls and 60 % o f W cclls do
so (Stone and Fukuda 1974). W cells have large receptive
fields and project mainly to subcortical nuclei such as the
medial interlam inar nucleus and superior colliculus. This
suggests that W cclls arc involved more with the control o f
vergence than with stereopsis. However, Pettigrew and
D reher (1 9 8 7 ) found cells in cortical area 19 o f the cat,
which received inputs from W -type ganglion cells, and were
tuned to zero disparity or to uncrossed disparities.
After sectioning one optic tract o f the rhesus monkey,
Nissl staining o f the retina revealed that some ganglion cells
survived in both ipsilatcral hem iretinas (Sto n e et al. 1973).
These surviving ganglion cells m ust therefore have projected
to the contralateral optic tract. Retrograde labeling o f gan­
glion cells ot the macaque monkey with horseradish-perox-
idasc revealed a few ipsilaterally projecting cells in the nasal
retinas and a few contralaterally projecting cells in the
tem poral retinas. Both types o f cell were w ithin a P-w idc
vertical strip around the midvertical meridian, which
expanded to 3° in the pcrifoveal region (B u nt and M incklcr
1977).
Fukuda c t al. (1 9 8 9 ) obtained similar results in chc
Japanese macaque using retrograde labeling with peroxidase
and fluorescent dyes and physiological recording. There was
a marked asymmetry in the perifoveal region. Ipsilaterally
projecting cclls bounded the nasal fovea, bu t there were
only a few contralaterally projectin g cells on the tem poral
edge o f the fovea.
Cow ey and Perry (1 9 8 0 ) found no evidence o f nasotenv
poral overlap in the superior colliculus o f the rhesus
monkey.
3. Bifurcating ganglion cells R am on у C ajal (1 9 1 1 )
observed, in several mammalian species, bifurcating
axons in the optic chiasm that appeared to send
branches to opposite hemispheres. However, these
axons may not have originated in the retina.
Cunningham and Freeman (1 9 7 7 ) concluded that m ost
cclls in the far tem poral retina o f rats send axons to
both optic tracts. Cowey and Perry (1 9 7 9 ) detected
uncrossed axons by injecting horseradish peroxidase
into one L G N o f rats. They concluded many axons
arising in the tem poral retinas bifurcate and send
branches to both hemispheres.
However, Jeffery et al. (1 9 8 1 ) pointed out that many
axons in the optic tract arise from cells in the cortex.
They injected ditferenc retrograde tracers in the two lateral
geniculate nuclei o f t h e rat. These tracers revealed only a
few ganglion cells in the tem poral retina that sent axons to
both geniculate nuclei and hence to both cortical hem i­
spheres. In cats, also, the axons o f a few ganglion cells in
the temporal retina bifurcate and project to both cerebral
hemispheres (Illing 1 980).
A lthough the ganglion cells that give rise to bifurcating
axons are in the parts o i the retina that overlap in the visual
field, they seem to be too sparse to play a role in stereopsis.
In any case, it is difficult to see what role they could play.
Bilateral projection from the foveal region could explain
foveal sparing, in which vision is preserved around the
fovea following damage to one visual pathway. However,
eccentric fixation may create a false impression o f foveal
sparing (W illiam s and Gassel 1962). Also, foveal sparing
does n o t always occu r; som etim es there is foveal splitting,
in which the scotom a partitions the fovea.
The results o f a study by Leventhal et al. (1 9 8 8 ) may
solve this problem. Horscradislvperoxida.se labeling in the
macaque revealed cells in the nasal retina that projected
ipsilateraliy but no cells on the tem poral side that projected
contralaterally. From this, it follows that damage to one-
visual pathway should produce foveal sparing in the co n ­
tralateral eye and foveal splitting in the ipsilateral eye. They
cited clinical cases that conform ed to this prediction.
5.3.5 CORPUS CALLOSUM
The corpus callosum carries signals from one cerebral hem i­
sphere to the other. In each hem isphere, transcallosal fibers
originate in a recip ien t zone, and connections trom the
other hem isphere term inate in a p ro je ctio n zo n e. In each
hemisphere the two zones are coextensive and form the
callo sal zon e (Van Essen et al. 1 9 8 2 ). In chc primary visual
cortex the callosal zone is approximately coextensive with
che transition zone— che zone that receives incompletely
segregated inputs from the L G N . Thus, each callosal zone
spans the 17/18 border in cats or the V I/ V 2 border in
monkeys and receives inputs from near the vertical retinal
meridians. In both cats and monkeys, the boundary region
is well served by interhcm isphcric connections (C houdhury
c t al. 1 9 6 5 ; Hubei and W iesel 19 6 7 ; Harvey 1980).
In the cat, callosal connections have been traced with
anterograde and retrograde staining agents. A t the level o f
the fovea the callosal zone is about 1.5 mm wide, which rep­
resents an area o f visual space extending about 2" on either
side o f the m idline. T h e region broadens out symmetrically
above and below che fovea to reach a width o t about 20'J at
an eccentricity o f 30° (Payne and Siwek 1 9 9 1 ). The rate at
which the width o f the callosal region increases roughly
corresponds to the race ac w hich che size o f the receptive
fields o f cortical cells increases. This means that, at each
eccentricity, the callosal region contains approximately che
same num ber ot cortical cells (Payne 1991).
C ells in areas 17 and 18 o f the cat cerebral cortex that
receive callosal con nection s occur in periodic stripes. The
stripes becom e more evident further than 2 mm from the
17/18 border. They correspond to stripes that stain for
cytochrom e oxidase (Boyd and M atsubara 1994).
In the monkey, 80% o f cells with transcallosal co n n ec­
tions occur near the V 1/V 2 border and arc from the foveal
area. The o ther transcallosal cells are from retinal regions
above and below the fovea and extend 7 mm into V 2 trom
the V I /V2 border in finger-like bands. In V I , the terminals
ot these neurons are confined to cortical lavers * 2, 3, 4 B ,
and 5. In V 2 , they occur in all layers (Kennedy et al. 1986).
Theoretically there are three principal ways in which
callosal fibers can co n n ect cells in the tw o hemispheres.
1. Transmidline connections C o n n ectio n s o f this type link
cortical cells in the two hemispheres that receive inputs
from locations in the two eyes on opposite sides o fth e
vertical m idline. The linkages occur between cortical
cells that arc equal distances on either side o fth e
V 1/V 2 border. These con nections are said to form a
m irror-sy m m etric p attern , as illustrated in Figure 5.15.
('e lls linked in this way are therefore able to process
binocular disparities that span the m idline. Fine
m idline disparities could also be coded by the narrow
zone o f overlapping direct inputs from the two visual
hemifields. Bu t, we will see that callosal con nections in
V 2 and o ther extrastriate areas extend well beyond the
m idline and can therefore code large disparities that
cannot be coded by direct visual inputs.
2. Corresponding connections C o n n ection s o f this type link
cortical cells in the tw o hemispheres th at receive inputs
from neighboring locations on the same side o f the
m idline in the two retinas. They form a n o n m irro r-
sym m etric p attern , as illustrated in Figure 5.16. These
connections could code disparity between stimuli that
arise from one h alf o f visual space. However, these
disparities are already coded by direct inputs from the
tw o eyes along pathways that segregate at the chiasm.
If these callosal con nection s exist, it is not clear what
function they serve.
3. Monocular connections C o n n ection s o f this type link a
cell with an input from one eye with a cell in the
opposite hemisphere with an input from the same
location in the same eye, as illustrated in Figure 5.17.
These connections do not code binocular disparity
because they link inputs from locations in one eye. Like
corresponding con nection s, they form a n o n m irro r-
sy m m ctric p attern . They could help to create a
seamless impression o f the visual scene by linking cells
in each recina chac respond to the same stimulus.
Lewis and Olavarria (1 9 9 5 ) found different patterns o f
callosal connections in different regions o f the callosum o f

A rea 17 A rea 17
4 3 1 -2 -3 -4
C o rp us callosum
Figure5.IS- T ransm idlinecallosalcon nections. Л rep resentation o l callosal
co n n cccio n s chac link co rtica l cclls rccciv in g inputs from op p osite sides
o f the m id lin c in the tw o eyes. In this exam ple, cells in the tran sitio nal
zones innervated by the crossed pathways from che tem poral
h em iretin as arc linked . A lso, cells in V I innervated by the crosscd
pathw ays from the nasal h em iretin as arc linked. T h e linkages form a
m irro r-sy m m etric p attern ab ou t chc m id line.
the rat. M edial and lateral callosal regions form ed trans-
m idline connections conform ing to the mirror-symmetric
pattern. These con nection s could code disparities spanning
the m idline. The lateral callosal region formed m onocular
con nection s betw een cortical cells serving the same region
in one eye. These conform ed to the nonsym m ctric pattern.
We will see in Section 6 .4 .6 d that these patterns develop in
different ways.
/ sphere. Similarly, a cell that codes retinal position - 1 in
Olavarria (1 9 9 6 ) used fluorescent dyes со trace cal­
losal linkages in the cat. They tound many m onocular
M idline
C o rp us callosum
s. i*. C orresponding callosal connections C allo sal co n n e ctio n s th at link
co rtica l cells rccciv in g inputs from the sam e lo ca tio n s in the tw o eyes. In
this exam ple, cclls in the tran sitio n zon es innervated by crossed
pathways from the tem p oral h em iretin as arc linked to cclls in V l
innervated by crosscd pathways from the nasal hem iretinas. The
linkages form a n on sym m ctric p attern a b o u t the m idline.
connections betw een cells that receive inputs from the same
location in the same eye. For example, in Figure 5 .1 7 , a cell
in area 17 that was 3 mm away *
from the 17/18 border was
linked to a cell in che transition zone o f the other hem i­
sphere. A ccll that codes retinal position 1 in area 17 o f the
left hemisphere connects with a cell that codes the same
retinal location in chc transitional zone o f the right hem i­
area 17 o f the right hemisphere connects with a ccll that
codes the same position in the transitional zone o f the left
 M idline
D ecussated
A re a 17 Sr.- tem po ra l tra cts A rea 17
Transition
zones
1в A rea 18
4 3 2 1^0 - 1 0 - 1 - 2 - 3 - 4 4 3 2 Л 0 ^ 0 ^- 1 -2 3 4
C o rp us callosum
Figure5-17. M on ocu larcallosalcon n ection s. C allo sal c o n n e ctio n s th at link
co rtic a l cclls receivin g inputs fro m th e sam e lo catio n in on e eve. In this
exam ple all the inputs ari.se in the tem p o ral retinal hcm ifields. 'Ih c
c o n n e c tio n s form a n on sym m etric p attern a b o u t the m id line.
hemisphere. In each case, a cell outside rhe transitional zone
con nects with a cell inside the transitional zone and both
cells receive inputs from the same location in the same eye.
M onocular callosal con nection s in the cat conform to
ocular dom inance colum ns in a predictable way. Olavarria
(2 0 0 1 ) found that m onocular callosal connection s form
stripes that m atch ocular dom inance stripes. Callosal co n ­
nections w ithin the transition zone correlated with colum ns
dom inated hy rhe contralateral eye. But callosal co n n ec­
tions in area 17 in the opposite hemisphere correlated with
colum ns dom inated by the ipsilatcral eye. The same rela­
tionships were evident in strabism ic cats. Figure 5 .1 7 shows
th at this pattern is what one would predict from m onocular
callosal connections. The inputs to the transition zone in
one hemisphere are from the contralateral eye, while those
to area 17 in the other hemisphere are from the ipsilatcral
eye. Figures 5.15 and 5 .1 6 show that for both transmidline
and corresponding callosal connections, the inputs to both
hemispheres are from the contralateral eye.
'I here seems to be no evidence about w hether cats
have m irror-sym m etric callosal connection s or w hether the
pattern o f con nection s varies in different parts o f the
callosum.
Visual areas V 2 , V 3 , V 4 , VP, M S T , and the inferotem -
poral cortex in the m onkey also receive transcallosal inputs
(Van Essen and Zcki 1 9 7 8 ; Maunsell and Van Essen 1987).
Areas with large receptive fields, such as M S T and the infer-
otcm poral cortex, show the m ost extensive inputs from the
ipsilateral visual field. Callosal connections are m ost dense
near the representation o f the vertical meridian. This helps
investigators to identify boundaries o f those areas (Van
Essen et al. 1982).
H istological procedures revealed that the callosal zone
extends about halfway across area V 2 o f the monkey. These
connections link inputs from locations in the tw o eyes on
opposite sides o f the vertical m idline. They therefore co n ­
form to the m irror-sym m etric pattern (Abel ct al. 2 0 0 0 ).
They could serve the detection o f coarse disparities p ro ­
duced by o b jects near the m idline. There are no reports o f
nonsym m etric callosal con nections in the monkcv.
Single-cell recordings in V 4 o f the alert monkey revealed
that purely inhibitory transcallosal con nections extend sev­
eral degrees beyond the vertical m idline. Ir has been sug­
gested that these widespread inhibitory influences are
concerned with color constancy and figure-ground segrega­
tion rather than with stereopsis (D esim one e t al. 1993).
A natom ical studies on human brains revealed transcal­
losal terminals along the boundary between areas V I and
V 2 and in surrounding areas (C larke and M iklossy 1990).
Use of fM R I in humans showed that transcallosal regions
are particularly extensive in areas such as M T and the lateral
occipital area that have large receptive fields (T ootell et al.
1998).
It seems that inform ation carried by the callosal path­
way is confined to low spatial and low tem poral frequencies
and high contrasts (Berardi and Fiorentini 1987; Berardi
c t al. 1987).
Callosal projections o t visual inputs have been revealed
psychophysically in humans. Subjects used one hand to
press one o f two keys to indicate whether a m onocular
target was to the left or to the right o f fixation. The proce­
dure was repeated with the other hand. Reaction time was
25 ms shorter when the visual target was projected to the
same h a lf o f the brain as that controlling the manual
response, even when the target was only 15 arcm in away
from the m idline (H arvey 1978). This result argues against
the ideaofoverlap o f visual projection in the midline region.
It is what one would expect if chc longer reaction cimc
involves a longer route through chc callosum . Lines and
M ilner (1 9 8 3 ) measured simple manual reaction tim es and
obtained an advantage o f about 2 .4 ms when che scimulus
was in che same h a lf o f the brain as chac controlling the
hand. The simple reaction tim e is a purer measure ol inter-
hem ispheric conduccion cime chan che choice reaction time
used by Harvey.
The corpus callosum could serve che follow ing func­
tions:
1. C reation o f a unified field o f view.
2. Supplem enting binocular inputs to cortical cells serving
che midline region. Saint-A m our ec al. (2 0 0 4 ) found
chac cwo acallosal subjects could noc decect plaid
m otion when cwo superimposed d ichoptic gratings
were presenced in che m idline region. Normal subjeccs
reporced plaid m otion wich these stim uli, and all
subjects reported plaid m otion in stimuli away from the
m idline region.
3. Providing for che detection o f binocular disparity across
the m idlinc. This topic is discussed in Section 11.9.
4 . Providing for the transfer o t visual-m otor skills from a
trained hand to che untrained hand or between
hemifields. People lacking a corpus callosum or those
w ho have had a calloseccom y• show deficits in all tasks
that involve transfer o f inform ation between
hemispheres (Gazzaniga and LeD oux 1978; Lassone
e t al. 1 995).
The functions o f the corpus callosum have been
reviewed by Lcporc et al. (1 9 8 6 ) and Kennedy e t al. (1 9 9 1 ).
Tlie developm ent o f the corpus callosum is discussed in
Section 6 .4 .6d.
5.4 N E U R O P H Y S I O L O G I С A L
PROCEDURES
This section provides only a b rief review o f procedures used
to study the structure and functions o f the nervous system.
5. 4. 1 HISTOLOGICAL PROCEDURES
5 .4 .1 a S ta in in g P ro ced u res
Nerve cells can be stained in a slice o f neural tissue and
viewed in a co n fo ca l m icroscope (see S ection 2 4 .2 .3 ). In che
N issl m eth o d , aniline dyes arc used to stain ribosomal
R N A to reveal the shape o f the cell bodies (somaca) o f neu­
rons. In the G o lg i m eth o d , neural tissue is stained with
silver sales. Ram on у C ajal used chis m ethod to trace neural
structures and con nection s in the recina. The mcchod
is difficult to apply, and the results are unpredictable.
C ertain types o f cell, such as amacrine starburst cclls in the
retina, do not take up the silver salts. Furtherm ore, only
very few o f the stainable cells take up the stain in a given
application. This is an advantage because it allows individ­
ual cells to be isolated from overlapping cells.
In the N auta m eth o d , cells or axons in a structure such
as the I.G N are destroyed or severed in the living animal.
Som e tim e later, staining reveals degeneration o f cells or
axons in corresponding areas o f the visual corcex (H ubei
and W iesel 1 9 6 9 ). This staining procedure is som etim es
difficult со apply.
In more rcccnc m ethods, particles, proteins, or dyes are
injected into preserved or living cells in a cell culture
through a visually guided fine pipetce. In anocher mcchod,
known as p h o to fillin g , all the cells in a cell culture absorb
chem ical agents. Particular cells are then irradiated wich a
fine laser beam . This oxidizes one o f che chem ical agents
into a fluorescent form , which diffuses throughout the
selected cells. The 3-D structure o t che selected cells can
be recorded by a sensitive cam era attached to a scanning
microscope. Scanning m icroscopes are described in
Section 2 4 .2 .3 .
C h em ical agents o r flu o rescen t dyes can be injected
into living neural tissue, where they are absorbed by neu­
rons and tran sp o sed in eicher che anterograde direction to
nerve terminals o r in the retrograde direction to the ccll
soma. The agent can be visualized in the dead anim al by
staining, by fluorescence, or by radioactivity. C ells that pro­
duce branching axons can be detected by a double labeling
technique. Discincc dyes are injected in regions where che
suspected branching axons term inate. The originating cells
are those that acquire both dyes by retrograde cransporc
(van der K o o y e ta l. 1980).
In one procedure, the enzyme horseradish peroxidase is
transported retrogradely from a site o f injection in the living
animal to ccll bodies, where it is detected histochcm ically
after the anim al has been killed. This type o f procedure
reveals the m ultiple sources ot afferent fibers entering a
particular neural structure, such as a region o f the cortex.
Neurons contain in trin sic ch em ical m arkers, such
as a protein that is specific to a given type o f ccll. Specific
proteins can be recognized because they bind to specific
com m ercially available antibodies marked with fluorescent
dyes. This procedure is known as im m u n oh isto ch em istry .
Iilood scrum contains many (polyclonal) antibodies.
Single (m on oclon al) antibodies that bind to specific pro­
teins arc obtained from purified ccll lines derived from
m ice cancers.
In the procedure known as in situ h ybrid ization a
radioactively labeled synthetic sequence o f nucleic acids,
known as a p ro be, is created. W hen applied to a section o f
brain tissue, the probe binds ro a specific m RN A m olecule
responsible tor assembling a given protein in the ribosomes
o f cells. After unbound probe m olecules arc washed away,
neurons containing the labeled probe are revealed.
 The shape and identity o f a cell is evident under the
m icroscope it chem ically marked proteins are distributed
throughout the cell. However, it may be difficult to isolate
single cells from am ong cells o f the same type. I f the protein
is localized in the synapse, the cells containing it will be dif­
ficult to identify unless the synapses occur in well-defined
layers, such as the inner plexiform layer o f the retina.
D etection o f an intrinsic protein that is specific to a given
type o f cell can be com bined with a staining procedure that
reveals the whole cell. In this way one can identify the ncu-
rotransm itters or synaptic receptor proteins used by specific
types o f cell.
These and other procedures for observing the m icro­
structure o f cortical circuits have been reviewed by Sm ith
(2 0 0 8 ).
There are various procedures for labeling cells that arc
sensitive to particular stim uli. In au torad iograp h y a mix­
ture o f tritiated proline and tritiated fructose o r dcoxyglu-
cose labeled with carbon 14 is injected into the eye o t a
living anim al. The radioactive tracer gradually travels up the
optic nerve and becom es concentrated in metabolically
active cells in layer 4 o f the visual cortex. The eye o f the
living anim al is then exposed to particular stim uli for an
hour or more, which causes the radioactively labeled sugar
to be selectively
ф
absorbed bv
i
neurons in the visual cortex
that respond to that stimulus. The resulting patterns o f
radioactivity in thin sections o f the visual cortex arc
recorded on film to produce autoradiographs.
This process reveals all cells in a given slice o f visual
cortex that respond to a particular stimulus feature, tor
example vertical lines. The separate slices o f an autoradio­
graph can be com bined by com puter reconstruction into a
com plete 3-1) pattern o f cells responding to a given stim u­
lus feature, as illustrated in Figure 5.44.
5 .4 .1 b M icroscopy
In a conventional m icroscope, light trom out-of-focus parts
o f a specim en dilutes the focused image, although com puter
algorithm s can help to remove out-of-focus images.
Separation between image planes can be improved more
effectively by using the co n fo ca l scan n in g m icrosco p e.
A p o in to f light is focused in an aperture in the o b ject plane.
The illum inated point or fluorescence em itted from the
specimen is imaged in a confocal aperture in front o fth e
detector, which may be a video cam era or a photom ultiplier
( Boyde et al. 1990). Light trom planes o ther than the plane
o f focus does n o t enter the image aperture. I his is known as
near-field m icroscopy as opposed to conventional far-ficld
microscopy in w hich the lens is som e distance from the
specim en. The focused beam must scan the specim en to
produce a full image. Resolution is improved by using a
laser beam rather than light trom a conventional light
source. M ore details about confocal m icroscopes are pro­
vided in Section 2 4 .2 .3 . The confocal m icroscope allows
one to direct a recording electrode to particular cells in cell
cultures or in the living brain.
In the tw o -p h o to n scan n in g m icro sco p e fluorescent
dyes are excited when they absorb two photons o f near
infrared light alm ost simultaneously (D en k et al. 1 9 9 0 ; Tsai
et al. 2 0 0 2 ). Two photons com bine their energy to excite a
dye m olecule th at norm ally requires dangerous ultraviolet
light. The specimen is irradiated by a focused pulsed laser o f
about 100 fs ( 1 0 o l s) duration at a repetition rate o f 8 0
M H z. The long wavelength o f the laser does not damage
living tissue. A xial resolution is improved over that o f co n ­
ventional scanning m icroscopes because the probability o f
tw o-photon absorption decreases rapidly away from where
the laser is focused. Also, long-wavelength light penetrates
neural tissue to a depth o t about 1 mm, which is greater
than the penetration o f visible light. Photobleaching and
tissue damage is confined to the neighborhood o t the
focused laser beam . Also, the local excitation o f dye m ole­
cules allows the image to be detected w ithout the use o f a
confocal pinhole aperture.
The resolution o f any conventional m icroscope is lim ­
ited by the diffraction lim it, or N yquist lim it. The resolu­
tion lim it is about 2 0 0 nm laterally and 6 0 0 nm axially.
Recently, several procedures have extended resolution down
to about 45 nm in three dimensions.
The sim u lated em ission d ep letion m icrosco p e
( S T E D ) improves resolution by projecting an annular laser
beam (the S T E D beam ) around the prim ary laser beam.
The S T E D beam suppresses fluorescence round the diffrac­
tion pattern produced by the primary beam , leaving only
the fluorescence produced by the center o f rhe diffraction
pattern. This new m icroscope allows one to view activity-
driven changes in synapses and activity o f actin filam ents
w ithin dendrites at about 2 8 frames per second with a reso­
lution o f about 6 0 nm (Niigerl and Bonhoeffer (2 0 1 0 ). In
another procedure, fluorescent dyes attached to specific
cells or m olecules are repeatedly switched on and o f f by a
laser beam. Resolution is improved because only a random
subset o f probe m olecules is activated during each activa­
tion cycle. Also dves with different colors may be activated.
The images from several activation cycles are collated to
form a single high-resolution image. There are several ver­
sions o f this procedure, such as stochastic optical-recon-
struction m icroscopy (S T O R M ) and photoactivation
localization m icroscopy (P A L M ). Lateral resolution o f
25 nm has been achieved by these procedures. Images p ro ­
duced by focusing at different depths w ithin a specimen can
be com bined to create 3 -D images (H uang et al. 2 0 0 8 ).
These m ethods allow several proteins to be labelled and
localized in 3-D on the prcsynaptic and postsynaptic m em ­
branes o f synapses w ithin the brain (D ani e t al. 2 0 1 0 ).
Scanning a volume o f neural tissue with a single beam o f
light using a tw o-photon or confocal m icroscope takes
up to 1 s, which provides inadequate tem poral resolution
for recording action potentials. H olckam p et al. (2 0 0 8 )
overcame this problem by illum inating a tw o-dim ensional
sheet o f neural tissue with a collim ated beam that allows
the whole focal plane o f the m icroscope to be imaged at
the same time. The sheet o f illum ination is eoupled to the
m icroscope objective so that the tissue can be rapidly
scanned in depth. Photoblcaching o f the tissue is avoided
because illum ination falls on each layer o f tissue for only a
short tim e. The m ethod may be applied over a long period.
H olckam p e t al. called this procedure o b jectiv e-co u p led
p lan ar illu m in atio n m icroscopy.
Scanning neural tissue in depth by changing the m icro­
scope objective or by deflecting m irrors is too slow to cap­
ture events related to neural signals, which occur on the
order o f milliseconds. Reddy ct al. (2 0 0 8 ) have developed a
svstcm in which a laser beam is steered almost instanta-
neously to any location in a 3 -D space by two pairs o f iner­
tial-free acousto-optic deflectors. This new system will
allow one to simultaneously visualize events occurring in
3 -D dendritic structures.
The con stru ction o f 3 -D images o f neural activity that
change in real tim e is com putationally intensive. But new
hardware and software have reduced the cost o f com puter
systems. See Feng et al. (2 0 0 7 ) for a review o f these new
systems.
5.4.2 USE OF IN V I T R O T I S S U E SLICES
Slices ot brain tissue may be kept alive or grown in culture
dishes. T h e procedure was first used in rhe 1920s, bur the
in v itro study of neural activity had to wait until the devel­
opm ent o f m icroelectrodes in rhe 1950s. Slices o f neural
tissue retain synaptic con n ection s but lack normal inputs
and necessarily contain many damaged cells. Individual cells
are m ost easily observed in slices thinner than 2 5 0 jUm .
Thicker slices preserve synaptic structures. Slices o f neural
issue are usually kept alive for about 12 hours, but this can
be extended to days or weeks. Em bryonic nerve tissue may
be cultured, and its developm ent may be studied over a
period o f m onths. The cells may form synaptic connections
and show spontaneous electrical activity. Em bryonic cells
from d istin ct regions may be cocultured to reveal interac­
tions betw een them .
Particular types o f cell may be grown in isolation, which
allows one to study the effects o f introducing defined
factors. However, the effects o f one factor studied in isola­
tion may not predict the effects o f that same factor when
o ther factors arc present. Also cultured neurons o f a single
type can form synapses only with themselves (autapses).
Ultimately, m echanism s found in vitro should be investi­
gated in the intact nervous system, or in vivo.
5 .4 .2 a S ta in in g Living Cells
F lu o rescen t tra ce r dyes, such as lucine yellow, can be
injected into neurons in slices of living neural tissue.
Synaptic con n ection s betw een two cells can be identified by
injecting the cells with different fluorescent dyes that em it
light o f different wavelengths. Three-dim ensional images o f
cells can be constructed by use o fth e confocal microscope.
Brain slices can be kept alive for long periods, so the growth
o f axons, dendrites, and synapses may be observed (D ailey
1964). These and related m ethods used to elucidate the
cellular structure o f the retina are reviewed in Masland and
Raviola (2 0 0 0 ).
In im m unohistochem ical staining, a fluorescent an ti­
body binds to specific neurons or specific proteins in a cell
culture. The same tissue can be labeled with several fluores­
cent probes and then scanned with a confocal m icroscope
with laser beams o f several wavelengths.
In another procedure, a gene that expresses a marker
agent is introduced into the genom e o f a virus. The viruses
used for this purpose are com m on human viruses geneti­
cally modified to render them nontoxic. The virus is injected
into a selected region o f the nervous system or into a cell
culture, where it attaches to the cell mem branes o f neurons.
It becom es absorbed in to the cytoplasm and eventually into
the cell nucleus, where it expresses the marker agent (see
Davidson and Brcakeficld 2 0 0 3 ).
A com m only used marker agent introduced in this way
is a green flu orescent p ro te in (G F P ) derived lrom a jelly­
fish (C halfie et al. 1 9 9 4 ). Lines o f tran sg en ic m ice have
been developed that express G FP or spectral variants in spe­
cific types o f neuron throughout the nervous system (Feng
et al. 2 0 0 0 ). In an extension o f rhe transgenic procedure,
Livct et al. (2 0 0 7 ) used m ultiple fluorescent proteins to
label hundreds o f axons and synapses in distinct colors in a
local volume o f living neural tissue. They called this the
rainbow system .
The small size o f the G F P m olecule allows it to difluse
evenly throughout the cell, including the dendrites and
dendritic spines. It does not spread to the extracellular space
or to neighboring cells (L o et al. 1994). The protein is n on­
toxic and does n o t require added substrates. The fluorescent
cells may therefore be observed in slices o f living cortex or
in the living brain through a window in the skull. In this
way, it is possible to observe changes in dendrites and den­
dritic spines during synaptogenesis or during a learning
process.
The G FP protein may be fused with o ther proteins spe­
cific to subcellular com partm ents, including the ch rom o­
somes (R o b in et et al. 1996). This procedure has revealed
that chrom osom es have defined positions in the nucleus
and that they are in constant shuddering m otion, which
probably facilitates gene interactions and helps proteins to
find their binding sites in the genom e (M arshall 2 0 0 2 ).
5 .4 .2 b S y n a p tic A c tiv ity an d M o le c u la r In te r a c tio n s
N one o f rhe above procedures reveals synaptic activity
directly. In a procedure being developed for this purpose.
neuron cultures are infected with a virus con taining a fluo­
rescent protein (luciferase) coupled to a protein that binds
specifically to synaptic vesicles. D uring synaptic activity the
vesicles release the luciferase in to the extracellular medium,
which has been injected with luciferin. The com bination o f
luciferase and luciferin creates a burst ol fluorescence, which
is observed in a m icroscope. A bou t 2 4 synaptic vesicles
must be released to produce a visible response (M iesenbock
and R oth man 1 997).
It is now possible to visualize dynamic interactions
between protein molecules in a single cell using enzym e
frag m en t co m p lem en ta tio n assays (E G A s). An enzyme is
split into two parts, each o f which is fused with a protein.
W hen these proteins interact, the enzyme halves com bine
to form an active enzyme that causes fluorescence in a
substance injected into the cell (Sp otts e t al. 2 0 0 2 ).
Procedures used to study the developm ent ot the
nervous system arc reviewed in Section 6.2.
5 .4 .2 c E lectrical R e co rd in g in C ell C u ltu res
In cell cultures or thin brain slices a recording electrode can
be directed under the m icroscope to particular cells identi­
fied by a fluorescent dvc. In these in vitro preparations, the
long-range con n ection s o l the neurons are disrupted and it
is not possible to stim ulate the cells from a sense organ.
Recently, it has becom e possible to record from identified
cells in vivo (M argric et al. 2 0 0 3 ). Particular cells are labeled
with fluorescent dyes that are excited only when they absorb
two photons simultaneously, as described in Section
24 .2 .3 c. C clls up to л depth o f 0.5 mm can be identified and
recorded from . Axial resolution is improved over that ot
conventional scanning m icroscopes because the probability
o f tw o-photon absorption decreases rapidly away trom
where the laser is focused.
In the patch clam p p ro ced u re, a hollow electrode is
applied to the m em brane o f the cell. In the whole-cell pro­
cedure, the underlying m em brane is punctured. This pro­
vides m ore precise recording o f fast current changes than
does a fine penetrating electrode. Agents, such as enzymes,
may be injected into the cell and their effects on the cells
response or chem ical com position measured. In a second
procedure, a fold o f m em brane, which ideally contains one
synaptic pore, is sucked into the end o f the electrode.
A ncurotransm itter o r synthetic ligand is applied through
the electrode. This binds to receptors on the patch o f m em ­
brane and the resulting electrical activity is recorded. In
m icro io n o p h o re sis a neurotransm itter is applied through
a fine pipette to a postsynaptic mem brane, and the response
o f the neuron is measured by a m icroelectrode.
A ligand is any chem ical th at binds to a specific recep­
tor. Since all excitatory synapses in rhe brain respond ro rhe
ncurotransm itter glutam ate, this naturally occurring neu­
rotransm itter cannot be used to distinguish one type o f
synapse trom another. But synthetic ligands have been
discovered that bind specifically to one type o f synapse. We
will see in Section 5.5.2 that such synthetic ligands have
been used to distinguish different types o f excitatory and
inh ibitory synapses. Excitatory potentials generated by
sodium channels are inhibited by tctro d o to x in derived
from the Japanese pulfcr fish. O th er toxins derived from
frogs cause sodium channels to open. We will see that
these toxins have been used to investigate the role o f action
potentials in cortical plasticity.
5.4.3 M ETH O D S APPLIED TO THE
LIVING BRAIN
5 .4 .3 a O p tic a l Im aging
O p tical im aging involves recording activity-relayed changes
in the reflectance o t neural tissue. The m ethod was used
first with in vitro slices o f neural tissue by H ill and Keynes
/ 4
( 1 9 4 9 ). It is now used in the living brain (Frostig 2 0 0 2 ).
Changes in reflectance can be enhanced by infusing the
living neural tissue with a dye that changescolor in response
to neural activity.
V oltage-sensitive dyes applied to the cortical surface
bind with the m em branes o f neurons. Newer dyes have lim ­
ited toxicity. Changes in m em brane potential produced by
neural impulses cause changes in fluorescence. An electrical
stim ulus is adm inistered ro a given location or the animal is
exposed to specific stimuli. Photodiodes or a video recorder
are used ro d etect rhe changes in fluorescence over a region
ot the cortical surface (Blasdcl 1992a; O rbach and Van
Essen 1993). 'I he m ethod has a tem poral resolution o f 2 ms
and a spatial resolution o f 5 0 to 100 f l m (Grinvald and
Hildesheim 2 0 0 4 ). A single pixel in the recorded image
does not indicate the activity o f a single neuron bu t rather
the mean potential change mainly from the dendrites o f
several neurons. O n e must allow tor the tact that dendrites
in a given cortical area may arise from neurons in a neigh­
boring area. However, by observing the effects o t different
stim uli or o f the same stimulus at different strengths, the
spatial resolution o f the m ethod can be improved to about
5 0 fJ m . The method has been used to record the spread
o f cortical responses over the visual cortex and to study
cortical dynamics.
Y an get al. (2 0 0 7 ) used a voltage-sensitive dye to record
neuronal activity w ithin a 1 -c n r area o f V 1/ V 2 in alert
4
monkeys. Reponses to dashed lines sweeping radially
revealed the cortical mapping o f retinal meridians.
Responses to concentrically swept lines revealed the m ap­
ping o f retinal eccentricity over the same area. The mapping
had a precision o f about 0 .2 mm and was obtained over a
recording period o t only 4 minutes.
C alciu m -sen sitiv e dyes becom e fluorescent in response
to calcium ions released during synaptic transmission. The
dye can be loaded through m icroelectrodes into individual
neurons. Yuste and Katz (1 9 9 1 ) developed a m ethod for
loading calcium-sensitive dyes in to hundreds o f neurons in
slices o f living brain tissue. M ore recently, the dyes have
been loaded into the living brain (Stosiek et al. 2 0 0 3 ).
Stim ulus-specific regions o f neural activity in the visual
cortex may also be mapped by staining naturally occurring
chem icals associated with neural activity, • such as cv * to-
chrom e oxidase (T ig g cs c t al. 1 9 9 2 ), G A B A (H endry et al.
1 9 9 4 ), and protein kinase (H en d ry and Kennedy 1986).
It was m entioned in Section 5.4.2a that lines ot trans­
genic m ice express genetically encoded fluorescent proteins
in specific types o f neuron. Neural activity and m orpho­
logical changes in a specific area o f the brain can be viewed
by a 2-ph oton contocal scanning m icroscope (Section
5.4.1 b) through a window in the head o f such m ice. An area
can be viewed over a period ot weeks.
Neural activity also induces im m ed iate early genes to
express proteins required tor the growch or m odification o f
synapses. Im m unocytochem ical staining reveals the pres­
ence o f these activity-dependent factors in particular neu­
rons (Chaudhuri c t al. 1 9 9 5 ). O n e such gene, known as Arc,
expresses a protein in dendrites only when the neuron is
excited (Lyford et al. 1 995). This leaves a lasting trace in
the developing visual cortex that can be revealed in tissue
sections. Tli is m ethod has been used to observe the devel­
opm ent o f the visual cortex (Tagawa et al. 2 0 0 5 ).
Dves
* introduce deleterious side effects. Even w ithout
dves, active cortical areas reflect slightly less light than inac­
tive areas. These intrinsic changes in reflectivity on the sur­
face o f the cortex can be photographed. Illum inating the
surface o f the co rtex with light ot wavelengths between 6 0 0
and 6 3 0 nm reveals fairly rapid changcs in reflectivity due
to changes in hem oglobin. Wavelengths o f 5 5 0 or 8 5 0 nm
reveal the slower changes in blood volume ('I s o e t al. 1990;
Frostig 19 9 4 ; Pouratian and Toga 2 0 0 2 ). The method has
been used on the exposed cortical surface o f humans under­
going surgery (Pouratian et al. 2 0 0 3 ). However, even small
movements o f the brain, such as those caused by breathing
o r the pulse, degrade the record. The m ethod has low tem ­
poral resolution and reveals changes only in the surface o f
the cortex. However, new optical methods are being devel­
oped that reveal neural activity in deep neural tissue with
high tem poral resolution (See Frostig 2 0 0 2 ).
O ptical m ethods reveal only the average activity o f
many cells, with a resolution o f no more than 100//m. In an
exciting developm ent, O hki et al. (2 0 0 5 ) loaded a calcium -
sensitive dye in to the som ata o f thousands o f neurons in a
given region o f the visual cortex o f living rats and cats. All
the neurons that were excited bv/ a defined visual stimulus
becam e fluorescent. Fluorescent neurons in a region about
4 0 0 f.lm in diam eter were viewed simultaneously by tw o-
photon microscopy. All the active neurons to a depth o f
about 4 0 0 Цт could be observed by focusing the photon
beams to ditferent depths. However, this depth did not
extend as far as cortical layer 4 , where visual inputs arrive in
the cortex.
Tli is new method allows one to view the activity o f
thousands o t neurons in a region ot the brain at single-cell
resolution. O h ki e t al. could observe the distribution o f
cells tuned to ditferent orientations and directions ot
m otion with a precision o f 2 0 - 3 0 Цт , w hich is far higher
than that obtained by other m ethods. This method has
great potential. However, it does not have the temporal
resolution required to record action potentials. Also, for
some unknown reason, calcium-sensitive dyes are poorly
absorbed by cells in adult animals. Sonic dyes are taken up
by both neurons and glial cells. However, cell-specific dyes
have been developed. Also, transgenic mouse lines are avail­
able that express fluorescent protein in acell-specific manner
(Ikegaya et al. 2 0 0 5 ).
5 .4 .3 b E le c tro p h y s io lo g y
In single-cell electrophysiology a fine electrode is injected
into the brain through a hole in the skull. The electrode may
be a fine glass tube filled with an electrolyte, but the m ost
com m only used electrode is a tungsten filam ent coated with
an insulator. In extracellular recording, the tip o f the elec­
trode is placed near a neuron. It records m ainly the neural
spikes produced by the nearest cell but not pre- or postsyn­
aptic currents ot particular neurons. In intracellular record­
ing, an electrode with a tip o f less than 1 fAin in diam eter
penetrates rhe cell m em brane. It registers excitatory or
inhibitory synaptic potentials o r currents with respect to a
grounded reference electrode placed outside the cell.
The electrode is guided to particular regions o f the brain
with the help o f a brain atlas. However, which cell an elec­
trode contacts is partly a m atter ot chance, and it is not
always possible to be certain w hat type o f cell it is. W ith
m ultiple electrodes, responses may be obtained trom several
cclls in a given neighborhood. This procedure is usually car­
ried o u t on the anesthetized and paralyzed anim al, but it
can also be applied to an alert animal since, once applied,
electrodes cause no discom fort.
Single-cell recording has also been performed in sub-
cortical and cortical regions o f the human brain during
surgical procedures for conditions such as Parkinsons
disease and epilepsy (Engel et al. 2 0 0 5 ).
Traditionally, single-cell recordings have been used to
record changes in responses o f a cell as a stimulus, such as a
bar o f light, is moved over the cclls receptive field. This pro­
cedure typically reveals the distribution o f excitatory and
inhibitory zones w ithin the receptive field.
Using a single stimulus probe to plot the structure o f a
receptive field is a tim e-consum ing procedure. The reverse
co rre la tio n p roced u re is more efficient (D eA ngelis et al.
1993a). In this procedure a continuous series ot briefly
exposed bar-shaped stimuli is presented. The stimuli occur at
different positions w ithin the spatial confines ot the recep­
tive field and at ditferent tim es w ithin the tem poral epoch
over which the response o f the cell persists. The responses o f
the cell arc then cross-correlated backward in time
with the input to yield the spatiotem poral response profile
o f the cell. The method works only i f the cell behaves
linearly, and Can theref ore be applied only to simple cortical
cells.
In a developm ent o f this procedure called local sp ectral
reverse co rre la tio n a dynam ic dense noise pattern is pre­
sented to an area about three tim es larger than the receptive
field o f a cortical cell. Spike trains recorded from the cell are
correlated with the frequency spectra o f the noise pattern.
This reveals local variations in frequency tuning within the
receptive fields o f both simple anil com plex cortical cells,
and also effects due to surround suppression (N ishim oto
et al. 2 0 0 6 ).
Recording from single cells is tim e-consum ing, espe­
cially when one wishes to map responses o f cells over large
areas o f the cortex. H ubei and W iesel (1 9 7 7 ) remarked that
single-cell recording is “like trying to cut the back lawn with
a pair o f nail scissors.” The following electrophysiological
procedures allow one to record neural activity over large
areas, but they have lim ited spatial resolution.
5 .4 .3 c E le c tro e n c e p h a lo g ra p h y
In electroencephalography, electrodes are applied to the
scalp, and the pooled activity o f cells in the underlying
cortex is recorded as defined visual stimuli are presented to
the subject.
Because o f their high level o f interconnectivicy, cortical
neurons tend to fire in synchrony. Furtherm ore, subgroups
o f cells tend to fire at different frequencies. In addition to
these spontaneous firing patterns, groups o f cells tend to
respond together in characteristic ways in response to par­
ticular stim uli. The synchronous firing o f groups o f cells
generates fluctuating electrical fields that can be detected
either at the surface of the brain o r on the scalp.
Electrical fields generated by the visual co rtcx are known
as visual evoked p o ten tia ls {VF.Ps). Pyramidal cells are the
m ost likely source o f VF.Ps. A pyramidal cell runs at right
angles to the cortical surface and forms an electrical dipole
when it generates nerve impulses. A single electrode on the
scalp is affected by the activity o f thousands o f pyramidal
cells, since the meninges, skull, and scalp diffuse and aver­
age the potentials arising from the underlying area o f tissue.
Records can be taken onlv from cortical tissue that runs
parallel to the surface o f the brain and not from tissue
w ithin fissures.
Prom inent types o f synchronous activity arising from
the visualcortex in clu d caip h aw av csatafrcq u cn cy between
8 and 13 H z,evid ent in awake subjects, d elta waves between
0.5 to 4 Hz that arise in the sleeping subject, and b e ta waves
between 14 Hz and 3 0 Hz that arise when rhe su bject is
engaged in an attentive task. G am m a waves at even higher
frequencies are detected in single cells or small groups o f
cells but n o t at the scalp.
In a typical experim ent, rhe experimenter relates the
location, magnitude, and form o f VEPs to parameters o f the
stimulus. A well-defined repetitive visual stimulus is applied
and the response is then filtered and averaged over many
cycles o f stimulus repetition. Signal averaging emphasizes
com ponents in the V E P that are time-locked to the repeat­
ing stimulus. It attenuates com ponents due to extraneous
stimuli and intrinsic noise, w hich, being unrelated to the
stimulus, average out over several stimulus repetitions.
Standard signal-averaging procedures overlook episodic
noise such as bursts and oscillations. These events can be
characterized by phase-locked sp ectral analysis, which
measures the difference between responses to each cycle ot a
periodic stimulus and the response average. Standard signal-
averaging procedures also tail to register variations in
response to particular cycles o f a periodic stimulus. Such epi­
sodic activity generated by the stimulus, but n o t time-locked
to it, is revealed by standard power sp ectru m analysis, as
peaks in the autocorrelation function (S c h iffe t al. 1999).
In another procedure, responses o f the same region to
distinct stimuli are recorded or recordings are made o fth e
responses o f distinct cortical regions to the same stimulus.
The degree ot coherence (shared power) betw een these
recordings as a function o f stimulus frequency is used to
derive a coherence function. A coherence function is the
frequency dom ain analog o fth e (squared) cross-correlation
fu n ction , and its value varies betw een 0 and 1. In this way,
one can assess the exten t to which distinct stim uli evoke the
same response and distinct cortical regions respond to the
same stimulus.
A com m only used procedure is to identify prom inent
peaks and troughs in the V E P according to their amplitude,
latency, anil polarity. There are many sources o f uncertainty
in interpreting these com ponents. For instance, H arter
et al. (1 9 7 3 ) reported that only the late ( 2 0 0 - 2 5 0 ms) co m ­
ponent o f the evoked response reflects the activity o f b in ­
ocular cells, as indicated in a greater response to identical
stim ulation to both eyes than to rivalrous inputs. O th ers
have found that only the early com ponent ( 1 0 0 - 1 6 0 ms) is
correlated with stereoscopic vision (Regan and Spckreijse
1 9 7 0 ). Results also depend on electrode position, stimulus
contrast, and, as wc will see below, the spatial and temporal
properties o fth e stimulus. There is also a good deal o f inter­
subject variability. Regan (1 9 8 9 ) has provided a thorough
review o f human brain electrophysiology.
5 A .3 d M agn с to en cep h a lo g ra p h y
In m agnetoencephalography, the m agnetic fields generated
by neural activity in the human brain can be recorded with
supercooled m agnetom eters (see Regan 1 9 8 9 ; Hamalainen
et al. 1993). M agnetic signals, unlike electric signals, are not
smeared by the skull. This m ethod and electroencephalog­
raphy are the only non invasive procedures with m illisecond
tem poral resolution.
 5 .4 .3 c Tom ography have a tem poral resolution o f about 2 s and a spatial resolu­
tion o l abouc 1 mm. Ic provides m ore inform ation than the
In positron-em ission tom ography ( P E T ) a sugar con tain ­
F.F.G o r PF.T scan.
in '; a radioisotope, such as 0 ( ., is in jcctcd intravenously.
The fM R I record consists o f voxel units, each o f which
W hen a positron em itted by the isotope interacts w ith an
indicates chc collcccivc accivitv in thousands o f neurons.
electron, two gamma rays arc em itted in opposite direc­ j

Single voxels show only a weak sensitivity to th e orientation

tions. Each pair o f rays triggers a pair o f coincidence d etec­
o f a stimulus or to the direction o f attention. However,
tors on opposite sides o f the head. Several pairs o f detectors
multivariate techniques applied to the spatial pattern ol
are placed in an annulus and the intersection o f the diam e­
voxels over a large area o l the visual cortex can reveal more
ters jo in in g active detectors indicates sources o f positron
details o f responses (Leopold and W ilk e 2 0 0 5 ).
em ission in the plane o f the annulus. Sources o f activity in a
M apping the visual areas o l che human cortex is difficult
volume o f the brain are detected by several annuli stacked
because they lie mainly in deep sulci, which vary in position
to form a cylinder. To improve sampling density, the cylin­
and complexity from one person to another. Also, discinc-
der oscillates through a small angle about its central axis.
cions between areas are noc easy to define. Modern computers
Active sites recorded in a 3 -D axis system indicate regions
allow cortical areas to be mapped in a variety o f configura­
o f high glucose metabolism in the brain. Regions o f high
tions (Van Essen e ta l. 2 0 0 1 ) (P ortrait Figure 5 .1 8 ). By ana­
glucose metabolism arise in regions o f high synaptic activity
lyzing images in a series o l planes the folded co rtical surface
(Lriksson et al. 1 9 9 0 ). The m ethod has a spatial resolution
can be represented in a planar map.
o f up to about 1.5 mm but poor temporal resolution. It is
The fM R I procedure has produced retinocopic maps ol
labor-intensive and expensive.
V I and extrastriate visual areas in the human brain. This
was done by recording activity produced by flickering tex-
cured patterns in che form o f rotating segments and expand­
5 . 4 . 3 f M a g n e tic R c s o n a n c c Im ag in g
ing rings (see Engel 1996). The maps are similar to those ol
M agnetic resonance imaging (M R I) was developed in the
1980s. A part o f the body is exposed to a hom ogeneous
m agnetic field with a strength o f betw een 1.5 and 4 .7 Tesla.
This aligns chc m agnetic m om ents o f protons in chc nuclei
o f elements with odd atom ic weight. Hydrogen is the most
com m on atom o f chis cypc in chc brain. A pulse o f radio
waves o f a specified frequency m om entarily perturbs the
alignm ent of- chc nuclci o f hydrogen acorns. O n rccurning со
the aligned state, the atom s em it radio waves at a frequency
and with a dccay constant characteristic o f the chem ical and
physical structures in which they lie. By applying a small
gradient со chc applied m agnetic field across chc brain and
by changing the orientation o f this gradient, one can obtain
d istin ct radio signals related to position w ithin che living
brain (Narasim han and Jacobs 1 964). The head must be
held firmly in one position.
In che 1990s M R I signals began to be used to detect
transient local increases in the level o f oxygenated blood
due to local synaptic activity in the central nervous system
(Ogaw a ct al. 19 9 2 ; M enon ec al. 1998a). These signals arc-
known as blood-oxygen-level-dependent ( B O L D ) signals,
and chc procedure is known as functional magnecic rcso­
nancc imaging (f.V lR I). After sensory stim ulation the local
change in blood oxygen peaks after about 1.5 s (Vanzetta Р1фие*.|*. D av id С Van Essen. H e o b tain ed a B.S. in ch em istry from the
and Grinvald 1 999). A less localized changc in blood flow C a lifo rn ia In stitu te o f T ech n olog y in 1 9 6 7 and a P h .D . from Harvard
in 1 9 7 1 . H e con d u cted p o std o cto ral work w ith Г). H . H ubei and
takes several seconds. The am plitude o f che fM R I signal
T . N . W ic s c l a t H arvard, w ith J . K . S. Jan sen at the U niversity o f O slo ,
increases linearly with the scrcngch o f local neural accivicy and w ith S. M . Z c k i at U niversity C o lleg e, L o n d o n . H e o b tain ed an
over a m oderate range. See Logothetis and W andell (2 0 0 4 ) academ ic ap p o in tm en t in the division o f biology at the C a lifo rn ia
and Logothetis (2 0 0 8 ) for reviews o f fM R I. In stitu te o f T e ch n o lo g y in 1 9 7 6 . In 1 9 9 2 he was appointed Edison
Professor o f N cu rob io logv at W ash in g to n U n iv ersity S c h o o l ol
The fM R I procedure is noninvasive and does not
M ed icin e, S t. L ou is, where lie is the d ire cto r o f th e M cD o n n ell C en te r
involve exposure to radiacion. Ic may chcrcforc be applied o f H ig h er Brain F u n ctio n . In 2 0 0 2 he w on the K ricg C o rtic a l
over a long period. Although the signal level is low it can D iscov erer Award (C a ja l C lu b ).
the corresponding areas in the m onkey brain, boundaries
betw een visual areas can be mapped by recording the loca­
tions where traveling waves o f neural activity triggered by
m oving stim uli reverse in direction.
The m ethod can locate cortical areas sensitive to partic­
ular stim uli and measure changes in response associated
with changes in stimulus location, contrast, color, and
m otion (H ceger 1 9 9 9 ). It can also d etect neural activity
associated with changes in attention (Section 5 .9 ), with
perceptual changes in ambiguous stimuli (Section 4 .5 .9 b ), - 3 -2 -1 0 1 2 3 4 5 6
and with binocular rivalry (S ectio n 1 2 .9 .2 f). It can detect >/ilisecond Second M in u te H o ir D ay

activity created by illusory effects such as the m otion after­ T em poral resolution (log s)

effect (C ulham c t al. 1 9 9 9 ) and subjective contours. It is

also used to localize neural deficits (W andell 1999).
Typically, a specified test stimulus and a baseline stim u­
lus are presented for a few seconds many times. At each
location, the activity induced by the baseline stimulus is
subtracted from that induced bv¥ the test stimulus. The dif-
ference signals are superimposed on a map o t the cortex to
reveal where activity has increased in response to the defined
stimulus. Since the hemodynam ic response lags the neural
response by about one second, the m ethod cannot be used
to track m ost rapid changes in neural response. However, it
can detect onset tim e differences betw een the responses
from different regions o f the brain with an accuracy o f
about 3 0 ms. For example, when the subject perform s a
visual m otor task, it can detect differences in response times
betw een visual and m otor areas that correlate with reaction
times determ ined behaviorally (M enon et al. 1998b ). Also,
it can detect changes in response strength that occur as the
temporal interval betw een tw o stim uli, such as tw o flashes
o f light, is increased up to about 100 ms (Ogaw a et al.
2000).
Signals from fM R J have m ultiple com ponents. The in i­
tial dip is believed to originate from oxygen transport from
capillaries associated with local neural events. Later signals
originate from m ore global effects o f deoxvgenation and
blood flow. U nder certain conditions, the local com ponent
can be enhanced by using two stim uli, such as orthogonal
gratings, which generate differential responses in indepen­
dent groups o f neurons. The local fM R I response can
resolve orientation and ocular dom inance colum ns in alert
monkeys and humans (Grinvald et al. 2 0 0 0 ; K im et al.
2 0 0 0 ; C h en g e ta l. 2 0 0 1 ).
The spatial and tem poral resolutions o f m ethods o f
studying neural systems are depicted in Figure 5.19
(C hurchland and Sejnow ski 1 9 8 8 ). M ethods o f brain
mapping are reviewed in Toga and M azziotta (2 0 0 2 ).
F ig u r e у 1 9 . M e t h o d s f o r s t u d y in g t e r n a r y p r o t e s t in g . (A fro m C h u r< h U n 4
areas and thus affect regions rem ote from the site o f the
lesion. Also, neighboring areas may, over time, take over the
functions o f the ablated region.
In the em bryo o f certain animals, tissue from one region
o f the nervous system (the d on or region) may be trans­
planted in to another region (the host region). In certain
anim als, sense organs may be transplanted or an extra sense
organ may be transplanted from another anim al (D u n n ett
and Bjorklund 1992).
In tran sg en ic proced u res, a foreign gene is introduced
into the fertilized egg ot an anim al, usually a mouse. In a
related procedure, one o f the genes o f an animal is disabled
so that it no longer produces a particular protein. In this
way, the effects o f the absence o f that protein may be stud­
ied. G en etic procedures are discussed in more detail in
Section 6.2.
5.4.4 CONTROLLING NEURAL ACTIVITY
Several procedures have been devised for directly
controlling neural activity in the absence o f sensory sti­
mulation. These procedures are used for the following
purposes:
1. To trace neural connections through the com bined use
o f stim ulating and recording procedures.
2. To investigate the overt behavioral effects o f stimulating
specified neurons.
3. ’lo investigate rhe effects o f stim ulation on the ability
o t animals to detect, discrim inate, o r interpret specific
stimuli.

The traditional m ethod for controlling local neural

5 .4 .3 g N eural A blation and G ra ftin g
Lesions may be made surgically or by application o f a chem ­
ical agent. The anim als behavior is then examined. It is
often difficult to restrict damage to a defined area o f the
brain, and the lesion may cu t connections betw een brain
activity is to apply an electric current through an electrode.
The wave o f electrical depolarization locally releases neu­
rotransm itter. The m ethod can be applied to tissue cultures
or to an alert animal. It provides precise tim ing but has poor
spatial resolution because all neurons in a certain range are
affected. Also, electrical stimulation can n ot be used to
inhibit neural responses.
Both excitatory and inhibitory responses may be p ro­
duced by the local application o f excitatory or inhibitory
neurotransmitters. The procedure has been refined by trans-
fusing the neural tissue with neurotransmitters that remain
inactive until photolvzed by local application o f ultraviolet
light. The light is said to “uncage” the neurotransmitter.
However, the method has limited temporal and spatial
resolution.
In 2 0 0 5 a group at .Stanford University laid the founda­
tion for o p to g cn e tics (Hoyden c t al. 2 0 0 5 ) . Genes that
express light-sensitive opsins and promoters that control
their expression are derived from algae and packaged in a
virus. W h en injected into the brain the virus delivers the
opsin genes to neurons in wide areas o f the brain. The opsin
proteins are expressed only in those cells that activate the
specific promoter. The proteins are related to rhodopsin
and have no adverse effects on neural tissue. W h en trig­
gered by light o f a specific wavelength the opsins in that
particular group o f cells can rcversiblv excite or inhibit
neural responses in the intact animal. For example, when
locally excited by blue light, one opsin ( C h R 2 ) depolarizes
neurons to produce excitatory action potentials. W hen
excited by yellow light, the other protein (N’p H R ) releases
calcium ions that hyperpolarize and therefore inhibit the
same neurons Zhang et al. ( 2 0 0 7 ) . Millisecond pulses ol
yellow light may inhibit single action potentials or continu-
ous light may maintain inhibition over a period o f time.
The procedure has high temporal and spatial resolution
although it may be difficult ro deliver the trigger light to
deep regions in the primate brain. Thus the experimenter
may control the activity o f specific types o f neuron. At the
same time, other wavelengths may be used to excite fluores­
cent dyes that indicate which neurons have responded.
Also, at the same time, the behavior o f the animal may be
observed. Thus, application o flig h t pulses o f various wave­
lengths may used to finely control neural activity and
observe that activity. It remains to be seen whether these
procedures can be applied to neural tissue in deep layers o f
the brain.
In transcranial m ag n etic stim ulation a magnetic field
is induced in the brain by applying a brief high-current
pulse through a coil o f wire held over the scalp. The mag­
netic field induces an electric current in the brain, which
flows at right angles to the lines o f the magnetic field. The
electric currcnt triggers a mixture o f excitatory and inhibi­
tory activity in the brain tissue beneath the coil, which is
typically 9 cm in diameter. The effects are therefore n ot very
local. The procedure has been used to investigate gross
changes in the activity o f the m otor cortex following strokes
and skill acquisition. It has also been used ro study the
effects o f temporary disruptions o f activity in defined
cortical areas. For example, it has been used ro study rhe
effects o f stimulation of the visual cortex in blind people.
The method has also been used to study the effects o f
changes in cortical activity that outlast the period o f stimu­
lation (sec Barker 19 9 9 ; Siebncr and Rothwell 2 0 0 2 ).
5 .5 T H E V IS U A L C O R T E X
5 .5 .1 C O R T IC A L C ELLS
5 .5 .1 a T h e G e n e r a l S tr u c tu r e o f
C o r t i c a l N e u ro n s
A typical cortical neuron consists o f a cell body, or soma,
from which emerge one o r more basal dendrites and a single-
axon. The fluid inside the neuron is known as the cytosol,
and all the contents o f the cell other than the nucleus arc-
known as the cytoplasm . Each cell is lined by a membrane.
The soma contains the nucleus, which contains the ch ro ­
mosomes. It also contains the m ito ch o n d ria , which are
concerned with cell metabolism.
In neurons, .is in other cells, the outer membrane o f the
nucleus extends through the cytoplasm as a folded phos­
pholipid membrane known as the end oplasm ic reticulum.
O n e part o f the membrane is studded with ribosom es,
which are the sites o f protein synthesis. Synthesized protein
molecules migrate from the endoplasmic reticulum to
another reticular structure known as the G o lg i apparatus,
where they are converted into, for example, glycoproteins,
hormones, and neurotransmitters. The proteins also receive
molecular labels that determine their final destinations after
they leave the Golgi apparatus.
Neurons, like other cells, also contain a cv to sk elcto n
consisting o f microtubulcs, microfilaments, and neurofila­
ments. M icro tu b u les are lined with polymerized molecules
of che protein tubu lin. In neurons, vesicles move along che
microtubules carrying material from the soma to the axon
terminal by an terog rad e tran sport. This is particularly
important when the cell is growing. Vesicles also travel from
the axon terminal to the soma by retrog rad e tran sport.
This is important for conveying signals to the nucleus
regarding the proteins required by the growing cell. Vesicles
travel at a speed o f up to one meter per day.
The m icrofilam en ts consist o f strands o f the protein
actin. We shall see in Section 6 .4 .3 that they are involved in
the growth o f axons and dendrites. The neurofilam ents
consist o f strong strands o f long protein molecules. ‘I he
c c n tro s o m c is a central com ponent o f the cvtoskelcton
(see Scction 6.4.5b).
The neocortex contains two main types o f excitatory
neurons, several types o f inhibitory neurons, and many
types o f glial cells. Excitatory neurons are circular spiny
stellate cells, m ost o f which radiate dendrites in all direc­
tions, and pyram idal cells that have triangular cell bodies
with a single long apical dendrite and several shorter basal
dendrites (Figure 5 .20 ). Inhibitory neurons are devoid o f

------ 1 ------
I
r-
Chandelier cell
$. 10. ly p cf e f c d i i n th e т ат т лЧ лп iitu .il cortex. D o tte d lilies in d icate boun d aries o f co rtic a l layers.
spines and, on char account, are called sm o o th cclls (see
Figure 5.20).
In the macaque visual cortex there are approximately
1 2 0 ,0 0 0 neurons per cubic millimeter, which is about twice
as many as in other pares o f the cortex ( O ’Kusky and
C olonnicr 1982). There are about the same number o f glial
cells. O n average, there arc over 2 ,0 0 0 synapses per cell, and
each cortical cell provides between 7 ,0 0 0 and 8 ,0 0 0 syn­
apses to other cells. Each cell connects to thousands o f other
cells (divergence) and receives inputs from thousands ol
other cells (convergence) (Salin and bullier 1995). Details
o f cell types in the visual cortex are provided in Peters and
Rockland (1 9 9 4 ).
The basic dendritic morphology ol neurons is deter­
mined genetically. For example, cortical stellate cells and
pyramidal cells develop in cell culture even when isolated
from neighboring cells (Threadgill et al. 1997). However,
we will see in Chapter 6 that the detailed patterning o f den­
drites depends on sensory inpucs and on interactions with
neighboring cells.
5 .5 .1 b Pyram idal C ells
•
Pyramid cclls occur in the cerebral cortex o f mammals, birds,
fish, and reptiles. They make up abouc 7 5 % ot neurons in
— — — _v
Types of excitatory cells
1СЮ u m
Large basket cell Small basket cell Bouquet cell
Types of sm ooth inhibitory cells
(Pre^CilbctronJ Wtc«] miwid.p.rmhac.r. fmm U*<wi)
the mammalian neocortex. Their axons form chc white
matcer o f che cerebral corcex. Pyramidal cells occur in all eor-
cical layers except layer 1. Л basal dendritic tree descends
from the base ot the soma and an axon with apical dendrites
ascends from the apex o f the soma. The apical dendrites o f
pyramidal cells in layer 5 form distinct vertical clusters, which
ascend inco layers 4, 3, and 2. Back-propagating sodium
action potencials initiated in the somata o f these cells can
facilitate subthreshold calcium action potentials initiated by
stimuli impinging on apical dendrites (I.arkum et al. 1999).
This produces synchronous coupling between inputs arriv­
ing at different layers in the visual cortex. Pyramidal cells o f
layer 4 have cone-shaped clusters o f apical dendrites.
The d en d ritic shafts o f all excitatory* neurons contain a
multitude o f small d en d ritic spines. A pyramidal cell has
approximately 10,000 spines. The postsynaptic membranes
o f most excitatory synapses occur on the heads o f dendritic
spines. Each spine is connected to the dendritic shaft by a
narrow neck wich high electrical resistance. Thus,each spine
is a localized synaptic compartment. M ost spines do n ot
contain microrubulcs buc do concain acycoskclcton o fc o n -
cracrile actin filaments, which cause rapid changes in spine
structure, especially in developing neurons (Section 6.4.3).
Small modifications o f the morphology o f spines can alter
the efficiency o f synaptic transmission and the filtering
properties o f the synapse (Tsay and Yuste 2 0 0 4 ). It is
believed that most plastic changes responsible for learning
occur at dendritic spines (Section 6.5.1).
Each pyramidal cell receives about 10,000 synaptic
inputs, o f which 7 5 % are excitatory. Excitatory inputs from
neighboring stellate and pyramidal cells arrive on synapses
on dendrites near the soma (proximal dendrites). Inputs
from distant pyramidal cclls, the thalamus and other brain­
stem nuclei, and from the basal forebrain arrive on the distal
dendritic tuft.
M ost inhibitory synapses on pyramidal cells occur on
dendritic shafts on the axon and ccll nucleus (soma). They
arise trom cortical inhibitory stellate cells, the brainstem,
and the basal forebrain (claustrum).
Axons o f pyramidal cells are the major output co m p o ­
nents o f the neocortex. They contain only excitatory (gluta-
matergic) synapses. Axons from pyramidal cells in layer 6 o f
the primary visual cortex project to the extrastriate cortcx.
M ost o f them project to just one extrastriate area. However,
a few cells in cat area 17 project to both areas 18 and 19
(Bullier et al. 1984). Also, a tew cells in monkey V I project
to both V2 and M T (Sincich and H orton 2 0 0 3 ) . A larger
number o f M T cells project back to both V I and V 2. Thus,
feedforward projections arc more target-specific than arc
feedback projections.
Pyramidal cclls o f V I also project to ipsilatcral and per­
haps also to contralateral subcortical regions (Creutzfeldt
1977). The subcortical regions include the pretectum, supe­
rior colliculus (Berman et al. 1 975), pulvinar, I.G N , and
other areas ot the thalamus (Gattass et al. 1979; Casanova
e t al. 1989; Fitzpatrick et al. 1 994), the caudate nucleus, and
the cerebellum by way o f pontine nuclei (Brodal 1972).
Details o f cortical efferents are provided by Swadlow (1 9 8 3 ).
Pyramidal cells in area V I receive excitatory feedback signals
from the extrastriate visual areas to which they project.
Pyramidal cells also form excitatory networks within
V I (Jo h n so n and Burkhalter 1 997). In cortical layer 6 there
are eight types o f pyramidal cells. O n e type receives and
transmits signals to magnocellular layers 4 B and 4C(X.
Another type receives and transmits signals to parvocellular
layers 2 , 3 , and 4C(3. O ther types transmit and receive inputs
within the same layer. O n e type receives and transmits to all
cortical layers (Briggs and Callaway 2 0 0 1 ) .
Feedback signals trom extrastriate areas teed onto
relatively few inhibitory G A BA ergic interneurons in V I .
Feedback from area V 5 in monkeys improves the responses
o f cells in V I , V 2 , and V 3 to figure-ground stimuli (Hupc
et al. 1998). Feedback from higher visual areas may
also enhance responses to stimuli to which the animal is
attending (Section 5.9.2).
5 .5 .1 c T em p oral D y n a m i c s o f Pyramidal C ells
Pyramidal cells in the mammalian neocortex have been clas­
sified into tour types according to their temporal dynamics.
Regular sp iking neurons fire rapidly at stimulus onset but
adapt to a steady level within about 100 ms. Fast spiking
neu ron s show little or no adaptation and are usually in h ib­
itory. B u rstin g o r ch atterin g neurons produce periodic
bursts o f 2 to 6 spikes with interburst intervals o f 3 0 to
50 Hz. In trin sic-b u rstin g neurons tire with a burst ot
spikes followed by a pause and a tonic Spike train (C onnors
an d G u tn ick 1990; Gray and M c C o r m ic k 1 996). These dif­
ferences depend on the intrinsic properties ot ion channels
on the cells soma and dendrites (Solom on et al. 1993).
They have been modeled by equations derived from the
H o d g k in -H u xley e q u a tio n s o f time-dependent responses
ot ion channels on neural membranes (W ilson 1999b).
Similar differences exist in the response properties o f
m otor neurons, such as those controlling eye movements
(Section 10.10).
5 .5 .1 d S p in y S te lla te C e lls
Spiny stellate cells are the second type o f excitatory cortical
cell. They occur only in cortical layer 4. Almost all inputs to
the primate visual cortcx from the I.G N impinge o n spiny
stellate cells. These cells project horizontally within layer 4
and to a lesser extent to other layers, but their dendrites
remain mainly within the same local vertical column o f
cclls. S o m e spinv stellate cells in layer 4 B o f the primate
visual cortex project directly to the middle temporal area
( M T ) (N’assi and Callaway (2 0 0 7 ).
O n ly about 10% o f excitatory synapses impinging on
spinv stellate cells ot layer 4 originate from the L G N , the
rest originate from subcortical nuclei, neighboring spiny
stellate cells, and pyramidal cells, especially along recurrent
axons from layer 6 (Fitzpatrick ct al. 1985; Freund et al.
1989; Ahmed et al. 1994). Recurrent excitatory circuits arc
therefore very prominent in the visual cortcx.
5 . 5 . l e S m o o t h I n h ib it o r y C e lls
Sm ooth cortical cclls arc inhibitory (G A BA ergic) interneu­
rons that release the neurotransmitter У-amino-butyric
acid, or G A B A . Inhibitory synapses form about 15 to 2 0 %
o f synapses in the visual cortex. Inhibitory interncurons
receive both excitatory and inhibitory inputs onto synapses
on their somata.
There are three main types o f inhibitory interncurons:
chandelier cells, basket cells, and bouquet cells. Figure 5.20b
shows that they differ in their patterns ot dendritic arboriza­
tion, but the functional significance o f the ditferent types is
not known (Anderson et al. 1993; Markram ct al. 2 0 0 4 ).
They also differ in thespeed and regularityof their responses.
Som e maintain a steady response to continued stimulation
while others adapt (see Gupta et al. 2 0 0 4 ) .
Interncurons occur in all cortical layers, including layer
1, which is devoid o f excitatory cells. They arc most dense in
layers 4 A and 4 B , which receive geniculocortical inputs
(Douglas ct al. 1995). Although most interneurons operate
over short distances, axons o f basket cells spread laterally up
to 2 mm (Kritzcr et al. 1992). Interneurons do not send
axons outside the cortex. Som e types o f interneuron occur
only in particular cortical layers. Sonic G A B A crgic cells
slowly release neuropeptides that can cither excite or inhibit
other neurons (Douglas et al. 1 995). Inhibitory synapses
are discussed in Section 5.5.6b.
5.5.1 f G lial C e lls
In the central nervous system o f vertebrates there are at least
ten times more glial cells than neurons. There are two main
types o f glial cell— microglia and macroglia. M icro g lia
defend against invading microorganisms, act as phagocytes
in removing dead cells, and provide trophic factors, includ­
ing neurotrophins, to other glial cells and neurons. They
also direct the migration o f neural stem cells to damaged
areas o f the adult C N S o f the mouse (Aarum et al. 2 0 0 3 ).
M acroglia consist o f astroglia and oligodendrocytes.
Astroglial cells include astrocytes, Bcrgmann glia, and
Miiller cells.
W h en stained, a stro cy tes appear as star-shaped cells,
but the branching ramifications o f each ccll fillapolyhedral
volume with little overlap between the domains o f neigh­
boring cells. Each ccll has five to eight major extensions,
each o f which ramifies into fine appendages. In the human
cortex, there are about four astrocytes tor every neuron.
Astrocytes perform a variety o f trophic functions. Some
form the protective seal between blood capillaries and the
brain, known as the blood-brain barrier. They deliver glu­
cose to neurons from blood capillaries. Astrocytes near syn­
apses remove surplus neurotransmitter from the synaptic
cleft and extracellular space, and help to maintain ionic bal­
ance, especially the balance o f potassium ions. Reduction o f
the number o f glial cells in the vicinity of synapses reduces
synaptic efficiency (O liet c t al. 2 0 0 1 ).
Before the 1990s it was believed that glial cells served
only tropic functions. It is now known chat many astrocytes
form a reticular network linked by gap junctions (low-resis-
tancc synapses that allow direct electrical coupling). Glial
cells envelope synapses o n dendritic spines. A single cortical
astrocyte can form more than 3 0 ,0 0 0 gap junctions with
itself or with adjacent astrocytes. Activation o f an astrocyte
depends on release o f calcium ions (C a 2') from the cell’s
endoplasmic reticulum. Ncurotransmitters released at syn­
apses activate receptors on glial cells and evoke waves of
Ca ions. Waves o f intracellular C a ions also arise spontane­
ously, especially in the developing nervous system. Glial
cells may be involved in generating synchronous neural
activity (Alvarez-Maubecin ct al. 2 0 0 0 ; Havdon 2 0 0 1 ;
Newman 2 0 0 3 ) .
Neurons conduct brief action potentials at high speed
over long distances, astrocytes conduct slow, long-duration
calcium spikes over short distances. Long-range transmission
o f C a ions over the astrocytc network may be responsible
lor cortical spreading depression.
It has been claimed that astrocytes in cell cultures release
glutamate and other molecules, such as adenosine and
G A B A , to either the prcsynaptic or postsynaptic membranes
o f neurons. This process is known as gliotransm ission. It
has also been claimed that gliotransmission modulates syn­
aptic transmission between neurons (Bezzi et al. 2 0 0 4 ;
Perea et al. 2 0 0 9 ) . However, more recent evidence suggests
that astrocytes do nor modulate excitatory synaptic trans­
mission, at least in the hippocampus (Agulhon et al. 2 0 1 0 ;
H am ilton and Atrwell 2 0 1 0 ).
We will see in Sections 6.4.4 and 6.5 that astrocytes are
also involved in synaptogenesis, cortical development, and
synaptic plasticity. They have been shown to be a source of
regeneration in damaged retinas o f chickens (Fischer and
Reh 2 0 0 1 ) .
O lig o d en d ro cy tes form myelin sheaths around axons
in the central nervous svstcm.
i
Schwann cells form che
sheaths in the peripheral nervous system (Section 6.3.3c).
The structure and connections o f astrocytes and oligo­
dendrocytes are subject to experience-dependent changes
(Jo n es and G reenough 2 0 0 2 ).
5 .5 .2 C O R T IC A L SYN A PSES AND
N E U RO T R A N S M IT T E R S
M ost neurons in the central nervous system have a ccll body,
or soma, from which a com plex dendritic tree and a single
axon arise. The dendricic tree o f excitatory neurons consists
o f branching shafts, each with a multitude o f dendritic
spines. Dendritic trees contain thousands ot synapses and
spread over hundreds o f micrometers. The dendrites o f
inhibitory (sm ooth) neurons have tew spines. The single
axon branches into collaterals some distance from the soma.
The soma, axon, o r dendrites can form prcsynaptic or post­
synaptic structures. However, axons form m ost o f t h e prc­
synaptic elements (synaptic boutons) that convey signals to
the dendrites o f other neurons. Dendritic spines form most
o f che excitatory postsynaptic elements. They receive signals
from synaptic boutons o f other neurons and convey them
to che soma and chen to the axon, which is the main output
pathway o f the neuron.
In che cat s visual cortex, 8 4 % o f synapses are excitatory,
and about 8 0 % o f these occur on dendritic spines, 2 0 % on
dendritic shafts, and only 0.1% on the cell body (soma) o f a
postsynaptic cell. Inhibitory synapses arc usually formed on
smooth dendrites o f intcrncurons. Mosc o f chcm occur on
dendritic shafts rather chan on dendritic spines, and 7%
occur on the som a (see Edwards 1 995). Thus, most synapses
on somata are inhibitory. Dense collections o f synapses arc-
called glom eruli.
Synapses are less than one micron in diameter and occur
at densities o f about 4 billion per mmr in rhe rar correx (see
M cAllister 2 0 0 7 ).
 Synapses on dendrites near the soma are known as
proxim al synapses, while those remote from the soma are
known as apical synapses. Theoretically, inputs from apical
synapses should be attenuated relative to those from proxi­
mal synapses because they have further to travel before
reaching the soma. In pyramidal cells o f the neocortex,
excitatory potentials reaching the soma arc indeed weaker
from distal synapses than from proximal synapses. However,
in neurons in the hippocampus, potential amplitudes are
independent o f their site o f origin because distal synapses
have a compensatory increase in the density ot glutamate
receptors (W illiam s and Stuart 2 0 0 3 ) . The implications o f
these differences are discussed in Section 6.5.2.
Until the middle o f the 2 0th century there was a lively
debate about whether synaptic transmission was electrical
o r chemical. W e now know that both types o f synapse exist.
Synapses that involve direct transmission ot ions are known
as electrical, or voltage-gated synapses. Those that involve
the secretion ot a chemical neurotransmitter are known as
ligand-gatcd synapses. There are two types o f ligand-gated
synapse, ionotropic synapses and metabotropic synapses.
The types o f synapse set out in Table 5.1 will now be briefly
described.
5 .5 .2 a V oltage-G ated Synapses
M ost voltage-gated electrical coupling between neurons
occurs at gap ju n ctio n s. Adjacent membranes o f neighbor­
ing cells contain well-aligned channels formed by proteins
known as co n ncxin s. There arc at least 10 connexins in the
mammalian central nervous system. Som e occur only on
specific types ot cell. Electrical current is carried across the
channels mainly by potassium ions, but small molecules
may also pass. (lap junctions are triggered by a voltage dif­
ference between the two cells produced by a nerve impulse.
T a b le 5 ./ . T Y P F .S O F C O R T I C A L S Y N A P S E
VOLTAGE-GATED
T rig g ere d by a v o lta g e c h a n g c a cro ss gap ju n c tio n s .
I.KiANDGATF.D
In v o lv e n c u r o tr a n s m itte r s a c e ty lc h o lin e , s e r o to n in , g lu ta m a te .
Io n o tr o p ic
T rig g ere d d ire c tly by a n c u r o tra n s m itte r .
A M PA ty p e
K a in a tc ty p e
N M D A ty p e
M e ta b o tr o p ic
T rig g ere d by n c u r o tr a n s m itte r -4* c a sc a d e o f v cco n d a ry m o le c u le s.
IN H IB IT O R Y SY N A P SES
In v o lv e th e in h ib ito r y n c u r o tr a n s m itte r G A B A .
Generator potentials produced by sensory receptors acti­
vate voltage-gated synapses. Voltage-gated synapses may be
unidirectional or bidirectional. They have a high threshold,
but are last acting and capable ot synchronizing responses
in neural tissue. They conserve the sign o f depolarization o f
the presynaptic membrane.
In cold-blooded animals, gap junctions continue to
be fast acting when chemical synapses are slowed by
low temperatures. Thus, in some invertebrates and lower
vertebrates, gap junctions are used in escape and warning
mechanisms.
G ap junctions occur in the vertebrate retina, where they
help to improve the signal-to-noise ratio (Section 5.1.3).
They also occur throughout the primate neocortex (Bennett
and Zukin 2 0 0 4 ).
Electrical couplings across gap junctions are prominent
between neurons during the development o f the nervous
system. Specific connexins expressed in certain brain areas
only in early development are crucial for neuron differentia­
tion and synaptogenesis (Maxeiner et al. 2 0 0 3 ).
G ap junctions con nect inhibitory interneurons in the
thalamus, ccrebellum, and cerebral cortex. There seem to be
two independent networks o f connected interneurons—
fast spiking and low-threshold spiking (Galarreta and
Hestrin 2 0 0 1 ) . It is believed that these networks facilitate
synchronization o f neural activity.
5 . 5 . 2 b I o n o t r o p i c L ig a n d -G a te d Synapses
The structure o f a typical d irect, or io n o tro p ic ligand-
gated synapse is shown in Figure 5.21. I he axon o f the
presynaptic cell forms presynaptic m em b ra n es at each
o f a series o f small swellings, or b o u tou s, which are 0.5 to
1.0 ,um in diameter. Each bouton contains m itochondria
and a reserve pool o f synaptic vesicles. The vesicles are
synthesized in the G olgi apparatus and bound to a web o f
contractile microfilaments o f actin. Each vesicle is about
3 0 nm in diameter. A typical presynaptic membrane
M itochondrion
Bouton
V esticles with
connecting filam ents
S ynaptic
cleft P ostsynaptic density
A ctin m icrofilam ents
E ndoplasm ic reticulum
Spine a pparatus
D endritic spine
r>«»< s.21. D iagram o f a typical (ortu at synapse. fan, b l . u J . 1991}
contains hundreds o f vesicles, each loaded with about 1,500
molecules o f neurotransmitter. Neurotransmitter molc­
culcs formed in the cytoplasm arc pumped into vesicles by
vesicular transporter molecules embedded in the vesicle
wall. Tli us, transporter molecules control the concentration
o f neurotransmitter molecules in the vesicles (Varoqui and
Erickson 1997). Specific transporter molcculcs have been
identified for glutamate, G A B A , and other neurotransmitters
(Bcllocchio et al. 2 0 0 0 ).
Vesicles migrate from the reserve pool to rhe presynap­
tic membrane, where they are ready for release. O n ly a few
vesicles are available for quick release at any instant. After a
period ot intense synaptic activity, the pool ot available
vesicles becomes depleted. It can take several seconds to
replenish the vesicles. Removal o t calcium ions trom the
synaptic terminal after intense activity accelerates the rate
o f vesicle recovery (Wesscling and Lo 2 0 0 2 ) .
A nerve impulse triggers an influx o f calcium ions into
the presynaptic cell, which releases a cascade ot chemical
events involving phosphorylation o f the protein synapsin
by the enzyme ca lm o d u lin -d ep en d en t protein kinase II
( C a M K I I ) (Turner ct al. 1999). Synapsin molecules are
arranged on actin filaments associated with synaptic vesicles
(Sankaranarayanan ct al. 2 0 0 3 ) . These molecules release
vesicles containing neurotransmitter from the reserve pool
so that they can migrate to the active zone at the synaptic
membrane.
W h en the synapse is activated, vesicles that have
migrated to the active zone fuse with the presynaptic
membrane— a process known as ex ocy to sis (Zcnisek et al.
2 0 0 0 ) . Neurotransmitter molecules are thereby released
into the synaptic cleft in less than a millisecond. The m ol­
ecules cross rhe cleft, which is about 2 0 nm wide, and attach
to rcccptor molecules on the postsynaptic membrane. O ne
action potential in the presynaptic membrane releases about
2 0 0 synaptic vesicles.
At many synapses, vesicles arc released spontaneously at
a very low rate trom a resting p o ol. These vesicles generate
m in iatu re postsynaptic p o te n tia ls,o r minis. Tagging vcsi-
cles with fluorescent molecules has revealed that vesicles
released spontaneously from the resting pool are distinct
trom vesicles released by neural activity trom the reserve
pool (Frcdj and Burrone 2 0 0 9 ) . Furthermore, spontane­
ously released vesicles may be released some distance
from the synaptic clcfi and activate distinct locations on
the postsynaptic membrane. Spontaneous potentials may
be involved in tuning synaptic sensitivity (Section 6.5.4).
After synaptic transmission, neurotransmitter mole­
cules arc rapidly absorbed from the synaptic clcft by astro­
cytes and a sodium-ion process on the presynaptic
membrane. Spent vesicles are recycled and recharged with
neurotransmitter. Recycling o f single vesicles has been
observed by introducing molecules that produce fluores­
cence when released from the vesicle. Som e vesicles, espe­
cially those at small synapses, do not fully collapse but make
only a brief contact with the ccll membrane and arc recyclcd
rapidly. This so-called kiss-and-run retrieval o f vesicles helps
to conserve resources (Harata c t al. 2 0 0 6 ).
O th er vesicles take several seconds to be recvcled or
remain on the presynaptic membrane until there is another
nerve impulse (Aravantis ct al. 2 0 0 3 ; G andhi and Stevens
2 0 0 3 ) . It seems that some vesicles migrate between the prc-
synaptic membranes o f neighboring synapses (D arcy et al.
2 0 0 6 ) . Tli is may help to coordinate the firing patterns o f
neighboring synapses.
There are three main groups ot neurotransmitter—
am ino acids, catecholamines, and monoamines. Figure 5.22
shows examples from each group. In the cerebral cortex all
excitatory synapses involved in the rcccption and proccss-
ingot information trom the sense organs use the neurotrans­
mitter glutam ate. Inhibitory synapses use theclosely related
am ino acid 7-am ino-butyric acid (G A B A ). C ortical syn­
apses that use other neurotransmitters arc described in
Section 5.5.2g.
The release o f ncurotransmitter from one vesicle at each
synaptic bouton can be regarded as one quantum ot synap­
tic excitation. It has been claimed that a synaptic bouton
releases only one vesicle at a time. Each vesicle contains a
fairly constant number o f neurotransmitter molecules,
which activates almost all the receptor sites on the adjacent
postsynaptic membrane. According to this view, the
strength o f response at a synapse depends on the number o f
receptors at the site (Korn and Faber 1991). Ninio ( 2 0 0 7 )
questioned this view and concluded that single vesicles
do not saturate the postsynaptic membrane. Thus, response
strength depends on the number o f vesicles released (see
Stevens 1995) and on the number ot receptor molcculcs
A m in o a c id n e u ro tra n s m itte rs
G lutam ate C O O H - C H 2 - C H 2 - CH - N H 2
I
CO O H
Y-aminobutyric acid COOH - CH2 - CH2 - CH2 - NH2
(G A B A)
A c a te c h o la m in e n e u ro tra n s m itte r
A drenaline
A m o n o a m in e n e u ro tra n s m itte r
HO
CH2 - CH2 - nh2
Serotonin
Figure s .: 2. E xam ples o f н см ош ш уп Ш еп .
on the postsynaptic membrane. Synaptic activity leads
to an increase in the number ot receptor molecules (see
Scction 6.4.4).
Neurotransmitters activate receptors lining the postsyn­
aptic membranes o f excitatory synapses. These membranes
occur mostly on spines that are distributed in great num­
bers along each branch ot the dendritic tree ot the postsyn­
aptic cell. The receptor m em brane o feach excitatory synapse
contains a dense collection ot receptor sites, actin-binding
protein molecules, and a heterogeneous population o f
actin filaments and proteins that torm a molecular scatfold.
The whole structure is known as the postsynaptic density
(K im and Shcng 2 0 0 4 ) . The pre- and postsynaptic m em­
branes are held in register by filamentous proteins that span
the synaptic cleft. These molecules have been implicated in
synaptogenesis and synaptic plasticity (McAllister 2 0 0 7 ).
Dendritic spines can be small and blunt, elongated, or
elongated with an expanded end (pedunculatcd). Actin
microfilaments that torm the cell cytoskcleton extend into
the dendritic spines. Microtubules that extend down the
dendritic shaft do not extend into the spines.
Receptor molecules line p o res in the postsynaptic
membrane through which ions pass into the postsynaptic
ccll. A cylinder formed from five glycoprotein molecules
surrounds each pore, as shown in Figure 5.23. The five
glycoproteins differ to form distinct reccptor subunits that
determine the specificity o f responses to diverse inputs'
(M onyer et al. 1992). W h en activated by a neurotransmit­
ter, the molecules lining the pore momentarily change their
shape and allow ions to pass. The channel then closes and is
refractory for a few milliseconds. The flow o f ions can be
4
measured by applying a patch clamp over the pore.
The clamp is a fine glass pipette containing the neurotrans-
mitter or a synthetic ligand molecule, which binds to the
receptor.
Pore
F igurc 5 . 1У G en era! stru ctu re o f a n io n o tro p ic recep to r p ore.
Rcccptorson ligand-gatcd synapses can be experimentally
activated by an agonist, which can be a naturally occurring
ncurotransmittcr or an amino acid extracted from another
source. A synapse may be blocked by an an tag o n ist, which
can be a natural inhibitory ncurotransmittcr or a synthetic
4 «
molecule.
Rcccptor molcculcs spanning the postsynaptic m em­
brane are anchored to mobile actin filaments within the cell
by specific actin b in d in g proteins. These proteins regulate
the polymerization o f actin and control the arrangement o f
the actin filaments. C ontraction ot actin filaments trans­
forms blunt spines into the other types during early devel­
opm ent and during learning in the adult. Depolymerization
o f actin reduces the number ofclusters o f N M D A receptors
and the number ot spines containing A M PA receptors
(Allison et al. 1998). These receptors are described in the
next section.
Since ligand-gated synapses involve the diffusion o f
molecules across a relatively wide synaptic cleft they are
much slower than voltage-gated synapses. However, they
have low thresholds and act as amplifiers, since presynaptic
activity releases many molecules o f neurotransmitter.
Each muscle fiber receives only an excitatory input, typ­
ically from only one motoneuron, through a synapse involv­
ing the neurotransmitter acetylcholine. In contrast, each
neuron in the ccntral nervous system
J
receives many
J
cxcit-
atory inputs, mostly on dendritic spines, and many inhibi­
tory inputs, the most effective o f which impinge on the ccll
body. The resulting potentials propagate electrotonically to
the cell body, where they are integrated over a certain time
period to produce action potentials in the axon. There may
also be a few synaptic inputs on the axon, which modulate
the action potentials.
The production o f energy in all tissues involves cycles ot
ph osph orylation and dephosphorylation o f molecules.
Nerve impulses and neurotransmitters in all types ot ligand-
gated synapses lead to the production o f enzymes known as
p ro tein kinases. Each kinase phosphorylates and thereby
activates a particular protein in the neuron cytoplasm.
Som e activated proteins trigger release ot neurotransmitter
in presynaptic neurons, others set o t f complex chains o f
chemical events in the postsynaptic neuron, which are
responsible for growth and learning.
Chemicals produced by synaptic activity travel to
the ccll nucleus and trigger protein synthesis. In protein
synthesis, the nucleotide base triplets in the D N A o f the
chromosomes in the cell’s nucleus arc transcribed into mes­
senger R N A (m R N A ). The m R N A molecules pass through
small pores in the nucleus membrane into the cytoplasm,
where they attach to the endoplasmic reticulum. There the
information is translated into a sequence ot amino acids
required for a particular protein. Protein molecules are
then transported along microtubules to where they are
needed. More details o f these mechanisms are provided in
Section 6.6.1.
 5 .5 .2 c Types o f Io n o tro p ic R ecep tors
There «ire three types o f ionotropic receptors on the post-
synaptic membranes o f ligand-gated cortical synapses. For
all o f them, the excitatory neurotransmitter is an amino
acid derived from glutamate. Synapses vary in the types and
distributions o f receptor molecules and in the types o f ion
channels on the postsynaptic membrane, which determine
how they transform inputs into nerve impulses. Although
all types o f receptor respond to the same glutamate neu­
rotransmitter, each type is identified by its response to a
specific agonist derived from other sources. The three types
o f receptor are:
1. A M PA receptors These receptors are identified by their
response to a -amino-3'hydroxy-5-methylisoxazole-
4-proprionic acid (A M PA). They are also known as
qu isq u alate receptors. The receptor molecules on the
postsynaptic membrane o f dendritic spines consist o f
molecular complexes composed o f subunits G lu R I to
G lu R 4 . Activation o f A M PA receptors opens sodium-
or potassium-ion channels. This process mediates most
o f the rapid excitatory synaptic transmission in the
mammalian central nervous system.
2. K ainate receptors (KARs) These receptors are identified
by their response to kainatc agonists extracted from
plants. These agents are more potent and more specific
than glutamate— the endogenous cortical
neurotransmitter. Like A M PA receptors, kainatc
receptors open sodium- or potassium-ion channels, but
show a longer activation than do A M PA receptors.
3. NM DA receptors These receptors are identified
by their response to the synthetic agonist N -m eth y l-
D -a sp a rta te ( N M D A ) . They are also sensitive to a
number o f other chemical agents, such as glycine and
polyamines. Activation o f these N M D A receptors
opens calcium-ion channels in addition to sodium and
potassium channels.
Receptors for N M D A contain three main subunits.
Subunit N R l is required for synaptic activation, and sub­
units N R 2 an d N R 3 modulate the response (ValtschanofF
and Weinberg 2 0 0 1 ). Subunit N R l is fast acting while sub­
unit N R 2 responds more slowly (Banke and Traynelis
2 0 0 3 ). Variations in the subunits produce diversity in the
way synapses respond to a given input. Thus different neu­
rons process similar inputs in different ways. Also, the com ­
position o f the subunics can determine how a neuron
responds to converging inputs. For example, cortical pyra­
midal neurons respond to high-frequency local inputs
from rhe same hemisphere but only to low-frequency cal­
losal inputs from the opposite hemisphere (Kumar and
Huguenard 2 0 0 3 ) . Thus, a given neuron can process inputs
from different channels in fundamentally different wavs.
Receptors at N M D A synapses have a prolonged response
and are under strong inhibitory control. They also have
the unique feature that they are blocked by extracellular
magnesium ions. They respond only when these ions
are driven out by depolarization o f the postsynaptic
membrane induced by simultaneous activation o f associ­
ated n o n -N M D A receptors on the same postsynaptic
membrane.
Activation o f receptor molecules on the postsynaptic
membrane allows an influx o f calcium ions into the post-
synaptic spine. This activates calmodulin-dependent p ro ­
tein kinase 11 (C a M К 11) and other enzymes, which increases
the numbers and synaptic efficiency o f A M PA receptors
(Sm art 1 997). Activation o f N M D A receptors also leads to
protein synthesis and cvtoskeletal changes in dendritic
spines. We will see below and in Sections 6.4.3 and 6.5 that
these stimulus-contingency features o f N M D A receptors
allow them to mediate growth, plasticity, and learning in
the visual cortex.
The three basic types o f receptor (A M P A , kainatc, and
N M D R ) arc subdivided into at least 16 subtypes that are
identified by their responses to synthetic ligands containing
dilferent peptide subunits (Hollm ann and Heinemann
1994).
The variety o f receptors provides a molecular basis lor
diversity and specificity o f postsynaptic mechanisms. The
different types o f receptor are differentially distributed
in the mammalian brain, although N M D A and Л М Р Л
receptors tend to occur together on the same postsynaptic
membrane (Kaczmarck et al. 1997). Thus, they arc activated
by release o f glutamate in the same synapse. Ihc signifi­
cance of this coactivation is discussed in Section 6.5.1.
Geniculocortical transmission in cortical layer 4 o f the cat
is mediated mainly by A MPA and kainatc synapses. All
three types mediate intracortical transmission in layers 1 ,2 ,
and 3 (Larson-Prior et al. 1991). In the human striate cortex,
N M D A receptors are most dense in layers 1 to 4 C , with
highest density in layer 4 C . A M PA receptors are m ost dense
in layers 1 ro 3 and least dense in layers 4 B and -1C. Kainatc
and metabotropic receptors are fairly evenly distributed.
The types o f synapse do not vary between cortical columns
(Albin 1991).
5.5 .2d M c ta b o tr o p ic L ig a n d -G a ted Synapses
In an in d ire ct, o r m eta b o tro p ic ligand-gated synapse,
the ncurotransmitter binds to a receptor consisting o f
an extracellular ligand-binding region, a transmembrane
region, and a cytoplasmic region in the cell. The cytoplas­
mic region binds to a G -protein (guanosine triphosphate
binding protein) (Kunishima e t al. 2 0 0 0 ) . The activated
subunit o f rhe g-prorein moves along rhe intracellular
surface and activates a cascade o f molecules, known
as second messengers. O n e second messenger is cA M P
(cyclic adenosine monophosphate), another is nitric oxide.
Second messengers have widespread effects in che cell,
including gene activation. M etabotropic synapses fall into
eight classes according to the amino acid sequence o f the
receptors on the postsynaptic membrane. They are identi­
fied by their responses to synthetic agonists and antagonists
(Riedel 1996). They respond to hormones and to a variety
o f neurotransmitters, including glutamate, norepinephrine,
and serotonin. M etabotropic synapses have an onset time o f
hundreds o f milliseconds. W h ich is much longer than that
o f ionotropic synapses.
5 .5 .2e In h ib ito ry Synapses
Inhibitory interncurons in the cortex work in partnership
with excitatory pyramidal cells but are shorter and faster
acting than pyramidal cclls. There is a bewildering diversity
o f interncurons. M ost o f them are excited o r inhibited
by two or three neurotransmitters, which include nora­
drenaline, muscarine, serotonin, and glutamate (Parra et al.
1 998). The main inhibitory neurotransmittcr produced by
interneurons in the cerebral cortex is У -am in o -bu tyric
acid ( G A B A ) , an amino acid derived from glutamate (Mize
and Marc 19 9 2 ; Gutierrcz-Igarzact al. 1996). The molecule
exists in various forms, which bind to different receptor
molecules. Ion channels on the postsynaptic membrane o f
an inhibitory synapse consist o f a cluster o f five receptor
subunits each with an extracellular peptide, a transmem­
brane sequence, and a large intracellular loop (D e Bias
1 996). Fast acting G А В А Д receptors are o f the direct io n o ­
tropic type, and G A B A ( receptors are o f the slow-acting
metabotropic type (M oss and Smart 2 0 0 1 ) . Interncurons o f
the same dynamic type are connected by electrical synapses,
which generate synchronized spikes within cach o f the two
networks (G ibson et al. 1999).
Inhibition can work in two ways. In h y pcrpolarizing
in h ib itio n the change in membrane potential is determined
by the linear sum o f negative and positive currents. In
sh u n tin g in h ibition the excitatory response is reduced
by a nonlinear increase in membrane conductance (Borg-
Graham et al. 1998). Inhibitory synapses near the zone
where nerve spines are generated producc proxim al in h ibi­
tion, which is capable o f blocking all excitatory responses
o f the cell. Inhibitory synapses on particular dendrites
produce distal in h ib ition , which can selectively inhibit
particular branches o f the neuron or produce graded
inhibition (Vu and Krasne 1992).
In general, inhibitory interneurons modulate the thresh­
old for initiation o f action potentials on dendritic spikes,
and play a major role in controlling the activity o f cortical
neural networks. Short- and long-range lateral inhibitory
interactions fine-tune neurons to specific stimulus features,
such as orientation (Section 5.5.6b). Feedforward, and
feedback inhibition generates synchronous and oscillatory
responses (Section 4.3.4). Inhibitory circuits are also
involved in attcntional gating (Section 5.9).
Autapses are synapses made by a neuron onto itself.
Fast-spiking inhibitory interneurons form autapses, which
decrease the rate o f repetitive firing. They modulate the syn­
chrony of firing ol neural networks to which the interneu­
rons arc couplcd (Bacci c t al. 2 0 0 3 ).
5 . 5 . 2 f R e c e p to r s on P resy n a p tic M e m b r a n e s
The presynaptic membranes o f excitatory neurons and
inhibitory interncurons can contain kainate, A M FA, or
N M D A ionotropic receptors or metabotropic receptors
(Lerma 2 0 0 3 ).
Activation ot presynaptic receptors by glutamate is a
retrog rad e sign alin g system. Activated receptors modu­
late the release o f neurotransmitters in both excitatory and
inhibitory synapses (Engelman and M acD erm otc 2 0 0 4 ) .
Som e presynaptic receptors are autoreceptors activated by
the neurotransmitter released by the same presynaptic
membrane. They are also activated by cannabinoids released
from the postsynaptic membrane (Freund et al. 2 0 0 3 ) .
O th er presynaptic receptors are activated by distinct
neurotransmitters released by neighboring neurons.
Cholinergic receptors are triggered by afferents from cen ­
ters in the basal forcbrain. S o m e receptors involve G A BA-
mediated presynaptic inhibition, while others facilitate
neurotransmitter release. The functions o f receptors on pre-
synaptic membranes arc n ot known (M acD erm o tt et al.
1999; Pinheiro and Mullc 2 0 0 8 ).
5 .5 .2 g O t h e r C o r t i c a l N e u r o tr a n s m itte r s
The neocortex receives inputs from a variety o f subcortical
areas, each involving a distinct neurotransmitter. These are
amines rather than glutamate. C ortical cells contain a vari­
ety o f receptors for each o f these amine transmitters. They
act as modulators o t neural activity in the cortex rather than
transmit sensory information or motor outputs.
Afferents trom the basal nucleus o f M cv
в
n ert in the ros-
tral brainstem project to m ost parts o f the thalamus, where
they constitute about 9 0 % o f brainstem afferents. They
relay to all parts o f the neocortcx, terminating in synapses
that release the neurotransmitter acctv lch o lin e. These cho-
linergic neurons excite fast nicotinic and slower muscarinic
receptors, and have indirect inhibitory effects through
G A B A receptors. Cholinergic neurons also project from
the claustrum in the basal forebrain directly to pyramidal
cclls and G A B A interneurons in all parts o f the cortcx
(Section 5.5.4b).
Cholinergic afferents operating through nicotinic
receptors promote intracolumnar inhibition, while those
operating through muscarine receptors reduce some forms
o f inrralaminar inhibition (X ian g e t al. 1 998). These sys­
tems regulate the How ot information in the cortex. They
seem to control selective attention and perhaps conscious­
ness (M cG eh ce and Role 1996; Perry et al. 1999). They are
involved in chc generation o f hallucinations and cognicivc
disorders in conditions such as schizophrenia, epilepsy, and
Alzheimer’s disease (sec Alkondon et al. 2 0 0 0 ).
Inputs from the substantia nigra and ventral tegmentum
also project to the ncocortcx, especially the prcfrontal cortcx.
Their synapses involve the neurotransmitter dopam ine.
Five different receptors tor dopamine are distributed in
distinct regions o f t h e central nervous system. Dysfunction
o f this system is implicated in Parkinsons disease and
schizophrenia.
Fine unmyelinated axons originating in the locus
coeruleu s in the dorsal pons provide a diffuse innervation
ot the cerebral cortex, largely to layer 6 (Levitt and Moore
1979). Neurons from the dorsal portion project to the
visual cortex. Their synapses release the ncurotransmittcr
norep ineph rine. The locus coeruleus is probably associated
with attention and has been implicated in cortical plasticity
(Section 8.2.7h).
Axons trom the raphe nucleus and p o n tin e reticu lar
form atio n project to all cortical areas. Their synapses release
the ncurotransmittcr seroto n in . In the monkev4 visual Figure D a v id H . Hubert. B o rn in W in d so r, C an ad a, in 1 9 2 6 . H e
graduated in m athem atics and physics in 1 9 4 7 and in m ed icin e in 1 9 5 4 ,
cortex, rhe strongest projection is to layer 4. In the cat, there
b oth from M c G ill U n iv ersity in M o n treal. B etw een 195*4 and 1 9 5 8 he
are some serotonin axons in layer 4 during the first tew con d u cted research at th e W alter Reed A rm y In stitu te o f R esearch . In
weeks o f life. In the adult cat, the strongest projection is to 1 9 5 8 he m oved со the lab o rato ry o t S . K ufflcr at th e W ilm c r Institu te o f

layers 1 to 3 (Gu et al. 1990). These projections seem to be
involved in the control o f the sleep-waking cyclc. Synapses
in many cortical cells contain receptors for all these neu-
rotransmittcrs in addition to receptors for glutamate.
Peptides secreted by the Golgi apparatus in the soma o f
nerve cells are carried to the axon terminal, where they act
as neurotransmitters. E n d o ca n n a b in o id s are specialized
neurotransmitters released from the active postsynaptic
membrane. They thus act as retrograde transmitters (see
Section 6.5.3).
Synaptogenesis and changes in synapses that occur
during learning are discussed in Section 6.4.4.
5 .5 .3 R E C E P T I V E F I E L D S O F C E L L S IN
T H E V IS U A L C O R T E X
A neuron within the visual cortex responds when an appro­
priate stimulus tails within a specific retinal area. That area
is defined .is the receptive field o f th e co rtica l cell, and its
position in the retina is Specified by the location ot its center.
Receptive field centcrs arc represented retinotopically
within each layer o f the visual cortex, although this arrange­
ment is perturbed by local random scattering of the same
order o f magnitude as the size o f the receptive fields at each
location (Hubei and Wiesel 1 9 77 ) (Portrait Figures 5.24
and 5.25).
We will sec in Section 5.5.6 that the response ot a corti­
cal cell can be modified by stimuli that fall well outside the
receptive field defined by single stimuli.
Each spiny stellate cell in layers 4A and 4 C o f the visual
cortex receives a direct input trom only one eye. These cells
Jo h n H o p k in s I lo sp ital. In 1 9 5 9 th e w hole lab o rato ry m oved to
H arvard U niversity M ed ical S c h o o l to torm the new D e p a rtm e n t o t
N cu robiology. In 1981 he w on the N obel Prize in M cd icin e w ith
T o rsten N . W ie se l and R og er Sperry.
have circular-symmctric reccptive fields that resemble those
o f either the parvocellular or magnocellular cells in the
L G N that teed into them (Blasdcl and Fitzpatrick 1984).
Thus, their response does not depend on the orientation o f
the stimulus. The other cxcitatory cclls in the primary visual
cortex are pyramidal cells. M ost o f them have elongated
reccptive fields and respond most vigorously to bar stimuli
that are aligned with the long axis. They are said to show
orientation specificity (Scction 5.6.2). They fall into two
classes, simple cells and complex cells, according to the
organization o f their reccptive fields, and their functional
properties.
Each sim ple ccll receives inputs from about 3 0 cclls in
the L G N . The receptive fields o f some simple cells have a
symmetrical (cosinc) distribution o f zones— a central cxcit­
atory zone and two inhibitory flanks (O N -cen ter cells) or
an inhibitory center with flanking cxcitatory zones ( O F F -
center cells). The receptive fields o f other simple cells have
an asymmetrical (sine) distribution o f zones— an cxcitatory
zone flanked by a single inhibitory zone, as depicted in
Figure 5.26. Excitatory zones are known as O N -rc g io n s
bccausc they show an cxcitatory postsynaptic potential
(E P S P ) to stimulus onset and an inhibitory postsynaptic
potential (IP S P ) at stimulus offset. Inhibitory zones arc
known as O F F -r e g io n s because they show an I PSP at stim ­
ulus onset and an F.PSP at stimulus offset (Fcrstcr 1988).

f.rui. i.iv Tontcn N . W ietel. B orn in U p p sala, Sw eden , in 1 9 2 4 . H e
ob tain ed an M .D . a t the K arolinvka In stitu te, S to c k h o lm , in 1 9 5 4 and
was p o std o cto ral fellow and assistant professor in o p h th alm o lo g y a t the
Jo h n s H op kins U n iv ersity M ed ical S c h o o l from 1 9 5 5 to 1 9 5 9 . In 1 9 6 0
he m oved to H arvard M ed ical S c h o o l, where he becam e R o b ert
W in th ro p professor o f n cu robiolog y. In 1 9 8 3 he m oved to the
R ock efeller U n iv ersity in N ew York, w here lie wav V in cc n t and Brooke
A sto r Professor o f N cu ro b io lo g y and university president from 1 9 9 2 to
1 9 9 8 . H e is now presid en t em eritus. In 1 9 7 8 to 1 9 7 9 lie was president
o f th e S o ciety tor N euroscience. H e has received m any hon ors,
in clu d in g th e 1981 N obel Pri/.c in M ed icin e w ith David H u b c la n d
R og er Sperry, tlic Fricndcnw ald Award o l th e A ssociation for Research
in V ision and O p h th a lm o lo g y in 1 9 7 5 , th e K arl Lash Icy Pri/.c o t the
A m erican P h ilo sop h ical S o c ie ty in 1 9 7 7 , th e L cd lic Prize from H arvard
U n iv ersity in 1 9 S 0 , and the H elen K eller Prize tor V isio n Research in
1996.
-+ Ч --
(a)
n ^ -
(b)
Figurc$.2 l. Types o f rcccptivcficU . (a) A n O N -c c n te r rcccptivc field o f
a ganglion c c ll. (b ) A n O F I ’-c c n tc r rcccptivc field o t л ganglion ccll.
( c ) - ( g ) R cccp tiv c fields o f sim ple cclls in cat visual co rtex . T h e rcccptivc
fields arc show n w ith preferred o rien ta tio n s o t 4 5 * . (AdjpuJ from Hubd*ml
Wioc* 1962)
Tlic inhibitory potentials sharpen responses ro briefstimuli
and improve orientation selectivity.
In V I o f rhe monkey, simple cclls with a single excit­
atory zone receive excitatory inputs from only the parvocel-
lular or only the magnocellular layers o f the I.G N . Some
simple cells have multiple excitatory zones and may receive
mixed parvocellular and magnocellular inputs (Malpeii
et al. 1981).
Tlic frequency o f response of a simple cell to a stimulus
filling its receptive field is a linear sum o f its responses
to spots of light falling in each O N and O F F zone of its
receptive field. Thus, simple cells integrate luminance in a
linear fashion. M ost simple cclls have little or no main­
tained discharge in the absence o f stimulation. A simple
cell does not respond to even illumination of its receptive
field, because, with even illumination, excitatory responses
are canceled by inhibitory responses. As a dark-light grating
o f appropriate spatial frequency and orientation is moved
over the receptive field of a simple cell the response of the
ccll is maximal when the bright bars coincide with the
O N -zones and zero when they• coincide with the O F F -
zones. The ccll acts as a half-wave rectifier with rcspccr to
the spatial distribution ot dark-light bars falling within its
rcccptivc field.
The full range of stimulation is covered because simple
cells occur in pairs with opposite spatial phase— sine and
cosine (Heeger 1992b). Elongated G abor patches, as defined
in Section 4.4.2, provide a reasonable fit to the 2-D response
profiles o f simple cells in the visual cortex o f the cat (Jones
and Palmer 1 9 87 ) and of the monkey (Ringach 2 0 0 2 ).
In spite o f their basic linearity, simple cells show three
types o f nonlinearity— their response saturates at high
stimulus contrasts, they respond more rapidly at high
contrasts, and their response to superimposed orthogonal
stimuli is less than their response to a stimulus in one orien­
tation (cross-orientation inhibition). These nonlinearities
could arise from a gain-control mechanism that depends
on scaling (dividing) the cell’s response by the pooled activ­
ity o f neighboring cclls— a process called norm alization
(Carandini and Heeger 1 994). Normalization makes it pos­
sible for a cells response to critical features o f the stimulus,
such as motion, orientation, and binocular disparity, to be
independent o f stimulus contrast.
The receptive fields of co m p lex cells are not clearly seg­
regated into excitatory and inhibitory zones. This causes
them to integrate luminance in a nonlinear fashion. A grat­
ing drifting across the rcccptivc field o f a simple ccll pro­
duces a modulated response. However, the same stimulus
produces an unmodulated response in complex cells. Even
so, complex cells are selectively tuned for orientation,
spatial frequency, and direction of motion.
Hubei and Wiesel (1 9 6 8 ) found that many cortical
cells have inhibitory zones at either one end ot their recep­
tive field (single end-stopped) or at both ends (double
end-stopped).
 Simple cells tend to be stellate cells and complex cells
tend to be pyramidal cells. However, this correlation
between structure and function is noc perfect (G ilbert and
W iese1 1979). In Hubei and W iesels hierarchical model,
simple cells teed inco complex cclls. G hosc ec al. (1 9 9 4 b )
revealed only polysynaptic excitatory connections from
simple to complex cells and monosynaptic excitacory co n ­
nections from complex to simple cells in che cat. There is
evidence that the phase invariance o f complex cells arises
from recurrent cortical inpucs from ocher complex cells
rather than from a pooling o f inpucs from a sec o f simple
cells wich differing phase sensitivities (C h an ce ec al. 1999).
Som e complex cells receive inpucs trom only rhe parvo-
cellular o r only che magnocellular layers o f chc I.G N . Ocher
complex cells receive a mixed input (Malpeli et al. 1981).
The structure o f receptive fields o f cortical cclls is dis­
cussed in more detail in Section 5.6. M ost cells in the visual
cortex o f cats and primates receive inputs from both eyes
(Section 5.7.2). These binocular cells therefore have two
receptive fields, one in each eye.
There is a predominance o f simple cells in the primary
visual cortex o f cats. In the monkey, no more than 2 2 % o f
cells in V I were designated simple by the spatial mapping
criterion. However, by the criterion o f response modulation
to a drifting grating, about 5 0 % o f monkey V I cells were
designated simple ( O ’K e efeeta l. 1 998). Kagan et al. ( 2 0 0 2 )
used both criteria on the same cells and found that 14% o f
cells were simple cells with nonoverlapping responsive
zones and 7 8 % were complex cells with overlapping zones.
They suggested that high estimates ot the number o f simple
cells by the modulation criterion arose from classifyingcells
with overlapping zones as simple cells.
Wc will see in Section 5.6.2b that the orientation tuning
o f cortical cells is at least partly determined by interac­
tions between simple and complex cells and inhibitory
interneurons.
5.5.4 VISUAL C O R TIC A L P R O JEC TIO N S
5 .5 .4 a P rim a ry In p u ts to th e V isu a l C o r t c x
The primary visual cortex in each hemisphere is mainly on
the banks o f the calcarine sulcus. This is the deep horizontal
fissure on che medial surface o f the occipical lobe ac the
caudal pole o f chc ccrebral corccx. The visual corccx o f sub-
primates is known as Brodm anns area 17. In primaces, it is
referred to as V I . It is also known as the striate co rtcx
because o f the prominent stripe o f Gennari it contains.
Each optic radiation projects from the main layers o f
the L G N to form the m ajor inpuc со che ipsilateral primary
visual cortex. Intralaminar neurons in the L G N also projecc
to che visual cortex. Som e L G N afferents bifurcate and
project to both V I and V 2 (Kennedy and Bullier 1985).
'Ihc recinocopic order o f incom ing axons in chc primary
visual corccx o f each cerebral hemisphere is preserved.
The cencral parts o f che recina are represented near che
caudal pole o f the occipital lobe, and the monocular cres­
cents are represented more rostrally. The vertical meridian is
represented along the border between V I and V 2. Each
hemisphere receives a topographic representation o f che
concralaceral halt ol visual space.
Monkeys have direcc visual inpucs со M T from konio-
cellular cells o f che L G N (Sin cich ecal. 2 0 0 4 ) . Koniocellular
cells have large receptive fields and cheir input to M T could
account for che survival o f some sensicivity со mocion in the
absence o f V I ( B a r b u r e ta l. 1993).
5 .5 .4 b O t h e r Inputs to th e V isual C o r tc x
The lateral geniculate nucleus is not the only subcortical
nucleus to send inpucs со che visual corccx. The neocortex as
a whole, including che primary visual cortex and other visual
areas, receives inputs from more chan 2 0 subcorcical areas.
These include the nucleus o f Meynerc, che subscancia nigra,
che locus coeruleus, and che poncine reticular system chac
were mentioned in Section 5.5.2g. They also include the
superior colliculus, hypothalamus, the pulvinar, and the
claustrum.
The pulvinar is part o f che thalamus wich a neural struc-
ture similar to chat o f che L G N . Ic is noc evident in small
mammals. Ic increases in relacive size in primaces, and espe­
cially in humans. There are some direcc inputs from che
concralaceral eye, buc che pulvinar receives most o f its
inputs from the ipsilateral cerebral cortex. Ic sends recipro­
cal conncccions со V I , V 2 , V 4 , M T , and che parietal, infcr-
occmporal, and prefrontal cortcx (see Stepniewska 2 0 0 4 ).
There are also connections from the pulvinar to audi­
tory and somatosensory areas (Adams e t al. 2 0 0 0 ; Gutierrez
ec al. 2 0 0 0 ) . The pulvinar contains a crude map ot the co rti­
cal sheet, including ac lease cwo reprcsencacions o f che visual
field. However, representations o f neighboring cortical
areas overlap, which provides for indirect inceraccions
bccween cortical areas. The overlap regions in the pulvinar
correspond to regions with direct cortical interactions. This
is referred to as the "replication principle” (Shipp 2 0 0 3 ) .
The pulvinar is implicated in the control o f visual atten­
tion (Robinson and Petersen 1992; Levitt ct al. 1995;
G riev eetal. 2 0 0 0 ) . It probably processcsstimuli that require
rapid responses, such as visual looming, that signifies
impending collision (K ing and Cowey 19 9 2 ; Mcscre ec al.
1 9 9 2 ; Beer e ta l. 2 0 0 2 ) .
Responses o f some cclls in che pulvinar arc niodulaced
by the posicion o f the eyes, like responses o f cells in the pari­
etal cortex. These cells chus code signals in a hcadcentric or
bodycentric frame o f reference. Som e pulvinar cells respond
before the onset o f self-initiated arm movements, even
before responses occur in the primary motor cortex or
posterior parietal cortex (Cudeiro et al. 1 989).
'Ihc claustrum is a narrow band o f neurons in the basal
forebrain with reciprocal connections with many areas o f
chc cerebral cortex, including visual, somatosensory, and
auditory cortical areas. O n e part oi the claustrum contains
a topographical map o f the contralateral visual held and
binocular cells sensitive to stimulus motion and orienta­
tion. In the cat, claustral affcrents project to layers 1 ,6 , and
4 o ft h e visual cortcx. Som e affercnts that reach layer 4 co n ­
tact inhibitory interneurons and seem to be involved in
i
end-stopping o f receptive fields (Sherlc and LeVay 1983;
LeVay 1986; Edelstcin and D enaro 2 0 0 4 ) .
The primary visual cortex also receives inputs from
higher visual centers in the cerebral cortex, including the
temporal occipital area (D isder et al. 1 9 9 3 ), M T (Section
5.8.4b), and the lateral intraparietal area ( L I P ) (Felleman
and Van Essen 1991).
Recent evidence indicates that V I receives inputs from
the auditory cortex and from the polysensor у area o f the
temporal lobe (Falchier et al. 2 0 0 2 ) . These inputs could be
involved in the take over o f the visual cortex by auditory
inputs in the congenitally blind (Section 8.1.4b).
5 . 5 . 4 c C o r t i c a l M a g n ific a tio n F a c to r
The co rtica l m agnification facto r (M ) is the distance in
millimeters between two points on the surface o f t h e visual
cortex that corresponds to one degree o f visual angle in the
visual field (Daniel and W hitteridge 1961). The distances
can be measured along radial (isopolar) lines or along isoec-
centricity lines. The two measures, which are n ot the same,
may be combined ro yield an areal m agnification factor,
which is the area (in m n r ) o f cortex devoted to each area o f
visual angle (in deg2).
The area of cortex devoted to the fovea is disproportion­
ately greater than that devoted to the peripheral retina.
A bout 3 0% o f the human visual cortex is devoted to the
central 3° o f the retina. In the macaque M is about 16 mm/°
at the fovea. Also, more visual cortex is devoted to the lower
visual field than to the upper visual field (Van Essen et al.
1984; Tootell et al. 1988d ).
The right and left eves are represented in the visual
cortex bv alternate ocular dominance columns. The col-
umnsrun mainly parallel to the vertical meridian. Therefore,
the magnification factor should be about twice as large
across ocular dominance columns than along them. Sakitt
(1 9 8 2 ) claimed that, in the macaque monkey, the visual
cortex extends about twice as far across to ocular d o m i­
nance columns than it does parallel to the columns. Tootell
c t al. ( 1 9 8 8 d ) agreed that there could be some expansion o f
cortical representation perpendicular to ocular dominance
columns buc pointed out that the shape of the visual cortex
varies widely from animal ro animal and provides no basis
for inferring the anisotropy o f cortical magnification.
Blasdel and Cam pbell (2 0 0 1 ) used an optical technique to
map the projection o f the retina on the monkey visual
cortex with great precision. In the foveal region the ocular
dominance columns are perpendicular со the border
between V I and V2. Magnification was 1.5 greater along
the vertical meridian (across ocular dom inance columns)
than along the horizontal meridian. In monkey V 2 , cortical
magnification was reported to be about 1.5 greater across
stripes than along stripes (Shipp and Zeki 2 0 0 2 b ).
In primates, M decreases with increasing retinal eccen­
tricity. Cowey and Rolls ( 1 9 7 4 ) estimated M for humans
from impressions o f light (phosphenes) evoked by elec­
trodes implanted at various locations on che visual cortex
(sec Brindley and Lewin 1968). At an eccentricity o f 2°,
M was approximately 4 mm/° and declined monotonically
to 0.5 mm/0 at an eccentricity o f 25°. Another estimate puts
M at 11.5 mm/° for the human fovea (Drasdo 1977).
The change in the magnification factor as a function o f
eccentricity is known as M scaling. For all positions in che
visual field, a microeleccrode must move between 2 and
3 mm over the surface o f the monkey visual cortex before an
entirely new region o f t h e visual field is represented (Hubei
and Wiesel 1974a). This suggests that the same number o f
millimeters o f visual cortex is devoted to each ganglion-cell
receptive field. O n e estimate is that 0 .8 8 mm o f human
visual cortex is devoted to one ganglion-cell receptive field
(Ransom -H ogg and Spillmann 1980). It follows that the
cortex devoted to each degree o f visual field is directly
related to the mean size o f ganglion-cell receptive fields
(Rolls and C ow ey 1970; Rovamo and Virsu 1979; Virsu
and Rovamo 1 979). But the mean size o f receptive fields is
inversely related to visual acuity.
In summary, ganglion-cell receptive fields, and hence
areas o f the retina that can just resolve two stimuli, are rep­
resented by equal areas in the visual cortex. Because gangli­
on-cell receptive fields are smaller and therefore denser in
the fovea than in chc periphery o f the retina, the fovea
claims proportionately more of the cortical surface (M is
greater). W h en allowance is made for the decrease in
M with increasing eccentricity, grating resolution, vernier
acuity, and stercoacuity are about the same at all eccentrici­
ties (Levi et al. 1 985). Thus, visual hyperacuity depends on
the number o f processing units in the visual cortex that are
devoted to a task irrespective o f retinal location. A com pli­
cating factor is chat receptive fields in the central retina are
fine enough to provide an adequate sampling o f t h e image
produced by the eyes optics, but receptive fields in the
periphery undersample the image.
There has been some dispute about whether the varia­
tion in M arises simply from differential density o f ganglion
cclls over the retina, or, w hether each foveal ganglion ccll
feeds into more cortical cells than each ganglion cell from
the peripheral retina. In the macaque, Wassle et al. ( 1 9 9 0 )
counted three to four ganglion cells for each foveal cone,
one ganglion cell per cone at an eccentricity o f about 15°,
and many more cones than ganglion cells in the periphery.
They concluded that che 1 0 0 0 -to -l change in ganglion
ccll density with increasing eccentricity accounts for the
change in M.
 Azzopardi and Cow cy ( 1 9 9 3 ) cam c со chc opposite
conclusion. They used a retrograde tracer со determine
directly the number o f ganglion cells projecting со mea­
sured areas o f the seriate cortex o f the macaque monkey.
Foveal cones were allocated 3.3 times more corcical cissuc
than peripheral cones in one animal and 5.9 times more in
a second animal (see also Perry and Cowev 1985).
Using che same recrograde cracer method, Azzopardi
et al. ( 1 9 9 9 ) showed thac chc racio o f parvocellular со mag­
nocellular units in the macaque L G N decreased from a
mean o f 35:1 at the fovea to 5:1 at an eccentricity o f 15°.
However, the fovea was represented ac higher levels in the
visual system to a greater extent than predicted trom gangli­
on-cell density. Popovic and Sjostrand ( 2 0 0 1 ) came to rhe
same conclusion from an analysis ot human visual resolu­
tion and ganglion-cell density, and chc paccern o f f M R I
responses trom human V I as a function ot the area ot a
rotacing checkerboard (Engel ec al. 1997).
Bijl ec al. ( 1 9 9 2 ) produced psychophysical evidence chac
changes in ganglion-cell densicy account for the variation
o f concrasc sensitivity over the visual field for high spatial
frequencies. However, they found thac, for low spatial fre­
quencies and for the detection o f localized disks, perfor­
mance depended on variations in both ganglion-cell density
and the degree o f overlap o f receptive fields, especially in
the nasal hemifield.
It has also been claimed that, for the parvocellular
system, the number o f afferents from the L G N per unit area
o f VI is nearly constant. However, for magnocellular
system, the number o f afferents per unit cortical area
increases steeply with increasing eccentricity (Schein and
Monasterio 1987). There is a constant number ot m agno­
cellular afferents per point image, defined as the area of'
cortex activated by a stimulus at a point in space. This is
equivalent to che number o f recepcive-field centers of'
ganglion cells chac overlap a given poinc on the retina.
5 .5 .4 d T o p o lo g y o f C o r tic a l M ap p in g
Schwartz ( 1 9 8 0 ) described the mapping o f the retina onto
the primary visual cortex by che conformal logarithmic
function,
(0 = * Io g (z + rf) (3)
where 2 is a complex number denoting the position ot a
point on the retina, 0) is a complex number representing the
position o f the stimulus on the cortex, and k and a are co n ­
stants. A function is conformal i f its first derivative (in this
case che magnification factor) is isotropic (independent o f
orientation) and if the sizes ot local angles are preserved.
S c h ira e ta l. (2 0 0 7 ) used f M R I to derive che mapping o f
V I and V 2 in humans со within 0.5° o f the center ot the
retina. 'Ihey found thac the complex-log funccion overesti­
mated the dependency ot the areal magnification factor on
radial direction near the fovea. They derived a modified
version o f the function that provided a good fit to their
data. Their function contains a shear factor that corresponds
to the magnification factor being larger across ocular
dominance columns than along them.
Schwartz ( 1 9 8 0 ) illustrated how, in a logarithmic m ap­
ping, the cortical images ot squares of different sizes are
transformed into images o f rhe same size and shape, but in
different locations. In a similar way, retinal images that arc
rotated with respect со each other are transformed into
images differing in spatial phase. Schwartz argued that the
recognition o f size- and orientation-invariant features in
the image formed by such a system reduces to the com puta­
tionally simpler process o f deriving translation-invariant
properties. According to this view, the logarithmic retin-
ocortical mapping is part o f a process for extracting size-
and orientation-invariant properties o t visual objects.
O n e problem wich chis theory is that the invariance
applies only to images centered on the fovea. The image ot a
given o b ject changes in size and shape as it is translated over
the retina (see Cavanagh 1982; Schwartz 1 983). Another
problem is that this theory o f shape recognition is essen­
tially a template-matching model. Such a model applies
only to very simple invariant features.
But there is a deeper problem associated with any theory
o f o b ject recognition based on the topology o f corcical
mapping. The geometrical layout o f the cortical “image” is
n ot represented in the activity o f cortical cells. Corcical cells
code che local sign o f their origin on che retina not their
location in the cortex. All features are coded in che central
nervous system in terms o f ccll connections and the simul­
taneous and successive patterns o f cell firing, not in terms o f
che spacial dispositions o f cells on the corcical surface. The
notion o f a topographic code, in the sense ot the spatial
arrangement o f cells over a surface, ceases to have any sig­
nificance beyond the retina. Spatial maps in the cortex
demonstrate со an experimencer where spatial information
is processed but, tor the perceiver, the spatial organization
o f the stimulus is represented only by spatiotemporal
patterns ot neural connections.
Cortical mapping in V I in each hemisphere has four
prominent features:
1. 1,be mapping is approximately M -scaled "I his allocates
equal space in the cortex to equally discriminable
regions o f oculocentric space.
2. The mapping is topographic Ic preserves the spatial order o f
inputs. However, cortical mapping is discontinuous across
the visual hemifields, and alternating columns ot visual
cortex in each cerebral hemisphere are devoted to each
eye (Section 5.7). Laceral inhibition is required only
between cclls that are near neighbors because lateral
inhibition serves со attenuate che response from regions
o f local homogeneous activity, thus accentuating the
response from regions wich high gradients o f activity.
 This ensures thac information regarding changes in as layer 4 C p , and in layer 4 Л (Hubei and W iesel 1977;
stimulation passes to the next level o f analysis, thereby Toocell ec al. 1988a). Cells in che middle o f layer 4 C receive
economizing on information transmission (Barlow 1961). inpucs from layers 4 C a and 4 C / J . and therefore inputs
Also, pooling of spatial anti other information is required from both parvocellular and magnocellular layers o f the
more often over small regions than over larger regions. L G N (see Yoshioka cc al. 1 994). Som e L G N inpucs, prob­
Thus, keeping spatially contiguous regions together ably W cells, projecc со superficial levels o f layer 3 and
economizes on chc lengths o f dendritic connections. sparsely со layer 1, ac lease in che cac and squirrel monkey
(Ficzpatrick e t al. 1983).
3- The mapping prorides uniform coverage for each featu re
Layer 4 B o fth e visual cortex contains a dense horizontal
Each cortical location contains a complete set o f cells
plexus o f myelinated axons. A majority o f cells are pyrami­
tuned to che following visual features: eye o f origin,
dal cells and a minority are spiny stellate cells. Magnocellular
color, orientation, spatial frequency, and motion
cclls in layer 4C o r project mainly ro the spiny stellate cells
(Swindale et al. 2 0 0 0 ).
in layer
/ 4 B in the same 1-mm-wide vertical column o fco rti-
4. The mapping is continuousfo r each featu re In each cal tissue (Yabuta er al. 2 0 0 1 ) . The spiny stellate cells receive
location, the different values o f orientation preference only magnocellular inputs and pass them on со layers 2 and
and mocion preference are mapped in order, wich 3 in che same column and со neighboring columns (Katz
discontinuities at chc end o f each sequence o f feacure et al. 1989). Many pyramidal cells o f layer 4 B receive both
values (Das and G ilbert 1 997). These mappings are parvocellular and magnocellular inputs (Sawatari and
discusscd more fully in Section 5.7.1. An ordered Callaway 19 9 6 ; Yabuta and Callaway 1998). We will see
mapping juxtaposes cells that process similar features later that cells in layer 4 B that carry magnocellular signals
within a local region o fo cu lo ccn tric space, so that local project to M T in che dorsal stream ot visual processing,
neural processes, such as facilitation and inhibition, can while those carrying mixed signals project со V 2 .
be achieved economically. Parvocellular cells in layer 4 C(3 projecc abundandy Co
blob and incerblob regions o f layers 2 and 3. These regions
T he responses o f some cells in the primary visual cortex are defined in Section 5.6.6.
and other visual areas are modulated by the direction o f Layer 4Ccc also projeccs sparsely со layer 5, and layers
gaze (see Sections 5.8.4c). 4 C a and 4 С Д project sparsely to layer 6.
Many cells in layers outside layer 4 are binocular. Layers
2 anil 3 project strongly to layers 5 and 6, which project
5.5.5 C O R T IC A L LAYERS
back inco layers 2, 3, and 4 (Gilberc and W iesel 1979;
The mammalian visual cortex is a convoluted sheet o f tissue Ficzpatrick et al. 1985). These relationships are shown in
about 3 mm thick. It consists o f six main layers designated Figure 5.27.
layers 1 to 6, with layer 1 at the outer surface and layer 6 Pyramidal cells in layer 5 o f rhe monkey V I receive
bordering the inner white matter. Details o f cortical layers inputs trom all other layers, but mosc o f chcm do noc
are presented in Section 6.4.2. Layer 4 is known as the gran­
ular layer. O th er layers are extragranular. The white matter
consists o f bundles o f axons that project to and from sub­
cortical nuclei and between cortical regions.
The primary visual cortex o f t h e cat (area 17) receives
inputs from chc A laminae o f che L G N — the laminae where
X ganglion cells ccrminate. C ortical area 18 receives some
inpucs from che A laminae and from chc С laminae— chc
laminae where Y ganglion cells terminate. Area 19 receives
inputs from che С laminae and from cxcrageniculacc cell
groups (see Hollander and Vanegas 19 7 7 ; Pasternak ec al.
1995).
The primary visual cortex o f primates ( V I ) receives
inputs from all the main laminae o f t h e I.G N . Inputs from
each eye project to distinct spiny stellate cells in layer 4.
Inpucs from L G N intcrlaminac reach ochcr cortical and
subcortical areas (Section 5.8).
Inputs from the magnocellular laminae o f t h e primate
L G N terminate in spiny stellate cclls in the upper half o f
layer 4 C , known as layer 4 C a . Inputs from the parvocel­ s. 2 " . In rracorticalconnections o f th e car's visu al cortcx. The num bers refer
lular laminae terminate in che lower half o f layer 4 C , known to layers o f chc visual co rtc x . (AtL*«c<J frvm Gilbert iod Wk»cI ]$№)
project out o f V I . Instead they form feedback connections
with cells in layers 2 and 3, and 4 B (Briggs and Callaway
2 0 0 5 ).
The major output from V I to V 2 arises from pyramidal
cclls in layer ЗА (Lachica ct al. 1992). Axons from pyrami­
dal cells in layer 6 o f the primary visual cortex project to the
thalamus and claustrum.
Cell connections in the visual cortcx have been reviewed
by Henry ( 1 9 9 1 ) , Valvcrde ( 1 9 9 1 ) , Peters and Rockland
( i 9 9 4 ) , and Callaway (1 9 9 8 a ).
5.5.6 LATERAL C O R TIC A L C O N N E C T IO N S
5 . 5 .6 a E x c it a t o r y L ateral C o n n e c t i o n s
M ost excitatory and inhibitory synaptic connections onto
cortical neurons arise from other cortical neurons. Collaterals
from the axons o f pyramidal cells in primate cortical layers 2,
3 , 4 , 5, and 6 o f V I and V 2 project horizontally up to 8 mm.
This represents several reccptive-field diameters.
O ptical recording from the surface o f the visual cortex
in conjunction wich microelectrode recording has revealed
that a local visual stimulus induces neural spikes in a small
area and subthrcshold activity over a wider area (Das and
Gilbert 1995a). By applying a voltage-sensitive dye to the
visual cortcx o f the monkey, one can observe the spread o f
neural activity evoked by a locally applied visual stimulus in
real time. Activity was found to spread over the cortex Irom
its initial locus at a velocity o f between 100 to 2 5 0 JUm/s.
The activity covered an area with a radial space constant ot
1.5 mm along ocular dominance columns and o f 3 mm
orthogonal to the columns (Cirinvald e t al. 1994).
According to one escimate, derived from horseradish
peroxidase labeling, 8 0 % ol horizontal connections are with
other pyramidal cclls and are excitatory, while 20 % are with
smooth inhibitory interneurons (M cG uire ec al. 1991).
However, chese anatomical differences do n ot determine
che relacive screngths ot inhibitory and excitatory co n nec­
tions, because the effects o f inhibition could be amplified
relative to the effects o f excitation. In monkey V I , surround
suppression is most extensive in layer 4 B , while surround
summation is most extensive in layer 6 (Sccniak et al.
2001).
Excitatory horizontal projections from pyramidal cells
are typically longer along one axis and produce spaced clus­
ters o f predominantly excitatory synapses (Rockland and
Lund 1982, 1983; G ilbert and Wiesel 1985; Rockland
1985). These long excitatory connections have been investi­
gated by retrograde tracing with 2-dcoxyglucose, by corre­
lating discharges o f pairs o f cells over various time delays.
They have also been investigated by autoradiography after
monocular stimulation by differently oriented gratings
(Schm idt ct al. 1997a).
These procedures have revealed that, in rhe cat, long-
range excitatory connections link pyramidal cells with a
similar preference for stimulus orientation (Nelson and
Frost 1 9 8 5 ; T so et al. 1986; G ilbert and W iesel 1989;
Hirsch and G ilbert 1991). The same preferential linkage
has been found in layers 2 and 3 o f the visual cortex o f tree
shrews ( B o s k in g c t al. 1997) and in layer 3 o f squirrel and
owl monkeys (Sincich and Blasdel 2 0 0 1 ).
Thus, cclls with axially aligned receptive fields are co n ­
nected more richly than cclls with parallel receptive fields,
which in turn are connected more richlvi than cclls with dis-
tinct orientation preference. W e will see in Section 5.5.6c
that connections between aligned receptive fields could
enhance the visibility o f continuous edges.
Retrograde tracing has revealed that lateral connections
in cortical layer 6 have relatively small terminal clusters and
originate in giant Meynert cells (Rockland and Knutson
2001 ).
In primates with strong ocular dominance columns, any
anisotropy o f lateral connections related to orientation
tuning o f cells is difficult to detect because it is masked by
an anisotropy related to eye dominance. Stettlcr ct al.
( 2 0 0 2 ) infected cells in a local area o f V I o f the macaque
with an adenovirus that expresses a green fluorescent
protein ( G FP). The protein spreads to all parts ot an infected
ccll, but n ot to other cells. Figure 5 .2 8 Л shows chc laceral
spread ot pyramidal cells traced trom a stack of images p ro­
duced by a confocal microscope. The connections spread
over a diameter o f about 7 mm, which corresponds to abouc
4° o f the visual field at an eccentric icy o f 4°. Theconneccions
cover between eight to ten orientation columns. Beyond
the first Г , they show a 0.5° periodic clustering that matches
the periodicity o f columns defined by orientation tuning.
Stettlcr et al. used the same procedure to map the lateral
connections in V I formed by feedback from V 2 . Figure
5 .2 8 B shows these connections. They spread over about the
same area as the intrinsic connections buc less densely. They
show some periodic clustering, but chis does noc match the
periodicity o f orientation columns.
Adorjan et al. (1 9 9 9 ) developed a model o f orientation
tuning based on intracortical excitatory connections.
Lateral linkages are more com m on between columns ot
the same ocular dominance than between chose o f opposice
dominance and becween blobs and blobs or interblobs and
incerblobs chan bccween blobs and inccrblobs (Livingscone
and Hubei 1984; Yoshioka ec al. 1996). Binocular regions
o f chc visual corccx arc nocconnccccd со monocular regions
(M alach et al. 1993).
5 .5 .6 b In h ib ito r y L a tera l C o n n e c t i o n s
Estimates, based on eleccrophysiological recording, o f che
percentage o f cells in che visual cortex ot che cat chac exhibit
surround suppression vary from 10% to 80% . Buc some
investigacors used a criterion o f 100% suppression while
others used less srringenc criteria. Also, some investigators
measured inhibition only from the end o f the receptive

1 mm
------- 1 A 3 2 out o f 37 cells. For most of these cells, suppression was
i'
В grating. For binocular cells in all cortical layers, there
Figure s.is. L a te r a l connections in 17 . (A ) H o rizo n tal c o n n e ctio n s from a
lo cal region in th e upper layers o f m acaque V I . The cen tral region is left
b lan k . ( B ) Feed back c o n n e ctio n s in layer 1 o t V I arising from all layers
o f a lo cal region in V 2 . (From Stcttlcr ct aL 2 0 0 2 " . t h pcrtnm iun In x a KUrvici)
field, while others measured inhibition all round the
rcccptivc field.
Short-range and mainly inhibitory connections in area
17 ot the cat extend up to 8 0 0 Цт . They decline in number
with increasing distance from a given point on the cortical
surface. In contrast to the patchy arborization ol long-range-
excitatory lateral axons, these short-range connections are
largely circular symmetric and independent o l orientation
preference ( К ritz cret al. 1992; B o sk in g etal. 1997).
Das and G ilbert ( 1 9 9 9 ) measured the strength o f the
largely inhibitory connections between pairs o f neurons in
the upper layers o l cat area 17 as a function o f their lateral
separation and orientation tuning. The strength o f co n n e c­
tions declined with increasing separation of the Stimuli and
was largely independent o f the orientation tuning o f the
cells at separations up to 8 0 0 ,Um, O ptical imaging was
used to plot the pattern o f orientation preference o f cclls
over the cortical surfacc. In regions where orientation pref­
erence changed smoothly, neighboring pyramidal cells
had similar orientation tuning and overlapping receptive
fields. Das and G ilbert suggested that inhibitory interac­
tions between such cells sharpen their orientation tuning.
In regions where orientation preference changed rapidly
(pinwhcels), neighboring cells had distinct orientation
tuning and nonoverlapping receptive fields. They suggested
that interactions between these cells are associated with
processing features such as corners and T-junctions.
Sengpiel et al. ( 1 9 9 7 ) measured responses o l cortical
cells in cat area 17 to an optimally oriented grating filling
the receptive field as a function o f the orientation of a sur-
roundinggrating. S o m e surround inhibition was evident in
weakest when the two gratings were orthogonal. For other
cells, inhibition was weakest when the gratings had the
same orientation. O th er cells showed maximal inhibition
at flanking orientations or over a wide range of relative
orientations.
The response o f a cortical cell should increase as an opti­
mally oriented grating increases in size to fill the cell’s recep­
tive field. Further increases in the size o f the grating should
reduce the cclls response. Walker ct al. ( 2 0 0 0 ) investigated
this question by recording responses of cells in cat area 17 to
circular optimally oriented gratings. As the size o f the grat­
ing was increased, the responses at first increased and then
leveled off’ as the grating filled the rcccptivc field. W ith fur­
ther increase in size, the grating extended beyond rhe classi­
cal rcceptivc-field and the response of 5 6% o f simple and
complex cells fell by between 10% and 100%. There was no
correlation between suppression and the orientation of the
was very little surround suppression for stimuli presented
separately to the two eyes.
In the cat, there is evidence o f inhibitory interactions
in the L G N (O zeki et al. 2 0 0 4 ) . Matsubara et al. ( 1 9 8 5 )
found lateral interconnections in area 18 ot the cat
between cortical cells with orthogonal orientation prefer­
ences. These connections spanned only 2 mm and were
inhibitory (G A BA ergic).
Buhl et al. ( 1 9 9 4 ) described three types o f local inhibi­
tory interneurons in th eh ip p o ca m p u so fth e rat. (1) “Basket
cells” synapse on the somata ot principal cells and cause
rapid hyperpolarization followed by rebound. These cells
could cause synchronous firing o f large cell populations.
(2) “Axo-axonic cclls” synapse only on the initial segment
o f the axon o f the principal cells. They seem well suited to
control the discharge o f principal cclls. (3 ) “Bistratified
cells” make synaptic contact with the base and apical den­
drites ot principal cells and have properties like those ot
Hebbian synapses (Section 6.5.1).
There is thus a division o f labor between different in h ib­
itory interneurons in controlling the synchronous activity
ot cortical cells. M ost inhibitory connections arc local,
buc only a few long-rage connections arc required со induce
long-range oscillatory activity (Buzsaki et al. 2 0 0 4 ).
Szabadics ct al. (2 0 0 1 ) found similar inhibitory nccworks
in the somatosensory cortex o f the rat. It is not vet known
4 в
whether similar inhibitory nccworks exisc in che visual
corcex.
W e will see in what follows chac che balance o f excita­
tion to inhibition in chc visual corcex depends on che rela­
cive posicions,orientations,spacial frequencies, and eoncrascs
o f stimuli. Furchermore, inhibicory and excitacory effeccs
may occur in che same cell with different latencies.
5 .5 .6 c F u n ction s o f Lateral C o n n e c tio n s
Lateral cortical connections could serve any or all o f the fol­
lowing functions:
1. Response norm alization Lateral inccraccions m ay be
involved in normalization ot the response ot a cortical
cell. Normalization is a nonlinear process that divides
the response o f a cortical cell by the pooled response o f
surrounding cclls (Carandini and Hcegcr 1994). It
renders the response o f cortical cells to features such as
oricncacion, m otion, and disparicy independent o f
stimulus contrast (Section 5.6.2d). Lateral connections
may also be involved in che regiscracion o f chc
brightness o f surfaces (Rossi and Paradiso 1999).
2. Im proved visibility at low contrast Lateral interactions
improve the visibility o f low-concrast stimuli.
According to one cheory, chc screngch o f chc inhibicory
surround ot receptive fields ot cortical cells is reduced at
low contrasts (Somers ec al. 1 9 9 8 ). Sccniak ec al. (1 9 9 9 )
found no evidence o f a consiscent change o f chis kind.
Instead chcv found chac chc extent o f the cxcicatory
region ot receptive fields increased at low contrascs.
They suggesced chac, ac low concrasc, cxcicacory
conneccions develop bccween cortical neurons
with overlapping receptive fields. Ac high concrasc,
these connections are inhibited. This theory also
involves removal o f inhibitory influences at low
contrast.
Interactions between stimuli also depend on their
relative contrascs (Lcvicc and Lund 1997). Stimuli thac
manifest orientation-specific or spatial-frequency-
spccific inhibitory interactions at high contrasts show
mutual facilitation at low contrasts (C an n o n and
Fullcnkamp 1993; Kapadia ec al. 2 0 0 0 ) . The response ot
cells in the ca ts visual cortex со a grating ju st above the
concrasc threshold was facilicaccd by che collinear
flanking gratings with separations up со abouc 12"
(M izobe ec al. 2 0 0 1 ) . Ac higher contrasts, facilitation
was replaced by mutual inhibition. This suggests thac
inhibicory mechanisms have a higher threshold than
excitatory ones. The imporcanc ching ac low concrascs is
со see chc stimuli, even chough they may n ot be clearly
discriminated trom each other.
The visibility* o f a central stimulus at or below threshold
is increased by che addition o f suprachreshold
surrounding stimuli (Knierim and Van Essen 19 9 2 ;
Grinvald c t al. 1 994). This is because noisy fluctuations
in activity due to surrounding stimuli contribute to the
response o f the subthrcshold central stimulus and bring
it into the detectable range by a process known in
physics as response reson an ce. This type o f interaction
could enhance the visibility o f weak pares o f a paccerncd
stimulus. Stemmier et al. (1 9 9 5 ) have modeled these
inhibitory and facilicacory processes.
3. Sharpening orientation tuning Surround suppression
relatively enhances the response in regions where
orientation changes. It can be understood as a mechanism
tor detection o f orientation contrast. Similarly, human
discrimination o f a change in che oricncacion o f a line is
better when surrounding lines are orthogonal rather dien
parallel to che cesc line (Li ec al. 2 0 0 0 ). These inccraccions
depend on long-range laccral connections. Scccccr ec al.
(2 0 0 0 ) developed a model o f these processes.
4. Detection o f figuralstim uli A region that differs from its
surroundings appears as a figure on aground. Also,
collinear stimuli that define an edge are more visible
than noncollincar stimuli. Both these effects could
depend on lateral conneccions within the visual cortex.
They arc discussed in Section 5.6.7. Lateral connections
may also explain some geometrical illusions, tilt
contrast, and figural aftereffects in which a stimulus
appears displaced away from a neighboring stimulus
(see Howard 19 8 2 , Chapter 4).
5. Comparison o f widely separated stimuli I .ong-rangc
cortical connections could be involved in the task o f
comparing stimuli some distance apart. Kohly and
Regan ( 2 0 0 2 a ) found thac humans could rapidly
compare che oriencacions and locations o f luminance-
defined cesc bars several degrees aparc while ignoring
scimuli placed bccween them. Subjects could noc have
looked from one bar со che ocher because the bars were
presenced for only 160 ms. N or could subjects have
attended to the bars sequentially because the bars were
presented in different locations from trial to trial.
Subjects could perform the same task when the bars
were defined only by motion or only by disparity.
They could do chis even when the two bars were
defined by distinct features (Kohly and Regan 20 0 2 b ).
Kohly and Regan concluded that the visual system
contains a comparator mechanism that mediates fast
comparisons between stimuli some distance apart.
6. Construction o f specialized receptivefields C ortical cells
linked by short-range cxcicacory conneccions could be
 involved in chc construction o f detectors tuned to
specific patterns, such as corners and T junctions. This
would increase the sparseness o f coding and the
effic ienc y o f neural transmission and storage (sec
Scction 4.2.6c). There is physiological and
psychophysical evidence lor angle d e tecto rs that arc
tuned to the angle between lines rather than to the
orientations o f single lines (Sillito e t al. 1995; Heeley
and Buchanan-Sinith 1 9 9 6 ; Regan et al. 1996). Thus,
even at an early stage o f processing in the primary visual
cortex, orientation detectors engage in interactions that
could be involved in the detection o f higher-ordcr
features o f the visual world. In cortical area V 4 , most
cells respond better to angles and curves than to simple
lines (see Section 5.8.3a).
7. M asking The response o f a cell in the visual cortex to a
grating is reduced when an orthogonal grating is
superimposed on the gracing, even when the
superimposed grating is n ot visible when presented
alone. Masking effects o f this kind are usually explained
in terms o f intracortical inhibition or in terms o f
inhibitory influences arising in higher centers. However,
Carandini ct al. ( 2 0 0 2 ) reviewed evidence that masking
is due to depression o f thalamocortical inpucs.
8. Interactions between stimuli in different eyes Lateral
connections are involved in interactions between
dichoptic stimuli. Thus, a cortical ccll that responds
only to excicacory inputs from one eye may be
suppressed by inpucs presented to the other eye
to which that cell does not normally respond
(Scction 11.4.1).
9. Adaptation to scotomata Lateral pathways may be
involved in adaptations to cortical scotomata. For
example, amputation o f a linger in the adult monkey
causes cclls in che affccced region o f che somacoscnsory
corcex со become sensicive со inpucs from adjacenc
fingers (Merzcnich cc al. 1983).
A 10'J lesion in one retina of adult cacs did noc affccc the
recinotopic organization o f the corresponding region o f the
visual cortcx. But after removal of the other eye, cclls serv­
ing the lesioned region began to respond to stimuli in the
adjacent region (Kaas ec al. 1990). Silent regions in the
L G N do n ot recover, so cortical recovery must involve
changes within the cortex.
Schmid e t al. ( 1 9 9 6 ) found that after a local lesion was
induced in one retina o f the adult cat, the corresponding
cortical region began to respond со scimuli applied near che
lesion. Firing races were unusually low and cransicnc. The
change was evident within a few hours after che induction
o f a recinal lesion (Calford ec al. 1998). Local deaccivacion
o f long-range cortical projections abolished these responses
(Calford et al. 2 0 0 3 ).
These facts suggest that inputs arc conveyed to reacti­
vated cortical cells through horizontal axons o f cells with
similar orientation preference (Darian-Sm ith and Gilbert
1995). Part o f this elfccc could be due со a lowering o f the
chrcshold o f horizoncal cclls or chc removal o f G ABA ergic
inhibicory influences around the affected area (Gilbert
and W iesel 1992; Das and G ilbert 1995a; C h in o 1997).
But there is also evidence o f axonal sprouting ol laterally
projecting neurons (D arian-Sm ith and G ilbert 1994).
A localized lesion in one retina o f kittens during the
critical period o f development abolished responses o f cor­
responding cortical binocular cclls to stimulation o f thac
region. However, after some time, che corresponding bin­
ocular cclls began со respond Co scimuli applied со regions
round che lesioned area (C h in o ec al. 2 0 0 1 ) .
A lesion in che monocular zone o f chc peripheral recinal
creaces adeafferenccd region in the contralateral V I of adult
monkeys. After several months, some cells in chc deaffer-
enced region began to respond to stimuli applied to the
boundary o f the retinal binocular zone. B u t most cclls were
unresponsive after a year (R osa ct al. 1995). Thus plasticity
varies with location in the visual cortex.
O ccluding a local region o f the retina creates an artifi­
cial scotoma. O cclusion o f the retinal rcccptivc field o f a
cortical ccll in the cat accompanied by stimulation o f the
surrounding retinal area over a period o f 10 minutes caused
a five-fold increase in the area ot the occluded receptive field
(C h in o cc al. 19 9 2 ; Pecccc and Gilberc 1992).
A local artificial scotoma applied in one eye also
expanded chc rcccpcivc fields o f corcical cclls serving chac
region in che ocher eye (Volchan and G ilbert 1995). This
suggests chac expansion o f the rcccpcivc field is due со
recruitment o f previously subchreshold lateral conneccions.
Orientacion tuning and ocular dominance ot the cells were
not affected, and receptive fields returned со chcir normal
size when scimulaced (D as and Gilberc 1995b).
D cA n gelisccal. ( 1 9 9 5 ) failed со find changes in che size
or scruccurc ot corcical rcccpcivc fields ot cacs during appli­
cation o f an artificial scotoma. They found only short-term
and reversible changes in the responsiveness ot surrounding
cclls. A small stimulus near the boundary o f an artificial sco­
toma was perceptually displaced toward the center ot the
scotoma (Kapadia ct al. 1994).
Thus there is uncertainty about the extent o f cortical
plasticity in the adult cortcx. See Wandell and Sm im akis
(2 0 0 9 ) for a revie w o f this question.
Kalarickal and Marshall (1 9 9 9 ) produced a com puta­
tional model o f these processes, based on plasticity o f in h ib­
itory and excitatory lateral connections.
10. Long-tenn changes in cortical responses Lateral pathways
could be involved in long-term stimulus-dependenc
changes in cortical responses. Long-term changes in
synaptic conduccivicy along laceral pathways in the
ca ts visual cortcx have been induced by pairing
 synaptic responses with conditioning shocks o f
depolarizing current (H irsch and G ilbert 1993).
11. Short-term memory an d attention Local recurrent
neural networks involving a balance between
excitation and inhibition generate patterns o f stable
activity that could be responsible for short-term
memory (Durstewitz et al. 2 0 0 0 ) and the e lfe c ts o f
attention (Shu Y et al. 2 0 0 3 b ).
5 .5 .7 B L IN D S I G H T
In blindsight, residual visual functions are evident in m o n ­
keys lacking a visual cortex or in monkeys or humans with
lesions in the visual cortex (Weiskrantz 1987; Stoerig and
Cow cy 1997). The residual functions do not usually evoke
с о nsc ious aware ness.
The pupillary response and optokinetic nystagmus sur­
vive removal o f V I because these responses are controlled
by subcortical centers (Brindley ct al. 1 9 6 9 ; Pasik and Pasik
1982).
Blindsight could be due to visual inputs to cxtrastriate
areas routed through subcortical centers such as the supe­
rior colliculus. pulvinar, and claustrum. For example, mosc
neurons in monkey M T remain weakly responsive to visual
stimuli after complete removal o f V 1 ( Rodman et al. 1989).
The cells in M T still showed directional selectivity and bin-
ocularitv. If these cells receive inputs from the pulvinar,
their direction tuning must arise in M T , because the pulvi­
nar does n ot contain direction-tuned cells after removal o f
V I . Sincich et al. ( 2 0 0 4 ) found visual inputs to M T from
koniocellular cells that occur between the parvocellular and
magnocellular layers o f the L G N . These cclls have large
receptive fields, and their input to M T may account for the
survival ot some sensitivity
Л
to motion after removal ot V I .
M ovingstimuii in the blind hemifield o fh u m an patients
evoked f M R I responses in V3 and M T even though the
patients were n ot aware o f the stimuli (G oebel e t al. 2 0 0 1 ).
Transcranial magnetic stimulation o f M T , but not o f V 3,
impaired the ability o f hemianopic subjects to detect
motion coherence in an array o f spots (Alexander and
Cowey 2 0 0 9 ).
Patients with cortical lesions who exhibit blindsight are
particularly sensitive to m otion. However, Azzopardi and
Cowey ( 2 0 0 1 ) found that, although patients could detect
motion and discriminate the direction o f motion o f simple
bars, they could not discriminate the direction of motion ot
gratings, plaids, or random-dot patterns.
Several contam inating factors must be taken into
account when assessing blindsight. Hemianopic patients
may have islands o f intact receptors in the affected hemi-
ficld o r detect scattered light (Fendrich et al. 1 992). This
could n ot explain blindsight in patients with the entire
cerebral hemisphere removed. Also, hcmisphcrcctomizcd
patients could n ot detect any features o f visual stimuli after
light scatter o n to intact regions o f the retina had been co n ­
trolled (K ing et al. 1 9 9 6 ; Faubert et al. 1 999). See Cowcy
( 2 0 1 0 ) for a review o f blindsight.
5 .6 S T IM U L U S T U N IN G OF
C E L L S IN V I
5. 6. 1 C O N T R A S T S E N S I T I V I T Y OF
C O R TICA L CELLS
In response ro a drifting grating, simple cells in the visual
cortex o f the cat fire at a frequency that depends on stimu­
lus contrast. M ost cells have a contrast threshold below a
contrast o f 0 .05 (Skottun et al. 1987). Above the contrast
threshold, firing frequency shows an initial acceleration and
then a linear dependence on contrast up to a contrast ot
about 0 .3 , after which the response saturates at a contrast o f
about 0 .7 5 (Dean 19 8 1 ; Albrecht and H am ilton 1982).
The slope, o r gain, o f the contrast/response function varies
from cell to cell, as does the position o f the linear portion o f
the function along the contrast axis. For binocular cells, the
slope o f the contrast/response function was steeper for a
stimulus presented to the dom inant eye than for one pre­
sented to the nondom inant eye, but was most steep when
the stimulus was presented to both eyes (Chao-yi and
Creutzfeldt 1984). C ortical cells also adjust their contrast
sensitivity by scaling their response by the pooled response
o f neighboring cells. This type o f automatic gain control is
called respon se n orm alizatio n (Carandini and Heeger
1994). The variance o f the response o f cortical cells increases
with increasing response amplitude (Tolhurst et al. 1981).
This may account for why contrast discrimination is best at
low contrasts (W ebers law).
Hawken and Parker ( 1 9 8 4 ) found that cells in the visual
cortex o f the monkey with relatively high contrast sensitiv­
ity were segregated from those with relatively low sensitiv­
ity. They identified the former with the magnocellular
system and the latter with the parvocellular system. The
contrast sensitivity o f L G N cells is similar to that o f cells in
V I . However, cells in M T (Section 5.8.4b) have enhanced
contrast sensitivity. This is probably because many m agno­
cellular cclls converge to form the receptive fields o f cells in
M T , which are about 100 times larger than the receptive
fields o f cells in V I (S c la r e ta l. 1990).
The contrast threshold o f a cortical cell as a function o f
the spatial frequency o f a drifting grating defines the cells
contrast-sensitivity function. The perceived spatial fre­
quency o f gratings increased as contrast was reduced
(Georgeson 1 980). This suggests that, as contrast is reduced,
the peak spatial frequency o f a cortical cell is reduced.
Therefore, at low contrast, a grating o f a given spatial fre­
quency optimally stimulates a cell that normally responds
to a higher spatial frequency. In conform ity with this sug­
gestion, the peak spatial frequency o f cortical cells tuned to
frequencies above 0 .6 5 cpd fell slightly as contrast was
reduced (Skoccun et al. 1986a).

5 . 6 .2 O R l l i N T A T IO N T U N I N G

5 .6 .2 a O r i e n t a t i o n T u n in g F u n c tio n s

It was explained in Section 5.5.3 that ganglion cells have

circular receptive Helds buc chat cortical cclls inco which
they feed have elongated receptive fields. Boch simple and
complex cclls in V I respond best when a line or edge is ori-
ented along the long axis o f the cell’s receptive field. The
scimulus orientation thac evokes the scrongcsc response in a
given cell is its preferred o rien tatio n . The funccion relating
chc firing race of a ccll со chc oricncacion o f a line ccnccred
within its receptive field is ics o rien tatio n tu n in g fu n ctio n .
An example from the cac is shown in Figure 5.29. The full
tuning bandwidth o f a cell is indicated by the width o f the Fifwc5.30. R u ssellL . DcValois. B o r n in A m e s . I o w a , in 1 9 2 6 , b u t s p e n t th e
tuning function ac half chc hcighe o f ics maximum response. firs t 1 7 y e a r s o f h i s life w i t h h i s m i s s i o n a r y p a r e n t s i n I n d i a . H e
o b t a i n e d h is Л . В . a t O b c r l i n C o l l e g e i n z o o l o g y a n d p h y s i o l o g y in
Band widths o f cells in the monkey striate cortex range from
1 9 4 7 a n d a P h . D . in p h y s i o l o g i c a l p s y c h o l o g y t r o m t h e U n i v e r s i t y o f
6 “ (sharply peaked cuning) со 180° (flac cuning). The mean M i c h i g a n in 1 9 S 2 . F o l l o w i n g a p o s t d o c t o r a l a p p o i n t m e n t in G e r m a n y ,
is about 40°, which covers about a quarter o f the maximum h e j o i n e d t h e f a c u l t y a t I n d i a n a U n i v e r s i t y in B l o o m i n g t o n . L a t e r , lie

range o f 180° (DcValois ct al. 1982) (Porcraic Figure 5. 30).
The oriencacion bandwidch, decermined psychophysi-
cally in humans by a masking procedure, has been found to
decrease wich increasing spacial frequency o f a cesc gracing
from about 60° ас 0.5 cpd to 30° at 11.3 cpd (Phillips and
W ilson 1984). Although orientation-sensitive cells respond
mosc reliably to stimuli orienced ac che peak o f che tuning
function, their sensitivity to changes in orientation is great­
e r on che sceep flanks o f the cuning funccion, where the
change o f response per unit change in orientation is greatest
(Sco b ey a n d G abor 1989).
S tim ulus orientation (deg)
F.*u»e$. 2 *. O rkntation tuning fu n ction o f л cortical c c ll
o f a s i m p l e c c l l in t h e c a t ’s v is u a l c o r t c x t o t h e o r i e n t a t i o n o f a lin e .
D i s t a n c e a is h a l f t h e w i d t h o t t h e t u n i n g J u n c t i o n a t h a l f - a m p l i t u d e ,
a n d i n d i c a t e s t h e c e l l s o r i e n t a t i o n s e l e c t i v i t y . T h i s p a r t i c u l a r f u n c t i o n is
a sy m m e trica l. Bars arc stan d ard errors.
T u n in g fu n ctio n
(К с Л м и и fro m I i r ^ j d u n d i r . J A lbu*
b e c a m e p ro fe sso r o f p s y c h o lo g y a n d p h y sio lo g ic a l o p tic s a t the
U n i v e r s i t y/ o f C a l i f o r n i a at B e r k e l e y/. H e d ie d in 2 0 0 3 .
It is believed that the orientation o f a stimulus is coded
by chc response o f che see o f dcccccors wich orientation
tuning functions that overlap the orientation o f the stimu­
lus. This p o p u la tio n -co d in g process is revealed in the tilt
aftereffect. Inspection o f a tilted grating for several minutes
causes a vertical grating to appear tilced in che opposice
dircccion. There is physiological evidence chac chis aftcrcf-
fecc is due to reduced response o f cells tuned to the orienca-
cion o f chc adapcacion scimulus relacive со chc response o f
cells tuned to neighboring orientations. This shifts the pop­
ulation response со a vertical tcsc gracing in a dircccion
opposite that o f the adaptation stimulus (Dragoi et al.
2 0 0 0 ) . However, there is also physiological evidence chac
che preferred orientation o f cells shifts away from che orien­
cacion o f an adapcacion stimulus (Jin ec al. 2 0 0 5 ) . This
second effect works in the opposice direction and reduces
che magnicudc o f che cilc afrcrcffccc.
C ratin g resolution, vernier acuity, and orientation dis­
crimination arc highesc when chc scimulus clcmcncs arc
aligned with the vertical or horizontal retinal meridians
rather chan wich oblique meridians. These anisocropics
com e under the heading o f the o b liq u e effect (see Howard
1982). Ic has been rcporccd chac chcrc arc more cclls runcd
to vercical and horizoncal orientations than to oblique ori­
encacions in chc visual corccx o f cac and monkey (DcValois
ec al. 1982). Ic has also been rcporccd chac cclls cuncd со chc
principal orientations are more narrowly tuned to orienta­
tion than arc cclls cuncd со oblique oricncacions (O rban
and Kennedy 1981). However, others had failed to find chis
anisocropy (W ilson and Sherman 1976; Poggio cc al. 1977).
These differences may have arisen because o f rhe small
number of cells sampled anti because of differences between
simple and complcx cclls and bee ween foveal and peripheral
cells.
Li cc al. ( 2 0 0 3 ) reinvestigated this question by record­
ing from over 4 ,0 0 0 cells in the visual cortex o f the cat
within 15° o f the foveal representation. Cells tuned to
principal orientations were more numerous and had nar­
rower tuning functions than cells tuned to oblique orienta­
tions. The anisotropies were evident only in simple cells,
especially those tuned to high spatial frequencies. Through
an analysis o f linear and nonlinear com ponents in orienta­
tion tuning o f simple cells, Li et al. concluded that intracor-
tical mechanisms plav a major role in the oblique effect.
Responses ot orientation-selective cells in the cat visual
cortex were largest when a grating was orientated radially
1 i*ur* $.ji. M k h a d P . Stryker. H e o b tain ed b is P h .D . in n curophysiology
with respect to the fovea (Levick and Thibos 1 982). This is
Irom M l Г. H e is professor in th e K eck C e n te r for Integrative
known as the radial bias. Pavnc and Herman ( 1 9 8 3 ) found N eu ro science a t the U n iv ersity o f C a lifo rn ia at San Francisco.
that cclls with receptive fields within 12° o f the fovea
preferred horizontal or vertical stimuli. However, a prefer­
ence tor radial or circumferential stimuli was also present. Each com partm ent is activated by a stimulus in a distinct
Vidyasagar and Henry ( 1 9 9 0 ) found that only monosynap- orientation. Comparcmencs wich different oriencacion tuning
tically driven cortical cells showed a radial bias. The radial
4
are randomly distributed over the dendritic tree (Jia et al.
bias could arise subcortically. 2 0 1 0 ) . The overall tuning o f a ccll must therefore arise from
The peripheral retina ot the monkey also has a radial the integrated activity over the dendritic tree.
organization (Schall cc al. 1986). At eccentricities beyond The opposing idea is that orientation tuning arises from
20°, human observers are more sensitive to a radial gracing excitatory or inhibitory interactions between cortical cells.
than to gratings in other orientations (Rovamo et al. 1982; Sillito ( 1 9 7 5 ) claimed that orientation tuning was lost after
Temme ec al. 1985; Westheimer 2 0 0 3 ). A radial bias has intracortical inhibition was abolished by application of
been found by f M R I in both humans and monkeys (Sasaki bicucullinc to the ca ts visual cortex. However, single cclls
ec al. 2 0 0 6 ) . * injected with an inhibition blocking agent retained their
orientation tuning (Nelson ct al. 1994). Thus, direct inhibi­
tory inputs are n ot necessary for orientation tuning ot cor­
5 .6 .2 b M ech an ism s o f O riencacion T u n in g
tical cclls, but they could scill be involved.
Hubei and W iesels original idea was chac che oriencacion There is evidence that both mechanisms are involved in
selectivity ot a cortical cell derives from the fact that each
4
orientation tuning. The initial cxcitatory inputs from chc
excitatory corcical cell receives inpucs from several L G N L G N produce broad orientation tuning o f cortical cells,
neurons with overlapping circular receptive fields that are which is then sharpened by mucual facilitation o f corcical
aligned on che rccina. Confirmacion o f chis idea in che cac cells tuned со the same orientation coupled with mutual
and ferret has been provided by Stryker ( 1 9 9 1 ), Chapman inhibition o f cclls cuncd to other orientations (Sillito ct al.
et al. ( 1 9 9 1 ) , Reid and Alonso ( 1 9 9 5 ) , and Fcrster cc al. 1980a; Hata et al. 1988; Volgushev et al. 1993; Sato et al.
( 1 9 9 6 ) (Portrait Figure 5. 31). 1996; C ro o k ct al. 1997; F.yscl et al. 1998). Intracortical
In cacs, few neurons in layer 4 C B are scrongly cuncd со inhibition could sharpen the tuning o f cclls for boch spacial
orientation, but cells to which they project in layers 2 - 3 arc frequency and orientation by attenuating their response to
strongly tuned. Dye injected into layer 4 o f chc visual corcex low spatial frequencies (Vidyasagar and Mueller 1 994). In
ot tree shrews revealed that, in each location in layer 4, cells one model, intracortical inhibition and the amplifying
with aligned circular rcccpcivc fields projecced со the same effects o f recurrent excitation enhance the preexisting weak
cell in layers 2 - 3 со form an orientation-tuned cell (M ooser orientation tuning created by orientation bias in L G N neu­
ec al. 2 0 0 4 ) . Thus converging inputs from cells with aligned rons or by convergence o f inputs from the L G N wich
circular receptive fields provide che inicial oriencacion aligned receptive fields (Vidyasagar et al. 1996). Shevelev
tuning. However, tuning is refined by other excitatory and ct al. (1 9 9 8 ) found that intracortical inhibition sharpens
inhibitory processes. the orientation tuning o f one class o f cortical cells but p ro­
Two-photon imaging revealed that calcium signals are duces stimulus dependent changes in preferred orientation
generated within discincc comparcmencs o f che dendricic and tuning width in a second class o f cells, which they called
trees ot cells in lavers 2 - 3 of the mouse visual cortex.
A
“scanners.”
 Hirsch ct al. ( 1 9 9 8 ) found that the temporal attributes
ol excitatory responses o f simple cells in cat area 17 to ori­
ented stimuli matched those o f inputs from the L G N .
However, inhibitory responses were governed mainly or
wholly by cortical interneurons linking cells with opposite
contrast polarity. This separation o f excitatory and inhibi­
tory processes could endow the visual cortex with a wider
dynamic range. Hirsch et al. ( 2 0 0 3 ) revealed two types o f
inhibitory intcrncuron in layer 4 of the cats visual cortex.
Both were driven by L G N inputs. For one type, designated
in h ib ito ry sim p le cells, the receptive fields were similar to
those o f excitatory simple cells except that the subregions
had opposite contrast sensitivities. The inhibitory cells and
their excitatory neighbors also had similar orientation
tuning. These cells could improve orientation and spatial-
frequency selectivity and increase the stability o f cortical
activity (Lauritzcn and Miller (2 0 0 3 ).
The receptive fields and temporal properties o f the other
type, designated in h ib ito ry co m p lex cclls resembled those
o f excitatory com plex cclls. These cells were not tuned to
orientation. They could perhaps help to make the responses
o f orientation-tuned excitatory cells invariant to contrast.
Perhaps the response ot cortical cells tuned to orienta­
tion is enhanced by a tendency tor spatially aligned
ganglion cells to fire in synchrony (see Meister 1996).
Mechanisms o f orientation tuning have been reviewed by
Ferster and Miller ( 2 0 0 0 ) and Shapley et al. (2 0 0 3 ).
5 .6 .2 c T em p o ral A spects o f O rie n ta tio n T u n in g
Inhibitory or excitatory mechanisms, precortical or co rti­
cal, that help to determine the orientation selectivity ot a
cortical ccll could involve feedforward loops o r recurrent
feedback loops. Celebrini e t al. ( 1 9 9 3 ) demonstrated that
the orientation sclectivitv o f cclls in rhe visual cortex o f the
monkey is present and fully tormed in the first 10 ms
o f their response. O th er investigators have found that,
although optimal orientation tuning o f most cells in the cat
visual cortex is stable over the first 100 ms, tuning becomes
sharper during this period (Volgushev et al. 1995).
Sharon and Grinvald ( 2 0 0 2 ) used voltage-sensitive dyes
to measure the dynamics o f orientation tuning in area 17 o f
the cat. Tuning width did not vary over time, as o n e would
expect from feedback processes, but response amplitude
increased between 5 0 to 8 0 ms after stimulus onset, suggest­
ing a tccdback mechanism. However, voltage-sensitive dyes
average responses o f many neurons and therefore do not
measure the dynamics o f single cells.
Shevelcv et al. ( 1 9 9 3 ) tound that only about 3 7 % o f
cells in the cat visual cortex showed stable optimal tuning
during the first 6 0 0 ms o f their response The other cclls,
identified as “scanners,” showed systematic shifts in tuning,
first in one direction and then in the other.
Ringach et al. ( 1 9 9 7 ) found that the orientation tuning
o f cells in layer 4 C o f the monkey visual cortex were broadly
tuned to orientation. O rientation tuning developed 3 0 - 4 5
ins after stimulus onset. The orientation preference o f these
cclls remained stable throughout the response period. By
contrast, many cells in other layers showed two peaks, and
their preferred orientation was not stable over time. They
concluded that the broad orientation tuning ol cells in
layer 4 C arises from a direct feedforward mechanism but
that the narrower tuning o f cells in other layers arises from
intracortical inhibition.
These results support the idea o f two classes o f orienta­
tion detectors. The first class have rapid onset ot tuning that
relies on feedforward mechanisms. This fast feedforward
mechanism allows the animal to assess the orientation o f a
stimulus rapidly. The second class ( “scanners”) rely on recur­
rent circuits, and their orientation tuning is modified by the
short-term characteristics o f the visual task.
Mazer e t al. ( 2 0 0 2 ) challenged these findings. They
used the reverse correlation procedure (Section 5.6.4b) to
measure the temporal dynamics of spatial-frequency and
orientation tuning o f cells in V I o f alert monkeys. They
found very few cells for which orientation tuning or
spatial-frequency tuning varied substantially over time.
They concluded that orientation sclectivitv arises from
the convergence o f visual inputs with similar temporal
dynamics.
The response o f a V I neuron to an optimally oriented
grating is reduced by superimposition o f an orthogonal
grating. This type o f response is known as cross-oricntation
suppression. Smith et al. ( 2 0 0 6 ) tound that the effect
occurs so quickly that it must depend on dircct feedforward
signals or fast-acting retinal interneurons. In surround
suppression a neurons response to a grating is reduced by
the presence o f a surrounding parallel grating. The long
latency o f this effect suggested to Smith et al. that it depends
on feedback from higher centers.
5 .6 .2 d Im m u n ity to C h a n g e s in C o n t r a s t
As contrast increases, o n e might expect that stimuli outside
the preferred orientation ot a cortical cell would begin to
excite the ccll. This would broaden the orientation tuning
o f the cell. This is known as the iceberg effect. However,
changes in contrast have very little effect on the orientation
selectivity o f cortical cells (Sclar and Freeman 1982).
O n e theory is that contrast independence is achieved by
inhibitory/ interactions between cortical cells tuned to dif-
fcrcnt orientations. For example. Trover et al. 0 9 9 8 ) pro­
posed such a mechanism for contrast independence. In the
model, L G N inputs have an orientation-tuned com ponent
that varies with the spatial phase o f rhe stimulus relative to
that of the receptive field, and an untuned com ponent that
is n ot sensitive to phase. Excitatory cortical connections
between cells with the same phase sharpen the tuned
com ponent, while inhibitory connections between cclls in
antiphase eliminate the untuned component.
 Another theory is that contrast independence is
achieved solely by feedforward mechanism. For example,
Finn e t al. ( 2 0 0 7 ) propose that independence results from
nonlinear properties of the excitatory pathway, such as nor­
malization o f responses over different cortical cclls and
response saturation.
There is evidence that receptive fields of ganglion cclls
lose their inhibitory responses at low luminance (Section
5.1 A c). However, cells in the visual cortex o f cats and m o n ­
keys retain their tuning to orientation and m otion at low
luminance (Ram oa ct al. 1985; Duffy and Hubei 2 0 0 7 ).
According to this evidence, the orientation tuning o f co rti­
cal cells is n ot afiected by changes in the organization of
ganglion-cell rcccpcivc fields.

5 .6 .3 S PAT 1A 1. -P F. R I О D I C I T V T U N I N G

Cortical cclls arc also differentially tuned со che spatial peri­

odicity of a grating within their receptive field (Cam pbell
and Robson 1968). Such cclls are said to have a preferred
spatial frequency although, strictly speaking, spatial fre­
quency cannot be specified within a restricted area. The s Л2 . A nthony M ovshon. B o m in N ew York in 1 9 5 0 . H e o b tain ed л
P b .D . in ncuroph ysiology an d visual psychophysics from C am brid ge
spatial-lrequcncy tuning function ot a ccll is the change in
U n iv ersity in 1975- In 1 9 7 5 he jo in ed th e d ep artm en t o l p sy ch ology at
firing rate as a function o f the spatial frequency o f a
N ew York U niversity, w here he is now Silver Professor. From 1991 to
stimulus grating ol fixed contrast. The spatial-frcquencv 2(103 he was an investigator o f chc H oward H ughes M edical Institute.
tuning functions o f simple and complex cclls in the cats H e was elected to the N ational A cadem y o f S cicn cc s in 2 0 0 8 .

visual cortex have a full bandwidth at half amplicude o f

between 0.6 and 1.9 octaves (Movshon et al. 1978) (Portrait
Figure 5 .32 ). The spatial-frequency channels serving che
central retina o f the cat seem to be spaced at half-octave
intervals over a tocal spacial-frequency range o f 2.5 occaves
(Pollen and Feldon 1979). Thus, neighboring channels
overlap, and abouc six channels cover che cocal range o f
spatial frequency.
Psychophysical evidence reviewed in Section 4.4.1b
suggests that the central region of the retina is served
by abouc seven discincc spacial-frequency channels with
overlapping tuning functions.
For chc besc response, che scimulus muse fill the cells
receptive field. But it must n ot extend beyond it, because
scimuli oucside che classical receptive field can modify the
response of a cortical cell. Simple cells in the visual cortex of
cat and monkey, on average, responded best when about 2.5
cycles ol a grating fell within the receptive field (D e Valois
ct al. 1985). C om plexcells responded best to about 3 cyclcs.
N o cells preferred more than 7 cycles within their receptive
field. Simple cclls, and most com plcx cclls tuned to a nar­
rower range ot spatial frequencies had receptive fields with
more cycles.
The preferred spatial frequency o f cortical cells is essen­
tially the same for different stimulus contrasts (Albrecht
and Hamilton 1982; Skoccun ec al. 1986a). The sensitivity o f
cells to changes in orientation and spatial frequency improves
with increases in contrast buc reaches a maximum ac quice
low contrasts (Skottun et al. 1987). Sceniak et al. ( 2 0 0 2 )
found that spatial-frequency tuning is sharpened at low
contrasts tor cells in V I , especially for cells sensitive to high
spatial frequencies. '1 his sharpening seems со be due to
expansion o f the excitatory region ot receptive fields at low
concrasc.
During the initial 5 0 ms o f response, cells in V I o f the
macaque became more sharply cuned to spacial frequency
and their preferred spatial frequency shifted upward
(Bredfeldt and Ringach 1002). Thus, it takes time for cells
in V I to reach their final response characteristic.
Prolonged exposure to a gracing o f a parcicular spacial
frequency reduces the sensitivity of cells in V I that prefer
thac frequency. Also, the tuning functions o f cells tuned to
neighboring spatial-frequencies are skewed away from the
spacial frequency o f chc adaptation grating. C clls tuned to
the orchogonal spatial frequency are not affected. Kohn
( 2 0 0 7 ) reviewed these and other adaptation effects.
Parker and Hawken ( 1 9 8 5 ) measured (a) spatial-
frcquencv tuning functions o f cclls in the visual cortcx o f
the monkey tor a high-contrast grating, (b) the change in
probability o f firing o f a ccll .is a function o f a changc
in spatial frequency and, (c) sensitivity o f cells to a change
in spatial phase o f a grating. The results were comparable to
psychophysical measures o f human hyperacuity.
A non-Fourier stimulus is one not defined bvs modula-
tion o f luminance. Such scimuli are also known as second -
o rd er stim uli. For instance, a second-order grating can be
made by superimposing a low-frequency modulation o f
contrast on a high spatial-frequency sinewave grating. Since
mean luminance does n ot vary at the modulation frequency,
the grating contains no Fourier com ponents at that fre­
quency. However, many cortical cells o f the cat responded
when the second-order spatial frequency fell within their
spatial-frequency bandwidth (Z h ou and Baker 1994;
Marcschal and Baker 1998).
Responses to other second-order stimuli, such as a
grating formed by modulation o f relative motion or modu­
lation o f binocular disparity, have been tound at higher
levels o f the visual system. Ic has been proposed chac second-
order stimuli are processed in specialized visual channels.
For example, i f che outputs o f first-level filters that respond
to a contrast-modulated grating are rectified and squared,
they can be used to create a rcccptivc field chat is similar
to one that responds to a luminance-modulated grating
(Z h ou and Baker 1996). There is ample psychophysical evi­
dence that we perceive second-order stimuli, as will become
apparent at various places in chis book.
5 . 6 .4 S PA T I О T F. M P O RA L T U N I N G О F
C O R T IC A L CELLS
5 .6 .4 a T u n in g to M orion
In submammalian vertebrates, such as frogs, turtles, and
birds, cells tuned to direction o f motion are tound in the
retina (Macurana et al. I 9 6 0 ; Maturana and Frenk 1963;
Jensen and Dcvoe 1983). Motion-selective cells are also
found in the retinas o f some mammals, such as rabbits and
squirrels (Barlow and Hill 1963; Michael 1968).
O n ly a few motion-selective cclls have been found in
the cat retina (Sto n e and Fabian 1966), and none has been
found in the primate retina (D e M onasterio 1978). Visual
evoked potentials trom the retina (E R G s) and the cortex o f
humans have revealed that most, if not all, processing o f
motion occurs in the cerebral cortex (Bach and Hottmann
2000).
M ost cells in the visual cortex o f primates respond best
when the stimulus moves in a particular direction, the
preferred d irectio n . The axis o f the preferred direction o f
an orientation-tuned ccll is at right angles to the long axis o f
its receptive field (Livingstone 1998). Thus, the columnar
organization o f cells in the visual cortex based on axes o f
preterred motion corresponds to the columnar organiza­
tion based on preferred orientation. Som e cclls respond to
movem ent in either direction along a given axis and are said
to be bidirectional. Some cclls in the visual cortex o f the cat
respond over a wide range o f stimulus velocities but may be
dircccionally selective over only high or only low velocities.
Ocher cells respond only over low velocities (Duysens ec al.
1987).
For cells in V2 and M T o f monkeys, Snowden et al. (1992)
obtained direction tuning functions with a halt-width at
half-amplitudc o f about 5 0 й. For cclls in M T , Treue c t al.
(2 0 0 0 ) obtained a value o f about 30°. Although cells in M T
responded most vigorously to stimuli moving in the pre­
ferred direction, they were m ost sensitive to changes ot
m otion when the stimulus excited the ccll on the flank o f its
direction tuning tunction.
It has been proposed that only two or three cemporal-
frequency channels are required to account for human
speed sensitivity, as opposed to direction sensitivity (Sm ith
and Edgar 1994).
Relative motion is a more potent stimulus than absolute
motion. Thus, neurons in V I o f the monkey responded
more vigorously to relative m otion o f random-dot displays
than to homogeneous motion o f che docs (C a o and Schiller
2 0 0 3 ) . Cells sensitive to relative m otion have also been
found in M T (Section 5.8.4b).
5 .6 .4 b Sp atiotem p oral Responses o f C o r tic a l Cells
The delay between the response o f an L G N relay ccll and
that ot its associated cortical cell is about 3 ms, and the
monosynaptic delay between cortical cells is about 1.5 ms.
Many cortical cells show a biphasic response to a brief
stimulus.
C o rtical cells are differentially tuned to temporal fea­
tures o f stimuli falling within their receptive fields. Also,
cells in V I o f the monkey show a lower cu to ff and greater
diversity in their temporal-frequency bandwidth than do
ganglion cells or L G N cells (Hawken et al. 1996).
The amplitude transfer function o f a cell describes che
amplitude o f the cells response as a function o f either the
temporal or spatial frequency of the stimulus. The phase
transfer function describes the temporal or spatial phase o f
the cell’s response as a function o f the temporal or spatial
frequency o f the scimulus respectively. From the phase
transfer function it is possible to inter the latency o f a co rti­
cal cell and whether it has an odd- or even-symmetric recep­
tive field (H am ilton et al. 1989). The amplitude and phase
transfer functions together specify the sp atiotem p oral
transfer function ot a cortical cell. In a linear system, the
amplitude and phase o f the response is n ot affected by
changes in contrast. W h ile variations in contrast have little
or no effect on the shapes o f the amplitude and spatial phase
transfer functions o f cortical cells o f cats and monkeys, an
в
increase in contrast causes a tcmporal-frcquency-dcpcndent
advance in temporal phase and a shortening ot latency
(A lbrecht 1995).
O n e can think o f a cortical cell as having a spatiotempo­
ral tuning tunction and a spatiotemporal structure to its
receptive field. Plotting the spatiotemporal structure o f the
receptive field o f a cortical cell using a single stimulus probe
is a time-consuming procedure. The reverse correlation
p ro ced u re is more efficient ( D cA ngclis et al. 1993a). Bar-
shaped stimuli are presented at different positions and at
different times within the receptive field. The responses o f
the cell are cross-correlated with the inputs to yield the spa­
tiotemporal impulse response o f the cell. The method works
only if che ccll behaves linearly, and can therefore be applied
only to simple cortical cells.
An example o f chc spacioccmporal structure o f chc
receptive field o f a simple-cell is shown in Figure 5.33A .
Each slice represents chc momencary activity within the
excicacory and inhibitory regions o f the receptive field. The
sequence along the time dimension represents the temporal
phasing o f the response. Figure 5 .3 3 B shows the plot o f the
receptive field along one spatial dimension on the abscissa
and over time on the ordinate. In the first example, the
positions o f the excitatory and inhibitory regions arc-
constant over time, and the ccll is said to show space-tim e
separability. The response ot the cell is the simple product
o f its spatial response and its temporal response. Note that
100 ms
0 Space, x (dog) 4
bifurc 5.H. Spatiorem poral response p rofiles o f sim ple id ls in air's visual ior rex.
(A ) E ach panel is th e reccptive-field profile o f t h e cell a t л particu lar
tim e after stim ulus o n set. W h ite areas rep resent responses to a flashed
b rig h t bar and dark areas are responses to a flashed dark bar. T h e
p ro jectio n o t the panels prod uces the sp atiotem p oral profile o t the
ccll lo r o n e spatial d im en sion ov er tim e. Solid lines arc boundaries o f
brigh t-excitatory* "on ” response regions. D ashed lines are boundaries
o f dark-excitatory, "otF” response regions. ( B ) Sp atiotem p oral response
profiles o t sim ple cclls Irom 8-w cck -old ca t. The exam ple on th e left
shows sp acc-tim e separability in w hich the response profile is the
p ro d u ct o f the space and tim e profiles. The exam ple o n the right show *
spacc-tim e inseparability. This ccll is selectively responsive to m o tio n in
th e d ircccio n o f t h e - tilt" o f spatiotem poral region s in the receptive field
profile. (From DcAiifcclivct al. UwJ « mIi pmn Hilort)
the temporal response o f this ccll is biphasic. In the second
example, there is a spatial shift o f activity within the recep­
tive field over time. The ccll is said to show space-tim e
inseparability (space and time interact). Cells o f this type
show a prefcrcncc for stimuli moving in the direction in
which their spatiotemporal tuning function is ''tilted” in
the spacc-time domain.
Cells with space-time separable response profiles are
generally not selective tor a particular direction ot motion.
After allowing for the nonlinearity o fth e response ofsimple
cells to contrast, DcAngclis et al. (1 9 9 3 b ) predicted the
direction selectivity o f simple cells from che spatiotemporal
profiles ot their receptive fields. The results indicated that
simple cclls embody a linear spatiotemporal filter (see also
M cLean and Palmer 1989, 1994).
The spatiotemporal structure o f the receptive fields o f
complex cells cannot be derived trom their responses to
single spots or bars, because the responses are nonlinear.
However, responses ot complex cells to two spots or bars
have been used to examine their spatial frequency tuning
and motion selectivity (M ovshon et al. 1978; Emerson et al.
1 992). Responses to two stimuli have also been used to
explore the disparity sensitivity o f complex cells, as described
in Scction 11.4.1.
Mazer et al. ( 2 0 0 2 ) used the reverse correlation proce­
dure to measure the temporal dynamics ofspatial-frcquency
tuning and orientation tuning o f cells in V I o f alert m o n ­
keys. The spatial-frcqucncy and orientation tuning o f
most cells were separable. However, there were small insep­
arable components. A few neurons showed a decrease in
the bandwidth o f orientation tuning with increasing spatial
frequency. Also, there was ccndency tor cclls with longer
latencies to be tuned to higher spatial-frequencies.
5 .6 .4 c M o d els o f Sp atio tem p oral Responses
T he so-called en erg y m odel has been used to account for
the spatiotemporal responses ot cortical cells. In this
model, cortical cells summate inputs from two or more sub­
units, which could be simple cells. Each subunit has a linear
spatiotemporal filter followed by static nonlinearities that
half-rcctify and square the output (Adelson and Bergen
1 985). In o n e form o f the model, rectification results in one
pair ot subunits responding to luminance increase ( O N
units) and the other pair to luminance decrease ( O F F
units). In each pair, one unit is 90° phase shifted in space
and in tim e with respect to the other, to torm a pair in
quadrature.
Emerson (1 9 9 7 ) produced physiological evidence for a
two-subunit energy model for simple cells. Gaska et al.
( 1 9 9 4 ) tested the model by deriving the sccond-ordcr
W iener kernels (Section 3.4) from responses to white noise
of complex cells in the monkey visual cortex. The kernels
predicted the way the cells responded to drifting gratings,
and the results were consistent wich the energy model.
 Peterson et al. ( 2 0 0 4 ) found that the spatiotemporal
tuning ot neighboring pairs ot simple cells in area 17 ot the
cat showed temporal phase differences o f less than the 90°
predicted by the simple energy model. They suggested that
the directional selectivity o f some cortical cclls in the cat is
4
derived from phase offsets between LCiN alfcrents feeding
into the ccll. O th er cclls derive their direction selectivity
by summing activity from nonselective cortical cells that
differ in spatial and temporal phase. The minimum phase
difference required for direction selectivity is less than 90".
The energy model predicts many features o f the feedfor­
ward responses o f many simple and complex cells, such as
the way they respond to single bars, double bars, drifting
gratings, and white noise. However, the model does not
account for how responses ot simple and complex cclls arc-
modified by activity in neighboring cells or by feedback
trom higher centers. For example, Hccger ( 1 9 9 2 a ) pro­
posed that the output o f complex cells is normalized by the
mean response ot neighboring cells. Jacobson et al. (1 9 9 3 )
concludcd that a cascade o f linear filtering followed by
rectification and squaring provides a more accurate descrip­
tion o f simple cells than o f complex cells. However, they
produced evidence that, even tor simple cells, other forms
o f non linearity, such as surround suppression, play a
significant role in their response.
Jagadcesh e t al. ( 1 9 9 7 ) recorded intracellular synaptic
potentials in simple cells in the cat visual cortex evoked by a
sequence o f stationary sinewave gratings. A linear model
applied to the data predicted rhe direction selectivity o f
the cclls, but the tuning width indicated by the synaptic
potentials was wider than that indicated by the extracellu­
lar action potentials. It thus seems that a nonlinear mecha­
nism between the synaptic input and the output sharpens
direction sensitivity.
Reid c t al. ( 1 9 9 1 ) found some evidence o f sharpening o f
directional selectivity o f simple cclls by nonlinear inhibi­
tory interactions. Removal o f intracortical inhibition by
chemical suppression ot CiABA reduced directional selec­
tivity o f simple cells in areas 17 and 18 o f the cat (Crook
e r a l . l 9 96 , 1997).
O th er aspects o f spatiotemporal coding were discussed
in Section 4 .3 . M otion sensitivity in higher visual centers is
discussed in Section 5.8.
5 . 6 .5 C E L L S T U N E D TO M U L T IP L E
FEA TU RES
T he response o f each neuron in the visual cortex is modu­
lated by changes in each o f several visual features. Thus, a
given neuron can n ot be said to code a n y o n e feature unam­
biguously.
Responses are said to be separable when rhe tuning
function for one feature is not affected by the value o f
another feature. Ideally, the response o f rhe cell (firing rate)
is the sum o r product o f the responses to each feature.
Separable tuning simplifies the process o f detecting varia­
tions in single features in a population o f cells.
Cells in V I that are tuned to motion direction have
inseparable space-time tuning Junctions, as explained in the
previous section. Otherwise, most cells in the primary visual
cortex have separable tuning to orientation, m otion, and
disparity (Grunewald and Skoumbourdis 2 0 0 4 ) . Different
stimulus features are distinguished by the cooperative activ­
ity ot the population o f cortical cells tuned to that feature.
This is known as popu lation coding. For example, the ori­
entation o f a line could be uniquely coded by the output o f
the set o f orientation-sensitive cclls that rhe given stimulus
excites. The direction o f motion ot the same line could be
coded by the output o f the set o f motion-sensitive cells that
it excites. Since the two sets o f cells arc at least partly dis­
tinct, each stimulus feature is coded distinctly (see A bbott
and Sejnowski 1 999).
Tliis simple view has been challenged by evidence that
the same population response over a cortical area can be
produced by stimuli possessing different combinations
o f motion direction and orientation. Basole et al. ( 2 0 0 3 )
argued that the idea o f population coding is based on the
use o f drifting gratings that move and vary in spatial fre­
quency, only in a direction orthogonal to the grating. They
dissociated motion direction and orientation by using a set
o f similarly oriented short line elements that drifted in a
direction that was orthogonal or nonorthogonal to the
lines. O ptical imaging in the visual cortex o f ferrets revealed
patterns o f cortical activity over populations o f cells tuned
to different orientations. W h en the short lines moved in an
orthogonal direction, rhe response pattern was similar to
that produced by a grating o f long lines drifting in the
same direction. However, when the lines moved in a nonor­
thogonal direction, the response pattern resembled that
produced by a grating moving in a different direction. In
other words, the same population response in orientation-
tuned cclls was produced by twro stimuli moving in different
directions.
liasole et al. pointed out that short line elements possess
stimulus energy at many orientations in the Fourier domain.
W hen a short line moves, each orientation com ponent
moves at a speed that depends on its orientation to the
direction o f motion. The peak o f the population response
dependson th cco m p on cn t whose speed isoptimal. Changes
in the speed o f t h e drifting line elements changed the pat­
tern o f cortical response and also the preferred orientation
o f single cortical cells. The long lines o f a large grating pos­
sess energy over a small range o f orientations so that changes
in the speed o f a grating produced much less change in the
pattern o f cortical response or the orientation tuning o f
single cells.
Basole et al. concluded that these results are difficult to
reconcile with the idea o f population coding in V I .
However, they did not report whether the ferrets could dis­
criminate the orientations ot the stimuli that produced the
same population response. Given chat die stimuli w ercdis-
eriminable, they must have produced different responses
somewhere in the visual system. In fact, there must have
been differences in V I because all subsequent stages receive
their input directly o r indircctlv from V I .
At the primary level o f visual processing in V I it is desir­
able to code low-level features simultaneously/ over the
whole visual field— preattentive vision. If cells in V I were
not jointly tuned it would be necessary to have a complete
set o f single-feature detectors for each feature at each loca­
tion. Population coding using cells tuned to several features
but with separable tuning functions economizes on the
number of cells. However, this system is not economical in
terms o f metabolic energy because, with typical natural
scenes, most cells are active most ot the time. Also, because
o f response saturation and noise, the tuning functions
are not completely independent. Thus, population coding
involves some loss o f information (Grunewald and
Skoumbourdis 2 0 0 4 ). Nevertheless, population coding is
the best system for dctccting low-level features simultane­ Fig«r<£.34. M arg aret IIbn g R itcy . B orn in Shanghai in 1 9 4 1 . She ob tain ed
an М .Л . in scien ce ed u catio n at C olum bia U n iv ersity in 1 9 6 6 and a
ously over the visual field. But it is not suitable tor detecting
P h .D . in n curoanacom y w ith H . J . R alsto n at Stan ford U n iv ersity in
high-level features based on particular combinations o f stim­ 1 9 7 0 . Sh e con d u cted p o std o cto ral work w ith R . W . G u illcry at the
uli. That requires cells with inseparable tuning functions. U n iv ersity o f W isco n sin and A . Lasansky and M . F ou rtes at the
Responses are insep arable when a ccll is responsive to N ation al Institu tes o f H ea lth . Sh e was on the facu lty o f th e D ep artm en t
o t A n atom y at th e U n iv ersity o f C a lifo rn ia at San Fran cisco trom 1973
particular com binations ot different features. Tuning to
to 19iS 1. In 1981 she jo in ed the D e p a rtm e n t o f C e llu la r Biology,
particular feature combinations involves nonlinear pro­ N cu rob io logy, and A n ato m y at th e M ed ical C o lleg e o f W isco n sin ,
cesses, and is characteristic of cells that respond to high- w here she is now professor. R ecip ie n t o f th e M artin Luther K in g
level features. For example, cells in the medial temporal H u m an itarian Award, M ed ical C o lleg e o t W isconsin in 1 9 9 7 , and the
R oy and S h errin g to n Award presented by the G o rd o n Research
cortex ( M T ) respond to specific com binations o f disparity
C o n fe re n ce o n "B ra in E n ergy M etab olism and B lood F lo w ” in 2 0 0 6 .
and m otion (Section 11.5.2) and cells in the interior tem­
poral cortex respond selectively to faces. Since stimuli
exhibiting a particular high-level feature occur infrequently,
cells that respond to that feature are inactive most o f the investigated the physiological properties o f regions with
time. D etection ot such features is said to involve sparse high levels o f cytochrom c oxidase and found that they arc
coding. It would be impossible to simultaneously engage all centered on the ocular dom inance columns and contain
high-level feature detectors tor each stimulus in the visual cclls not tuned to orientation. These regions arc called
field. blobs, or puffs. The spaces between the blobs have a lower
For a given stimulus, the visual system engages only concentration o f cytochrom
a
e oxidase and arc known as
those high-level processes relevant to the task being per­ in terb lo b s. The centers o f the blobs are about 0.4 mm apart,
formed. In any case, visual resolution is severely degraded making about 5 blobs per m n r and a total of about 15,500
a few degrees away from the fovea, which means that in chc binocular visual field o f the macaque (Schein and
high-level detectors in the periphery can detect only coarse M onasterio 1987). The density ot blobs is about halt this
features. F.yc movements and attention funnel activity value in the monocular visual cortex. The number o f L G N
from V I to those high-level detectors that the perceiver is parvocellular cells projecting to each blob remains constant
interested in dctccting. at about 1 10 over the visual field o f the monkey. C ytochrom e
oxidase blobs seem to be present in all primates and form
elliptical patches aligned with ocular dominance columns
5.6.6 C Y T O C H R O M E O XIDA SE A R E A S O F VI
in primates with such columns. They also occur in area 17
In 1978, Margaret W ong-Rilcv informed Hubei and Wiesel o f the cat (Murphy ct al. 1995).
that she had found clusters o f cells with a high concentra­ O cular dominance columns have also been revealed bvф
tion of c y to c h ro m e oxidase in monkey V I . Cytochrom e staining for cytochrom e oxidase in autopsy specimens o f
oxidase is a metabolic enzvme
* found in rhe mitochondrial the brains o f humans with monocular loss (Section 5.7.2a).
membrane ot neurons. Its concentration is a sensitive indi­ C ytoch rom c oxidase is concentrated in cortical layers
cator o f neuronal activity (Wong-Riley 1979a, 1989) (Portrait 4 A and 4 C — layers associated with the parvocellular
Figure 5 .34 ). Tw o years later, H o rton and Hubei (1 9 8 1 ) system— and in layer 6, which projects to subcortical nuclci,
Figure$.3$. Jo n a th a n С H orton. B o rn in E d m o n to n , C an ad a, in 1 9 5 4 . He
ob tain ed an Л .В . from S tan fo rd U n iv ersity and a P h .D . from Harvard
U n iv ersity w ith D . H u b cl and Г. \X icscl. In 1 9 9 0 he jo in ed the faculty
a t the U n iv ersity o f C a lifo rn ia , San Francisco, where he is the W illiam
F. H oy t pro fesso r o f n eu ro-op h th alm olo g y, vice ch a ir o f the
D e p a rtm e n t o f O p h th a lm o lo g y , and a m em b er o f the neu roscience
p rogram . H e rcccivcd th e T rou tin an -V cron n cau Prize from the
Pan-A m erican A ssociation o f O p h th a lm o lo g y ( 1 9 9 9 ) , a Lew R .
Wavvcrman M erit Award from Research to Prevent B lind n ess ( 2 0 0 0 ) ,
and the A Icon Research In stitu te Award ( 2 0 0 5 ) .
including che L G N (Snodderly and C u r 1995). The litera­
ture on cycochrome oxidase in che visual corccx was reviewed
by W ong-Riley ( 1 9 9 4 ) and Sincich and Horton (2 0 0 5 a )
(Portrait Figure 5 .3 5 ). Cells in the blobs and intcrblobs
have been distinguished in the following ways, although
there is some debate about some ot these distinctions.
1. It has been claimed thac mosc blob cells arc noc cuncd to
orientation, while almost all interblob cells are tuned to
orientation. However, F.dwards ct al. ( 1 9 9 5 ) found no
correlation between orientation tuning and blobs.
2. The excitatory regions o f the receptive fields o f blob
cclls are larger than those ot interblob cclls (Snoddcrlv
and Gur 1995).
3. It has been claimed that color-opponent ganglion cclls
converge on so-called double-opponent cclls in
cytochrom e oxidase blobs (Tootell ct al. 19 8 8 c)
(Portrait Figure 5.36). Some blob cells specialize in red/
green opponcncy, others in bluc/ycllow opponcncy.
These cclls produce signals related to local color
contrast, which arc independent ot overall luminance,
since an increase o r decrease in luminance affects the
inputs in the same way, leaving the difference signal the
same (Gouras 1991). An opponcncy mechanism
typically operates with respect to a resting discharge.
R oger B. //. Tootell B orn in San Fran cisco . H e ob tain ed a B .A .
in psychology a t the U n iv ersity o f C a lifo rn ia , San ta B arbara, in 1 9 7 5
and a P h .D . at Berkeley in 1 9 8 5 . H e con d u cted p o std o cto ral work at
H arvard M ed ical S ch o o l. H e gained an academ ic ap p o in tm en t in
n cu ro biolog y at H arvard M ed ical S c h o o l, in 1 9 8 8 . H e is now professor
o f radiology a t H arvard M cd ical Sch oo l.
which may explain why maintained neural discharges in
the dark occur specifically in cytochrome-oxidase
regions (Snodderly and Gur 1995). This also explains
why cytochrome-oxidase cells show high metabolic
activity.
It has also been claimed that onlv a few interblob
cells show some color opponcncy (Livingstone and
Hubei 1984). However, evidence for the relationship
between color coding and cytochrome-oxidase
blobs is not conclusive (see Sincich and H orton
2 0 0 5 ).
4. Blob cells respond best to gratings with low contrast,
low spatial frequency, and high temporal frequency.
Interblob cells prefer higher contrast, high spatial
frequency, and low temporal frequency (Toocell ec al.
1 9 8 8 b ; Shoham ec al. 1997).
5. In the binocular cortex, blobs occur in rows, which tend
to be superimposed on the ccntcrs o f ocular dominance
columns (H o rto n 1984; T so et al. 1990). Cells in these
regions respond to excitatory inputs from only one eye.
Cells in intermediate regions respond to both eyes.
However, using voltage-sensitive dves, Landisman and
T so (2 0 0 2 ) found that about 2 5 % o f cytochrome-
oxidase color patches extended across ocular dominance
columns. M onocular enucleation in adult monkeys
leads to a reduction o f cytochrom c oxidase activity in
ocular dominance columns corresponding to that eye
(H o rto n and H ocking 1998a).
6. Ы оЬ cells o fsim ila r type tend to be laterally connected,
as do interblob cells. Blob cells and interblob cells do
not interact (Ts’o and G ilbert 1988).
7. Blob cclls o f V I project mainly to thin stripes in V 2 ,
which process color. Interblob cells project to thick and
pale staining interstripes o f V 2, which process colorless
form (see Section 5.8.2).
T he functional properties o f cells in the blob and
intcrblob regions arc not sharply segregated; border cclls
can show both color and orientation specificity (T s’o and
G ilbert 1988). Also, the contrast sensitivity and spatial-
frequency tuning o f cortical cells change gradually between
blob and intcrblob regions (Edw ardset al. 1995).
In the monkey, blobs receive inputs from the magnocel­
lular layers ot the L G N routed through cortical layers 4 C ( *
and 4 В and from parvocellular layers routed through corti­
cal layers 4 Л and 4 C f i . T he interblob regions receive par-
voccllular inputs through layers 4 Л and 4C/3 and from
mixed magnocellular and parvocellular inputs from cells in
the middle o f layer 4 C (Lachica ct al. 1992, Yoshioka c t al.
1994). Both regions therefore receive mixed magnocellular
and parvocellular inputs.
There are two views about the significance o f the blob-
intcrblob division o f the parvoccllular system. According to
Livingstone and Hubei, it represents a dichotomy into a
channel specialized for color but n ot form and a channel
specialized for colorless form. DeValois and DeValois
(1 9 8 8 ) proposed a different scheme in which the primary
distinction between blobs and interblobs is in spatial-fre-
qucncy tuning (see also DcValois 1991). This schcmc is
illustrated in Figure 5.37. Blobs contain cells tuned to low
Vertical
Left eye Right eye
f * . rc 5.3?. P irtw bed organ ization o f p rim a te visu al cortcx. Each m o d u le (b lo b
plus in tcrb lo b region ) is d om inated by on e eve. A lo n g radii, cclls are
tuned to progressively h ig h er spatial frequ en cies b u t have the same
orien ta tio n preference. O rie n ta tio n preferen ce ch anges sequentially
around the cen ter o f the m od u le. (Г о т DcV*bi**Ad DcValoi*
spatial-frequency stimuli (coarse detail) and the interblobs
contain cells tuned to high spatial-frequency stimuli
(fine detail), with a gradual transition between the two,
rather than a dichotomy.
/
DcValois and DeValois argued that the predominance
o f color-coded cells in the blobs is a simple consequence o f
the f i c t that parvoccllular cclls operate as color-opponent
cells for low spatial frequency stimuli and as luminance-
contrast cells for high spatial-frequency stimuli. This accords
with the analysis provided by Ingling (Section 11.5.4).
They also argued that the finer tuning tor orientation in
the interblobs is a consequence o f the fact that cells tuned
to higher spatial frequencies also have narrower tuning
for orientation. The two views both end up with a similar
division o f cell types, but the DeValois scheme makes this
division consequent on a fundamental segregation o f cells
according to spatial-frequency tuning.
5 .6 .7 C O N T E X T U A L A N D F IG U R A L
R E S P O N S E S IN V I
5 . 6 .7 a E f f e c t s o f C o n t r a s t i n g C o n c e n t r i c S tim u li
S o m e cells in the cat’s visual cortex respond more vigorously
to an optimal stimulus filling the receptive field when the
stimulus is surrounded by stimuli that have a contrasting
orientation, size, spatial frequency, or direction ot motion
(Nelson and Frost 1978; G ilbert and W iesel 1 9 9 0 ; G ilbert
et al. 19 9 1 ; Kooi ct al. 1 9 9 4 ; Kastncr ct al. 1996; Walker
ct al. 1999; Jones ct al. 2 0 0 2 ) .
Similar effects have been found in primates. In V I o fth e
alert monkey chc response o f a ccll to a particular stimulus
tended to be suppressed when a textured surround was
added. The degree o f suppression increased with increasing
density o f the surround (Knierim and Van Essen 1992).
Responses o f cclls in V I to a line were enhanced when the
line was surrounded by lines in a different orientation
(Nothdurft ct al. 2 0 0 0 ) . C clls in V I and V 2 o f the monkey
responded more strongly to a disk o f parallel lines when
background lines were orthogonal rather than parallel to
the lines in the disk (Marcus and van Essen 2 0 0 2 ; Muller
et al. 2 0 0 3 ).
For some cells in the cat visual cortex, the inhibitory
effect o f similarly oriented stimuli could be evoked dichop-
tically (DeAngelis et al. 1994). This suggests that it depends
on intracortical inhibitory connections rather than those in
the L G N .
The response of cells in V I ot alert monkeys to a tex­
tured region filling the receptive field varied according to
whether the region differed trom its surroundings in dispar­
ity, color, luminancc, m otion, o r orientation (Lam m c 1995;
Zipser.et al. 1996). However, G um m ing and Parker ( 1 9 9 9 )
could not rcplicatc the modulating effect o f t h e disparity o f
the surround.
A similar response enhancem ent occurred when m o n ­
keys detected a patch shaded to simulate concavity set
am ong patches shaded со simulate convexity (b ee ec al.
2 0 0 2 ) . The response ot cells to an even area o f illumination
varied with chc illumination o f che surrounding area in a
manner analogous to changes in the perceived brightness ot
a gray patch as the luminance o f chc surround is varied
(Rossi and Paradiso 1999).
These inhibicory mechanisms could provide a physio­
logical basis for che percepcual segregacion o f texcured
regions, since the response o f cells ot this type would be
enhanced by texture boundaries.
Psychophysical evidence shows that visual acuity and
shape discrimination arc degraded when a test stimulus is
flanked by similar stimuli (Sections 4 .8.3, 13.2.3). The
processes responsible must be cortical, since the effects are
present when che ccsc and flanking scimuli are presented
to different eyes (Westheimer and Hauske 1975). Also,
a texture element is easier to detect when surrounded by
different rather than by similar elements.
5 .6 .7 b R esponses to A ligned S tim u li
In the cats visual cortex, Nelson and Frost ( 1 9 8 5 ) revealed
a highly specific torm ol facilitation between neurons
wich aligned oriencacion tuning functions. In alert m on­
keys, chc response o f complex cells in V I со a line was
enhanced when a collinear line was added oucsidc chc
receptive field (Kapadia et al. 1 9 9 5 ,2 0 0 0 ) . Also, cells in VI
responded more vigorously when a sec ot aligned line clc-
mencs in a display o f random lines was made more salienc by
increasing che number or decreasing che spacing of che
aligned lines. The change in scimulus saliency was reflected
in the ability ot che monkeys со dccecc chc aligned lines
(Li ec al. 2 0 0 6 ) .
Evoked pocencials trom che human visual cortex were
stronger for a set o f aligned scimuli chan for a sec o f scimuli
wich differenc oricncations (Polac and Norcia 1996).
Lateral interactions in the visual corcex arc influenced
by che relative contrascs ot stimuli. Responses o f cells in the
cat visual cortex to a low-contrast G abor patch were
enhanced by a flanking high-contrast and aligned G abor
patch. However, responses to a high-concrasc G abor pacch
were reduced by boch aligned and orchogonal flanking
G abor pacchcs (Polac ec al. 1998).
The preferential linkage ot cortical cells with aligned
rcccptivc fields could serve as a mechanism for alignment
detection, as discussed in Section 4 .5 .2 c (M itchison and
Crick 1982). For example, collincar stimuli show mutual
facilitation o f detectability to a greacer degree chan scimuli
wich similar oriencacions buc which are noc collinear (Polac
and Sagi 1 9 9 3 , 1 9 9 4 ) (Porcraic Figure 5 .38 ).
Normally, che increased response ot a cell со increasing
scimulus screngch is accompanied by a proporcional increase
in variability ot responses со repeated stimulus presenta­
tion. However, increases in responses o f cells in cat area 17
to a G abor patch in the presence ot flanking collinear
h
Figvrc 5 .Л U ri P olat. B orn in Israel in 1 9 5 3 .1 Ic o b tain ed a B .S c. from the
H ebrew U n iv ersity,Jeru salem , in 1 9 7 7 and a P h .D . in n cu ro b io lo g y
wich D o v Sagi at the W cizm an n In stitu te o t Scien ce in 1 9 9 3 . I Ic
worked a t the S m ith -K cttlcw cll F.vc
4
Research In stitu te in San Francisco
from 1 9 9 3 to 2 0 0 0 . H e is now se n io r scien tist in the G o ld sch lcg cr live
Research In stitu te at Tcl-A viv U niversity.
patches were not accompanied by increased variability
(Kasamatsu ct al. 2 0 0 1 ) . Thus, collinear stimuli improve the
signal-to-noise ratio, especially near the threshold.
Facilitatory interactions in the visual cortex could help
in che percepcion ot a concinuous figure chac is pardy
occluded (Seccion 4.5.2c). Sugica ( 1 9 9 9 ) found chac cells in
V I ot che monkey responded со a bar with a disk across its
center when the disk was stcrcoscopically in front o f the bar
so as to create che impression o f a concinuous bar beyond an
occludcr. The cclls did noc respond when rhe disk was scc-
reoscopically beyond che bar elements. Dragoi and Sur
(2 0 0 0 ) have modeled orientation-specific facilicacory and
inhibicory interactions in che visual corcex.
The perception ot a subjective contour in a blank region
between aligned edges, as in che Kanizsa criangle (Figure
2 2 .2 0 ) could be due со laccral corcical inccraccions. Cells in
VI and V 2 o f che monkey responded со a figure defined by
subjective- concours indicated by disconnected but aligned
boundaries (von der Heydc and Pecerhans 1989; Marcus
and van Essen 2 0 0 2 ) . The response laccncy o t such cells was
abouc 7 0 ms in V2 but 100 ms in V I . This suggescs chac che
response in V I was due со feedback from V 2 (Lee and
Nguyen 2 0 0 1 ) . Cells chac responded со subjective concours
had end-scopped recepcive fields and responded со shore
scimuli chac cerminaced in line ends or corners wichin che
cells receptive field (H eider ec al. 2 0 0 0 ).
Laceral connections o f pyramidal cells in visual areas
such as che interior ccmporal corcex and che ccmporal
polyscnsorv area (area S T P ) cover an area more chan six
rimes chac o f pyramidal cells in V I (Elscon ec al. 1999).
Presumably, chis is due со che seleccivicy o f chcsc areas
tor complex stimuli thac span a large area. W e will see in
Section 5.8 thac more complex cypes o f figural processing
occur in V 2 , V 3 , and in che ventral processing path­
way. Neural activicy in differenc pares o f chc brain chac
underlies a particular percept may be linked by response
synchronization (see Section 4.3.4).
5 . 6 . 7 c E ffe c ts o f S tim u lu s O r g a n iz a tio n
Л related question is whecher a group of lines organized
inco a recognizable shape evokes a greaccr response in che
visual corcex chan the same lines in random order.
I.i ncs forming a pattern evoked a greater f'M КI responsecontrast-dependent changes in the size o f receptive fields.
in the human laceral occipical corccx than did randomly However, they found that only lateral connections in the
arranged lines (Murray etal. 2 0 0 2 ) . However, V I responded
less vigorously to a patterned stimulus than to the random
lines. Similar differences were found between randomly
moving dot arrays and coherent motion thac defined a
shape. Murray ec al. suggested that stimulus redundancy
detected in higher centers feeds back to V I . In other words,
activity in V I is reduced after a simple paccern has been
discovered in a complex scimulus.
Neurons in V I o f che alerc macaque monkey responded
more vigorously to texture elements belonging to a figure
chan со che same elemencs belonging со a ground region
(Lam m e 1995). However, Rossi et al. ( 2 0 0 1 ) found that
cells in V I responded to a figure region only when a cexturc
boundary fell in the receptive field. They concluded thac VI
neurons signal ccxcure boundaries but do not distinguish
between figure regions and ground regions.
There has been conflicting evidence about whether fig-
ural effects in V I arise within V I or involve feedback from
higher centers. In one study, the orientation-specific sur­
round effect in cat area 17 cook only 8 to 2 0 ms to develop,
which suggests that it does not depend on feedback trom
higher centers {Knicrim and Van Essen 1992). In a more
recent study, surrounding lines produced nonspecific inhi­
bition during the initial period after stimulus presentation.
The orientation-specific effect occurred with a latency ot
about 7 0 ms, suggesting that it arose from feedback from
higher centers (Nothdurft et al. 1 999). However, Hupe
ec al. ( 2 0 0 1 a ) found thac inaccivation o f V2 did noc atfecc
interaction effects in V I , at least in anesthetized monkeys.
Furthermore, C ro o k et al. ( 2 0 0 2 ) found that facilitation
produced by surrounding collinear stimuli was reduced or
abolished by focal inaccivacion o f collinear neighboring
cells in V I .
Lee ec al. ( 1 9 9 8 ) proposed that the late ( > 1 0 0 ms) pare
o f che response o f V I neurons is influenced by feedback
from higher visual cencers responsible for figure-ground
segregation. 'I he early componenc o f response o f V I neu­
rons occurred whecher or nor che monkey percepcually reg-
iscered chc scimulus objccc (as indicaced by saccadic
rcfixacion), buc the late response was absent when the object
was n ot registered. The late response was also absent in
anesthetized monkeys (Super et al. 2 0 0 1 ).
Tli is latter finding may explains why Hupc et al. (2 0 0 1 b)
did not observe feedback in V I with a 100 ms delay in anes­
thetized monkevs. Thev did find chac che firsc 10 ms o f
response o f V I neurons to a moving bar was affected when
M T was inactivated by cooling. However, one need not
conclude that feedback from M T occurs with such short
latency, because the bar was already moving before itentercd
the receptive field o f t h e ccll being recorded.
Angelucci et al. ( 2 0 0 2 ) argued from anatomical and
physiological evidence that monosynaptic lateral co n n e c­
tions in V I o f t h e monkey extend tar enough to account for
extrastriate cortex extended far enough to account for tig-
ural interactions that depend on stimulus tigural features.
Tli is issue is not yet resolved.
5 .6 .7 d E ffe c ts o f D iffe r e n c e s in P erceived Size
It is generally thought that the area o f excitation in V I is a
function o f the size o f the stimulus. However, Murray et al.
( 2 0 0 6 ) found that the area o f the f M R I response from che
human visual cortex increased about 20 % when an object
was merely made to appear larger. This was still true when
they controlled for differences in the contrasts o f the back­
ground. They concluded that the receptive fields o f cells in
V I increase in size as a function o f rhe perceived discance o f
an objccc. Such changes in reccptive-field size have not been
revealed in recordings from single cells. However, the
tuning ot some cells in V I , V 2 , and V 4 со changes in
stimulus size has been found to depend on che discance o f
the stimulus (D obbins e t al. 1998). Another possibility is
that, as the perceived distance o f a given o b je ct increases,
there is a larger spread ot activity over lateral connections
in V I .
5.6.8 EFFEC TS OF LEA RN IN G ON TU N IN G
F U N C T IO N S IN VI
Changes at synapses that occur during learning are discussed
in Section 6.4.4. Cortical plasticity in development is dis­
cussed in Section 6.5. A variety o f simple visual tasks, such
as vernier acuity and orientation discrimination improve
with practice (see Section 4 .9 ). Improvement o f stereoacu­
ity with practice is discussed in Section 18.14. The present
seccion deals with changes in the responses o f cells in the
visual cortex that accompany improvement in visual tasks
with practice.
The response properties o f cortical cclls are often inves­
tigated in anesthetized animals. This procedure cannot
dcccct effects due to highcr-order processing such as recog­
nition o f objects, attention, or motivation. A growing body
of evidence trom work on unancsthetizcd animals indicates
thac these factors modify the responses o f cortical neurons.
The concept o f sets o f cortical cclls with fixed tuning func­
tions to specific stimulus features must give way to a view o f
the cortex as a highly flexible organ in which the response
characteristics o f cclls arc conditional on simultaneous
activity in other cortical and subcortical centers in the brain
and on feedback from higher centers.
The receptive fields o f cells in che somatosensory cortex
and auditory cortex undergo considerable reorganization
following either intracortical microstimulation or sensory
stimulation (Dinse c t al. 1 9 9 0 b ; Recanzone et al. 1993).
W ith in area 17 o f chc cat, long-term changes in synaptic
conductivity along lateral pathways have been induced by
pairing synaptic responses with conditioning shocks o f
depolarizing current (H irsch and G ilbert 1993) (Section
5.5.6). This suggests thac lateral pathways are involved in
stimulus-dependent changes in cortical responses. Collinear
line segments arc easier со detect chan nonaligncd segmencs
(Scction 4.5.2b). The facilitator у effect o f alignment may be
modified by attention or by learning (Ito e t al. 1998).
In iontophoresis, charged molecules are introduced into
tissue by an clcctric current. M cLean and Palmer (1 9 9 8 )
paired stimuli with specific orientation or spatial phase with
iontophorecic applicacion ofexcicacory glucamace or inhibi­
tory G A B A to chc visual cortex o f cats. This procedure pro­
duced long-term increases or decreases in the response o f
cortical cells to stimuli close to the orientation or spatial
phase o f t h e conditioning stimuli.
’Ihere is conflicting evidence about whether tuning
functions o f neurons in the primary visual cortex are
affected by training on a specific discrimination task.
Schoups et al. ( 2 0 0 1 ) trained monkeys over a period o f
months со idencify che parcicular oriencacion o f a gracing.
This increased che slope o f che orientation tuning functions
o f cells in V I tuned ro orientations close ro che trained o ri­
entation. It produced no change in the preferred orienta­
tion o f cells, the number o f cclls responding to the trained
orientation, o r response variability.
G hose ct al. ( 2 0 0 2 ) trained monkeys in an orientation
discrimination task over a six-month period. Improvement
was oriencacion specific buc only marginally locacion spe­
cific. They found no changes in oriencation tuning o f
cells in V I o r V 2 chac could account for chc improved
oriencation discrimination. It is noc clear what caused the
difference between chcsc results and those o f Schoups cc al.
Furmanski et al. ( 2 0 0 4 ) trained monkeys for one m onth
со dccccc low-con erase oric need pacccrns. Training produced
a 3 9 % increase in the f M R I response from V I to stimuli in
che crained oriencacions. They suggesccd chac chere was an
increase in the number o f cells responding со these orienta-
cions, which implies chac some cclls changed cheir preferred
oriencacion.
The above cxperimcncs involved successive compari­
sons so chac chere was only one scimulus in view ac any
cime. Pcrcepcual learning involving the relative locations
or orientations o f simultaneously presented stimuli could
involve changes in the way cortical cells interact over hori­
zontal connections. Crist et al. ( 2 0 0 1 ) recorded from cclls
in the visual cortex o f two monkeys before and alter they
were trained on two casks. O n e cask was со dccccc when a
line was midway between two other parallel lines. The other
cask was со fixacc a scimulus. The monkeys showed substan-
cial improvement in the tasks, but the basic properties of
cortical cells such as cheir location, size, and oriencacion
cuning did noc change. However, improvement on the
bisection task was accompanied by a change in the way a
cclls response was modulated by chc presence o f a flanking
line. This change was noc evident when monkeys performed
chc fixacion cask.
In another experiment, Christ et al. trained monkeys on
a bisection task with three parallel vertical lines and on a
vernier-alignment task with three end-to-end vertical lines.
After training, all five lines were presented cogcchcr and chc
monkeys performed one or other task according to the
color o f che cencral line. W h en chey performed chc biscc-
cion cask, responses o f cclls in V I to che central line were
modulated by flanking parallel lines (side-flank tuning).
W h en they performed the vernier task, responses were
modulated by Hanking aligned lines (end-flank tuning).
Thus, the local neural network changed in a task-dependent
manner, even though chere was no change in chc scimulus.
In effect, the information provided by neurons in V I was
enhanced in a specific way according to chc cask.
In another experiment from the same laboratory two
monkeys were trained со dccccc an aligned sec o f line clc-
mencs in a random array of similar line elements (L i et al.
2 0 0 8 ) . Initially, responses o f cclls in V I to collinear lines
and randomly arranged lines were rhe same. After training,
an embedded set of collinear lines induced strong responses
specific to chc trained retinal location.
Thus local neural networks in V I modifvi their June-
cional scruccure in a cask-dependenc manner. This contex-
cual modification is presumably directed by signals arising
from higher levels in the visual syscem chac arc criggered by
attention to a specific stimulus and a specific task. These
higher centers must store chc required modifications so chac
the correct modification can be applied when the animal
performs a given cask.
Changes in the primary visual cortcx have been detected
after more complcx learning tasks. Visual scimuli having
behavioral relevance as a result of learning evoke stronger
responses in corcical cells. Thus, abouc one-chird o t chc cclls
in V I o f the monkey increased cheir response by abouc 2 0 %
when che stimulus was one chac che animal had been crained
co recognize (Haenny and Schiller 1988). A similar response
increment plus a narrowing o f orientation tuning was shown
by about chree-quarcers o f cells in area V4. Buc these effects
could have been related to a change in arousal.
Changes in tuning functions o f cells resulting from
learning have been found in M T and M S T (Section 5.8.4b),

г.*«.« s .j* C harles G ilbert; H e o b ta in ed д В .Л . from A m h erst C o lleg e in
197 1 and a P h .D . w ith D . H u b cl and T . W iesel from H arvard
U niversity in 1 9 7 7 . B etw een 1 9 7 7 and 1 9 8 S he held academ ic
ap p oin tm ents at H arvard M ed ical S ch o o l. In 1 9 8 5 he m oved to the
R ock efeller U n iv ersity in New York, w here he is now A rth u r and Jan et
Ross Professor. H e w on the K rieg C o rtic a l K udos, C o rtic a l D iscoverer
Prize in 1 9 9 3 and the W . A lden Sp enser Award in 2 0 0 2 . H e is a
m em b er o f th e N ation al A cadem y o f Scien ces.
V 4 (Section 5.8.3a), chc inferior cemporal corccx (Scccion
5.8.3b), and the frontal lobes (Seccion 5.8.4g ). Frith and
Dolan (1 9 9 7 ) reviewed the brain areas responsible for
modification o f responses according to stimulus familiarity.
See Buonom ano and M crzcnich (1 9 9 8 ) for a review o f co r­
tical plasticity, and G ilbert et al. ( 2 0 0 1 ) for a review o f t h e
neural basis o f learning (Porcraic Figure 5.39).
5 .7 C O L U M N A R O R G A N IZ A T IO N
OF THE CO RTEX
Lorente de N o ( 1 9 4 9 ) was the first person to propose that
chc cerebral corcex is organized inco columns. He studied
patterns o f synaptic linkages anatomically and showed that
they run predominantly vertically from layer to layer with
fewer connections running horizontally. Sperry e ta l. (1 9 5 5 )
provided the first functional evidence o f columnar organi­
zation. He lound that vertical slicing of the visual cortex
produced little or no ctfccr on the ability o f cats to perform
fine visual discriminations. Mountcastle ( 1 9 5 7 ) produced
the first clcctrophysiological evidence o f columnar organi­
zation by recording from single cells in the somatosensory
area o f the cat. He wrote,
neurons which lie in narrow vertical columns, or
cylinders, extending from layer II through layer IV
make up an elementary unit o f organization,
for they arc activated by stimulation o f the same
single class of peripheral receptors, from almost
identical peripheral rcccptive fields, at latencies
which are n ot significantly different for the cells o f
the various layers.
4
(M OUNTCASTLE ! 9 $ 7 ,p .4 0 S )
The cortex develops by columnar growth from progeni­
tor cclls lining the embryonic ventricles (see Chapter 6).
This lining contains a protomap o f the prospective
cytoarchitectonic areas (Rakic 1988).
5.7.1 CO LU M N T O P O L O G Y
The cells in each small column of tissue running at right
angles to the cortical surface o f the primary visual cortex
have the same tuning to stimulus orientation, although
there is sometimes a reversal oforientation tuning at layer 4
(D o w 1991). These columns ot similarly tuned cells arc
known as oriencacion colum ns. In each column there are
thousands o f cells with similar orientation preference. In
the cat and monkey, the orientation preference o f cclls
rotates smoothly through its full range of 180°, as one tra­
verses across the cortical surface through a distance o f
between 0.5 and 1.0 mm. W ith in each colum n a random
variation in orientation tuning is superimposed on the
transition ot tuning between columns ^Hethcrington and
Swindale 1999).
Binocular cells in each local column o f the visual cortex
have a predominant excitatory input trom one eye. They arc-
segregated from cells in a neighboring column that have a
predominant input trom the other eye. Left-eyc and right-
eye columns form alternating stripes over the surface o ft h e
cortex. These are known as o cu lar d o m in a n ce colum ns.
W ith in each ocular dominance column, the monocular
receptive fields ot each binocular cell have similar tuning tor
position, orientation, and temporal properties. Ocular
dominance columns are discussed in the next section.
Hubei and Wiesel (1 9 7 4 b ) favored the view that orien­
tation columns form bands orthogonal to the ocular d o m i­
nance bands. However, this ice -cu b e pattern o f columnar
organization had to be revised when it became evident that
columns containing cclls tuned to a particular orientation
do not form continuous bands. Instead they are interspersed
with patches o f neurons (blobs) containing cclls n ot tuned
to orientation. In some regions, known as lin ear zones, iso-
orientation contours run in parallel over distances o f
between 0.5 and 1 mm, and orientation preference changes
lincarlv wich distance across the contours. The linear zones
are interrupted by a variety o f nonlinear zones. At ridge­
shaped fractures, orientation preference changes abruptly
by less than 90°. At singularities, orientation preference
changes by more than 90°, increasing cither with clockwise
rotation or with counterclockwise rotation around rhe
singularity. This is the pinw hccl pattern depicted in

(a) Positive singularities
m \ \
v ^
t tty
m tl
(b) N egative singularities
Figure 5.-*o. Types o f sin gu larity fon n cd by pattern s o f lectors*
Figure 5.40a. Ac saddle points, orientation preference
rotates clockwise in cither direction trom one axis and
counterclockwise from rhe orthogonal axis (Blasdel 1992b;
Obertnayer and Blasdel 1993).
Ic has been suggested chat a giant M c y n c r t ccll occupies
the center o feach singularity (von Seelen 19 7 0 ; Braitenberg
and Braitenberg 1979). Mcyncrc cclls arc solitary giant
pyramidal cells in layer 5 o f che visual corcex thac send richly
branched apical dcndriccs inco cortical layers 1 and 2, and
other dendrites inco layers 5 and 6. These are che layers in
which intracorcical and subcortical connections originate
(Chan-Palay e t al. 1974). Large cells resembling Meynert
cells also occur in layer 6 o f V I and project directly to M T
and to the superior colliculus (Shipp and Zeki 1989), which
suggests that these cells are relaced to che processing ot
motion.
Singularities o f orientation preference (pinwheel cen ­
ters) tend to occur along che cencral axis o f each ocular
dominance column and coincide with peaks o f ocular d o m ­
inance (Crair ec al. 1997). Cycochrome oxidase blobs also
cend со occur along rhe same axes buc are noc coincident
with che singularities (Barcfeld and Grinvald 1992). Linear
iso-orientation contours tend to be orthogonal to the
boundaries between adjacent ocular dominance columns
(Blasdel ec al. 1 995). Fractures, where oriencacion prcfer-
cncc changes abrupcly by less chan 9 0 “, ccnd со be eichcr
parallel to or orthogonal со ocular dominance bands
(Blasdel and Salama 1986).
There has been some disagreement abouc che corcical
representation o f spatial frequency. It has been reported
that neurons in one layer o f che visual corcex o f che cac share
the same preferred spatial frequency (Berardi ct al. 1982).
Tolhurst and Thompson ( 1 9 8 2 ) found some local aggrega-
cion o f cells with similar spatial-frequency tuning but co n ­
cluded that spatial-frequency tuning is not closely tied to
either cortical layers or columns.
According to a study using optical imaging in the visual
cortex o f the cat, cclls preferring high spatial frequency
( X pathway) are segregated from those preferring low spa­
cial frequency ( Y pachwav). Regions coding low spacial fre­
quency tended to occur in rhe cencers o f ocular dominance
columns (H iibencr ec al. 1997).
Anochcr opcical imaging scudy on chc cac found chac
spacial-trequency domains, like orientation domains, were
organized continuously in pinwheel patterns (Everson etal.
1998). Issa et al. ( 2 0 0 0 ) produced a finer map ot spatial-
frequency domains in chc visual corcex o f che cac by co m ­
bining imaging with microeleccrode recording. They tound
a complccc and continuous represencacion o f spacial fre­
quency within each hypercolumn (0 .7 5 mm). The low and
high excremes o f che range tended со occur in discincc pin-
wheel singularities tor oriencacion preference. There was
no significant relacionship bccwcen low spatial-frequency
domains and ocular dominance columns. Issa ec al. argued
chac spacial-frequency excremes chac occur on chc cencers o f
oriencacion pinwhcels ensure chac all oriencacions are repre-
scnccd ac chesc rare buc imporcanc spacial frequencies. Less
cxcrcme spatial frequencies arc mapped concinuously round
chc oriencacion pinwheel.
Sirovich and Uglcsich ( 2 0 0 4 ) argued chat these optical
imaging studies were subject to artifacts arising from blood
circulation. Using an improved method, chey found no evi­
dence tor columnar organization for spatial frequency.
W hen chey reanalyzed the data from Everson et al. chey
tound thac they agreed with their own results.
The preferred direction o f motion o f a cortical ccll is
orthogonal со its preterred orientation. The com bined ori­
entation/direction preference o f a cell can thus be repre­
sented by a directed line element (a vector). Maximum
continuity o f both orientation and direction preference
would be achieved it, round each singularity, orientation
preference cycled twice through its 180" range o f values,
while direction preference cycled once through its 360°
range o f values. In the scheme depicted in Figure 5.40 a, ori­
entation/direction preference changes in an ordered
sequence round the ccntcr o f the singularity, so that cells
with a particular orientation/direction prctcrence radiate
out from the center to form a pinwheel pattern. C ells tuned
to progressively higher spatial frequencies are arranged ouc
from che center, and different blobs have different ch ro ­
matic properties (DeValois and DeVaiois 1988).
Theoretically, the pinwheel pattern is only one o f three
patterns that can be torined trom a vector field by con tin u ­
ous deformations involving a cyclic periodicity of 360°.
Concentric and radial paccerns define posicive singularities,
and a hyperbolic pattern defines a negative singularicv.
as shown in Figure 5.40. Consider a stimulus vector
(directed line element) moving clockwise over «1 circular
path round a singularity in a plane. If the orientation/direc­
tion preference ol the cells chat the vector encounters also
changes clockwise then the pattern o f preference forms
either a radial or concentric pattern, as in Figure 5.41a.
Iso-orientation loci and loci ofstim ulus alignment coincide
in the radial pattern but are orthogonal in che concentric
pattern. O n the other hand, a counterclockwise change in
stimulus preference produces rhe hyperbolic pattern in
Figure 5.41b (Penrose 1979). In this pattern, iso-orientation
loci coincide with loci o f stimulus alignment only along
cardinal directions. These are the only types o f singularity
that allow for continuous transformations o f vectors.
However, we shall see that cortical patterns contain
discontinuities.
For cells tuned to a particular orientation, those tuned
to motion in one direction are spatially segregated from
those tuned to motion in the opposite direction (BonhoeHer
and Grinvald 1993). Thus, orientation preference cycles
through its 180° range only once round each singularity.
(a) Positive singularities, 3 6 0 J rotation period
(b) N egative singularity
3 6 0 ' period
(c) Positive singularity (d) N egative singularity
180 period 180' period
r.*ort 5 .41 . The topology o jco rtica l columns. L ines rep resent loci o f icccp tiv c-
ficld align m en t. D o tte d lines represent loci o fc iju a l orien tation
preference. Bars w ith an arrow represent o rien ta tio n and d irection
preferences.
while direction preference changes through only half its
3 6 0 ° range. A second orientation singularity is required to
cover the other h a lf o f the range o f direction preference.
Since direction preference does not change round an
orientation singularity, the periodicity o f a cyclic change in
orientation preference becomes 180° rather than 360°. Let a
stimulus vector move clockwise over a circular path round a
singularity and encounter cells for which oriencacion pref­
erence also changes clockwise through 180°. This generates
the loop pattern shown in Figure 5.4 lc. The tri-radius pat­
tern shown in Figure 5 . 4 Id is generated when the cyclic
path and rhe changing orientation preference have opposite
signs. Fingerprints, Zebra stripes, and stripes on several spe­
cies o f fish conform to this topology. If a loop is assigned a
value o f +1 and a tri-radius pattern a value o l —1, a cyclic
path that contains one o f each type o f singularity has a
value ot 0. In general, the value o f any circular path over
the plane is the algebraic sum o f the values o f the singulari­
ties contained within the cyclic path. In both the loop and
tri-radius patterns all the iso-orientation loci are radial,
but the stimulus-alignment loci are radial only at certain
points.
Radial, concentric, and hyperbolic patterns, together
with linear grids, form the family o f differencial operators
(orbits) o l Lie groups (Section 3.7.1). Recordings trom
single cells distributed in a grid over the ca ts visual cortcx
have revealed a cyclic organization o f orientation prefer­
ence (Swindalc ct al. 1 9 8 7 ; D ow 1991). Cyclic patterns o f
orientation-selectivity have been revealed more directly by
the optical imaging ot lighc reflected trom the cortical sur­
face (T so et al. 1 990). Blasdel ( 1 9 9 2 b ) used optical imaging
to reveal both loop and tri-radius patterns ot orientation
preference in V I o f the monkey.
Regions o f the visual cortex responding to a grating pre­
sented in a particular orientation have higher absorption o f
red light because ot the presence o f deoxyhemoglobin.
Bonhoetfer and Grinvald ( 1 9 9 3 ) used this procedure to
produce detailed maps o f orientation preference in area 18
o f the cat. VCeliky et al. ( 1 9 9 6 ) , also, used optical imaging
and confirmed that orientation preference cycles once
round each singularity with a 180° discontinuity in direc­
tion preference, and that two singularities are required to
cover the full range o f direction preference.
Thus, iso-orientation domains are subdivided into
patches selective for motion in opposite directions. There is
some tendency for orientation singularities to occur in pairs
with opposite signs and to be connected by iso-orientation
bands running at right angles со che boundary between
the two ocular dominance columns that contain them
(Blasdel and Salama 1986; Bartfeld and Grinvald 1992).
C onn ection s between orientation singularities o f t h e same
sign form saddle points. Figure 5 .4 2 shows loci o f iso-
oriencation preference superimposed on ocular dominance
columns derived from optical imaging (Obermayer and
Blasdel 1993).
i-.fiurc5.i2. C ortical colum ns ofm on key /7 . Iso -o rien tatio n lines (gray) arc
draw n at in tervals o f 1 1 .2 5 ’ . Black lines arc b ord ers o t ocu lar
d om inan ce bands. (F rom O b erm ay cr and Blasd cl, C o p y rig h t 1 9 9 л by
chc S o c ic tv o f N eu ro scien cc)
It had been generally believed that cells at the center o f
orientation singularities at pinwhccl centers arc not tuned
to orientation. However, detailed single-cell recording near
the singularities revealed that they contain many cells
sharply tuned to orientation (M aldonado ct al. 1997). The
apparent lack ot orientation tuning arises when responses
arc averaged over the singularity. O h k i ct al. (2 0 0 6 ) used a
calcium-sensitive fluorescent dye to reveal the simultaneous
activity o f many cclls in pinwhccls in the visual cortex o f
cats (see Section 5.5.4d ). Many neurons selective to partic­
ular orientations were clearly present even near the pin-
wheel centers, although their responses were weaker and
more broadly tuned than those o f cclls away from the ccntcr.
A more recent study has revealed that cells in regions where
orientation preference changes slowly arc more finely tuned
to orientation than are cells in regions where orientation
preference changcs rapidly, as in the pinwhccl centers
(Nauhaus et al. 2 0 0 8 ).
Toward the end o f his life, Alan Turing ( 1 9 5 2 ), the p io ­
neer o f computer science, became interested in biological
form. He demonstrated theoretically that diffusion o fa c ti-
vator and inhibitor chemical morphogens over idealized
cclls in a growing organism results in a variety o f static or
oscillatory patterns. The type o f pattern depends on the
relative rates o f diffusion and the reactivity o f t h e m orpho­
gens (sec also P enget al. 2 0 0 0 ). These T u rin g p attern s have
been demonstrated in an actual medium and resemble the
columnar and blob-interblob patterns o f the visual cortex
(Kapral and ShoWalter 1995). It has been shown that inter­
actions between morphogens and their inhibitors can
account tor feather patterns in birds and hair-follicle pat­
terns in m icc (see Maini et al. 2 0 0 6 ) .
Swindale ( 1 9 8 0 ,1 9 8 2 ) (Portrait Figure 5.43) developed
a model o fth e development o f cortical columns. The model
is based on short facilitator у and long inhibitory neural or
chemical interactions between cortical cclls o f the same
Figure N icholas S im u late. B o rn in E dinburgh in 195 1. Me ob tain ed a
В .Л . in natural scicn ccs a t C am brid ge in 1 9 7 2 and a P h .D . w ith P.
B en jam in in n cu ro b io lo g y a t Sussex U n iv ersity in 1 9 7 6 . H e did
p o std o cto ral w ork w ith C . Blakcm ore and H . Barlow a t the
Physiological L ab oratory, C am b rid g e. H e was assistant professor in the
D ep artm en t o f P sychology and Physiology ac D alh o u sic U niversity
from 1 9 8 4 to 1 9 8 8 . C urrently, he is professor in the D ep artm en t o t
O p h th a lm o lo g y a t the U n iv ersity o f B ritish C o lu m b ia , C anad a.
type and opposite interactions between cells of the oppo-
site type (see also Linsker 1986). In a development o f t h e
model, orientation singularities tended to becom e centered
in ocular dominance columns it, during development, plas­
ticity o f selective tuning is turned off first within ocular
dominance columns (Swindale 1 992). A neural network
model o f the cyclic organization o f orientation tuning in
the visual cortex has been described by C osta ( 1 9 9 4 ).
McLaughlin et al. (2 0 0 0 ) developed a neural network
model o f orientation tuning based on both the anatomy
and the feedforward and feedback responses ofcells in layer
4 Cot o f macaque V I . They predicted that cells near pin-
wheel centers would be more sharply tuned to orientation
than cells away from the center. However, Maldonada et al.
failed to find such a difference in tuning. K an g er al. ( 2 0 0 3 )
produced a model that predicts homogeneous tuning
functions.
The topological complexity ot V I arises because its two-
dimensional surface maps multiple values o f each o f several
features. The mapping could be achieved by a selt-organizing
system that reconciles the following requirements (Kohonen
2001 ).
1. Complete regions Cells coding a complete range o f
stimulus features should be packed efficiently in each
cortical region.
2. Continuousfeatu re representation The full range o f Left-eye columns alternate wich righc-cyc columns. The pro­
values ot each feature should be represented jections of the ocular dominance columns on rhe corcical
continuously in cach cortical region. surface arc known as ocular dominance scripes.

3. Sim ilarity o f neighboring cells W ith in each feature

system, cclls with similar stimulus preferences should be 5 .7 .2 a M a p p in g O c u l a r D o m i n a n c e C o lu m n s
neighbors so as to economize on connections and
O cu lar dominance columns were firsc revealed by recording
facilitate the formation o f receptive fields of cells higher
from single corcical cells discribuced over che corcical sur­
in the visual system.
face (Hubei and W iesel 1959). Colum ns were then revealed
4. Feature separability Maps o f different features over the anatomically in the monkey by che Nauca method, which
cortex should be separable. For example, che mapping involves tracing areas o f cell degeneration in che corcex p ro­
of orientation preference is distinct from the mapping duced by selective destruction o f L G N cells arising from a
o f ocular dominance. See Yu et al. ( 2 0 0 5 ) for a given eye (Hubei and Wiesel 1 9 6 9 ), and by silver staining
discussion o f this issue. (L e V ay etal. 1 975).
Grafstein and Laureno ( 1 9 7 3 ) showed that a mixture of
'Flic sizes and shapes o f oriencacion columns are highly
tritiated proline and fructose injected into che eye o f a
variable among cacs, although gcnccicaliy rclaccd animals
mouse travels up che axons o f che optic nerve through relay
show some similarity in column scruccure (Kaschube ec al.
cclls in the L G N and becomes concentrated in cells in layer
2002 ).
4 of the contralateral visual cortex. The resulting patterns of
C ortical copology is noc immutable. Electrical stimula­
radioactivity in chin sections o f corcical cissue can be
tion of a ccll in the visual cortex o f adult cats over a period
recorded on film to produce autoradiographs.
o f several hours induced changes in che oriencacion tuning
Wiesel e t al. ( 1 9 7 4 ) used che autoradiograph procedure
o f cclls over a region extending several millimeters (Goddc
to reveal the ocular dominance columns in the macaque
ec al. 2 0 0 2 ). Single-cell recording revealed chac che preferred
monkey.
oriencacion o f neighboring cells was shifted toward chac o f
In a related procedure, deoxyglucose labeled with
chc stimulated cell. O ptical imaging o f chc cortical surfacc
carbon 14 is injected inco an animal, which is then exposed
revealed extensive restructuring o f the pattern o f orienta­
со scimuli presenced to one eye for an hour or more (Sokoloff
cion selectivity in thac neighborhood.
ec al. 1977). Cells taking up radioactive tracer in the hem i­
The copology o f ocular dominance columns is discussed
sphere contralateral to che injecced eye are chose chac nor­
in th eS cccio n 5.7.2c. For compuccr models o f chc copology
mally receive a scrong excitatory inpuc trom chac eye. Since
o f che visual corcex see Tanaka ( 1 9 9 1 ) , Erwin ec al. ( 1 9 9 5 ),
cells wich balanced ocular dominance also receive excicacory
Swindalc ( 1 9 9 6 ) , and Grabska-Barwinska and Malsburg
inputs from the ipsilaceral eye, che dark bands produced
(2 0 0 8 ).
by injection o f one eye must overlap those produced by
injection ot the ocher eye.
5 . 7 .2 O C U L A R D O M IN A N C E C O L U M N S
The separate autoradiographs from successive slices o f
Hubei and Wiesel ( 1 9 5 9 ) , working with che cac, provided the visual corcex can be combined by compucer rcconscruc-
the firsc evidence o f convergence o f inpucs from che cwo cion inco a complete pattern o f columns. Using data on che
eyes o n to cells in che visual corcex. In che macaque monkey, topography ot the visual cortex, the pattern ot ocular dom i­
they reported chac cach local group of cells in layer 4 C nance columns can be transposed onto a 3-D map o f the
receives excitatory inputs from only one eye (Hubei and visual cortex, as shown in Figure 5-44.
Wiesel 1 968). More recent evidence from alerc monkeys
suggests chac many cells in layer 4 C receive inpucs from
boch eves, racher chan from only o n e (Snoddcrly and Gur
1995). Ipsilaceral inpucs may derive from pyramidal cells in
layer 6 (W iser and Callaway 1997).
Signals are relayed from layer 4 C со cells in ocher layers
in che same vertical column o f corcical cissue. Mosc o f chese
cclls also receive inpucs from chc ocher eye from cclls in layer
4 C in a neighboring column (Hubei and Wiesel 1962).
Alchough binocular cclls in cach local column o f chc visual
corcex receive inpucs from boch eyes chey receive an excic-
acory input predominantly from one eye. The cclls arc said
to have ocular dominance. Cells with similar ocular dom i­
O cular dom in an ce ban ds o fm o n k ey visu al cortex. Pattern derived
nance form bands o f tissue running through the thickness o f from a series o f au toradiograp hs and transposed o n to a 3 - D m ap o f die
che corcex. These are known as ocular dom inance columns. v i s u a l C O r C e X . (From U V i y c t Д Cnpyngh* by i t * S o n n y o f N r tirnifiow c)

Figure 5*45. P hotograph o f o ttd a r dofu in an ce bands. T aken from chc visual
c o rtc x o t a living m onkey. D ark bands arc d om in ated by the left eve.
The bou n d ary betw een V 1 and V 2 is across chc cop o t chc picturc.
O cu la r d o m in a n ce bands d o n o t cross th is boundary. <FmmT.W al. i w ,
R cp n atcd with pctitmwon from A A A S)
In another method, dves sensitive to voltage changes
associated wich neural impulses are infused into the cortex
o f an alert animal. O n e eve
j is stimulated,7 and the ocular
dominance columns are revealed by scanning the cortical
surface with a video recorder (Blasdel 1992a). Neural activ­
ity causes slighc changes in the reflectivity o f the cortical
surface even without the use of dyes. These changes in co rti­
cal reflectivity can also be photographed. Figure 5.45 shows
an example ot an in vivo photograph ot ocular dominance
columns in monkey V I that were obtained in this way by
T so e ta l. (1 9 9 0 ).
O cular dom inance columns have been revealed in post­
mortem sections o f the human visual cortex (H itch cock
and Hickey 1980). They have also been revealed by staining
for cytochrom e oxidase o f V I taken from the cadavers o f
humans who had been blind in one eye. The columns arc
about 1 mm wide, running at right angles to the 1 7 - 1 8
border (Horcon and Hedlcy-Whice 19 8 4 ; Horcon ct al.
1 990). M ore recently, che complece pattern o f columns has
been revealed by cytochrome-oxidase staining flat-mounted
specimens o f the whole o f V I from six monocular humans
(Adams et al. 2 0 0 7 ) . Colum ns had a mean width o f
8 6 3 fJm. The number o f column pairs varied between
7 8 and 126, and the column patterns were highly variable.
Cytochrome-oxidase patches were centered on ocular
dominance columns in layer 4 C except in one specimen in
which patches and columns were noc aligned. Squirrel
monkeys show the same lack of correlation between cvto-
chromc'oxidasc patches and ocular dominance columns
(Section 5 . 7 . 2 f ).
O cu lar dom inance columns have also been revealed the
f M R I from the human corcex (M e n o n e ca l. 1997; Grinvald
e ta l. 2 0 0 0 ; C heng e t al. 2 0 0 1 ).
O cu lar dominance columns may also be mapped by
suturing or removing one eve and, some days later, preparing
slides o f the visual cortex stained for natural produces o f
neural activity induced by the open eye. These products
include cytochrom e oxidase (Florence and Kaas 1992;
Tigges et al. 1 9 9 2 ; DeYoe et al. 1 995), G A B A (Hendry
ct al. 1 994), protein kinase (H endry and Kennedy 1986),
and m R N A transcription molecules thac regulace gene
expression (Chaudhuri ec al. 1995).
The development o f ocular dominance columns is dis­
cussed in Section 6.7.
5 . 7 .2 b P ro p erties o f O c u l a r D o m i n a n c e C o lu m n s
In the cat’s visual cortex, in a region corresponding to a strip
extending 12" on eicher side o f t h e vertical midline, abouc
9 0% of complex cells and 7 0 % of simple cells are binocular.
O nly layers 4 and 6, which receive direcc inpucs from the
L G N , contain appreciable numbers of monocular cells.
Beyond 12°оп eitherside o fth e midline,contralateral inputs
gradually become more numerous than ipsilateral inputs.
Finally, in the monocular crescent, all cells receive their inpuc
only from the contralateral eye (Berman et al. 1982).
Each binocular ccll has two receptive fields, one in each
eye, with similar oculocentric positions. The two receptive
fields are similar in cheir tuning to orientation and spatial
frequency, and many have similar tuning to temporal fre­
quency and direction-of-m otion. They also have the same
length-summation, end-scopping, and simple or complex
characceriscics (Hubei and Wiesel 19 6 2 ; 1968; Maskc ec al.
1984; Skoccun and Freeman 1984; Hammond and
Fothcrgill 1991). The orientation preferences ot monocular
cells are distributed isotropically, while those o f binocular
cells, especially in the central retina, tend со clusccr abouc
horizontal and vertical meridians (Payne and Berman 1983).
Binocular cells that respond to excitatory inputs trom
eicher eye do so wich similar short latency. This suggests
chat they receive direct inputs from cells in layer 4 serving
che ipsilaceral and concralaceral eyes, racher chan a direcc
input trom one eye and an indirect input trom the other
(Ito et al. 1977). Also, the complete pattern o f synaptic
inputs from the two eyes, involving monosynaptic excit­
atory inputs and polysynaptic excitatory and inhibitory
inputs, are the same (Ferster 1990). The issue ot differential
response latencies is discussed further in Chapter 23.
This fundamental similarityф of the two monocular
receptive fields feeding inco a binocular ccll allows chc
visual syscem со match the images in che cwo eyes. This is a
prcrcquisicc for chc crcacion o f a unified binocular field.
Nevercheless, differences becween che receptive fields of
binocular cclls do occur. The com ponent monocular rcccp-
cive fields o f simple cells in each corcical column o f the cac
visual corcex have spacial phases chac vary bccween 9 0 and
180° (Pollen 1981; DeAngelis ec al. 1 999). This could allow
for econom y of linkages becween cells in phase quadracure,
as described in Seccion 4.4.1c. Ic could also allow for che
formacion ot complex cells wich responses indcpendcnc o f
stimulus position within the receptive field, and for noise
reduction. W e will see in Chapter 11 that differences in spa­
tial position o r phase o f the receptive fields o f binocular
cells form the basis for detecting binocular disparity and for
stereopsis.The region o f visual cortex containing a full 180"
cycle o f orientation preferences has roughly the same width
as an ocular dominance column. Regions containing a
full set o f orientation-tuned cells for each eye are called
hypercolumns. In the monkey, hypercolumns have a
diameter o f 0.5 to 1.0 mm at eccentricities up to at least 15 й.
There is a surprising degree o f variability between m em ­
bers o f t h e same species. For example, one macaque monkey
had 101 pairs o f ocular dom inance columns along the VI/
V 2 border, while another monkey had 154 pairs. Also,
mean column width varied between 3 9 5 and 6 7 0 jUm
(H orton and Hocking 1996a). Each hvpercolumncontains
all the cell types required for coding the full range o f visual
features in the area o f t h e visual field from which it derives
its inputs (Hubei and W iesel 1974a). Neighboring hvper-
columns receive inputs from overlapping retinal regions,
and each hypercolumn is fed by the same number o f gan­
glion cells. Excitatory and inhibitory dendritic connections
extend over several columns (see Section 5.5.6).
5 . 7 . 2 c T o p o lo g y o f O c u l a r D o m i n a n c e C o lu m n s
In the c a ts visual cortex, columns with left-cye ocular dom ­
inance form a series ot isolated patches and shore parallel
bands interspersed with similar patches and bands with
right-cye dominance. The bands often bifurcate or end in
blind endings (Lowel et al. 1988). They run mainly perpen­
dicular to the border between areas 17 and 18 (Lowel and
Singer 1987) and extend through all rhe layers o f the visual
cortex (Tootell et al. 1988c). In the cat, the bands in area 17
cluster about 0.4 mm in width but can be up to 0.55 mm in
both the central and peripheral visual field (Lowel 1994;
T iem an and Tumosa 1 997). The bands are wider in area 18
(Shatz et al. 1977; Anderson et al. 1988). In V I o f the
macaque monkey the ocular dom inance bands for the co n ­
tralateral eye were found to be about 0 .4 7 mm wide. Those
for the ipsilateral eye were about 10% narrower (Tychscn
and Burkhaltcr 1997).
In each half o f the visual cortex, the whole binocular
contralateral hemifield is retinotopically mapped onto the
ocular dominance bands o f the left eye, and again o n to the
ocular dominance bands o f the right eye. A long bands, this
representation is approximately continuous, although it
varies as a function o f changes in orientation preference
(Das and G ilbert 1997). Across ocular dominance bands,
there is an alternation between left- and right-eye bands.
For details o f how these interrupted retinotopic representa­
tions are organized see Hubei and Wiesel (1 9 7 7 ).
To some extent, ocular dominance bands follow isoec­
centricity lines. However, LeVay and Voigt ( 1 9 8 8 ) claimed
that the band pattern in the cat is determined mainly by a
tendency o f bands to run across the elliptical visual cortcx
at right angles to the 17/18 border. LeVay ct al. ( 1 9 8 5 )
found this tendency to be stronger in the monkey than in
the cat. They argued that this is the simplest way to co m ­
bine circular monocular retinotopic maps o n to an elliptical
surface. Also, it minimizes anisotropy o f the magnification
factor across and along bands. Anderson et al. (1 9 8 8 ) found
only a weak tendency for the bands in area 17 to run at right
angles to the 17/18 border in the cat, although this ten ­
dency was more pronounced in area 18. They pointed out
that L G N layers and the striate cortex have similar oval
shapes, so that the cortical axis is n ot elongated along any
axis by intcrdigitating L G N inputs.
Jones ct al. ( 1 9 9 1 ) developed a computational model
based on these differences between monkeys and cats,
which accurately predicts the different ocular-dominance
patterns in the two species. Similar models were developed
by G oodhill and W illshaw ( 1 9 9 0 ) and by Bauer (1 9 9 5 ).
Chklovskii ( 2 0 0 0 ) argued that the theory that the
topology o f ocular dom inance bands is designed to m ini­
mize cortical stretching does n o t explain the different ori­
entation o f bands in the parafoveal region. They proposed
that, in each part o f the visual field, ocular dominance bands
arc parallel to the direction o f the most frequently occur­
ring binocular disparity. They argued that, in the foveal
region, disparities are predominantly horizontal while, in
the periphery, they tend to follow isoeccentricity lines.
This arrangement minimizes the lengths o f connections
between cells that register disparate images, as illustrated in
Figure 5.46.
5 .7 .2 d O c u l a r D o m i n a n c e S c a lc
Hubei and W iesel ( 1 9 6 2 ) introduced a seven-group o cu la r
d o m in a n ce scalc. Cells in group 1 respond only ro inputs
from the contralateral eye, and those in group 7 respond
only to inputs from the ipsilateral eye. The eye nor evoking
a response in a given cell is known as the silent eye. ( ’ ells in
group 4 respond equally well to inputs from either eye, and
cells in the other groups have a corresponding degree ot
ocular dominance. In the monkey, 7 2 % o f cclls in V I fall
into groups 2 to 6 (Schiller et al. 1976). The way cells are
classified in a particular animal depends on the method
used to categorize the responses. For a given m ethod, it has
been found to be stable over a period o f 8 hours (M acy et al.
1 982).
The scale o f ocular dominance is based onlv on the
excitatory effects o f stimulation from each eye separately. It
takes no account o f inhibitory connections o r ot the few
cells that respond only ro binocular stimuli (Griisser and
Griisser-Cornehls 1965). The classification ot cortical cells
into ocular dom inance columns is further complicated by
the fact chat the ocular dominance o f some complex cells
varies over time and depends on the spatial frequency and
velocity o f the stimulus ( Hammond 1979, 1 981).
 Left retina
(■■sure5 .46 . O rien tation o fo cu la r dom in an ce bands. I he distan ce betw een
p o in ts in V I will be greater i f o cu la r d o m in an ce stripes arc orth og on al
to the d ire ctio n o t a disparity, as in (A ), than i f they arc aligned w ith the
d ire ctio n o f the disparity, as in (B ).
strong dom inance arc probably those chat codc large
disparities.
The effect produced by stimulation o f the silent eye may
be inhibitory and thus reduce the response evoked by stim­
ulation o f the dom inant eye. O n the other hand, it may
involve subthreshold facilitation and lower the threshold o f
response to stimulation o f the dom inant eye (Griisscr and
Griisser-Cornehls 19 6 5 ; Henry et al. 1 9 6 9 ; Bishop et al.
1 9 7 1 ; Poggio and Fischer 1977; K a to e t al. 1981).
Since all direct visual inputs to cortical cells in layers 4 C
and 4 A are believed to be excitatory, one must conclude
that che suppressive effects produced by stimulation o f che
silent eye involve lateral connections (Section 5-5.6).
Application o f bicucullinc (a G A B A antagonist) to the sur­
face ot the ca ts visual cortex caused cells that were strongly
or exclusively driven by one eye to becom e responsive to
both eyes (Sillito et al. 1980b).
Hammond and Kim ( 1 9 9 6 ) found that, for binocular
complex cells in the visual cortex ot the cat, the suppressive
effect o f stimulating the nondom inant eye on the response
to stimulation ot the dom inant eve
ф
varied with the relative
orientations and d irec tio n so f motion o fd ich o p tic stimulus
gratings. Som e cells showed interactive effects when paral­
lel gratings moved in opposite directions, others showed
effects when orthogonal gratings moved in orthogonal
directions, others when the gratings moved in either o f
these two ways, and still others when the moving gratings
В had different but similar orientations. A final group showed
no suppression or only variable suppression. These inhibi­
tory connections could be involved in binocular rivalry that
occurs between distinct images in the two eyes.
( A d .p it J iV »» ck U v m L h 1000 )

5 . 7 . 2 f O c u l a r D o m i n a n c e in N ew W o rld M o n k e y s

Several lines ot' evidence show thac cclls in the centers
o f ocular dominance columns have strong monocular
dominance, while cclls in intermediate positions receive
excitatory inputs from both eyes. Thus, radioactive tracer
injected into one eye migrates to the centers o f ocular dom ­
inance columns for chat eye (H o rto n and Hocking 1996c).
Also, monocular enucleation causes loss o l cytochrome
oxide activity in che centers o f ocular dom inance columns
lor that eye (H o rto n and H ocking 1998b).
5 . 7 . 2 c D i c h o p t i c In te ra c t io n s
The ocular dominance scale takes no account o f the
fact that almost all cells in groups 1 and 7 lying within
the binocular field, and classified as exclusively monocular
by Hubei and Wiesel’s criterion, are affected by the simulta­
neous stimulation ot the corresponding region in the
silent eye. In fact, cells with scrong ocular dominance
show evidence o f scronger binocular interactions o f
this type than do cells classified as having a balanced
binocular input (Gardner and Raiten 1986). Cells with
Primates evolved at least 6 0 million years ago. There are two
suborders. The first— the prosimians— includes tarsiers,
lemurs, lorises, and galagos. The other suborder— the
anthropoids— includes New World monkeys. O ld World
monkeys, and hom inoids (great apes and humans). The
New World monkeys (Platyrrhines) separated from the
Old W orld monkeys (Catarrhines) about 3 0 million years
ago(Fleaglc 1988).
O cular dom inance columns have been found in all O ld
World monkeys and hominoids that have been studied
(Hendrickson e t al. 1978; Tigges and Tigges 1979; Sengpiel
et al. 1996). They have also been found in at least one pros­
imian species, the bushbaby ( Galago ) (Glendenning ct al.
1976). New World monkeys have eye-specific laminae in
the L G N , although the parvocellular laminae are n ot as
well defined as in O ld World monkeys (H endrickson e t al.
1978). However, as we shall now see, n ot all New World
monkeys have well-defined cortical ocular dominance
columns.
The New W orld spider monkey [Ateles atcr) has
anatomically distinct ocular dom inance columns in V I ,
as revealed by autoradiography. They arc especially evident
in layer 4 B , and there is a good deal o f overlap between
them (Florence ct al. 1986).
The New World capuchin monkey (Cebus ape I I a) has
eye-specific L G N layers. Singlc-unit recording revealed that
most cells in the V I are binocular with a preference lor one
or the other eye. Staining tor cytochrom e oxidase revealed
ocular dominance columns in che V I (Rosa et al. 1992).
Staining applied 8 monchs after removal ot one eye also
revealed ocular dominance columns (Hess and Edwards
1987).
Squirrel monkeys {Saim iri scittreus) have excellent
stereoscopic vision (Livingstone et al. 1 9 95 ) (Porcrait
Figure 5 .4 7 ). However, early studies reported chac chey have
only tainc ocular dominance columns (Humphrey and
Hendrickson 1983; Tigges ec al. 1984). M ore recently,
staining tor cytochrom e oxidase after monocular enucle­
ation revealed that some squirrel monkeys had clear and
sharply segregated columns while others had very faint col­
umns. S o m e monkeys showed columns in only one region
ot V I . O n ly four out ot a group o f 12 monkeys showed
clear columns (Adams and Horton 2 0 0 3 ). In a scudy involv­
ing finer anatomical resolucion, ocular dominance columns
were observed in chc squirrel monkey, buc chey were only
abouc 225 ,Llm wide, che narrowest found in any animal.
They were organized in a fractured, irregular mosaic and
did not correspond with the discribucion o f cycochrome
oxidase blobs, as chey do in other animals (H orcon and
Hocking 1996b). Nevercheless, many monocular cells were
i.Smt 5.->* M argaret Livingstone. S h e graduated from M I T in 1 9 7 2 and
o b ta in ed a I’ li.D . trom H arvard M cd ica l S ch o o l in 1 9 7 9 . She
con d u cted p o std o cto ral w ork a t I’ rin ccto n and th e n w ith D avid H ubei
at H arvard. She has rem ained at H arvard M cd ical S ch o o l.
found in cortical layer 4 C o f squirrel monkeys lacking
ocular dominance columns (Adams and H orton 2 0 0 6 a ).
M ost cells outside layer 4 C were found со be binocular and
responded selectively to disparity, but few o f chcm showed
chc scrong ocular dom inance evidenc in Old World m o n ­
keys (Livingstone et al. 1995). Thus, ocular dominance col­
umns are not required for the occurrence o f monocular
cells in layer 4 G or for stereopsis. It seems chac squirrel
monkcvs
/ also lack cortical columns that selectively
i code
oriencacion, even chough che monkeys dececc scimulus
oriencation (Van Hooscr et al. 2 0 0 5 ).
Squirrel monkeys reared with one eye removed, showed
no evidence ot ocular dominance columns (Hendrickson
and Tigges 1 985). Two o f four squirrel monkeys made
strabismic at an early age showed some evidence ot ocular
dominance columns in layer 4C/3 o f V I (Livingstone
1 996). However, Adams and H orton ( 2 0 0 6 b ) poinced ouc
that since many normal squirrel monkeys show ocular dom ­
inance columns it is difficult to prove that strabismus has
any effect.
4
The New World owl monkey (Aofes) shows only taint
ocular dominance columns (Kaas cc al. 1976; Hendrickson
cc al. 1978). However, ocular dom inance columns may be
obscured by noise in autoradiography.
Adult New World marmosecs [Callithrixjacchus) show
no evidence o fo cu lar dom inance columns wich autoradiog-
raphy. O cular dom inance pacches evidenc in 3-m onth-old
marmosets disappear during the first year. These patches are
retained in adult animals reared with one eye occluded
(D cBruyn and Casagrande 1981; Spatz 1989; Sengpiel
et al. 1996). Ic is noc known whecher ocher New World
monkeys show chis early loss ot ocular dominance patches.
It seems unlikely that genes for ocular dominance co l­
umns evolved separately in New and O ld World monkeys.
The emergence o f columns after monocular occlusion in
New World monkeys suggests that the mechanism tor their
formation is present, even chough they are noc evidenc in
the normal adult. Epigenetic factors such as the area ot V I
and chc degree o f convergence o f visual atferencs may
account for variability among New World monkeys. The
size o f the cortex and che separacion o f che eyes arc larger in
larger animals, and ocular dominance columns seem со be
confined со chc larger species o f New World monkeys. The
squirrel monkey and che owl monkey have stereoscopic
vision. Thus, well-defined ocular dom inance columns arc
noc required tor stereopsis.
5 .8 O T H E R V IS U A L A R E A S
5 .8 .1 IN T R O D U C T IO N
Axons leaving the primary visual corccx emerge from pyra­
midal cells in layers above and below layer 4. Axons from
layers 2 and 3 project retinotopically со cxtrastriate areas.
Figure$•**£• C h ar!n G. Grots. H e o b ta in ed an Л .В . in b iology from
H arvard U n iv ersity in 1 9 5 7 an d a P h .D . in psychology from
C am brid ge U n iv ersity w ith L arry W eiskrantz in 1 9 6 1 . B etw een 1961
and 1 9 6 5 he was p o std o cto ra l fellow and assistant professor at M I T .
A fter tw o years a t H arvard U n iv ersity he m oved to P rin ceto n
U niversity, w here he in now professor o f psychology. H e is л m em ber o f
the N atio n al A cadem y o f Scien ces and was awarded the A m erican
Psychological A ssociation D istin g u ish ed Scien tific C o n trib u tio n Award
in 2 0 0 5 .
'Hie visual corcex also sends incracorcical fibers to visual
areas in che interior Cemporal corcex, che pariecal lobe, che
frontal lobe, and со several subcorcical nuclei (Gross 1973)
(Porcraic Figure 5.48).
Visual areas around che scriace corcex are known as che
extrastriate co rtex, or prescriate corcex, although these
cerms do n ot seem to have precise definitions. In primates,
the extrastriate cortex includes V 2 , V 3 , V 3 A , and V 4 in the
occipital lobe. It also includes the middle temporal area
( M T ) , the medial superior temporal area ( M S T ) , the ven­
tral posterior area (V P ), the ventral occipitotemporal area
( V O P ), and the ventral interparietal area ( V I P ) (Zeki 1974;
W ong-Riley 1 9 7 9 b ; Maunscll and Van Essen 1983a).
Thirty-two distinct visual areas have been revealed in
the brain ot the monkey, with over 3 0 0 pathways co n n ect­
ing them (Felleman and Van Essen 1991; Van Essen et al.
1 992). Together they occupy about 6 0 % ot the monkey
neocortex. No doubt other visual areas remain to be
discovered.
The retina is clearly mapped retinotopically in V I and
V 2. Using t M R I recording, Gardner e t al. ( 2 0 0 8 ) found
that all 12 visual areas in the human occipital cortex, includ­
ing M T , code stimuli retinotopically. At some higher level,
stimuli must becoded in a headcentric or bodvcentric frame
o f reference for judging the directions ot objects and tor
controlling arm movements (Section 3 4 .3 ).
At least ten visual areas have been identified in che pari­
etal lobe. These areas occupy most or all o f Brodmann’s
area 7. The inferior temporal cortex also contains many
visual areas (Gross 1973). The frontal lobe contains the
frontal eye fields and other areas related to visual functions.
lijere s.4*. M ain visual areas in the hum an cereb ral cortex. I he dorsal stream
goes from V I and V 2 throu gh V 3 to M T ( V 5 ) an d M S T and on to the
parietal lo be. Ih c %cntral stream goes from V I and V 2 to V 4 and the
in fero tem p oral co rtcx .
Many cells in all extrastriate visual areas arc binocular (Zeki
1979). Figure 5 .49 depicts the layout o f visual areas.
There is some uncertainty about the criteria for defining
dilferent visual areas. Zeki ( 2 0 0 3 ) proposed that a visual
area should have a more or less complete map o f the contral­
ateral visual field and a distinct set of anatomical co n nec­
tions and functional properties. Some, but not all, areas
have a distinctive cytoarchitecture.
In cars, both areas 17 and 18 receive inputs from the
L G N . In primates, V I receives almost all the direct visual
inputs from the main laminae o f the I.G N . Area V 2 receives
inputs from interlaminar layers only, either directly or
chrough che superior colliculus (Bullier ec al. 1994). Areas
V 4, and M T in primates receive some inpucs from boch che
main laminae and chc interlaminar layers o f the I.G N
(Bullier and Kennedy 1983).
M ost visual ccntcrs, along with other parts o f the n eo ­
cortex, are reciprocally connected to several subcortical
areas (see Section 5.5.4b).
The striate cortex ( V I ) in each cerebral hemisphere
contains a fine and well-ordered representation of the whole
contralateral visual hemifield. The visual hemificld is repre­
sented in a much less orderly fashion in each extrastriate
visual area. The representation is coarser in extrastriate areas
because the receptive fields are larger and there arc topo­
graphic discontinuities in the mapping from one visual area
to another. It seems that patterns ot discontinuities vary
between differenc individuals o f t h e same spccics (see Rosa
and Tweedale 2 0 0 4 ) . In some visual areas, parts o f the visual
field arc exaggerated relative to cheir representation in V I
and other parts are diminished or absent.
The cells within the boundaries becween one visual area
and another— for example, between V I and V 2 — have
receptive fields along either the vertical or horizontal

Iigiif. s.w. A lan Con ey. B o rn in Sunderland, England. H e obtain ed a
degree in natural sciences and a P h .D . at Em m anuel C olleg e, C am bridge.
A fter a year at the M edical S ch o o l o f R och ester University, he returned to
C am brid ge as a lecturer in the D epartm ent of Experim ental Psychology.
A fter a further year as a V isitin g Fulbright Fellow at Harvard University,
be w ent to L in coln C o lleg e, O x fo rd , as a Royal S o cicty research fellow
and a N uffield senior research fellow. H e becam e reader in experim ental
psychology a t O xford in 1 9 7 3 and ad h om in cm professor o f physiological
psychology in 1 9 8 1 . From 1991) to 1 9 9 6 he was d irecto r o f the M R C
Interdisciplinary Research C en tre for Brain and Behaviour. In 1 9 9 " he
becam e a M edical Research C ou n cil research professor. H e has been
president o f the European Brain and Behaviour S o cicty and the U K
Experim ental Psychology Society. H e is a fellow of the Royal Socicty.
retinal meridians. Fibers running through chc corpus callo­
sum connect regions representing the vertical meridians.
These boundary regions can сhe re to re be recognized by a
sudden change in recinotopic representation.
O n e consequence ot this juxtaposition ot cells from the
main retinal meridians is that retinotopic representations o f
visual hemifields in succeeding visual areas are mirror images
o f each other (Cow ey 1979) (Portrait Figure 5.50). This has
made ic possible to map borders ot visual areas in the human
cerebral cortex by inspecting f M R I images produced by
phase-encoded retinal stimuli (Sereno et al. 1995).
O n e might ask why, in some cases, cells with different
tuning functions are assembled in alternating columns
within the same visual area while, in ocher cases, they are
assembled in distincc cortical areas. The answer is probably
that cells are juxtaposed in the same area when lateral co n ­
nections are required between chem so chac chey can code
higher-order scimulus feacures, such as motion in depth.
Different cvpes ot cells are assembled in distinct areas when
extensive local interactions are not required because each
area is specialized for the processing o f a particular feature.
The processing o f cach type o f information requires cclls
wich distinct properties.
Som e visual areas operate in parallel, while ochers opcrace
in sequence to form a processing hierarchy. Parallel processing
occurs when chc outputs o f one area are processed in dis­
tinct ways. Hierarchical processing occurs when processing
carried o ut in a given area depends on information supplied
by another area. Beyond V I , visual areas become smaller
and the receptive fields o f cclls become larger and more
specialized. Also, beyond V I , the relationship between
response frequency and stimulus contrast bccom cs scccpcr
so chat cells have narrower dynamic ranges and act more
like on-oH switches (Sclar ec al. 1 990). This suggests that
the information processed at each stage o f a hierarchy is
available trom that scage buc is noc carried in detail to higher
stages (Lennie 1998). Each higher stage takes only that
information from the preceding stage that it requires for
the processing it performs.
Thus, each hierarchical stage provides a different level ot
information, and information from each stage is available
when needed. It higher centers are lost, we may not be able to
recognize things but weean still perceive the detailed structure
o f the visual world and perform basic tasks such as stimulus
detection and discrimination o f simple features. Thus, percep­
tion is not the end product ot a hierarchical process. Rather,
different types o f perceiving arc possible from the outputs o f
each stage ot processing trom V I to che highesc levels.
As one proceeds со higher visual cencers ic becomes
more difficult tor an investigator to determine what pro­
cesses arc occurring. Important differences between one
visual area and another may not be revealed by the tuning
characteristics o f single cclls but only bv properties o f larger
functional units. Even if patterns o f connections between
cortical cells are known, their functions are difficult to inter­
pret without knowing what the system is designed to accom-
plish.Anothcr problem is that simple stimuli may not reveal
differences between cortical areas. As one ascends the pro­
cessing hierarchy, cells are selective to ever more specific and
complex stimuli. It is difficult to decide which o f an infi­
nitely large set ot stimuli to use. Investigators often employ
a shotgun approach using an arbitrary set o f complex stim­
uli. Moreover, from mom ent to m oment, receptive fields ot
cortical cellschange in size and perhaps in tuning character-
istics according со the spatiotemporal properties o f the
stimulus. Also, visual experience or lesions can induce long­
term changes in receptive fields (Section 5.6.8).
O n ce the tuning specificity o f cells in a given area has
been determined there is still che quescion ot how chac
tuning was achieved. The scimulus seleccivicy o f cells in a
given visual area could be due со one or more ot che tollow-
ing processes.
1. Converging inputs Each cell could receive converging
inputs from cwo or morediscincdy cuncd cells in che
same or another cortical area. For example, a cell tuned to
two lines forming a corner may receive inputs from two
cells, each tuned to single lines in distinct orientacions.
2. L ateral connections Spccificicy could arise trom laccral
excitatory or inhibitory connections within a given area.
 It is debated whether orientation specificity o f cclls in
V I arises through convergence o f L G N inputs or
through intracortical connections (Section 5.6.2). But
the same issue arises at every transition trom one visual
area to another.
3. Feedback Specificity could arise, or at least be modified,
through feedback from an area higher in the processing
hierarchy.
M ost investigations ot single cells at or below the level
o f the primary visual cortcx have been conducted on anes­
thetized animals. Anesthetics probably mask effects of
feedback from higher centers, even at the level o f the L G N .
Also, anesthetics must surely affect even the basic process­
ing carried out by cclls in higher visual areas. The full
functions o f higher visual centers can be obtained only by
using alert animals.
5 . 8 .2 A R E A S V 2 A N D V3
5 .8 .2 a A rea V 2
Area 18 in cats receives some direct visual inputs from the
main laminae ot the L G N . In primates, V 2 receives visual
inputs from only interlaminar regions o f rhe L G N . About
9 0 % of visual inputs to V 2 com e trom V I .
In the macaque monkey, area V 2 is not partitioned into
ocular dominance columns. However, it shows alternating
stripes when stained for cytochrom e oxidase. The cy to -
ch ro m e -o x id a se strip es run over the surface o f V 2 approx­
imately perpendicular to the border with V I , as shown in
Figure 5.51, and extend through all cortical layers (Tootell
ct al. 1 983). F.ach stripe cycle is about 1 mm wide and
consists o f dark-staining thin and thick stripes and a
Anterior
Figure 5 -51 - C ytochrom e ox id ase areas o fib e visual cortex. S c c tio n from layer 3
o i the lateral surface o ( the visual c o rtc x o f th e squirrel m onkey, stained
fo r c y to c h ro m c oxidase. The s p o t t e d area is V I and the ad jo in in g
S trip e d a r e a IS V 2 . (Гшш Тоок11и>1. l9H3.KcpnntcdiYirh ршпшшп from ДАAS)
lighc-scaining in tcrstrip c. The surface o f area V 2 o f chc
macaque monkey has about 12 stripe cycles (R oe and Ts’o
1995).
W ith in each stripe cycle, a region of visual space is
remapped three times, once in the thin stripe, once in the
thick stripe, and o nce in the interstripe. At each stripe
border there is a topological “jum p back” discontinuity, like
that between ocular dominance columns in V I . Adjacent
stripe cycles represent adjacent regions o f space, and the
mapping is continuous between stripes o f a given type
across the cycles (R o e and T so 1 9 9 5 ; Shipp and Zeki
2 0 0 2 b ). However, there is considerable scatter ofreceptive-
field locations at the borders between the stripes.
In humans, the cytochrom e oxidase stripes o f V2 are
replaced by a rather disorderly jumble ot patches (see Tootell
ct al. 1996).
Hubei and Livingstone ( 1 9 8 7 ) proposed the following
tripartite projection from V I to V2.
1. The blob regions o f V I , which contain mostly
nonorientation-specific, color-coded cells ot the
parvocellular system, project mainly to thin stripes.
2. The intcrblob regions o f V I , which contain orientation-
tuned cells o ft h e parvocellular system, project to both
the nonstaining intcrstripcs.
3. Cells ot the magnocellular system project from layer
4 C a to pyramidal cells in layer 4 B o f V I and then
predominantly to the thick stripes o f V 2 (Blasdel et al.
1985; DcYoc and Van Essen 1985; Livingstone and
Hubei 1987).
Thus, Shipp and Zeki (2 0 0 2 a ) found cclls sensitive ro
motion direction (magnocellular) only in the thick stripes,
cclls sensitive to orientation mainly in thick stripes and inter-
stripes, and cells sensitive to color (parvocellular) mainly in
thin stripes. These functional divisions between stripes were
most evident in cortical layers ЗА and 3B. They were least
evident in layers 1, 2, and 6 — layers that receive feedback
from higher centers in which signals are integrated.
This division ot ccll types into stripes is n ot complete*.
There is also a magnocellular input to the thin stripes
(Nealcy and Maunscll 1994). Also, each type of stripe co n ­
tains cells tuned to color and depth, color and orientation,
or to all three features (T so et al. 1989; Levitt ct al. 1994;
G egen fu rtn eret al. 1996).
Sincich and H orton ( 2 0 0 2 ) proposed that V I to V2
projections arc organized into a bipartite system. According
to this system, cytochrom e oxidase blobs project to thin
stripes while intcrblobs project to both pale stripes and
thick stripes. They proposed that the distinct properties o f
pale and thick stripes arc produced in V 2 rather than by
having distinct origins in V I (Sincich et al. 2 0 1 0 ).
By com bining single-unit recording with in vivo
optical imaging T so et al. ( 2 0 0 1 ) revealed a finer functional
organization within each thin, pale, and chick stripe o f V 2. 5 .8 .2 b C o r tic a l A rea V 3
Each stripe contains patches tuned for color, orientation, or
In the monkey, V 3 forms a narrow strip along the dorsal
disparity. W ith in disparity-tuned patches mosc cells prefer
border o f V 2. It contains a representation o f the whole co n ­
vertical stimuli. Between colored patches and disparity
tralateral visual field. Cells serving the inferior quadrant o f
patches there are cclls jointly tuned to color and disparity.
the visual field have larger receptive fields, arc more direc­
W ith in colored patches, darker regions respond to equilu-
tion selective, and less color selective than those serving che
minant color and lighter regions to stimuli defined by
superior quadrant. This difference may be related to the fact
luminance.
that acuity is lower in the upper field than in the lower field.
The pulvinar (Section 5.5.4b), a thalamic nucleus, sends
These differences prompted Burkhalter et al. ( 1 9 8 6 ) to des­
inputs to the thick and thin stripes o f V 2 buc not со the
ignate the part o f V 3 representing the superior contralateral
interstripes (Levitt et al. 1995).
quadrant as' a distinct visual area, which they called area VP.
The tuning characteristics o f cells in V 2 resemble those
Buc Zeki ( 2 0 0 3 ) argued that such a division into distinct
o f cells in V I , except that cells in V 2 have larger receptive
areas' is unjustified.
fields, are m ore likely to be binocular, and are almost all
Area V 3 in monkeys is organized retinotopically and
complex cells (Zeki 1978).
receives inputs from V I , mainly from layer 4 B , and from
Cells in V 2 , unlike those in V I , responded to subjective
V 2. It projects to V 3 A , V 4 , the temporal visual area in chc
contours and texture-defined contours (von der Heydt et al.
ventral pathway, and to M T , M S T , and the posterior and
1984; Marcschal and Baker 1998).
ventral intraparietal areas in the dorsal pathway (Fcllcman
For about half the cells in V 2 and V 4 and some cells in
et al. 1997a; Lyon and Kaas 2 0 0 1 ) . Human areas V I , V 2,
V I o f the alert monkey, the response to an edge or line was
and V 3 seem to be homologous to those in macaque.
modulated according to which side ot a figure the edge or
Cells in V 3 , have larger receptive fields than cells in V2.
line belonged to, even though the stimulus in the receptive
M ost arc orientation selective. Cells with similar orienta­
field ot the cell remained the same (Z h o u et al. 2 0 0 0 ) . Some
tion tuning are organized into columns. A bout h a lf the
cells were also selective for the contrast polarity o f an edge.
cclls are selective for direction o f motion, especially those
Responses to border-ownership of an edge in a cells recep­
serving the lower visual field. They respond to first-order
tive field occurred when che edge that defined border own­
and second-order motion ot contrast-defined edges. Their
ership was well outside the receptive field (Zhang and von
response to second-order motion is greater chan chat o f cells
der Heydt 2 0 1 0 ). They concluded that these responses
in V I and V 2 (Sm ith ct al. 1998). Cells in V 3 prefer lower
depend on recurrent signals from higher centers. The
spatial frequencies and higher temporal frequencies than
response o f a ccll to the edge o f a figure with appropriate
cells in V 2 (Gegenfurtner et al. 1997).
sign was enhanced only when rhe monkey attended to rhe
Estimates o f the proportion o f cclls in V 3 showing color
figure (Q iu et al. 2 0 0 7 ) . Also, responses related to figural
selectivity vary between about 15% (Baizer 1982; Felleman
transparency, which were based on border ownership, took
and Van Essen 1987; Adams and Zeki 2 0 0 1 ) and 54%
110 ms to develop (Q iu ct al. 2 0 0 7 ) .
(G egenfurtner ec al. 1997).
The response o f a ccll to border-ownership quickly
About half the cclls in V 3 are tuned to binocular dispar­
changed when the border ownership o f the stimulus was
ity (Burkhalter and Van Essen 19 8 6 ; Felleman and Van
changed. However, the response persisted with a time co n ­
Essen 1987). In the macaque, cells in V 3 with similar join t
stant o f about 4 0 0 ms when the figure-ground cues were
tuning to orientation and disparity are organized into co l­
removed so as to leave the figure-ground relationship
umns (Adams and Zeki 2 0 0 1 ) . This organization is well
ambiguous ( O ’Herron and von der Heydt 2 0 0 9 ) . See
suited to the extraction o f higher-order disparities and dis­
Zhaoping ( 2 0 0 5 ) for a discussion o f this topic.
parity gradients required for the perception o f 3 - D form.
About 7 0 % o f cells in V 2 o f monkeys showed uniform
W e will see that V 3 projects to the posterior parietal cortex,
preference for orientation over their receptive fields. Buc
which is concerned with processing 3 -D form.
many cells showed different orientation preferences in sub-
Beyond V 2 and V 3 , visual processing is partitioned into
regions o f their receptive fields. Mosc commonly, subre­
a ventral pathway serving mainly the parvoccllular system
gions were tuned to orientations 90° apart. Thus, these
and a dorsal pathway serving mainly the magnocellular
cells responded selectively to local combinations o f orienta­
system. I lowever, this division is n ot complete. Fluorescent
tions such as angles, intersections, arcs, circles, hyperbolic
tracers revealed that the major pathways have distinct p ro­
and polar gratings (Hegdc and Van Essen 2 0 0 0 ) and rcxturc
jections to subcortical nuclei (Baizer et al. 1993).
elements defined by variations o f orientation (Hegde and
Van Essen 2 0 0 3 ; Anzai e t al. 2 0 0 7 ) . M ost response varia­
tion was accounted for by the first two principal co m p o ­
5 .8 .2 c C o r tic a l A rea V 3 A
nents o t the stimuli. Thus, cells in V 2 are n ot specialized
for the detection o f a narrow range o f complex shape Area V 3 A lies along the border o f V 3 but contains a distinct
characteristics. representation o f both lower and upper visual fields, and
distinct functional properties and connections (Felleman
and Van Essen 1 991). The border between V 3 and V 3 A
represents the vertical retinal meridian and is connected by
the corpus callosum to the corresponding region in the
opposite hemisphere. Area V 3 A receives inputs from V I ,
V 2 , and V 3. In the macaque, cells in V 3A have large recep­
tive fields and are less selective to the speed and direction o f
m otion than are cells in V 3 (G a s k a e ta l. 1988). By contrast,
f M R I procedures have revealed that V 3 A in humans is
m ore m otion selective than V 3 (Tootell et al. 1 997). Some
cells in V 3 A ot the alert monkey respond to the position o f
relatively small stimuli in a headcentric frame o f reference,
while others respond to stimuli in an oculocentric frame o f
reference (Galletti and Battaglini 1989).
5.8.3 T H E V E N T R A L PATH WAV
The parvocellular system projects mainly from V I , V 2 ,
and V 3 ventrally to V 4 and then to the inferior temporal
cortex, the superior temporal polysensory area, and frontal
cortex (Baizer ct al. 1 991). This is known as the ventral
pathway.
5 . 8 .3 a C o r t i c a l A re a V 4
An area in the lingual and fusiform gyri in the inferior por­
tion o f the occipital lobe o f humans is the homologue o f
area V 4 in monkeys. In primates, V 4 receives some direct
inputs from the L G N (Yukie and Iwai 1981; Biillier and
Kennedy 1983), which may explain why a patient lacking a
visual cortex retained some color discrimination (Stoerig
and Cowey 1 989). But V 4 receives most o f its inputs from
V I , about 5 0 % o f the outputs o f V 2 , and some outputs
trom V 3 (Nakamura c t al. 1 993).
In earlier studies, the anterior part o f V 4 was designated
V 4 A because cells in that part respond less strongly to
moving bars than do cclls in V 4. However, most investiga­
tors do n ot subdivide V 4 (Felleman and Van Essen 1991).
O n thebasisofhum an fM RI responses to colors, Hadjikhani
c t al. ( 1 9 9 8 ) distinguished between V4v and a new area,
which they called V 8 . But Wade et al. ( 2 0 0 2 ) and Zcki
( 2 0 0 3 ) found no sound basis for subdividing V 4.
There arc extensive lateral connections in V 4 , and cal­
losal connections are widely distributed within V 5 (Van
Essen and Zcki 1978). In V 4 o f the macaque only the cen ­
tral 35° o f the contralateral visual hemificld is represented,
in a crude and rather disorderly fashion. This m ay be related
to the fact that the cells have large receptive fields, which,
being color coded, are confined to the central retinal region
(Gattass et al. 1988). Retrograde labeling has revealed that
V 4 has modular compartments that receive inputs from
either thin stripes (parvocellular channel) or interstripe
regions (magnocellular channel) o f V 2 , and V 3/V 3A ,
although there is some cross-channel convergence (DeYoe
e t al. 1994). There are also reciprocal channel-specific
connections with the inferior temporal cortex (Felleman
et al. 1997b).
The properties o f the parvocellular system feeding into
V 4 and then to the inferior temporal cortex suggest that
these structures are specialized for pattern discrimination,
color vision, and fine stereopsis. Each ol these features will
now be discussed.
Many cells in V 4 o f the monkey are selective for orienta­
tion, although the widths o f their tuning functions are
broader than those o f cells in V I . Regions tuned to differ­
ent orientations are spatially organized, at least in the part
devoted to the central retina (G hose and T s o 1 997). Some
cells in V 4 are specifically tuned to the slant ot lines in depth
(H in kle and C o n n o r 2 0 0 2 ).
M ost cells are selective for the spatial frequency o f grat­
ings and tor the length and width o f bars (D esim one and
Schein 1 987). However,cells in thealert macaque responded
better to features such as angles and curves pointing in a
particular direction than to simple edges or bars (Pasupathy
and C o n n o r 1 999). Pasupathy and C o n n o r ( 2 0 0 2 ) were
able to reconstitute a stimulus shape from the responses o f a
population o f such cells.
Som e cells in V 4 o f the monkey respond selectively to
periodic patterns such as concentric gratings, radial pat­
terns, and hyperbolic patterns that resemble Lie orbits
(Gallant et al. 1993, 1996). The response o f these cells was
largely invariant over changes in the position of the stimu­
lus. Pigarev et al. ( 2 0 0 2 ) found that most cells in the
anterior part o f V 4 o f the monkey had elongated receptive
fields radiating out from the fovea. In the alert monkey,
these cells responded to radial motion. Similar cells were
tound in the corresponding area in the suprasylvian gyrus o f
the cat (Rodionova et al. 2 0 0 4 ) .
The receptive fields ot the specifically tuned cells must
be built up by com bining inputs from cells in V I or V 2.
Their construction is presumably helped by the patterns ot
orientation and direction preference exhibited in these
areas.
Som e cells in V 4 are selective for speed o f motion
(C h en g et al. 1 9 9 7 ), and some are selective for motion
direction. Som e cells respond selectively to motion-defined
boundaries (Tootell and Hadjikhani 2 0 0 1 ). It seems that
V 4 processes simple shape features required for the recogni­
tion o f complex shapes at higher levels in the ventral
pathway.
Responses o f cells in V 4 are subject to the effects o f
learning. Yang and Maunsell ( 2 0 0 4 ) trained monkeys to
improve their orientation discrimination for gratings co n ­
fined to a narrow range o f orientations and to a specific
location. After training, cells in V 4 with receptive-field
locations and preferred orientations within the trained range
showed enhanced responses and narrower orientation
tuning.
Lesions in V4 in monkeys do nor have much effect on
basic visual functions, such as contrast or motion sensitivity.
However, they severely disrupt performance on some form-
discrimination tasks, such as discrimination o f the relative
orientation o f lines or selection o f an o b je ct that differs
from other objects (Heywood et al. 1992; Schiller 1993;
Merigan 1 996). Ablation o f V 4 produced severe deficits in
the ability to select less prominent stimuli from an array, and
in the ability to generalize discrimination learning to new
stimuli (Schiller and Lee 1991). Similar symptoms have been
noted in a human patient with lesions in V 4 (Rizzo ct al.
1992). Merigan (2 0 0 0 ) produced evidence that these effects
are not due to abnormal levels ot crowding or disruption ot
attention. Responses in V 4 are modulated in complex ways
by the animals attcntional state (Section 5.9.2c).
It is not clear whether V 4 in humans is analogous to V4
in monkeys. Positron-emission tomography (PF.T ) revealed
that blood flow to V 4 was higher when human observers
discriminated the relative areas o t shapes that overlapped
than when they discriminated the areas o f shapes that did
not overlap (Larsson et al. 2 0 0 2 ). Human f M R l revealed
that V 4 is activated by shapes defined by illusory contours
o r by shapes defined by binocular disparity in random-dot
stereograms (M endola et al. 1999).
Blood flow to V 4, indicated bv * PET, increased when
human subjects viewed a colored display {Z ek i c t al. 1991).
Patients with lesions in V 4 suffer a form o f color blindness
known as cerebral ach rom ato p sia (Zeki 1 990). Patients
describe the world in terms o f gray, although the three cone
mechanisms are intact. Thcv* can discriminate between an
ordered and disordered array o f isoluminant chromatic
stimuli, as long as chey are adjacent (Hcvw ood et al. 1991).
Achromatopsia is often accompanied by other visual defects
such as loss o f contrast discrimination. C o lo r agnosia is a
ditferent disorder in which patients can discriminate colors
but are n ot able name them.
O n e patient with achromatopsia could see depth in a
random-dot stereogram presented with red-green anaglyph
filters even though he could n ot detect the red stereogram
elements when he looked through the red filter (Hendricks
ct al. 1981). Disparity detection must depend on processes
at a stage earlier than that responsible for the color defect.
In monkeys, V 4 lesions had little or no effect on color
discrimination or on the ability to select an odd color in an
array (Heywood et al. 1992). Perhaps achromatopsia
involves a deficit in color appearance rather than ot color
discrimination, or perhaps lesions in humans involve
white matter, which is spared by experimental lesions in
monkeys.
For the role o f V 4 in stereopsis see Section 1 1.5.3a.
5 . 8 .3 b In fe r io r T e m p o r a l C o r t e x o f O ld
W o r ld M o n k e y* s
The in fe rio r tem poral c o rte x ( I T ) in O ld World monkeys
receives mosc o f its visual inputs from V 4 and provides feed­
back to V4. There are also some direct visual inputs trom
interlaminar zones o ft h e L G N (H erndndez-G onzalezetal.
1 994). Some areas o f chc temporal cortex are purely visual,
while others receive visual, auditory, and somatosensory
inputs.
In the monkey, area I T consists o f two distinct but
interconnected cytoarchitectonic areas. The first is a poste­
rior area known as T E O . The second is an anterior area
known as Т Е . Area T E O has extensive connections with
the parietal lobe. Its connections to the trontal lobe are lim ­
ited to areas 8, 12, and 4 5 (Section 5 .8 .4 f). Area Т Е has
fewer connections with the parietal lobe than does area
T E O but more extensive connections with the frontal lobe,
namely to areas 8, 11, 12, 13, and 4 5 (W ebster et al. 1994).
Area IT also connects with the medial temporal lobe ( M T ) ,
as discussed in the next section.
All cclls in I T have large receptive fields that almost
always include the fovea and extend into both left and right
halves o f the visual field. The lateral connections o f pyrami­
dal cells are very much more extensive than in V I (Elston
e ta l. 1999).
Many cells in monkey I T respond selectively to a par­
ticular shape over a two- or four-fold change in the size o f
the stimulus (Sato et al. 19 8 0 ; Sary et al. 1993; Ito et al.
1 995). T he cells show the same selectivity when the stimu­
lus is moved several degrees away from the fovea o r as the
animal moves its gaze (D iC a rlo and Maunsell 2 0 0 0 ) . Thus,
the cells show considerable size and p o sitio n invariance.
Cells in I T responded to a grating whether ic was defined
by luminance contrast, by m otion, or by texture (S.iry et al.
1 995). The response to a given outline shape was not
affected when rhe contrast polarity was changed or when
the shape was mirror reversed. However, the response
changed when the figure-ground appearance o f the display
was changed (Baylis and Driver 2 0 0 1 ) . Therefore, cells in
I T respond to shape rather than to lower-level features char
define the shape or to the position, contrast polarity, or
orientation o f the shape. In other words, the cells show
cue invariance.
Cells in I T also respond to shapes defined by binocular
disparity (see Section 1 1.5.3b). Som e cells responded more
strongly to solid objects than to projected images o f che
objects, even when only one eye was open (Gross et al.
1 9 7 2 ). Janssen et al. ( 2 0 0 0 a ) found that about 5 0 % o f cells
in the lower part ot Т Е in the macaque were selective tor
disparity-defined 3 -D shape, while very few cells in the
lateral part o f Т Е showed this selectivity.
M ost cells in I T o f macaque monkeys respond to par­
ticular views o f one or more object. The response o f cells in
I T to familiar shapes in a particular orientation was
enhanced after monkeys had been trained to categorize the
shapes presented in that orientadon (Freedman et al. 2 0 0 6 ).
However, some cells in I T responded to all views o f one or
more o f a set o f familiar objects (Logothctis et al. 1995;
Booth and Rolls 1998). 'Ih ecclls showed view point invari-
an cc. The objects could have been codcd in terms o f
U r h e b e r r e c h tlic h g e s c h i i t z t e s Mater
features, such as color, which do not vary with orientation.
But the objects used by Booth and Rolls did n ot possess
such features, which suggests that viewpoint invariance
was built up by com bining the outputs o f cells sensitive to
particular views o f the objects.
Som e cells in the monkey superior temporal sulcus
( S T S ) ot the inferior temporal cortex respond selectively to
faces (Perrett et al. 19 8 2 ; Rolls e t al. 1994). 'I he responses o f
som e o f these cells are invariant with respect to the posi­
tion, size, and view o f the face (G o ch in 1996; Wallis and
Rolls 1997). The early part ot the responses o f neurons in
S T S was related to chc general features o f the face, while rhe
later parts o f the responses were related to the finer details,
such as the identity and expression o f t h e face (Sugase et al.
1999).
Area I T has no topographic organization (Fujita et al.
1992; Gross 1 992). Som e cells in IT, particularly the ante­
rior part (T F.), respond best to particular com binations o f
stimulus features such as texture, shape, and color, but they
respond at different rates to a variety o f stimuli (Tanaka
c t al. 1991; Kobatakc and Tanaka 1994). Neurons tuned to
similar complex stimulus features are aligned in columns
normal to the cortical surface. These cortical columns can
be regarded as units from which more complcx descriptions
can be constructed (Tanaka 2 0 0 3 ).
Tsunoda et al. ( 2 0 0 1 ) recorded from single cells and
registered the optical images from the surface o f I T o f m o n ­
keys as they were presented with a variety o f complex
objects. The results suggest that an o b ject is represented by
the activation ot a particular set o f cortical columns, each o f
which represents particular features o f rhe objcct. The same
techniques also revealed that some cclls in Т Е were acti­
vated by a particular spatial arrangement o f parts o f a co m ­
plex o b ject but not by the parts in isolation or by particular
simple features o f objects, such as color, or shape (Yamane
e t al. 2 0 0 6 ) . Also, many cells in monkey I T were tuned to
the 3-1) orientation and principal curvatures o f surface
elements (Yamane et al. 2 0 0 8 ) .
The majority o f I T neurons o f the monkey responded
selectively to those visual features o f objects that the ani­
mals used to categorize the objects (Sigala 2 0 0 4 ; Nielsen
e t al. 2 0 0 6 ) . Particular cells were not sharply tuned to par­
ticular shapes but responded to several shapes with related
features. Responses were enhanced in monkeys that had
been trained to discriminate between members o f a set o f
2 8 complex shapes. Also, after training, the responses o f
cells to different shape categories became more distinct
(Kobatake et al. 1998).
Kiani et al. ( 2 0 0 7 ) recorded responses o f several hun­
dred cells in I T o f alert monkeys to each o f a large set o f
familiar objects. The response patterns were similar for
objects that helonged to the same general category. Response
patterns reflected grouping o f stimuli into m ajor categories
such as animate versus inanimate, and into subcategories
such as human faces versus monkey faces. O bjects that had
similar sizes, orientations, or color did noc produce distinct
patterns o f response over the cell population. Therefore, the
population response reflected the categories into which the
monkeys classified familiar objects.
Lesions in the inferior temporal and medial temporal
cortical areas o f monkeys disrupt the ability to discriminate
between previously learned complex patterns. Lesions do
n ot affect discrimination o f simple features such as differ­
ences in orientation (H olm es and Gross 1 984). Therefore,
this area is implicated in the retrieval o f visual information.
Lesions in T E O disrupt the ability to learn complex
patterns (M ishkin 1982).
Area I T has reciprocal connections with the perirhinal
cortex o f the limbic system, an area associated with memory
encoding. Som e cells in I T responded specifically to co m ­
plex stimuli that a monkey had stored in short-term memory
in a delayed matching task (Miyashita 1 9 8 8 ; M iller et al.
1993).
W e will see in Section 5.8.4g that cells that respond to
familiar stimuli occur in the inferior convexity o f t h e fron­
tal lobe, to which I T projects. However, these cells retain
responsiveness to memorized stimuli for longer periods
than do those in I T (M iller et al. 1996). Also, it seems that
frontal-lobe cclls respond selectively to general stimulus
categories rather than to particular objects (Freedman et al.
2 0 0 3 ).
The superior tem poral polysensory area ( S T P ) lies in
the upper bank o f the superior temporal sulcus. It receives
information about visual motion from M S T o f t h e dorsal
stream and information about visual form from the inferior
temporal cortex (C usick et al. 1995). The S T P is closely
related to the ventral intraparietal area discussed in Section
5.8.4e.
Neurons in the S T P responded well to moving stimuli,
including complex patterns o f motion such as those p ro­
duced by a moving person (O ram and Perrett 1996;
Thompson et al. 2 0 0 5 ) . Som e cells in S T P responded selec­
tively to 3 -D structure defined by motion parallax (Anderson
and Siegel 2 0 0 5 ).
5 . 8 . 3 c H u m a n L a tera l O c c i p i t a l C o r t e x
The human lateral o ccip ital c o rtc x ( L O C ) lies between
V 3 and V 5. It is n ot clearly analogous to V 4 or M T o f Old
World monkeys. Larsson and Hccger ( 2 0 0 6 ) produced
f M R I evidence that each L O C contains two representa­
tions o f the contralateral hemifield, which they designated
L O l and 1 .0 2 .
The L O C showed stronger f M R I activity in response to
objects than to texture patterns. The objects could be famil­
iar faces, com m on objects, or abstract sculptures (Malach
et al. 1995). The f M R I responses from the anterior o f the
L O C were largely independent o f changes in the size or
location o f t h e stimulus (Grill-Spccror et al. 1999). Also,
the activation produced by a given o b ject was the same
whether the o b je ct was defined by luminance, texture, or
motion (G rill-Spector et al. 1998). Thus, responses o f the
human L O C , like those o f monkey I T show position, size,
and cue invariance.
The fM R1 response o f the human lateral occipital cortex
was weaker when the same shape was presented again com ­
pared with when a shape was replaced by a different shape.
Thus, che L O C responds strongly to changes in shape. The
f M R I response remained weak when the same shape was
presented whether or noc ic was partly occluded. However,
the response increased when che perceived shape ot an
ambiguous scimulus changed, wich no change in chc stimu­
lus (Kourtzi and Kanwisher 2 0 0 1 ) . Also, a change from a
line drawing to a grayscale rendering o f che same shape did
not activate the L O C , but the drawing ot an o b je ct pro­
duced a stronger response than a scrambled version o f the
drawing (Kourtzi and Kanwisher 2 0 0 0 ) . In other words,
the L O C responded to perceived shape rather than to an
unprocessed pattern o f stimulation.
There has been someconflictingevidence about whether
the L O C is activated more strongly by solid objects than by
two-dimensional shapes. Kourtzi and Kanwisher (2 0 0 0 )
found that activation was no stronger for line drawings o f
3 -D objects in which depth was represented by occlusion
and perspective than for 2 -D outline shapes. O n the other
hand, Moore and Engel ( 2 0 0 1 ) found that activation
increased when subjects perceived a given stimulus as a 3-D
o b ject rather than as a 2 -D arrangement o f parts. However,
che crucial factor may nor have been che 2 -D versus 3-D
appearance ot che stimuli. It may have been the fact chac the
parts o f the stimuli appeared connected into a single o b ject
only when che stimuli appeared solid. Both che 2 -D and the
3 -D scimuli used bv Kourtzi and Kanwisher were coherent
objects.
The fM Rl response to a stimulus weakens over repeated
presentations. Kourtzi et al. ( 2 0 0 3 ) found that f M R I
responses in the human L O C adapted to stimuli with rhe
same 3-D structure but different 2-D retinal shapes due to
rotation o f the object. Responses did not adapt to stimuli with
the same 2 -D shapes but different perceived 3 -D structures,
such as convex versus concave objects. This suggests that the
L O C is specifically sensitive to 3 -D structure.
Welchman et al. ( 2 0 0 5 ) measured f M R I responses
while subjects judged the dihedral angle formed by two
computer-generated slanted surfaces. Slant was defined
by various com binations o f perspective and disparity.
Responses in V 5 and L O C varied in accordance with
changes in the 3-D structure o f the display and wich the
weighcings thac different subjects assigned to the perspective
and disparity cues.
Murray et al. ( 2 0 0 3 ) recorded f M R I responses in the
L O C ro moving random-dot patterns, 2-D and 3-D line
drawings, and 3 -D shapes defined by m otion. Responses to
motion-defined shapes were confined to che superior lateral
area ot che L O C . Ic is possible chac other subregions devoted
to specific types o f stimuli will be found in the L O C by
methods with higher spatial resolution than f M R I.
In humans, face-selective neurons are found in the
fusiform face area (F FA ), which overlaps the lateral occipi­
tal area. Damage to this area can lead to deficits in Lice rec­
ognition, or pro so p ag n osia (Damasio et al. 1990). The
human f M R I revealed activity in the fusiform face area
when the ambiguous Rubin vase-face figure was seen as a
face but not when it was seen as a vase (Hasson et al. 2 0 0 1 ).
Thus, this area responds specifically to faces rather than to
local stimulus features that comprise the face.
In humans, f M R I has revealed that distinct regions o f
the interior temporal cortex are active during the process ot
memorizing complex visual stimuli and during retrieval o f
memorized items (Gabrieli et al. 1997). The response ot
cclls in the inferior temporal area is also modified by atten­
tion (Section 5.9.2c).
The f M R I procedure has revealed that the L O C in
humans is activated by both visual objects and objects
detected by touch (Amedi et al. 2 0 0 1 ).
5 .8 .3 d M e d ia l T e m p o r a l L o b e
The interior temporal cortex projects strongly to the medial
temporal lobe, which includes the parahippocampal gyrus,
hippocampus, perirhinal cortex, entorhinal cortex, and
amygdala. (Nava et al. 2 0 0 1 ; Squire et al. 2 0 0 4 ).
The parahippocampal region provides major inputs to
the hippocampus. Som e cells in the hippocampus respond
selectively to the location o f the animal in the visual envi­
ronment with which it is familiar. These are known as place
cclls { O ’Keefe and Nadel 1 9 7 8 ; Eskandar et al. 1992;
W ilson М Л and McNaughcon 1 9 9 3 ; R o lls e ta l. 1998; Best
et al. 2 0 0 1 ) . The hippocampus is also involved in ocher
forms o f memory (W ood et al. 1999).
Increased blood flow has been detected in the h ip ­
pocampus when human subjects recognize the spatial
coherence o f 3-D objects (Schacter et al. 1 995). Patients
with bilateral damage to che hippocampus were unable to
remember where objects had been seen (Gattan 1994) or to
associate a spoken word with visual stimulus (Bechara et al.
1995).
Cells in the perirhinal cortex, entorhinal corcex, and
amygdala o f the monkey are selectively responsive to c o m ­
plex objects, faces, or familiar places (Leonard ct al. 1985;
Suzuki et al. 1 997). Kreiman et al. ( 2 0 0 0 ) recorded from
single cclls in these three areas and from the hippocampus
o f alert human patients undergoing surgery for epilepsy.
The patients were given the task o f discriminating between
pairs o f objects, such as faces, buildings, and animals. O f
4 2 7 neurons tested, 14% responded selectively со chc
cacegory со which che shapes belonged.
Raizada and Grossberg (2 0 0 3 ) have developed a neural
model o f feedforward, feedback, and horizontal connections
in and between cortical layers and between the different
ccntcrs o f the ventral stream. The model simulates the
effects o f stimulus filtering, attention, and perceptual
grouping.

5.8 A TH E D O RSA L PATH WAY

In primates, the magnocellular dorsal pathway projects to

areas V 3 , the middle temporal area ( M T ) , and the medial
superior temporal area ( M S T ) (Shipp and Zeki 1985;
Krubitzer and Kaas 1 9 9 0 ; M otter 1991). It then feeds into
the superior temporal polvscnsorv area ( S T P ) and the pos­
terior parietal cortex. Figure 5.52 shows these relationships.
This system is specialized for coding low spatial
frequency, fast flicker and m otion, spatial location, and

VEN TR AL STREAM D O R S A L S TR E A M

F ro n ta l lo b e P re m o to r c o rte x ri^urc $.5>w P eter I I . Schiller.\ B orn in 1 9 3 1.1 le o b tain ed a B .A . in

h ip p o c a m p u s F ro n ta l lo b e
psychology from D u ke U n iv ersity in 1 9 5 5 and a P h .D . from C lark
1 ________ 1 ____ U n iv ersity in 1 9 6 2 . H e co n d u cte d p o std o cto ral w ork in the d ep artm en t
In fe ro te m p o ra l area P a rie ta l area o f psychology at M I T from 1 9 6 2 to 1 9 6 4 .1 Ic th en gained an academ ic
p osition at M I T , w here he now o ccu p ies the D o ro th y Poitras C h a ir for
m edical physiology. H e received an N1H M erit Award.

A re a V4 M T (V 5) a n d MST
Shape O rientation
coarse stereopsis. These functions are associated with the
C olour D isparity
D isparity Motion analysis ot the spatial positions and motions of objects, the
---------------- 1 ■—

I A re a V3 a n d V 3A A rea V6
visual motion arising from self-motion, and the visual guid­
ance ot motor responses (Ungerleider and Mishkin 1982;
Schiller et al. 1990; L ag aeetal. 1993; Hietanen and Perrett
O rientation
1996) (Portrait Figure 5.53).
C olour
D isparity Rizzolatti and Matclli (2 0 0 3 ) suggested that the dorsal
stream contains two substreams. The first is a d orso-dorsal
stream arising in areas V 6 and V 6 A , and feeding into areas
T h in s trip e s In te r s trip e s T h ic k s trip e s
Colour O rientation O rientation
M I P and V IP o f the parietal lobe, and then to the premotor
V2 C o lo u r Motion cortex. This stream is concerned with the control o f visually
D isparity D isparity
guided actions. The second substream is the ventro-dorsal
stream that arises in M T and feeds to the inferior parietal
lobe. This stream is concerned with space perception and
B lo b s In te r b lo b
the planning o f responses.
C o lo u r O rientation
D isparity The main areas o f the whole dorsal stream are depicted
C olour in Figures 5 .4 9 and 5.52.
V1

5 .8 .4 a T h e P a r i c t o - O c c ip i t a l R e g io n

The parieto-occipital region lies between the occipital

and parietal lobes. It contains areas V 2, V 3 , and V 3A .
The medial paricto-occipital region contains areas V 6,
LGN and V 6A .
A rea V 6 receives retinotopically ordered inputs from
V I , V 2, and V 3 , and projects to other ccntcrs in the dorsal
stream. The receptive fields o f its cells are larger than those
o f cclls with similar coding properties in area V 3 . In the
monkey, some o f t h e cells in V 6 have receptive fields defined
Figure 5.52. Pathways connecting visual areas. V isual areas o l chc m acaque
w ith an in d icatio n o f fu n ctio n a l sp ecialization *. (A&pr«! fVr<" P*YoriiufV*A in hcadccntric coordinates, which means that they remain
F w n 198Я1 fixed when the eyes move (Galletti et al. 1993).
 A rea V 6A contains cells chat receive both visual and
somatosensory inputs and is reciprocally connected to the
premotor cortex controlling arm movements. Lesions in
V 6 A o f monkeys produce misreaching to visual objects
wich the contralateral arm (Gallctti ct al. 2 0 0 3 ).
5 .8 .4 b C o r tic a l A rea M T / V 5
In monkeys, the middle temporal area ( M T ) is a small,
heavily myelinated area on the posterior bank o f the supe­
rior temporal sulcus. In humans, Y'5 is the area correspond­
ing to M T . These areas are specialized for detection o f
motion. In the cat, the suprasylvian co rte x (Clare-Bishop
area) is the main cortical area devoted to processing motion
(Rauschecker ct al. 1987; Kruger c t al. 1993).
There arc some inputs to M T from the superior collicu-
lus(Rodm an ct al. 1990; H artig ct al. 1991). There has been
conflicting evidence about the existence o f direct inputs
trom the L G N to M T . However, a recent study by Sincich
ct al. ( 2 0 0 4 ) has confirmed the existence o f direct inputs in
the monkey. M ost o f these inputs arise trom koniocellular
cclls that occur between the parvocellular and magnoccllu-
lar layers o f the L G N . These cells have large receptive fields,
and their input to M T could perhaps contribute to chc
survival ot some motion sensitivity after removal of V I .
Area M T receives its major inputs from layer 4 В o f V I ,
either directly or indirectly via V 2 and V 3 . It also receives
strong inputs from the parietal cortex.
The neurons that project directly from VI to M T
are mostly stellate cells in layer 4 B that convey only magno­
cellular inputs. The few pyramidal cells in layer 4 B that
project directly to M T probably also convey magnocellular
inputs. These direct inputs to M T are specialized for fast
transmission ot motion signals (Nassi and Callaway
(2 0 0 7 ).
Neurons in V I that project indirectly to M T are pyra­
midal cells that convey both magnocellular and parvocel­
lular signals. Inactivation o f this pathway in the alert
macaque specifically degraded the tuning o f M T cclls to
binocular disparity (Ponce et al. 2 0 0 8 ) . Inactivation ot the
V I to M T pathway did not disrupt vergence eye move­
ments. These results suggest that the indirect pathway
conveys disparity information from V I to M T.
M ost ot the target cells in M T are spiny stellate cells
(Anderson ct al. 1998). They arc binocular complex cells
with fast conducting axons (Maunsell et al. 1990; Movshon
and Newsome 1996).
Cells in M T back project to layer 6 in V I and a few cells
in layer 6 project to M T . ('e lls in M T also project to layer 1
but only for stimuli outside the central 10° o fth e visual field
(Shipp and Zeki 1989).
Area M T contains an irregular but complete topo­
graphic representation ot the contralateral visual hemifield.
The central 15° o f the hemifield occupies over half the sur­
face ot M T . There is also an emphasis on the lower temporal
»i*uxcs.5*- Jo h n M a u m d l. B orn G re a t Baddow , Essex, E n glan d , in 1 9 5 5 .
H e ob tain ed B .S c. in z o o lo g y a t D u ke U niversity in 1 9 7 7 and a P h.D .
in b iology a t the C a lifo rn ia In stitu te o f T e ch n o lo g y in 1 9 8 2 . He
con d u cted p o std o cto ral w ork w ith P eter Sch iller a t M I T . H e held
academ ic ap p o in tm en ts in the C e n te r tor V isual S cie n ce at the
U niversity o f R o ch este r from 1 9 8 5 to 1 9 9 2 . H e is now professor in the
division o f neu roscience and d ep artm en t o f o p h th alm o lo g y a t Baylor
C o lleg e o f M ed icin e, H o u sto n . H e is an investigator o t the H oward
H ughes M ed ical Institute.
quadrant o i the visual field (Van Essen et al. 1981; Maunsell
and Van Essen 1987) (Portrait Figure 5 .5 4).
The diameters ot receptive fields of cells in M T are about
10 times larger than those o f cells in V I and increase with
increasing eccentricity (Albright and D esim one 1987).
Receptive fields defined by single stimuli are surrounded by
regions within which stimuli do n ot have a direct effect but
modify the response to stimuli in the receptive-field center
(Allman et al. 1985). As one would expect from their mag­
nocellular inputs, cells in M T have high contrast sensitivity
and do not respond to equiluminant colored stimuli
(Tootell e t al. 1995).
The major function o f M l is the coding o f patterns o f
visual m otion for the control o f smooth pursuit eye move­
ments (Newsome et al. 1 988), postural control, and for
chc dcceccion ot objcccs moving in 3 -D space. M ocion-
sensitive cells o f M T are also tuned со binocular disparity
(Maunsell and Van Essen 1983b). This subject is discussed
in Sections 11.5.2a and 31.3.
In monkeys, lesions imposed in M T specifically elevate
mocion discrimination thresholds (Newsome and Рагё
1 988). A patient with bilateral lesions that included V 5 was
unable to experience objects moving in depth or objeccs
moving faster chan lOVs, even chough she could perceive
stationary objects (Zihl e t al. 1983).
Electrical stimulation of cclls in M T can influence a
m onkeys judgment o f t h e direction in which a random-doc
display wich a variable degree ot cohercnc mocion is moving
(Saitzman et al. 19 9 2 ; Nichols and Newsome 2 0 0 2 ). Also,
responses ot cclls in M T ot monkeys are reduced when
stimulated for some time by stimuli moving in the cells’ pre­
ferred direction. The magnitude ot this neural adaptation is
consistent wich the magnitude o f the motion aftereffect in
humans {van Wezel and Britten 2 0 0 2 ) .
M ost motion-selective cclls in M T o f the monkey arc
cue invariant, which means that they respond to first-order
motion o f luminance-defined contours but also to second-
order motion o f contours defined by concrasc, texture,
flicker, or disparity ( O ’Keefe and Movshon 1998; Albright
1992).
W it h moving sine-wave gratings, the m otion tuning
functions o f 7 5 % o f M T cells in the monkey varied with
the spatial frequency ot the grating. For one ot the cells,
preferred speed fell from 4 0 to 1 .5 7 s as spatial frequency
changed from 0 .1 2 5 to 4 cpd. However, with square-wave
gratings, which contain multiple spatial frequencies, speed
tuning was largely independent o f the spatial period ot the
grating (Priebc et al. 2 0 0 3 ). Since the images o f most natu­
ral objects contain a mixture o f spatial frequencies, M T
cells normally provide a signal that is independent o f the
torm and spacial-frequency content ot the moving stimuli.
Cells in V I arc responsive to boch the orientation and
the direction ot motion ot local stimuli. There is an essential
ambiguity in signals produced by a moving line. D etection
ot the pattern ot m otion o t a complex object requires sig­
nals from V I cells to be com bined. C ells in V I respond
selectively to com ponent motions o f superimposed gratings
moving in orthogonal directions, while cells in M T respond
to the composite plaid motion o f the whole display
(Snowden et al. 1 9 9 1 ; Movshon and Newsome 1996). Huk
and Heeger ( 2 0 0 2 ) noted the same preference for plaid
motion in f M R I recordings trom M T in humans. W h en
rhe perceptual coherence o f rhe plaids was reduced, rhe
response from M T declined. Rust et al. ( 2 0 0 6 ) produced a
cascade model in which M T cclls act as linear hirers thar
com bine signals trom populations ot nonlinear cells in V I .
However, M T cells do not com bine m otion signals
derived trom gratings presented dichoptically (Tailby et al.
2 0 1 0 ) . Thus cells in M T only com bine motion signals aris­
ing trom the same eye. In humans, dichoptic orthogonal
gratings producc rivalry rather than plaids, unless the grat­
ings are brief or have low contrast (see Section 12.3.6b).
Wc will now sec that M T is involved in the detection o f
patterns o f optic flow created by self-motion or by the
motion o f 3 -D objccts.
In the owl monkey, M T has distinct bands (Born and
Tootell 1 992). Cells in some bands respond best to motion
in the same direction over a large area and arc therctore sen­
sitive to motion produced by head rotation. Cells in other
bands have center-surround antagonistic receptive fields.
The response to a cencral moving stimulus is inhibited by
surround morion in the same direction and enhanced by
surround motion in the opposite direction (Allman et al.
1 985). These cells therefore respond besr to relative motion
(first spatial derivative o f m otion), which arises trom motion
parallax produced, for example, by lateral motion o f slant­
ing o r inclined surfaces o r o f surfaces at different distances.
O th er cclls respond best to the second spatial derivative o f
motion produced by motion ot 3-D curved surfaces. These
cclls seem to be designed to d ctcct velocity gradients in pat­
terns ot optic flow generated by selt-motion or to register
chc 3 -D layout o f objects from patterns o f relative motion
(X ia o ct al. 1995; Buracas and Albright 1 9 9 6 ; Treuc and
Anderson 1996). Liu and Van Hulle ( 1 9 9 8 ) developed a
neural network model o f the responses o f cells in M T to
morion.
M otion parallax between two objects is an ambiguous
stimulus tor relative depth unless the parallax is generated
by motion o f the head. Thus detection o f the sign o f depth
produced by m otion parallax requires the observer to com ­
bine information about motion o f the retinal images and
information about head motion (Section 28.3). Nadlcr
cc al. (2 0 0 8 ) recorded from cclls in M T o f two macaque
monkeys as they fixated a stationary stimulus while a patch
o f random dots was moved laterally
*
co-and-fro to simulate
various depths between the fixation point and the patch. In
the head-motion condition the motion o f the patch was
accompanied by sideways motion ot the m onkeys head. In
chc image-mocion condition the same retinal motion was
created but with the head scacionary. In the image-motion
condition M T cclls responded with opposite phase but
similar amplitude to both directions o f motion o f the patch.
In the head-motion condition, some cclls responded when
the motion indicated that the patch was far and other cells
responded when the patch was near. Thus, the cclls co m ­
bined image m otion with signals indicating head motion to
derive signals that indicated the sign o f relative depth
between the fixation point and the moving patch.
X iao e t al. ( 1 9 9 7 ) recorded trom M T o f macaque m o n ­
keys in response to the projected image o f a textured surface
rotating in depth. In this type o t display the velocity gradi­
ent o f the pattern o f m otion parallax indicates che slant o f
the surface. The orientation o f the rotation axis is indicated
by the direction o f chc gradienc o f motion parallax. A sub-
stancial number o f cells were selectively responsive to the
orientation o f the rotation axis. The cells had asymmetric
4
receptive fields appropriate tor the detection o f the direc­
tion o f motion (Rees et al. 2 0 0 0 a ).
The activity o f M T cclls is influenced by changes in the
perceived direction o f motion when chc physical stimulus is
unchanged. Bradley ct al. (1 9 9 8 ) trained monkeys со indi­
cate the direction o f motion o f an ambiguous 2 -D projec­
tion o f a revolving transparent textured cylinder. Many
neurons in M T changed cheir activity whenever the dircc-
cion-of-mocion percepc changed, even though che scimulus
remained the same. However, most o f chesc cells responded
more vigorously when the cylinder was seen rotating in a
given direction rather than in the opposite direction (sec
Section 11.5.2a). From the same laboratory, Grunewald
cc al. ( 2 0 0 2 ) obcained similar results in M T and some
stimulus related changes in some cells in V I . Dodd ct al.
(2 0 0 1 ) showed that the correlation between responses o f
cclls and the m onkeys reports arc not due to eye move­
ments, response bias, sensory adaptation, or attention to
particular locations o f the stimulus.
O n e can therefore predict an anim als response to
ambiguous or near threshold stimuli trom the response ot
cortical neurons. Such predictions are known as ch o ice
p ro b ab ilities (Britten ct al. 1996).
Cells in M T and M S T are subject to effects o f learning.
Zohary et al. ( 1 9 9 4 ) found a 13% increase in sensitivity ot
motion-sensitive cells in M T and M S T o f the monkey asso-
d ated with a 19% improvement in the ability to discrimi­
nate directions o f motion.
The f M R I response from V 5 in humans was stronger
during periods when a flickering random-dot display
appeared to move than when it appeared stationary (M uckli
ct al. 2 0 0 2 ). The response from V I did not change as the
percept changed. Activity in human V 5 , revealed by t M R I,
has also been found to be influenced by a motion aftereffect
induced in a stationary stimulus (H e ct al. 1998).
The P E T scan has revealed that V5 in the human brain
is specialized for motion (Z ek i et al. 1991). Magnetic reso­
nance imaging ( f M R I ) revealed that area V 5 is particularly
responsive to 3 -D stimuli undergoing rigid or nonrigid
motion (O rban et al. 1999) (Portrait Figure 5 .55 ). Also,
different regions of V5 respond to circular, radial, and trans­
lator)' patterns ot optic flow (M o rro n c et al. 2 0 0 0 ).
Increasing the directional coherence o f a display o f moving
Fifwc 5-5S- G uy O rban. I le o b ta in ed an M .D . in 1 9 6 9 . a degree in
en g in eerin g in 1 9 7 4 , and a P h .D . in n eu rophysiology in 1 9 7 5 , all from
chc U niversity o f Leuven, B elgiu m . B etw een 1 9 7 0 and 1 9 8 2 he was a
research assistant fo r the N atio n al Fund tor Scien tific R esearch and
associated lectu rer in the m ed ical sch ool a t the U n iv ersity o t Leuven.
Sin ce 1 9 8 2 he has been a professor in the D e p a rtm e n t o t N cu roscicn ccs
in th e m ed ical sch ool o t th e U n iv ersity o t Leuven.
random dots increases the fM R1 signal from V5 (Moutoussis
et al. 2 0 0 5 ).
O rban ct al. ( 1 9 9 5 ) identified an area adjaccnt to V 5 in
humans that responded to shapes defined by motion. They
callcd this the k in e tic occipital region ( К О ) . Using f M R I ,
Van O ostende et al. ( 1 9 9 7 ) found that this area responded
more strongly to motion-defined shapes than to simple
motion or to shapes defined by luminance contrast.
However, Zeki ( 3 0 0 3 ) disputes the claim that К О is a dis­
tinct visual area. He considers it to be part o f V3.
The fundus ot the superior temporal sulcus ( F S T )
receives inputs from M T . Mysore ct al. ( 2 0 1 0 ) found that
m ost cclls in the F S T ot monkeys were selective for specific
3 -D shapes defined by motion parallax, such as slanted
planes, saddles, and cylinders. The responses were independent
o f the position or size o f t h e stimuli. Area F S T contained
more cclls of this type.
5 . 8 . 4 c C o r t i c a l A rea M S T
The medial superior temporal cortcx (monkey M S T or
human V 5 A ) rcccivcs a major input from M T . Inputs co n ­
verge, so that receptive fields o f cells in M S T , especially in
the dorsal portion, are larger than those o f cclls in M T
(Ungerlcider and D esim one 1 986). This suggests that
reccptive fields o f M S T cclls arc constructed from the
receptive fields o f M T cells.
In monkeys, the threshold degree ot coherent motion in
a display o f random dots required to produce a response o f
individual cclls in M T and M S T was similar to the psy-
chophysicallv determined threshold. The two thresholds
varied in the same way to changes in stimulus properties
(Celebrini and Newsome 1994).
Cells in M S T are sensitive to patterns ot optic flow,
especially to global patterns o f visual motion such as trans­
lation, rotation, expansion/contraction, and rotation in
depth (fanning). Responses to motion were more position
invariant than those in M T (D uffy and Wurtz 1991, 1997;
Graziano ct al. 1994; Lagae et al. 1994; Bradley ct al.
1996).
The motion specificity o f M S T cells could be due to
inputs cither from subregions sensitive to distinct linear
directions (direction mosaic hypothesis) or from subre­
gions sensitive to similar patterns ot optic flow (vector field
hypothesis). Position invariance o f responses o f M S T cclls
supports the latter hypothesis, although M S T cells arc not
entirely position invariant (Tanaka ct al. 1989; Duffy and
W urtz 1 9 95 ) (Portrait Figure 5 .5 6 ). Som e M S T cells were
influenced by the direction ot gaze and by the direction o f
pursuit eye movements (Squatrito and Maioli 1996).
Cclls in M S T respond in ditferent ways to optic flow
due to self-motion and signals arising from the motion o f
objects. They could therefore be involved in coding the
direction o f heading as one moves through a 3 -D scene
(Page and Dutfy 1999; Logan and Dufty 2 0 0 6 ) . There are

F>Rurc5.S*- R obert И . W urtz. B orn in S t L ou is in 1 9 3 6 . H e received an
Л .В . from O b c rlin C o lleg e and a P h .D . trom the U niversity o f
M ich ig an w ith Ja n ie s O ld s. H e did p o std o cto ral w ork in the
d ep artm en t o f physiology, W ash in gton U niversity, and at th e N ational
Institu te o f H ealth . In 1 9 6 6 he jo in ed the lab o rato ry o f n eu robiology at
N 1H and in 1 9 7 8 he founded the lab oratory o l sen sorim otor research
in the N ational Eye Institute. R o b e rt W u rtz was elected to the N ational
A cadem y o f Scien ces in 1 9 8 8 , the Institu te o f M ed icin c o f th e N ational
A cadem y o f Scien ces in 1 9 9 7 , the A m erican A cadem y o l A rts and
Scien ces in 1 9 9 0 . H e was president o\ the S o c ie ty for N euroscience in
1990.
more cells in M S T responsive to radial expansion than cells
responsive to contraction (Gccsaman and Andersen 1996).
Expansion is associated with forward self-motion. Page and
Duffy (2 0 0 3 ) Found chat neurons in monkey M S T co m ­
bined visual and vestibular signals in coding heading direc­
tion. Elcccrical scimulacion of cclls in M S T ofalcrc monkeys
biased their judgments o f heading direction (Britten and
van Wezel 1998).
The responses o f cells in M S T were found to be inde­
pendent o f chc prcccding scimulus (Paolini cc al. 2 0 0 0 ) . In
other words, they were not tuned to specific changes in
chc flow field that might arise as the animal moves along a
complex path through the environment.
M any cells in M S T responded during pursuit eye move­
ments or со che retinal motions o f single spots or large dis­
plays thac iniciacc ditfcrcnc cypcs o f visual pursuic (Komacsu
and W urtz 1888a, 1 9 8 8 b ; Bradley ecal. 1996). This includes
visual pursuit o f objcccs moving in depch.
Som e cells in monkey M S T responded specifically to
objcccs rocacing in depch, some со objcccs rocacing abouc a
horizontal axis, ochers to objcccs rocacing abouc a vercical
axis (Saico ec al. 19 8 6 ; Sakaca ec al. 1986). Som e cells in che
dorsal M S T o f a lc r c monkeys responded со cilc alone, со
slanc alone, or to both the tilt and the slant o f a surface. Tilt
and slanc were defined by gradicncs o f motion o f random-
dot surface patches (Sugihara et al. 2 0 0 2 ) . Some cells in
chc lateral-ventral region o f M S T were jointly tuned to
motion and binocular disparicy. For some o f these cells chc
disparity preference in che ccncer o f che receptive field dif­
fered from chac in chc surround (Eifuku and Wurcz 1999).
They chus responded to spatial gradients ol disparity and
could be involved in perceptual segmentation o f moving
camouflaged objects.
The response o f motion sensitive cclls in M S T is sub­
stantially* the same whatever feature defines the motion
boundary. Thus, the preferred direction o f cells was che
same for mocion o f a d o t pactern, a solid or an outline
square, and o f a region defined by flicker (Gccsam an and
Andersen 1996). 'Hiis suggescs chat M S T is involved in che
dececcion ot shape from mocion. For chis purpose, one
would expecc connections со che inferior ccmporal corcex.
The dececcion o f binocular disparicy in areas M T and
M S T is discussed in Scccion 1 1.5.2a.
5 .8 .4 d R oscral S u p e r io r T e m p o r a l C o r t e x
M T and M S T are in chc caudal superior temporal corcex.
There has been some disagreement abouc che tunccions ot
chc roscral superior ccmporal corccx. Som e invcscigacors
have claimed chac ic is associated with spatial orientation,
while others have claimed chat ic is associated wich objccc
recognicion. The area receives polysensory inputs from che
inferior pariccal lobe o f chc dorsal scream associaccd wich
spacial oriencacion and from the inferior cemporal cortex
ot the vencral scream associaccd with objecc recognicion.
Therefore, this area is probably associated wich both func-
cions (see Karnath 2 0 0 1 ).
Vaina ec al. ( 2 0 0 1 ) found chac chis region was accivaced
in che human M R I when subjects performed discrimina-
cion tasks involving biological mocion, such as recognizing
a human walker from a pattern o f moving light poincs.
The traditional view is that lesions in the right inferior
parietal lobe cause visual neglect, in which the patient is
unable to fixate, accend to, or recall objeccs in che concralat-
eral field (Section 32.1.1). However, Karnath ct al. ( 2 0 0 1 )
found that neglect in patients wich no ocher visual-field
detects is due со lesions in che roscral superior cemporal
corcex, che basal ganglia, or pulvinar. They concluded chac
chesc three cencers form a cortico-subcortical network
underlying spatial awareness. The left superior temporal
cortex in humans is associated with language.
5 . 8 .4 e P o s te rio r Pariccal C o r c e x
The human poscerior parietal cortex includes che superior
parietal lobe, che inferior pariccal lobe, che intrapariccal
sulcus, and rhe medial parietal corcex. These areas are sec
ouc in Table 5.2. In che monkey, che intrapariccal sulcus is
subdivided, as shown in the cable, and the inferior parietal
lobe contains areas 7a and 7b.
Visual and eye-posicion signals interact at various sub­
cortical sites, including the superior colliculus (Sparks and
l . i b l e 5 .2 . A R E A S W IT H IN T H E P O S T E R IO R
P A R IE T A L L O B E .
S u p e r io r p a r ie ta l c o r tc x (B A 5 an d 7)
In fe r io r p a rie ta l c o r te x (B A 7 a , 7 b , 3 9 a n d 4 0 )
In tr a p a r ie ta l su lcu s
L a te ra l in tr a p a rie ta l a re a ( L I P )
M ed ia l in tr a p a rie ta l a re a ( M I P )
V en tral in tr a p a r ie ta l area ( V I P )
A n te r io r in tr a p a rie ta l a re a ( A I P )
M e d ia l p a rie ta l c o r tc x
Porter 1983) and pulvinar (Robinson et al. 1990). The
posterior parietal cortcx is the main center for coordination
o f visually guided movements o f arms, head, and eyes in
relation to an object to which an animal is attending
(Hyvarinen 1982; Bruce and Goldberg 1985; Medendorp
et al. 2 0 0 5 ).
T he position o f a visual o b ject is first coded in a retinal
frame o f reference, which must then be transformed into a
headcentric frame o f reference by taking eye position into
account. Finally, the position of the visual o b je ct must be
transformed into a bodvcentric frame o f reference for the
purpose of guiding limb movements (see Figure 4.7 ).
Som e cells in the monkey posterior parietal cortex
responded to a stimulus in a given retinal location, but
response magnitude depended on the position o f t h e eyes
in the orbits (Andersen et al. 19 9 0 ; Duhamel et al. 1992).
O th er cells were influenced by proprioceptive inputs from
one, two, or more arm joints (Mountcastle et al. 1975;
Leinonen et al. 1979) (Portrait Figure 5 .57 ). O th er cells
were influenced by proprioceptive signals from the neck
(Brotchie et al. 1995). O thers were active when the animal
reached tor or manipulated an o b ject in a given location.
Their activity was independent ot the trajectory of the arm
movement (Hyvarinen and Poranen 1974; Bushnell e t al.
1981; Bradley et al. 1996).
Recordings from the human parietal cortex using
f M R I revealed regions o f activity related to memory-guided
movements o f rhe eyes and arm in a gaze-centered frame o f
reference I’ Medendorp et al. 2 0 0 3 ).
Area 7a in the inferior parietal lobe contains binocular
cells with large receptive fields. It seems to be specialized tor
coding the bodvcentric positions o f objects in extrapersonal
space, tor directed reaching and navigation (Snyder et al.
1998). Area 7a has some inputs from rhe vestibular system
and trom centers that code eye position. It therefore receives
information required for coding the headcentric locations
ot objects (see Zipser and Andersen 1 988). Area 7a projects
heavily to the hippocampus, an area involved in spatial
memory and navigation (see Andersen 1997).
Пциг<*.$7. У ст ог R. Siauntcastle. B o rn in Sh clbyv illc, K en tu cky, in 191 8.
H e o b tain ed an M .D . from Jo h n s H op kins H osp ital in 1 9 4 3 . Sin ce
19-48 he has been at the Jo h n s H op kins U n iv ersity wSchool o t M edicin e.
H e was pro fesso r o f physiology from 1 9 5 9 to 1 9 8 0 and professor o f
n cu ro scicn cc from I 9 S 0 со 1 9 9 1 . Awards inclu d e the Lashlcv
4 Prize o f
the A m erican P h ilo sop h ical Society, the S c h m itt Prize and M ed al at
M .I.T ., the G o ld M edal o t the Royal S o ciety o f M cd icin c, chc G erard
Prize o f chc Sociccv for N eu ro scien ce, the Lasker Award, the M cG ov ern
Prize and M edal o f t h e A .A .A .S .. and the N cu ro scicn cc Prize o f the
N .A .S .
Siegel and Read ( 1 9 9 7 ) recorded from cclls in area 7a
o f monkeys viewing random-dot displays undergoing
translation, rotation, or radial motion in a frontal plane.
Som e cells responded differentially to opposite directions
o f optic flow, such as radial expansion versus contraction.
There was a predominance o f cells more sensitive to
expansion than to contraction. O th er cclls responded dif­
ferentially to distinct classes o f optic flow, such as radial
versus rotary*
motion.
Sakata ct al. (1 9 9 4 ) found many cclls in area 7a o f t h e
monkey that responded selectively to rotation of a slit in a
given direction in 3 -D space. The response o f some o f these
cells showed periodic changes when the monkey viewed an
ambiguous rotating trapezoid (Ames window) monocu-
larly. Som e cells responded best to motion in depth defined
by looming, others to motion in depth defined by changing
disparity, and others to motion in depth defined by either
stimulus (see Sakata e t al. 1997).
Ferraina et al. (1 9 9 7 ) recorded from cells in area 7a as
monkeys reached to objects that the animals fixated or did
not fixate. Som e cells responded selectively to eye position,
others to the position and motion o f the hand. But most
cells responded to a combination ol hand position and eye
position.
 The lateral and medial intraparietal areas ( L I P and
M I P ) receive visual inputs via V 3 A , M T , and M S T , as well
as auditory, somcsthctic, and vestibular inputs. They also
receive eye-position signals from the superior colliculus,
and inputs from the ccrcbcllum, basal ganglia, and frontal
lobes.
Area L IP projects to cortical areas concerned with the
generation o f arm movements, including M IP, the prefron-
tal motor cortex, and the neighboring parietal-reach
region (P R R ) (Batista and Andersen 2 0 0 1 ; Andersen and
Bunco 2 0 0 2 ) (Portrait Figure 5 .58 ). Area L IP also projects
to areas concerned with generating saccadic eye movements,
including the superior colliculus and the frontal eye fields
(Section 10.10.2).
In the monkey, L IP seems to be specialized lor coding
the headcentric positions o f stimuli to which the animal is
attending. Som e cclls responded preferentially to an
attended stimulus in a given headcentric direction, whether
or not the animal made an eve movement to the stimulus
(C olbv ct al. 1 9 % ) . O th er cclls responded to stimuli at a
given distance. Som e cells were tuned jointly to direction
and distance (Sakata ct al. 1980; Andersen and Mountcastle
1 983). These cells bring auditory and visual stimuli into a
com m on headcentric frame o f reference (Andersen and
Bunco 2 0 0 2 ).
F.Surt5.s*. R ich a rd /I. .b id erie» . H e ob tain ed а В .Sc. in B io ch em istry from
the U n iv ersity o f C a lifo rn ia , D avis, in 1 9 7 3 and a P h .D . in physiology
from Jo h n s H o p k in s M ed ical S ch o o l in 1 9 8 1 . H e was on th e faculty of
the Salk Institu te in L a Jo lla from 1981 to 1 9 S 7 and the facu lty o f M I T
from 1 9 8 7 to 1 9 9 4 . In 1 9 9 4 he jo in ed the B io lo g y D ivisio n o f C a ltc cli
in P.iv.ulcna, w here he i* th e Jam es C . Bosw ell professor o f neu roscience
and d ire cto r o f t h e Sloan C e n te r for T h eo retical N eurobiology.
R ecip ie n t o f t h e Sp en cer Award at C o lu m b ia U n iv ersity in 1 9 9 4 .
Many neurons in I.IP responded when the monkey was
about to make a saccadic eye movement or arm movement
(Snyder ct al. 1997, 1 998). O th er cclls responded in rela­
tion to eye movements in 3-D space (Section 10.10.2). The
responses o f these cclls in the alert monkey did not depend
directly on sensory inputs or m otor outputs. It seems that
they cncodc a movement that is about to occur, even after
the visual target has been removed (Eskandar and Assad
1999). Electrical stimulation o t cells in L IP evokes saccadcs
(Thier and Andersen 1998).
The stimulus selectivity of cells in U P depends on the
stimulus feature to which monkeys had been trained to
make a saccadic eye movement. Thus, cells showed location
selectivity after monkeys had been trained with location-
defined targets, and color selectivity after they had been
trained with color-defined targets (T oth and Assad
2002 ).
A change in the stimulus to which human subjects were
attending was associated with 1M RI activity in the lateral
intraparietal cortex (I.IP ). A change in the response made
to a given stimulus was associated with activity in the medial
intraparietal cortex (M I P ) (Rushworth et al. 2 0 0 1 ).
T he medial intraparietal c o rtc x ( M I P ) is specialized
for processing stimuli within reaching distance. Cclls in this
area responded to either somatosensory or visual inputs or
both, and were sensitive to stimulus features such as direc­
tion and movement. Some cells maintained their response
duringa memory-guided response (see Colby and Goldberg
1999).
Cells in the monkey superior parietal lobe (area 5)
responded selectively to rhe position o f the hidden arm and
also to the position of a visible false arm, if it was realistic
(Graziano et al. 2 0 0 0 ) . Ferraina et al. ( 2 0 0 9 ) recorded in
the superior parietal lobe while monkeys reached to m em o­
rized objects at different distances. The response o f 6 1 % o f
tested neurons depended on the starting position o f the
hand, while the response o f 13% depended on rhe vcrgcncc
angle ot the eyes. The results indicate that the superior pari­
etal lobe com bines information about eye position and
hand position to encode target distance from the initial
hand position, that is, in hand coordinates.
The ventral intraparietal area ( V I P ) receives inputs
from M T and M S T (Baizer ct al. 1991). Chem ical tracers
have revealed visual, tactile, vestibular, and auditory inputs
(Lewis and Van F.sscn 2 000). Electrophysiological procedures
have, also, revealed that some V I P cells are bimodal or mul­
timodal. Som e cclls responded to both visual and tactile
stimuli. The preferred direction for a visual stimulus was
correlated with the position o f a tactilc stimulus applied
to the head or body (D uham el et al. 1998). Som e cells
responded to visual motion and to vestibular stimuli
(Brem mer et al. 2 0 0 2 ) . These cells could be involved in the
detection o f self-motion. Som e cells responded to visual
and auditory stimuli. Their visual receptive fields overlapped
their auditory receptive fields (Schlack et al. 2 0 0 5 ).
 Cclls in monkey V IP arc specifically sensitive to optic
flow. Som e cells responded lx*st to a stimulus moving from
any azimuth direction toward a particular point on the
facc (impact direction) (C o lb y et al. 1 9 9 3 ). Som e cells also
responded to tactile stimuli applied to a particular location
on the face. Electrical stimulation o f these cells evoked
appropriate head withdrawal and defensive movements ol
the hand (C o o k e et al. 2 0 0 3 ).
O ther cells in V IP responded to textured surfaces
rotating in deprh or to patterns o f optic How simulating
rotation in depth. But these cells were not specifically sensi­
tive to rotation in depth, as were cells in M T or M S T
(Schaafsma et al. 1997). Vanduflel et al. ( 2 0 0 2 ), also, found
that motion in depth did not evoke specific fM R I responses
in the monkey ventral intraparietal area. However, this area
showed specific f M R I responses to motion-in-depth in
humans.
I.ike cclls in M S T , V IP cells show position invariance,
which suggests that the vector field mechanism operates for
them (Schaafsma and Duysens 1 996). Also, like some cclls
in M S T , some V IP neurons encode the direction o f visual
stimuli in terms o f headcentric coordinates (D uham el ct al.
1997).
The a n te rio r intraparietal area (A 1P ) receives inputs
from area L IP and projects to the premotor cortex
(Nakamura et al. 2 0 0 1 ) . Sakata ct al. ( 1 9 9 9 ) (Portrait
Figure 5.59) lound cells in A IP o f the alert monkey that
responded selectively to the visual shape, size, and 3-D
orientation o f objects that were being manipulated or
✓ representation o f the position and motion o f the body
H id fo Sak*rta. B orn in Sap p o ro , Ja p an , in 1 9 3 4 . H e graduated
in liberal a m in 1 9 5 5 and in m ed icin e in 1 9 5 9 from T o kyo U niversity.
H e o b ta in ed a D .M .S . in physiology from T o kyo U niversity in 1 9 6 4 .
B etw een 1 9 6 4 and 1 9 7 3 he held academ ic a p p o in tm en ts at O saka C ity
U niversity, th e Scrips In stitu te o f O cean o g rap h y in San D ieg o , and the
Jo h n s H op k ins U n iv ersity S c h o o l o f M ed icin e. In 1 9 7 3 he m oved to
th e T okyo M etro p o lita n In stitu te lor N c u ro s c ic n c c s where he becam e
head o f the L ab o ra to ry o f N cu ro scicn ccs. In 2 0 0 0 he becam e professor
ac N ih o n U niversity.
were about to be manipulated. Many o f these cclls were
binocular.
O th er cclls in A IP that responded moderately or not at
all to visual features o f objects showed selectivity for the
type o f handgrip involved in reaching for and grasping
objects o f different sizes, shapes, and orientations (Murata
ct al. 2 0 0 0 ).
DeSouza et al. (2 0 0 0 ) found an area in the human intra-
parietal sulcus that showed f M R I activity during pointing
to a visual target. The response was enhanced when subjects
looked in the direction of the pointing hand. They sug­
gested that this area could be involved in transforming reti­
notopic locations into arm-centered motor commands.
Areas A IP and LIP in the monkey showed f M R I activation
in response to both the 2 -D and 3-D structure o f small
objects consisting o f line elements, and o f small surface
patches (Durand et al. 2 0 0 7 ) .
Posterior parietal lesions in humans cause deficits in
grasping and manual manipulation (Pause et al. 1989).
Patients could imitate the finger movements o f another
person and had little loss of somatosensory sensitivity.
However, they were deficient in generating hand move­
ments in response to objects detected visually or factually.
T he f M R I from normal subjects revealed that area A IP is
specifically activated during grasping !,Binkofski et al.
1998).
In a related area in the lateral bank of the caudal intra-
parietal sulcus ( C I P ) o f monkeys, Sakata ct al. ( 1 9 9 9 )
found cells that were selectively responsive to the 3 -D ori­
entation o fb a rlik c objects portrayed in a stereogram. O th er
cells in the same general area responded selectively to the
3 -D orientation ot surfaces defined only by disparity in a
random-dor stereogram (Taira e t al. 2 0 0 0 ) . Many neurons
in this area also responded to the 3 -D orientation o f sur­
faces defined only by texture gradients. Their responses were
invariant over different patterns of texture (Tsutsui et al.
2002).
Shikata et al. ( 2 0 0 1 ) showed that areas within the intra­
parietal sulcus in humans showed FM RI activity when sub­
jects discriminated the 3-D orientation ot a surface defined
by the monocular cue o f texture gradient.
O n e can think o f the parietal lobe as containing a
and ot body parts in relation to external objects that
are guiding behavior (C oh en and Andersen 2 0 0 2 ).
M o to r com m ands and contingent sensory inputs (realfer-
ence) keep the representation updated (W olpert ct al.
1 998). However, mechanisms involved in willing a move­
ment and in detailed planning o f a movement remain
mysterious.
The role o f t h e parietal lobes in attention is discussed in
Section 5.9.2b. D efects in spatial perception and behavior
arising from damage to the parietal co rtcx are discussed in
Section 32.1. The visual control o f reaching is discussed in
Scction 34.3.
 For a review o f the parietal lobes see Stein ( 1 9 9 1 ) ,
C am initi ( 1 9 9 5 ). Sakata e t al. ( 1 9 9 7 ) , Galletti et al. ( 1 9 9 7 ),
and Andersen and Bu n eo ( 2 0 0 2 ).
5 .8 .4 Г F r o n ta l L o b e s
The distinction between ventral and dorsal processing
streams extends into the frontal cortex. In che monkey, the
posterior parietal cortex o t the dorsal stream projects to the
principal sulcus and arcuate regions o f rhe frontal cortex.
Cells in these regions respond to spatially localized stimuli
and maintain their response when the animal is required to
remember the location o f a stimulus after it has been
removed (Funahashi e ta l. 1989).
The interior temporal cortex ot the ventral stream proj­
ects to area 8 in the arcuate sulcus, area 12 in the inferior
prefrontal convexity, and areas 11 and 13 on the orbital sur­
facc o f the frontal cortex (Ungerleidcr et al. 19 8 9 ; Webster
e t al. 1994). The response o f cells in these regions is rela­
tively independent o f che size, orientacion, and color o f
complex patterns. Cells continued to respond to a pattern
during intervals when the animal was required to remember
the pattern (W ilso n et al. 1993). Lesions in these areas in
monkeys and humans produce deficits in the recognition o f
complex objects, such as faces and words.
Event-related f M R I in humans revealed that retention
o f items in spatial memory is associated with activity in
trontal area 8, while selection ot an item trom memory is
associated wich accivicy in froncal area 4 6 (Rowe ec al.
2 0 0 0 ).
Som e cells in che laceral prefroncal corcex o f monkeys
responded seleccively со computer images o f dogs and
cats chac che monkeys had been crained со carcgorize. Eye
movemencs and psychophysical tescing revealed that the
monkeys were responding ro many features o f che stimuli.
The cells responded to the same stimulus categories after
the boundaries between the categories had been changed by
morphing the shapes (Freedman et al. 2 0 0 2 , 2 0 0 3 ).
Cells in che prefrontal cortex o f alert monkeys chac
responded in che period between presentation ot a stimulus
and the m onkeys response to the stimulus did so in a
manner that varied with the type o f reward received
(W atanabe 1996).
Som e cells in the frontal cortex responded to “what”
features when monkeys were required to remember an
object. O th er cells responded to "where” features when
they remembered a location. Som e cells responded to either
“what” or “where” features according to the task. Ocher
cells responded со boch “what” and “where” features ac
rhe same time (R ao ec al. 1997). Thus, parvocellular and
magnocellular systems projecting to the troncal lobes have
different, buc overlapping, functions.
The ventral and dorsal streams converge on the frontal
eye fields (Bulliereral. 1 9 9 6 ). Cells in chis region responded
in relacion со eye movements thac a monkey was planning
со make (Kim and Shadlen 1998). Cells in che frontal eye
fields code eye movements in 3 -D coordinates. They pro­
duce signals for both version and vergence appropriate for
tracking an object in 3 -D space (Fukushima et al. 2 0 0 2 ).
T h iscom plcx signal must be decomposed so thac brainsccm
mechanisms responsible for version and vergence receive
correct signals (Section 10.10.3).
Cells in the frontal eye fields normally respond to any
stimulus to which the animal is about to make a saccadic
eye movement. In monkeys trained to fixate targets o f only
one color, cells in the frontal eve
•
field became selectively
responsive to stimuli o f that color (B ich o t et al. 1996).
5 .8 .4 g P r e m o t o r C o r t e x
In primates, the ventral intraparietal area ( V I P ) , che lateral
incraparietal area (L IP ), and medial superior temporal
cortex ( M S T ) project to area 7 b in the posterior parietal
lobe, which projcccs to the premotor corcex, especially che
ventral region (area 6 ). Tactile, visual, auditory, and propri­
oceptive sources o f information converge in the premotor
cortex, which is concerned with the control o f movements
ot the mouth, head, and arms. The premotor cortex projects
to the primary m otor cortex and spinal cord.
The premotor cortex contains a somatotopic represen­
tation o f the body, especially o f the arms, face, and mouth.
Som e cells respond preferentially to one sensory modality,
while other cells arc bimodal or trimodal (Kurata and Tanji
1988). For example, some cells in rhe premotor cortex
responded to tactile stimuli applied to a particular region o f
skm, to visual stimuli placed near che same region, and со
sounds originacing within a distance o f about 3 0 cm trom
the head (Graziano ec al. 1999).
In che monkey, a near o b ject approaching the body is a
particularly effective stimulus for rhe premocor corcex. The
receptive fields o f mosc visually sensitive cells in the prem o­
tor cortex do noc change with changes in che direction o f
gaze (Fogassi et al. 1996). For most cells with a tactile recep­
tive field on the arm, the visual receptive field moved when
the arm moved (Graziano et al. 1997). Also, most cells that
responded to the position o f the arm, as indicated by prop­
rioceptive scimuli, changed the location o f their visual
receptive field when the arm moved (Graziano 1999). Thus,
these “arm + visual” cells code visual stimuli in bodvcentric
J
coordinates. Similarly, for m ost cells that responded to
touch on a particular area on the face, the visual receptive
field changed as the head rotated. These “face + visual” cells,
like some cells in the VIP, code visual stimuli in headcentric
coordinates (Graziano ec al. 1997).
The responses o f many cells in rhe ventral premotor
corcex o f che monkey (area 6) were related со movements o f
different parts o f the forelimb (Kurata and Tanji 1988).
Many cells in che monkey premocor and m otor areas
responded in relation to only rhe direction or only che dis­
tance ot an arm movement to visual targets, while ocher
cells were jointly tuned to direction and distance (Fu c t al.
( 1 9 9 3 ). This topic is discussed further in Section 34.3.2.
The responses o f some cells in the monkey premotor
cortex were correlated with specific m otor acts such as
grasping an o b ject with the hand or mouth. Som e cells
responded in relation to movements oi the whole hand
while others responded in relation to precise grasping move­
ments o f the fingers (Rizzolatti ct al. 1 988). Postures involv­
ing the hand were systematically mapped with respect to
positions round the body (Graziano et al. 2 0 0 2 ) . Unilateral
ablation of area 6 in the macaque produced a failure to bite
food presented contralaterally to the lesion and inattention
to objects in the contralateral visual field. Electrical stimula­
tion o f local regions o f the monkey premotor cortcx evoked
coordinated postures o f hand and head (G entilucci et al.
1988).
Bimodal cells coding visual stimuli in armcentric and
headcentric coordinates have also been found in the puta-
men. This is a subcortical nucleus in the basal ganglia receiv­
ing inputs from the parietal lobe and premotor cortex
(Graziano and Gross 1993).
Reaching and grasping are discussed in more detail in
Section 34.3.
5 .8 .5 E V I D E N C E F O R D I S T I N C T P A T H W A Y S
5 .8 .5 a In teraction s B etw een Ventral and
D o rsal Pathways
The anatomical distinction between the ventral and dorsal
cortical streams is by no means complete. There is evidence
o f partial convergence o f parvoccllular and magnocellular
inputs even in the primary visual cortex (see Schiller ct al.
1990). In addition, there are extensive interconnections
between all visual areas, especially between rhe temporal
and parietal lobes (DcYoe and Van Essen 1988).
Although the main input to V4 is from the parvocellu-
lar system, a few sites in this area show evidence o f inputs
from the magnocellular system (Maunsell ct al. 1990;
Ferrera et al. 1992, 1994). Monkey M T receives strong
magno- and parvoccllular inputs from V I (Nassi c t al.
2 0 0 6 ) . The anterior superior temporal polysensory area
( S T P ) receives inputs from both dorsal and ventral path­
ways and contains cells jointly tuned to the form and motion
o f visual stimuli (O ram and Pcrrctt 1996).
Some cells in the monkey posterior parietal cortex (L IP )
responded differentially to different shapes, even when the
animal was not performing a m otor task (Sereno and
Maunsell 1998). However, neurons in L IP are n ot as sensi­
tive to differences between shapes as are neurons in the inf-
erotemporal cortex o f the ventral stream (I.ehkv and Sereno
2 0 0 7 ). Shape selectivity in 1.1 P may depend on inputs from
V 4 and the interior temporal cortex (Webster e t al. 1994).
Bur even if this is so, shapes are processed in different ways
in the two streams.
O n e reason for interconnections between regions p ro­
cessing ditferent features is that ambiguity in the location o f
contours defined by one feature can be resolved by refer­
ence to another feature. Thus, information flow between
different systems allows one to exploit redundancies in the
visual world.
5 .8 .5 b Sp ecific E ffects o f C ereb ral Lesions
The effects o f lesions within the parvoccllular and m agno­
cellular systems ot the monkey support the idea o f two
processing streams. Lesions in the parvocellular laminae
ot the L G N produced deficits in color vision, fine pattern
discrimination, and fine stereopsis (Schiller et al. 1990).
Lesions in the parvocellular retinogeniculate pathway
reduced chromatic sensitivity at all spatial frequencies and
achromatic sensitivity at high spatial and low temporal fre­
quencies (Merigan 1989). Lesions in V4 also produced
color-vision defects, although they were less severe and less
permanent than defects produced by lesions in the L G N .
Lesions in the inferior temporal lobe produced deficits in
object recognition (Pohl 1973).
Humans with lesions in the inferior temporal cortex
can n ot discriminate between shapes in a similar orientation
but can discriminate between shapes that differ widely in
orientation. Dijkerman e t al. ( 1 9 9 6 ) described a patient
with visual form agnosia arising from damage to the inferior
temporal cortex. She could not match the orientation o f
one disk to that o f another. However, she could accurately
grasp a disk displayed in ditferent orientations, presumably
through the mediation o f an intact parietal system (see
Section 5.8.4c).
Milner ( 1 9 9 7 ) described a patient with carbon m onox­
ide poisoning who could n ot discriminate between stimuli
that differed in size, orientation, or shape even though she
could perform skilled actions that required the registration
o f those stimulus attributes. The literature on the dissocia­
tion between perception and action was reviewed in Milner
and G oodalc ( 1 9 9 5 ) and is discussed in Section 34.3.5.
Lesions in the magnocellular laminae o f the L G N pro­
duce deficits in motion perception, high-frequency flicker
perception, and pursuit eye movements (Schiller et al.
1 9 90 ) as well as reduced contrast sensitivity for low spatial
frequency gratings modulated at high temporal frequencies
(Merigan and Maunsell 1990). Lesions in M T produce
similar deficits (Dtirstelcr et al. 1987). Lesions in the poste­
rior parietal cortex in man and other primates arc associated
with loss ot spatial memory, disturbances ot spatial atten­
tion, and defects in representing spatial relations (Critchley
1955). These defects are discussed in Section 32.1. Humans
with lesions in the parietal cortex can discriminate between
shapes but can n ot discriminate between rotated shapes
(Walsh and Butler 1996).
It has been proposed that rhe magnocellular system is
solely responsible tor coding depth and that the parvocellular
system is blind to binocular disparity (Livingstone and Hubei
1988). Cells sensitive to binocular disparity are certainly pres­
ent in areas V 3 and M T , which are considered part o f the
magnocellular system (Maunsell and Van Essen 1983b ;
Felleman and Van Essen 1987). However, the idea that dispar­
ity detection is confined to the magnocellular system must be
rejected, as we will sec in Section 11.5.4.
T h e picture that emerges is o f many retinotopically
coded visual areas, which process different visual features.
The system is hierarchical in that each area receives its inpurs
from the striate cortcx, sometimes by way o f other areas. The
system is also parallel in that there is divergence into distinct
areas that handle different visual features simultaneously.
Th e areas acting in parallel interact through lateral connec­
tions. At the same tim e, centers higher in the sequence send
recurrent signals back to earlier stages. Som e higher centers
receive visual inputs from the pulvinar o r other subcortical
centers before they receive inputs from V I . They could
therefore modulate inputs from V I by feedback (see
Felleman and van Essen 1991; Z eki 2 0 0 1 ). The system is
probably also multilayered in the sense that the output o f
cach processing unit is available to consciousness. Finally,
the parallel pathways converge into processes that determine
the perception o f com plex objects and events and action
(see Grossberg 19 9 0 ; Rockland and Van Hoesen 1994).
A simple view is that unitary percepts o f o b jects and o f
spatiotemporal relationships arise only after inform ation
from the interrelated parallel streams is com bined. But if
each visual feature were processed independently, some
means would have to be found to keep contours defined by
different features in register. The feature-binding problem
would be cased it the only unitary percept ot the visual
scene as a whole were that o f crudely processed general fea­
tures form ed before the streams segregate. D istin ct and spe­
cialized processing would be concerned only with rhe
analysis ot particular regions or features o f the primitive
scene. There may be no overall unitary percept derived by
com bining the outputs from parallel higher-order process­
ing streams. There is good evidence that parts o f a scene
that are not attended to arc perceived only in the crudest
term s for purposes such as control o f posture, detection o f
self-m otion, control ot eye movements, and redirection o f
attention.
The ultim ate representation o f the perceptual world
may be a high-level associative netw ork, which “consults"
visual inform ation provided by whichever visual centers are
relevant to a given task (H ochstein and Ahissar 2 0 0 2 ).
For example, if the task is that o f detecting o b ject boundar­
ies or discrim inating betw een simple stim uli, such as
two orientated lines, the netw ork may consult only V I .
It the task were that o f m otion discrim ination, it may
consu lt M T ,a n d ifitw e re that o freco g n izin g a visuaJ o b ject
it would consult the inferior tem poral cortex. A ttention
is the process that allows us ro consu lt different visual
processes.
5.8.6. M U L TIM O D A L RESPONSES
A m ultimodal, or cross-modal effect is one in which
the activity o f a cell is affected by stimuli in more than one
sensory modality. Crossm odal effects are o f four basic
types.
1. Nonspecific m odulation in unim odal areas M ost cells in
the primary visual cortcx arc unim odal, although some
cells that receive inputs from the peripheral retina also
receive inputs from the auditory co rtcx and the
polysensory area (S T P ) o fth e temporal lobe (Falchier
et al. 2 0 0 2 ). Also, nonvisual stimuli can evoke a
generalized response in V I . Thus, M urata et al. (1 9 6 5 )
obtained responses to pinpricks or a handclap in about
50% o f cells in the visual cortex o f the cat. A given cell
responded in the same way when the pinprick was
applied to different parts o f the body. This suggests that
the responses were due to general arousal rather than to
location specific cross-m odal innervation o f the visual
cortcx. Very few cells in V I responded to a tactile
stimulus.
2. Location-specific modulation in unim odal areas
Extrastriatc areas such as V 2 , V 3 , and V 4 arc
believed to be unim odal. However, fM R I responses
from the human lingual/fusiform region (V 4 ) revealed
that the response to visual stim ulation was boosted
bv
*
concurrent tactile stim ulation o f the hand when
the visual and tactile stimuli were in rhe same location
in external space. Tactile stim ulation alone had no
effect (M acaluso et al. 2 0 0 2 ). This type o f effect is
probably due to feedback o f signals regarding the
position o f the hand and o f the gaze from higher
centers.
3 . Location-specific responses in polysensory areas Several
areas o t the brain contain cells that respond in a
location-specific way to stimuli in more than one
modality. These are true polysensory areas because
cells respond to stimuli in either o f two or more
m odalities or to the com bination o t stimuli in more
than one modality. Polysensory areas include rhe
superior colliculus (Stein and M eredith 1 9 9 3 ), the
polysensory area (S TP) o f rhe tem poral lobe, the
parietal co rtex (Scctio n 5 .8 .4 c), and the prem otor
cortex.
4 . Responses to common features In cross-modal m atching
we judge som e attribute o f a stimulus in one m odality
with respect со the same attribute in another modality.
For example, we can set the length ot a seen rod to
m atch the length o f a felt rod. Presumably, at some
level in the nervous system, multimodal features
such as size, location, m otion, and sm oothness are
represented in a form that transcends particular
senses.
 5 .9 P H Y S IO L O G Y O F V IS U A L
A T T E N T IO N
General features o f attention were described in Section 4.8.
Any shift o f visual attention w ithin or between o b jects is
accom panied by changes in neural activity in different areas
o f the extrastriate cortex. There are tour types o f attention
enhancem ent o f the responses o f cortical cells. ‘Ih c first
results trom general arousal, the second is location specific,
the third is stimulus specific, and the fourth results from
learning. These effects will now be discussed.
5 .9 .1 G E N E R A L A T T E N T I O N M E C H A N IS M S
The activity o f relay cells in the L G N is enhanced in states
o f general arousal (Scctio n 5 .2 .2 d ). Livingstone and Hubcl
(1 9 8 1 ) found that cells in the primary visual cortex o f alert
cats generally show a reduced spontaneous firing rate and
an enhanced response to visual stim uli com pared with when
the anim al is asleep. Som e cells in V I and V 2 respond more
vigorously before saccadic eye m ovements but n o t specifi­
cally to eye movem ents to stimuli in the ce lls receptive field
(R obinson et al. 1 9 8 0 ; M oran and D esim one 1 9 8 5 ). In
o ther words, the enhanced response at the level o f the LG N
and early stages o f cortical processing is not location-
specific or feature-specific, but reflects a change in general
arousal.
In states ot reduced attention and sleep, cortical
cells engage in high-am plitude synchronous activity at
less than 10 H z. In the awake state, attention is accom pa­
nied by greater synchrony o f neural responses in several
visual areas at frequencies over 35 Hz (sec Section 4 .3 .4 ).
For example, the general activity o f V I o f the monkey was
higher and m ore highly synchronized 100 ms bctorc pre­
sentation o f a stimulus that che animal reported chan before
presentation o f a stimulus that the animal failed to report
(Super c t al. 2 0 0 3 ). T h e anim al was presumably more alert
when it reported the stimulus. Also, responses ot cells in
M T and M S T becam e synchronized ju st before an expected
stimulus was presented (C ardoso de O liveira ct al. 1 9 9 7 ).
The p u lv in ar is a part o f the thalamus that receives m ost
o t its inputs from the ipsilateral cerebral cortex. It sends
reciprocal con nection s to V I , V 2, V 4 , M T , and the parietal,
infcrotem poral, and prefrontal cortex (Stepniew ska 2 0 0 4 ).
There are also con nection s to auditory and somatosensory
cortical areas (Adams et al. 2 0 0 0 ; G utierrez e t al. 2 0 0 0 ).
The pulvinar contains a crudc map o f the cerebral cortcx,
including at least tw o topographic representations o f the
visual field. The pulvinar is im plicated in the control o f
visual attention (R obinson and Petersen 1 9 9 2 ; Levitt o ral.
19 9 5 ; Grieve et al. 2 0 0 0 ). It probably processes stimuli that
require rapid responses, such as visual loom ing chac signifies
impending collision (K ing and Cow cy 1 9 9 2 ; M estrc et al.
19 9 2 ; Beer eca l. 2 0 0 2 ).
A ttention was found to be autom atically allocated to a
loom ing stim uli on a collision trajectory even when subjects
were not aware o f the difference between such a stimulus
and one that was on a near-miss trajectory (Lin et al.
2 0 0 9 ).
Responses ot some cells in the pulvinar were modulated
by the position o f the eyes. O th er cells responded before the
onset o f scll-in itiated arm m ovem ents,even before responses
occurred in the primary m otor cortex or posterior parietal
corcex (C udeiro e t al. 1989).
The th a la m ic reticu lar nucleus (G uillery c t al. 1998)
and the p o n tin e reticu lar form atio n project ro all parts o f
the cerebral cortex through the m ediation o f the neu-
rotransm ittcr seroconin. These nuclei, along wich cencers
in the hypothalamus, are involved in the control o t the
slecp'Waking cycle.
The lo cu s co cru lcu s in the dorsal pons diffusely
innervates the cerebral cortex through the ncurotransm it-
ter norepinephrine {L ev itt and M oore 1 9 7 9 ). It is probably
associated with attention and has been im plicated in
cortical plasticity (Section 8.2.7h ).
The nucleus o f M eynert in the basal brainstem projects
to all parts o f the cerebral cortex through the m ediation o f
the neurotransm itter acetylcholine. This system seems to
control selective attention and perhaps consciousness
(M cG eh ee and Role 1 9 9 6 ; Perry et al. 1999). It is involved
in the generation ot hallucinations and cognitive disor­
ders in conditions such as schizophrenia, epilepsy, and
A lzheim er’s disease (see A lkondon et al. 2 0 0 0 ). This system
seems to provide region-specific atccntional m odulation o f
activity in the cerebral cortex (Sarter and Parikh 2 0 0 5 ).
Rats perform ing a task that required close attention to
stim uli showed an increase in acetylcholine release in the
frontoparietal cortcx. Rats making similar responses that
did n o t require close atten tion showed much less acetylcho­
line activity (Arnold ct al. 2 0 0 2 ).
Several lines o f evidence suggest that the right cerebral
cortex is involved in sensory attention. Rats lacking inputs
to che right cortical hemisphere from cholinergic neurons
in the basal forcbrain had impaired ability to detect
stimuli relevant со perform ance o f a learned cask. Loss o f
cholinergic inputs to the left hemisphere increased the
num ber o f false alarms when no scimulus was presenc.
M arinez and Sarter (2 0 0 4 ) concluded that the right cere­
bral hemisphere mediates stim ulus selection while the
left cerebral hemisphere m ediates executive aspects o f
attention.
G ood perform ance o t human subjects on a sensorim o­
tor task was associated with fM R I activation o f the right
frontoparietal co rtex coupled with decreased activity in
the left lim bic and eingulate areas (Law rence et al. 2 0 0 3 ).
These results accord with the fact that visual neglect is
associated with lesions in the right hemisphere (see
Scction 3 2 .1 .1 b ).
 5 .9 .2 L O C A T IO N -S P E C IF IC C O R T IC A L
E F F E C T S O F A T T E N T IO N
5 .9 .2 a L o ca tio n -S p e c ific E ffects in V I , V 2 , and V 3
The fM R I response in the lateral geniculate nucleus
increased w hen human subjects attended to a flickering
grating in the left or right hcmifield rather than to a foveal
stimulus ( O ’C o n n o r 1)H c t al. 2 0 0 2 ). Responses o fsin g le
cclls in subcortical structures, such as the superior colliculus
and pulvinar, increased when m onkeys redirected their
attention to the stimulus (R obinson and Petersen 1992;
Robinson and Kertzm an 1 995).
Responses o f cells in V' 1, also, are influenced by the locus
o f attention. For example, the response o f cclls in V I was
enhanced when the stimulus within the receptive field was
o n e for which monkeys had been trained to perform a dis­
crim ination task (Vidvasagar 1 998). However, the effects
o f attention on responses o f single cells in m onkey V I have
been generally found to be small (M aunsell and C o ok
2 0 0 2 ). Also, while attention strengthens the responses o f
cells in a given region it does n o t affect the tuning o f cells to
visual features such as orientation (M cA dam s and Maunsell
1999).
The effects o f attention are greater in later stages o f visual
processing. This is what one would expect ot a mechanism
designed to activate those high-level processes involved in
processing attended objects. All o f V I is active when we
view a scene, but activity is required only in the specific
higher processes that relate to the o b ject o f attention.
The fM R I showed large systematic changes in neural
activity in V I o f human subjects as they changed their
attention from one peripheral location to another
(Brefczynski and DeYoe 19 9 9 ; G andhi c t al. 1999).
However, subdural electrodes applied to a local area ot the
human visual co rtex revealed that attention produced only
modest response enhancem ent, similar to that shown by
single unit recording in monkeys ( Yoshor et al. 2 0 0 7 ).
A tten tion did n o t increase visual evoked potentials o f
cells in V I during the initial 50 ms after a stimulus was pre­
sented. It therefore seems that the facilitation evident in the
fM R I was due to feedback from the extrastriate cortex
(M artin ez et al. 1 9 9 9 ). The fM R I response in V I , V 2, and
V 3 was enhanced in humans while they made difficult
stimulus discrim inations (R ees et al. 2 0 0 0 b ). The enhance­
m ent was related to the location o f the stim uli and the
difficulty o fth e task but persisted during intervals between
stimulus presentations. Behavioral evidence for enhanced
visibility o f objects in an attended location was provided in
Section 4 .8.2c.
The local enhancem ent o f neural activity in an attended
4
area o f V I could be associated with activity in the corre­
sponding region o f rhe frontal eye fields associated with a
saccadic eye movement to a stimulus in that area. In co n fo r­
m ity with this idea, M oore and Fallah (2 0 0 4 ) found that
monkeys could d etect smaller changes in the lum inance o f
a stimulus when the corresponding area o f the frontal eye
fields was electrically stim ulated. The effect ceased when the
interval betw een stimulus onset and electrical stimulation
was greater than 3 0 0 ms.
5 .9 .2 b L o c a tio n -S p e c ific E ffe c ts in th e
D o rs a l S tream
M otion-sensitive cells in M T and M S T o f the monkey
responded more vigorously when the animal attended to
the m oving stimulus (Treue and Maunsell 1999). C ells in
M T o r M S T responded more vigorously when a monkey
attended to a stimulus m oving in the receptive field o f
the cell than when it attended to a stimulus outside the
receptive field, even though the two stim uli were identical
(Treue and Maunsell 1 9 9 6 ; C o o k and Maunsell 2 0 0 2 ).
Also, the m ost responsive part o f the receptive field o f
cells in monkev/ M T shitted in the direction o f the stimu-
lus w ithin the receptive field to which the monkey was
attending (W o m elsd o rfet al. 2 0 0 6 ).
The fM R I from V 5 (the center in the human brain co r­
responding to M T ) was m ost active when subjects attended
to a moving stimulus ( O ’Craven c t al. 1 9 9 7 ). Transcranial
m agnetic stim ulation o f human V I produces a stationary
phosphene. Stim ulation o f V5 creates a moving phosphene.
However, the m oving phosphene could n o t be seen when
the corresponding region o f V I was stimulated just after
stim ulation o f V5 (Pascual-Leone and W alsh 2 0 0 1 ). From
the tim ing o f these effects, Silvanto et al. (2 0 0 5 ) concluded
that feedback from V5 to V I influences the con ten ts o f
awareness arising trom activity in V I and V 5.
M any cells in the parietal lobe o f monkeys responded
more vigorously to a stimulus when the animals attended to
it, reached for it, fixated it, or were about to make a saccadic
eye m ovem ent toward it (Lynch et al. 1977; Bushnell et al.
1981; R obinson e ta l. 1 9 7 8 ,1 9 9 5 ). Sim ilar cells exist in the
prelunate and frontal lobes (W urtz et al. 1 9 8 0 ; Fischer and
Boch 1 9 8 1 ). For many o f these cells, the stimulus could be
either a visual or auditory target in a given location (Vaadia
e ta l. 1986).
The posterior parietal cortex and the prefrontal cortex
exhibited transient fM R I activity as human subjects shifted
their attention betw een visual and auditorv/ stimuli
(Shom stein and Yantis 2 0 0 4 ).
The P E T scan has also revealed that attention to a
particular place or a particular o b je ct produces activation
o f the parietal and frontal lobes in humans (Fink et al.
1997). The PF.T scan revealed activation o f the superior
parietal cortex when subjects attended to a peripheral target
whether or not they made an overt response. However, the
frontal cortex was activated only w hen subjects made an
overt response to the attended o b ject (C o rb etta c t al.
1993).
 Patients with damage to the parietal or frontal cortex
show increased reaction tim es when changing attention
from one o b ject to another (Petersen et al. 1989). In extreme
cases, patients totally neglect stim uli in the contralateral
hemifield. This topic is discussed in Section 32.1.1.
5 .9 .2 c L o ca tio n -S p c cific E ffects in the
Ventral Stream
Cells in V 4 o f the rhesus m onkey responded more strongly to
a grating when the animal attended to the grating rather than
to a stimulus outside the cclls receptive field. The tuning
curves o f the cells were not affected by a change in attention
(M cAdam s and Maunsell 1999). For a given ccll, attention
caused a proportional increase in its responses to stimuli in all
orientations. This suggests that attention produces a multi­
plicative scaling o f che response o f a cell (Maunsell and
McAdams 2 0 0 0 ). Cells in V 4 also increased their response to
a stimulus when it was near a second stimulus to which the
animal was attending, and the effect depended on the dis­
tance between the tw o stimuli (C o n n o r et al. 1996).
C ells in areas V 2 and V 4 showed a 3 0 - 4 0 % increase in
firing rate when monkeys attended со a locacion in which
they expected a stimulus to appear, even though there was
no stimulus in that location (Luck ct al. 1997). In human
cortical areas V 1, V 2 , and V 4 , {M R I activity increased when
subjects attended to a stimulus or со the location where a
stimulus was expected (K astner c t al. 1 9 9 9 ). A ttended and
expected stim uli also evoked fM R I activity in the parietal
lobe and frontal eye field. Presumably, the increased activa­
tion со expected stim uli in V I and V 2 was due to inputs
arising in these higher centers.
Electrical stim ulation o f the frontal eye fields in the
monkey at below the strength required to initiate a saccadic
eye m ovem ent enhanced neural activity in a recinotopically
corresponding site in V 4 (M o ore and A rm strong 2 0 0 3 ).
In the human inferior tem poral cortex (lateral occipital
cortex) the fM R I response was stronger when attention
was directed со an objecc placed am ong neighboring objeccs
(Kascner et al. 1 9 9 8 ).
C clls in V 4 have smaller receptive fields than do cclls in
higher centers o f the ventral scream. H o p f ec al. (2 0 0 6 )
hypochesized chac V 4 is involved when atten tion is directed
toward a small o b ject sec am ong small objeccs and rhe lat­
eral occipital cortcx is involved when attention is directed
to a large o b je ct set am ong large objeccs. This hypothesis
was generally confirm ed by chc relative fM R I activation of
the cwo areas.
5 .9 .3 S T IM U L U S -S P E C IF IC E F F E C T S O F
A T T E N T IO N
5 .9 .3 a Stim u lu s-Sp ecific E ffects in the L G N and V I
Accencion-selcccive processes may be relaced со specific
stim uli or со a specific visual feature rather than to a
stim ulus in a defined location that a person is fixating or
reaching for.
Bender and Youakim (2 0 0 1 ) measured responses o f
neurons in che L G N as monkevs
/ viewed a scimulus to which
chey had been trained со attend or an irrelevant scimulus in
che same location. C clls in the L G N showed no evidence
of attcncional m odulation. It was noted in the previous
section that the human fM R I indicates artentional m odu­
lation in the L G N . The difference between these results
could be due to use o f single-cell responses versus global
fM R I responses. It could also be due to the fact that the
fM R I study looked ac locacion-specific accencion whereas
chc single-neuron scudy looked ac scimulus-specific acten-
cion. Tliis is a general problem when using chese two proce­
dures со invescigace chc effects o f atcencion. See Murray
(2 0 0 8 ) for evidence on chis question.
A test spot superimposed on one region o f a reversible
figure-ground display, such as a Rubin s cross, is detected at
a lower lum inance when that region is seen as a figure than
when the same region is seen as ground (Frank 1923;
W citzm an 1963; W ong and Wcisscein 1 9 8 2 ). Neurons in
V I o f the macaque m onkey responded more vigorously to
texture elem ents belonging to a figure than to chc same
elem ents belonging to a ground region (Lam m e 1995).
For many cells in monkey V I , the response со a line
w ithin the receptive field is enhanced by the presence o f an
aligned line outside the receptive field (Kapadia et al. 1995).
This facilitatory effect was enhanced when animals attended
со the carget line and a com parison aligned line that they
had been trained со com pare in brighcness. Acccntion had
no facilitatory effect when animals attended ro a locacion
away trom che carget line. N or did the locus o f attention
affect the response o fcells to an isolated line (Iro and G ilbert
1999). This suggests that signals from higher centers involved
in learning and attention feed back ro V I . These signals
affect stimulus-specific interactions betw een cells in V I
with widely separated receptive fields. These top-down
effects could be used to m atch internal represen cations ot
stimulus configurations against current visual inpucs.
W h en monkeys selected a test bar in a particular orien­
tation from am ong bars in o ther orientations, cclls in V I
and V 2 showed enhanced response to the selected bar
(M o tter 1 9 9 3 ). Enhancem ent did n o t occur when monkeys
attended to a bar with no surrounding bars. Also, in V I o f
the monkey, response со a curved line chat che animal was
cracking was stronger chan that to an intersecting curve that
was n o t being cracked (Roelfscm a ec al. 1998).
It is reasonable to assume that detection o t simple visual
features precedes detection o f chc figure-ground organization
o f a visual scene, which must occur before attention can be
directed to a particular figure. Roeltsem a e t al. (2 0 0 7 )
recorded from cells in V I as monkeys perform ed a task that
required first feature detection, then figure segregation, and
finally selective attention to one o f tw o figures. A lter pre­
sentation o f a brief stimulus, feature-related responses had a
latency o f 4 8 ms, figure-related responses had a latency o f
5 7 ms, and responses related to selective attention had a
latency o f 137 ms. Thus, the different phases o f stimulus
processing were reflected in m odulations o i the responses
o f cells in V I . These results do not prove th at the different
processing phases are performed in V I . The response m od­
ulations with longer latency could depend on feedback
from higher visual centers.
5 .9 .3 b Stim u lu s-Sp ecific Effects in the
D o rsal Stream
C ells in m onkey M T responded more vigorously to a
moving stimulus when, in a discrim ination cask, che animal
selected a stimulus moving in the preferred direction o f that
cell (B ritten cc al. 1 9 9 6 ).
W hen humans attended to the relevant feature in a
dececcion task, they were beccer able to d etect a slight
change in color, m otion, or shape ot a set o t sim ilar objects.
Ac the same tim e, che region o f excrascriace cortex showing
mosc activity in a P E T scan varied according to which fea­
ture was being attended со. Atcencion to shape accivaced che
ventrom edial occipital region, and attention to movement
accivaced area V 5 , a region corresponding со m onkey M T
(C o rb etta et al. 1 991).
Atcencion has a large effect on the response o f cells in
various regions o f the pariecal lobe. The response scrength
o f cclls in the m onkey ventral intraparietal cortex (V IP )
increased the m ore che anim als attended to che scimulus in
a m o tion -d ctcctio n cask (C o o k and Maunsell 2 0 0 2 ). Cells
in che laceral incraparicc.il area (L IP ) showed Jicde response
со a stimulus in their receptive fields unless the stimulus was
behaviorallv salient, either because ic suddenly appeared or
because it was a stimulus to which the animal was about to
make a saccade (G o ttlieb c t al. 1 998).
The fM R I has revealed chac che human right anterior
incerpariecal area (A IP ) and superior parietal cortex are
involved in directing attention to a task-relevant o b ject in a
particular location when other o b jects are shown in differ­
ent locations, but not when the o b jects are shown sequen­
tially in the same location (Shafritz et al. 2 0 0 2 ). See Astafiev
ec al. (2 0 0 3 ) for m ore inform ation on the areas o f the human
parietal and frontal cortex involved in directed attention
and pointing.
C onstancinidis and Steinm ecz (2 0 0 5 ) found chac an
odd-colored square in an array ot nine squares presented tor
5 0 0 ms elicited the scrongesc response in m onkey area 7a
even when the m onkevs i were trained n o t to look at the odd
square. Thus, stimulus oddity is a salient stimulus whether
o r nor rhe animal responds to the odd stimulus. However, it
is n o t clear how much o f the response to the odd stimulus
was due to its sudden appearance. Sakata et al. (1 9 9 4 ) found
the response o f many cclls in area 7a in the parietal lobe
showed periodic changes when che m onkey viewed an
ambiguous rotating trapezoid (Am es window).
5 .9 .3 c Stim u lu s-Sp ecific E ffects in the
Ventral Stream
Attentional gating related to stimulus features has also been
revealed in area V 4 o f the monkey (M oran and D esim one
1985). Bender and Youakim (2 0 0 1 ) found that cells in the
pulvinar, V 2 , V 4 , and area 7a responded more vigorously to
an attended stimulus chan to an irrelevant scimulus.
C ells in V 4 have receptive fields betw een 2 and 4 Uwide
and respond со color and spacial accribuces o f scimuli. Cells
responded more vigorously when the color or lum inance o f
a bar in the receptive field o f t h e ccll m atched the color or
lum inance that the animal had been trained to select in a
discrim ination task. Response enhancem ent was indepen­
dent o f the location o fth e stimulus (M o tter 1994).
An effective scimulus feacure for a given cell is one со
w hich chac cell responds. W hen stim uli with effective and
ineffective features were presented simultaneously within
the receptive field o f a cell in area V 2 or V 4 , the cell
responded only when the monkey attended to the effective
stimulus (L u ck et al. 1 9 9 7 ; Reynolds ec al. 1999). W h en ic
attended to the ineffective stimulus, the response to che
effective scimulus was suppressed. An ineffective scimulus
presented outside the cells receptive field had no power to
in h ibit responses. In further experim ents, two different
effective stimuli were presented in the same receptive field
o f cells in V 2 or V 4. The cells responded m ost strongly to
whichever stimulus the monkey attended to. Thus, a signal
presumably arising from higher in che nervous system deter­
mined which ot two stimuli gained access to cells in V 2 and
V 4. Responses o f cells in V I , V 2, and V 4 were not enhanced
when monkeys attended to a single isolated stimulus.
Ogawa and Komatsu (2 0 0 4 ) arranged six stim uli in a
circle round a fixation point. O n e stimulus had a different
color and one stimulus had a different shape. M onkeys were
trained to make an eye movement to either the uniquely
colored stim ulus or to the uniquely shaped stimulus. Mosc
neurons in V4 showed a significanc increase in response
when the stimulus w ithin the rcccpcivc field contained che
feature to which che animal was responding.
The cffccts o f attention on responses o f cells in V 4 o f che
m onkey ac a given inscanc depend on che probability o f
occurrence o f a critical stimulus at chat instant. G hose and
Maunsell (2 0 0 2 ) trained monkeys to respond to a change in
the orientation o f a patch o f bars ac one o f tour locations.
The change occurred ac random cimes after the stimulus
appeared. The spike frequency o f cells in V 4 over time
reflected the changing probability that the stimulus change
would occur. Thus, attentional m odulation ot neural activ­
ity reflected che anim als anticipaced tim e o f occurrence o f
chc critical event.
A process o f attentional gating has also been revealed in
the interior temporal cortex o f the monkey. M any cclls in
chis area have recepcive fields covering chc whole recina.
Som e cells responded more vigorously when a feature ot the
stimulus, such as color, was one to which the animal had to
attend to in order to solve a discrim ination task (Fustcr and
Jervev 1 9 8 1 ). The response to an effective stimulus was
inhibited when the anim al attended to any ineffective stiin-
ulus. Also, cells in the tem poral cortex were activated when
monkeys found an o b ject they w ere looking for within a
com plcx natural scene. The activation occurred shortly
before the m onkeys moved their eyes to fixate the found
o b je ct (Shcinbcrg and Logothctis 2 0 0 1 ).
The fusiform area in the ventral occipitotem poral cortex
contains cells that arc specifically activated by faces. The
human fM Rl revealed activation in the fusiform area when
subjects imagined a face, although n o t to the same extent as
when they viewed a real face. Andrews et al. (2 0 0 2 ) found
that the fusiform area was activated, as revealed by the
fM R I, when people reported seeing the face interpretation
o f R u bins vase but not when they reported seeing the vase
interpretation.
The parahippocampal area was activated when subjects
imagined a fam iliar place (O 'C raven and Kanwisher 2 0 0 0 ).
This area is known to be associated with recognition ot
places. In change blindness, people are not aware o f changes
to unattended objects in a com plex scene when the scene is
momentarily interrupted.
Beck et al. (2 0 0 1 ) had subjects fixate a central stimulus
while an array o f faces or an outdoor scene was momentarily
J 4
interrupted. D uring the interruption, one o f the faces or
part o f the scene changed. The fusiform face area showed
fM R I activation only when subjects noticed the face
change. Similarly, the parahippocampal area was activated
only when the place change was noticed. 'Ih c parietal lobes
and prctrontal cortex were activated when either the face
change or rhe place change was noticed.
C clls in the hippocam pus and related areas o f the
m onkey respond selectively to com plex o bjects, such as
faces or fam iliar places. Kreim an et al. (2 0 0 0 ) recorded
from single cells in the hippocampus region o f alert human
patients undergoing surgery for epilepsy. The patients
were given the task o f discrim inating betw een pairs o f
objects, such as faces, buildings, and animals. O t 4 2 7 neu­
rons tested, 14% responded selectively to the category
to which the shapes belonged. The cells also responded
selectively when the patients imagined different categories
o f objects.
5.9 .3d G eneralized Feature-Based A tten tio n
The experiments m entioned so far in this section showed
that responses o f cells in various visual areas are influenced by
both the location and feature o f t h e attended object. Thus,
attention to a particular stimulus feature in a given location
enhances the response o f cells that serve that feature in that
location. But a true feature-based attcntional mechanism
that is independent o f spatial attention enhances the response
ot particular feature detectors wherever the stimulus is in
visual field. The following experiments demonstrate feature-
based attention that generalizes over the visual field.
The response o f a ccll in M T to a stimulus moving in a
given direction was modulated according to the direction
o f m otion o f a rem ote stim ulus to w hich the monkeys were
attending (Treue and Trujillo 1999). But this modulation
did not occur when the monkeys did not attend to the
rem ote stimulus.
M cAdam s and M aunsell (2 0 0 0 ) recorded from cells in
V 4 o f monkeys. The response o f a cell to the orientation o f
a G abor patch in its receptive field was enhanced when the
animals attended to the orientation o t a rem ote stimulus,
but not when they attended to the color o f the rem ote
(la b o r patch. Thus, attention to a specific feature enhanced
responses to that feature over the visual field.
Saenz et al. (2 0 0 2 ) asked human subjects to attend to
dots m oving in one direction in a 5" display containing dots
moving upward interspersed with dots moving downward.
The display was several degrees to one side ot a fixation
point. A display o f dots moving in only one direction was
displayed several degrees to the other side ot the fixation
point. The fM R I responses in V I , V 2, V 3 , and V 5 to the
single display were enhanced when the attended dots in the
mixed display were moving in the same direction as those in
the single display.
These experim ents dem onstrate that attention to a
particular stimulus feature can enhance responses o t cells
sensitive to the same feature, which is distributed over a
large area.
 6
D E V E L O P M E N T OF T H E VI SUAL SYSTEM

6.1 The evolution o f eves 30$

0
6.4.6 Development of cortical connections $45
6.1.1 Introduction >0.? 6.4.7 Ccll differentiation $48
6.1.2 Simple cycspo t s $04 6.5 Mechanisms o f neural plasticity $49
6.1.3 Lens eves 305 6.5.1 The Hebhian synapse $S0
6.1.4 Compound eyes $07 6.5.2 Spike timing-dependent plasticity 353
6.2 Experimental methods $ o s 6.5.3 Presynaptic processes in I.TP and LTD 35-#
6.3 Development o f the eye and visual pathways $09 6.5.4 Synaptic scaling 355
6.3.1 Development o f the eye $09 6.5.5 Compartmentalized dcndritic plasticity 355
6.3.2 Development o f the retina .Ш 6.6 Neural activity and cortical development 356
6.3.3 Growth of the optic nerve and tract $13 6.6.1 Neural activity and gene expression 356
6.3.4 Segregation o f axons at the chiasm 3/5 6.6.2 Spontaneous neural activity $58
6.3.5 Development of the LGN $18 6.6.3 Hcbbian synapses and visual development $58
6.4 Development o f the brain $21 6/i.4 1)eveIopment o f feature detectors $59
6.4.1 General development of the nervous system $2! 6.7 Development o f cortical columns $60
6.4.2 Growth o f cortical areas $ 2$ 6.7.1 Column segregation $60
6.4.3 Mechanisms o f axon guidance $26 6.7.2 Mechanisms of column development $62
6.4.4 Syn.iptogenesis $$$ 6.7.3 Induction o f ocular dominance columns $66
6.4.5 Formation of cortical layers $$9

6 .1 T H E E V O L U T IO N OF EYES C reationists assert that only a tully formed complex eye is

6 .1 .1 IN T R O D U C T IO N
The vertebrate eye is the m ost com plex m echanism that we
know. In his book On the Origin o f Species (1 8 5 9 ) Darwin
w rote:
“To suppose that the eye, wich all its inim itable co n ­
trivances . . . could have form ed bv natural selection,
4
seems, I freely confess, absurd in the highest degree.
Yec reason tells me, that if numerous gradations
from a perfect and com plex eye to one very im per­
fe ct and simple, each grade being useful to its pos­
sessor, can be shown со cxisc; it further, the eye does
vary ever so slightly, and the variations be inherited,
which is certainly the case; and i f any variation or
m odification in the organ be ever useful to an animal
under changing conditions o f life, then the difficulty
o t believing that a perfect and com plex eye could be
form ed by natural selection, though insuperable by
our im agination, can hardly be considered real.”
(p. 186)
any
0
use to an anim al. 'Ihe eve
•
is said to have irreducible
complexity. They conclude from this chac an eye could arise
only by intelligent design by a supernatural being. Hut both
the assertion and chc conclusion arc false. A simple light-
sensitive spot provides the basis for phototaxis and detec­
tion of the day-night cycle. Even plants orient their leaves to
the light. The com petitive advantages that animals gained
by each improvement o f light-detcction organs provided
strong pressure for their evolution from simple eyespots to
com plex camera-like eyes.
ЛИ eyes require a light-sensitive photopigm ent. In most
eyes it consists o f the protein opsin w ith an attached chro-
m ophore (Section 5.1 .2 b ). The photopigm ent is embedded
in a photorccepcor cell. There are cwo basic types o f p h o to ­
receptors, rh a b d o m cric and ciliary . Rhabdom eric recep­
tors are prevalent in annelids, molluscs, and arthropods.
They have apical microvilli and the phocopigm ent contains
r-opsin. Lighc evokes a depolarizing response. C iliary recep­
tors occur in che eyes o f higher vcrcebraces. They have an
apical cilium that forms a folded m em brane containing
phocopigmcnc. The phocopigmcnc concains с -opsin, and
light evokes a hyperpolarizing response. M any worms,
molluscs, and arthropods possess both types o f receptor.
Also, som e ganglion cells in many vertebrates contain
r-opsin (A rendt 2 0 0 3 ). This suggests that the photorecep­
tor m echanism s o f all anim als evolved from a com m on
ancestor, w hich contained both types o f receptor m echa­
nism (N ilsson and A rendt 2 0 0 8 ).
It is not possible to gain much inform ation about the
evolution o f eyes from fossils. However, the wide range o f
types o f eyes in living animals indicates how eyes may have
evolved. O n ly a general account is presented here. See Land
and Nilsson (2 0 0 2 ) lor a fuller account.
6 .1 .2 S IM P L E E Y E S P O T S
Eugltnu gracilis is a single-celled protozoan that both per­
forms photosynthesis like a plant and captures prey like an
animal. It has a single eyespot near its large flagellum. The
eyespot consists o f a paraflagellar body attached to the base
o f the large flagellum and a neighboring cluster o f red lipid­
like droplets, as shown in Figure 6.1. There has been some
uncertainty about the nature and location o f photopig­
ment. Jam es et al. (1 9 9 2 ) revealed that the absorption spec­
trum resembles that o f rhodopsin and that the pigm ent
m ost likely resides in the paraflagellar body. The eyespot
presumably controls the m otion o f the flagellum so as to
d irect the Euglena to light when it is photosynthesizingor
to food objects.
An eyespot must have light-absorbing pigments on at
least one side if it is ro register the direction o flig h t. W ith
no pigments, the receptor could register only the general
light level because it would respond in the same way for all
Large flagellum
P igm ented
<
droplets
P hotosensitive
p araflagellar body
R eservoir
C on tractile
vacuole
S m all flagellum
C hloroplast
N ucleus
V ario us cell
granules
1 mm
Fijorc 6 . 1. D iagram o f th e p rotozoan Euglena. Euglena has a sim ple eyespot
co n sistin g o f a p h otosen sitiv e body and p igm ented drop lets.
directions o fth e light. Pigm ent on ju st one side o f the recep­
to r provides at least some directional inform ation.
Echinoderm s (starfish, sea urchins, and sea cucum bers)
show visually mediated behavior including seeking shelter
in crevices from predators, daily m igrations, and color
changes. Som e sea cucum bers and starfish have ocelli on the
tips o f their tentacles (Yoshida et al. 1 9 8 3 ). However, in
m ost echinoderm s, photodetectors are distributed over the
transparent calcite endoskeleton.
The calcite plates covering the arms o f som e brittlestars
form into spherical structures 4 0 - 5 0 mm in diameter.
Aizenberg c t al. (2 0 0 1 ) produced evidence that these
structures serve as lenses that focus light on the underlying
photoreceptors. The surface o f the animal forms a
com pound eye.
Blevins and Johnsen (2 0 0 4 ) produced evidence that the
sea urchin (Strongylocentrotuspurpuratui) detects the direc­
tion o flig h t by using its spines to screen off-axis light from
photoreceptors distributed over the body surface. Sea
urchins responded to an o b ject subtending 10° but not to
one subtending 6.5° ( Yerram illi and Johnsen 2 0 1 0 ).
Som e flat worms (Platyhelm inthes) possess eyespots.
For example, the larva o f the parasitic trem atode [Multicotyle
purvisi) has two eyespots on the anterior margin o f the
dorsal side o f the body. Each eyespot contains two rhabdo-
meric receptor cclls that point in opposite directions, with
an associated pigmented cell. This arrangement presumably
improves the animal’s ability to d etect the direction o flig h t.
Each receptor is connected by a dendrite to a sensory cell
outside the eyespot, as shown in Figure 6 .2 (R oh d e and
Watson 1991).
Larval segmented worms (annelids) possess simple eyc-
spots. For example, larvae o f the polychaete ( CapitcH
species) possess a pair o f eyespots, each with one rhabdo-
m eric sensory ccll and o n e pigm ent cell, as shown in Figure
6 .3 (R hode 1 9 9 3 ). W rapping o f the pigm ent cell round the
receptor ensures that light com ing from one direction is
m ost effective. As they mature, the larval eyes are replaced
with eyes containing tw o or three sensory cells. These eyes
presumably have increased directional selectivity.
M ore com plex eyespots contain several photoreceptors
lining the inside o f an open eyecup. A layer ot pigm ent cells
behind the receptors ensures that only light com ing through
the aperture o f t h e cup stim ulates the receptors. Also, the
receptors facing in the direction o f a light source, such as
the sun, will be stim ulated m ost. Such eyes typically contain
up to 100 receptors and arc under 100 mm in diameter.
They have evolved independently many times (Salvini-
Plawen and Mayr 1 9 7 7 ). Som e o f them arc cverse eyes,
in which the receptors are on the aperture side o f the
nerves. O th ers arc inverse eyes, in w hich, as in vertebrate
eyes, the nerve fibers intrude between the aperture and
the receptors.
An eye w ith a very small aperture would be a pinhole
eye, analogous to the pinhole camera. Som e molluscs, such
 R habdom eres

M icrofibrils

N ucleus

Dendrite

P igm ent cell

H o riz o n ta l s e c tio n
l'i$m 6.-*. V ie eye o fN a u tilw . N autilus has tw o m ob ile lateral eyes ab ou t
R eceptor cell
1 cm in d iam eter. Л small ap ertu re fo rm s cru d c im ages o f
Dendrite M uscle fibers b iolu m in escen t o b je c ts on the retina. T h e eye has n o c o m c a or lens but
operates m ore like a p in h ole cam era. (I • wv . n g м e >

as che abalone ( H aliotis ) and the cephalopod Nautilus pos­

sess pinhole eyes.
N ucleus
Nautilus pam pilius is a living fossil that has remained
unchanged since the Jurassic, 4 0 0 m illion years ago. It has
R habdom eres tw o lateral eves
4
about 1 cm in diam eter with no corneas or
lenses (Figure 6 .4 ). The receptors line a cavity with a vari­
able aperture. Statocyst organs register body rotations and
m ediate com pensatory rotations ol the eyes so as to stabi­
lize the images (H artlin c c t al. 1979).
As in a pinhole cam era, the image ot the Nautilus eye
t.Ru.cfei. liye o t tre im to d c flat w orm (M ulticotyle purvisi). (R ed .— .. f a sharpens as the aperture is decreased. But a small aperture
R o h t lc jn J W a n c n И 9 1 }
lets in little light. The aperture o f the eye decreases from
about 2.8 mm to 0.4 mm as light intensity increases.
However its grating resolution is, at best, only about 11°
(M untz and Raj 1984). Nautilus forages at night at a depth
o f about 100 m. At this depth the only clearly visible objects
D ir e c tio n
o f lig h t arc spots o f biolum inesccncc em itted by small animals
and areas o f decaying m atter on which Nautilus feeds.
Its pinhole eye will form discinct images o f these spots.
These images, tactile and olfactory senses, and a lateral-line
system must be adequate for the environm ent in which
N u c le u s Nautilus lives.

6 .1 .3 L E N S F.YES
S u p p o r tin g
The full power o f vision depends on chc evolution o f eyes
capable ot torm ing an image. Such an eye requires either a
lens, a concave mirror, or a spherical array o f light guides,
each with a narrow acceptance angle. These types o fev e will
be bricflvj described.
S e n so ry
m ic r o v illi Lens eyes evolved, independently, in coelcnteratcs,
annelids, som e gastropods (snails and slugs), ccphalopods
1 цт
(squid, cuttlefish, and octopuses), arthropods, and fish.
S in g le Even a very simple lens is bccccr chan no lens since ic
p ig m e n t cell
improves resolution w ithout having to reduce the size o f
P ig m e n t
chc apercurc (pupil).
g r a n u le

Simply increasing the refractive index o f t h e fluid in a

b Rurc<>.v liycvpoc o fla r v a o t p olych actc, C ap itclla. fAJ^tcdfromRitodr 1993) simple cvccup improves resolution. Such eyes occur in som e
gastropods and molluscs but they do noc form a sharp
image (Land 1981).
Л lens is gready improved i f its rcfraccive index increases
coward its center. This reduces che focal length and increases
the effective apercure. Macchiessen (1 8 8 2 ) discovered chac
fish lenses have a refraccive-index gradienc. The focal lengch
o f such eyes is abouc 2.5 cimcs cheir radius. This is known as
che M atthiessen racio. We now know that the lenses o f all
vertebrace eyes have a refraccive-index gradient.
The full value o f a lens is achieved when the divergent
beam o t light trom each point o f an o b ject is converged
onto one point in the receptor surface. Unless che refractive
power o t the lens can be changed, only objects at a specific
distance are in focus. Hut even w ithou t accom m odation, a
lens provides considerable improvement.
Hox jellyfish (phylum C nidaria) are the m ost primitive
animals known to possess lens eyes. They have tour sets ot
eyes arranged around the mantle. Each set is on a structure
known as a rh op aliu m , which is about 0.7 mm long. Each
rhopalium has six eyes; an upper lens eye, a lower lens eye,
two pit eyes, and cwo slic eyes. Figure 6.5 depicts the lens
eyes o f Tripedalia cystophora, a small box jellyfish living in
C aribbean mangrove lagoons. Each lens eye has a cornea, a
lens, a pigm ent layer, and a retina. The lenses o f chc lower
eyes have a gradient o f refraction and produce a sharp image.
Hut che image is focused well beyond the retina, so that the
eyes can detect only large objects. The receptors o f che lower
eves have receptive fields with a half-width o t about 20°
(N ilsson et al. 2 0 0 5 ). The lower eyes and che slic eyes look
downward. The lenses o t che upper eyes produce a less sharp
Balloon cell
Neural
layers
G astric
cavity
S ta to c y s t
100 jim
Figure 6.5- A n e v e o f th e je lly fis h (T r ip e d a lia c y s to p h o r a ). ( R c J r ^ n and
from N ib*on cl jI. 2005)
image. They and chc pit eyes look upward through chc
refractive widow o f the wacer surface. The four rhopalia are
co n nectcd to a single nerve running round chc bell-shaped
mantle.
Hox jellyfish show positive phototaxis. C o ntractio n s o f
the mancle are controlled by the intensicy o flig h c falling on
chc lower lens eyes so as to keep the jellyfish in wcll-illumi-
natcd regions in the mangrove lagoon where their prev
(copcpods) aggregate (Ciarm and Bielecki 2 0 0 8 ). Box jelly­
fish also show visually guided obstacle avoidance. An object
in the water, such as the rooc ot a mangrove cree, subcending
a visual angle o f more than 12° triggered an avoidance
response (G arm et al. 2 0 0 7 ). B o th chcse responses are con-
crollcd by lighc falling on che lower lens eyes. The behavioral
significance o t che ocher eyes is noc yec known (G arm and
M ori 2 0 0 9 ).
In annelid worms, lens eyes have been found onlv in
polychaeces. For example, Vanadis tagensis is several cenci-
mecers long and swims in che ocean. It has cwo eyes, each
wich a cornea, pupil, lens, recina, and excrinsic muscles. The
lens is spherical buc its optical properties and whether it can
accom m odate are n o t known. The retinal detectors point
toward the pupil (everse) and are backed by a pigm ent layer.
A group o f light-sensitive cells, known as chc secondary
retina, occurs on one side o t che pupil (H erm ans and Eakin
1974).
Vanadis, like som e ocher polychaeces, lives in che ocean
ac a considerable depch, where long wavclcngchs bccom e
progressively accenuaced. W ald and Rayporc (1 9 7 7 )
suggcsccd chac chc main and secondary rccinas have differ­
ent spectral sensitivities. Com parison o f che cwo speccral
regions could allow che worm со dececc its depth in che
ocean.
C ornea
The eyes o t polychacte larvae consist ot only one pig­
Upper m ent cell and one or, occasionally, tw o sensory cells. The
lens eye
larval eyes may persist after the adult eyes have form ed and
are often referred со as anterior eyes (Suschhenko and
Purschke 2 0 0 9 ).
P igm ent
M ost molluscs have simple eyecups. Som e gastropod
layers
molluscs have lens eyes. For example, the eye o t the snail
H elix has a lens consisting o f a simple sphere o f jelly with a
refractive index higher than that of the surroundings.
Tli с periwinkle snail {L it tor in a irrorata ) inhabits che
Low er upper intertidal zone and is active when the tide is out. It
lens eye
has cwo eyes, each at the base o f one o f its tentacles. Each
eye has diam eter ot about 2 5 0 mm and contains a cornea,
pupil, and a spherical lens in which the refraccivc index
increases coward the core. The lens produces a sharp image
on the cvcrsc retina. Ic docs noc seem to have an accom m o­
C iliary la ye r o f retina
dative m echanism . The mean spacing o f the photodetectors
is about 1.7°. Behavioral data indicated that chc animals
could detect a vertical stripe 0.9" in diam eter (H am ilton
et al. 1983).
C ephalopod molluscs (squid, cucdefish, and octopuses)
have the m ost elaborate eves of all invertebraces. Their eyes
have all che features o f an advanced vertebrate eye, includ­
ing a cornea, pupil, lens, and retina. They have ciliary mus­
cles for focusing the lens and extraocular muscles. However,
there are some significant differences between cephalopod
eyes and vertebrate eyes. C ephalopod photoreceptors arc
rhabdom eric, while vertebrate photoreceptors are ciliary.
Cephalopod retinas are everse with only one neural layer.
Vertebrate retinas are reverse and have several neural layers.
These differences indicate that the eyes o f these two groups
evolved independently. They provide a remarkable example
o f convergent evolution.
Telescopes may use lenses or concave mirrors. M ost
anim al eyes use a lens, but the eyes o t scallops use a concave
m irror (Land 1 965). Scallops (Pecten) are bivalve molluscs
with up to 100 eyes, each about 1 mm in diameter, arranged
betw een small tentacles round the gap between the shells.
Each eye has a lens with hom ogeneous retractive index,
which abuts the retina. The image is therefore formed well
behind the retina. The eye’s spherical rear surface is lined
with a reflecting tapetum to form a concave mirror. The
m irror reflects light com ing through the lens to torm an
image on the spherical retina where it abuts the lens, as
shown in Figure 6.6.
N ot much is known about the evolution o f vertebrate
eyes. Jawless chordates, such as the hagfish, evolved about
5 5 0 m illion years ago. They have bilateral eyes with no lens,
iris, or extraocular muscles. In the two-layered retina.
Im age form ed by the lens
Figure 6.6. Diagram o f th e scallop eye. T h e le n s f o r m s a n im a g e w e ll b e y o n d
th e r e t in a . T h e l ig h t is r e fle c t e d fr o m t h e c o n c a v e ta p e tu m t o fo r m a
s e c o n d im a g e o n th e c o n c a v e r e tin a . (H m .c J fw n .llf u r o u LaoJ 196S)
photoreceptors co n n ect directly with ganglion cclls that
project to the hypothalamus. These eyes resemble the pineal
eye o f nonmammalian vertebrates.
Early vertebrates, such as lampreys, evolved about 5 0 0
m illion years ago. The eyes o f larval lampreys resemble those
o f t h e hagfish. Lampreys take several years to reach m eta­
morphosis. During this tim e the eyes develop a lens, cornea,
extraocular muscles, and a multilayered retina like that o f
higher vertebrates. C o ntin u ity in em bryological develop­
ment o f these eyes suggests that there was a similar
continuous evolution o f the eyes (Lam b et al. 2 0 0 7 ).
6 .1 .4 C O M P O U N D EYES
C om pound eyes probably evolved trom a collection ot eye­
spots in the C am brian, about 5 4 0 m illion years ago.
C om pound eyes from that tim e can be seen in fossil
Trilobitcs (see Section 3 3 .2 .1 ). A part from a few bivalve
molluscs and an annelid, com pound eyes are confined to
the arthropods, although not all arthropods have co m ­
pound eyes. Sigm und Exner (1 8 9 1 ) provided the first
detailed account o f com pound eyes. There are tw o basic
types of com pound eyes— apposition eyes, which occur
mainly in diurnal insects, and superposition eyes, which
occur in nocturnal insects and deep-water crustaceans.
Figure 6 .7 illustrates the basic structure o f an apposi­
tion eye. It consists o f many om m atidia. Eachom m atidium
has a cornea, a crystalline cone, and eight receptor cells
(rhabdom eres) that together form a radial structure known
as the rhabdom . The hexagon-shaped corneas form the
outer spherical surface o f che eye. The rhabdom acts as a
light guide in which all the light entering the cornea ot
chat ommacidium com bines to produce one sensory signal.
C rystalline
cone
Cornea
’ igm ent
cell
Rhabdom
R eceptor cell, consisting of 8
o r rhabdom ere rhabdom eres
m em brane
R eceptor
axons
Нд«гс 6.7. D ia g r a m o f s c c t i o n o f a n a p p o s it io n c o m p o u n d e y e.
Each om irucidium poincs со a slighdy differenc pare o f che
visual field so thac together they produce a mosaic image ol
the environm enc (H orridge 1980).
The field o f view (acceptance angle) o f an om m atidium
is chc angle chac ics cip subcends ac che nodal poinc o f che
corneal lens. This angle is typically at least Г . The angular
spacing of om m atidia is abouc che same. If om m atidia were
spaced more widely there would be m ultiple blind spots. If
they were spaced m ore closely, the receptive fields o f the
ommacidia would overlap unnecessarily. Consequently,
apposition com pound eyes have poor resolution. However,
they have a large field o f view and arc highly sensitive со
movement. Som e com pound eyes d etect che polarizacion o l
lighc. Som e inseccs, such as bees, flies, and che preying
mancis, have a specialized zone ot ommacidia with higher
resolucion. In this zone che eye is flattened and che facets are
larger. The flacccning allows m ore om m atidia to receive
light from a spoc, w hich gives higher resolucion.
In su p erp o sitio n co m p ou n d eyes the receptors torm a
single surface (recina) lying abouc halfway betw een chc sur­
face o f che eye and ics center o t curvacurc. The recina is sepa-
raced from che optical com ponents o f che eye by a clear
zone. Lighc rays entering neighboring om m atidia from a
single point in space are refracted, o r in some cases reflected,
to torm a single image point on the retina, as illustrated in
Figure 6.8. The overall image is erect. As many as 3 0 neigh­
boring om m atidia may concentrate light upon a single
receptor. Therefore, superposition eyes have better resolu­
tion and are m uch m ore sensitive chan apposition eyes.
For a fuller trcacmcnc o f the evolucion o f eyes see Walls
(1 9 6 3 ) and Land and Nilsson (2 0 0 2 ).
Depch-deteccion m echanism s in anim als wich com ­
pound eyes are discussed in S ection s 33.1 and 3 3 .2 . The
evolution o f frontal vision and stereoscopic vision is
discussed in Section 3 3.8.
C e n te r o f eye
+
Fi*vrc6.a. D ia g r a m o f a s u p e r p o s itio n c o m p o u n d e y e .
6 .2 E X P E R IM E N T A L M E T H O D S
The study o f che developm ent o f che visual syscem involves
a variety o f anatom ical and physiological procedures, some
o f which can be applied in the living animal (in vivo), while
others are applied in cultures o f living cells taken from the
brain (in vitro).
In the tran sp lan tatio n p roced u re, cells or whole organs
are transferred from one location (the donor region) to
another location (chc hose region) in the em bryo. This may
be the em bryo ot the same anim al or an em bryo o f a
differenc animal (D u n n ect and Bjorklund 1 9 9 2 ).
These procedures were pioneered by Roger Sperry
( 1 9 5 1 ), who won che Nobel Prize in 1981. They reveal
whecher chem ical agents responsible tor the growth o t par­
ticular cissucs are specific со che cissue or со che cellular
environm enc in which the tissue grows.
In the reroucing p roced u re, sensory neurons are caused
to innervate a region in the nervous system that they do not
norm ally innervate. For example, chis procedure has
revealed chac visual inputs rerouted to the auditory cortex
o f ferrets induced cells in the auditory cortex to develop
receptive fields like those o f cells in the visual cortex
(Section 6.4 .2 c).
Transplantation and rerouting procedures arc particu­
larly applicable in lower vertebrates, such as fish and
am phibians, which possess remarkable powers o f regenera­
tion. For example, Sperry (1 9 4 3 ) severed the optic nerves o f
tadpoles and allowed them to regenerate with rhe eyes
rocaced 180". Visually guided responses со flies were pcrma-
nendy reversed. Sperry concluded chac opcic nerves possess
a chem ical marker indicacing cheir origin in che retina.
The h e te ro ch ro n ic p ro ced u re involves transplanting
im m ature cells at one stage o t em bryonic development into
a culcure o f cells derived from anocher stage o f develop­
m ent. This procedure reveals the factors that determ ine the
cype o f cell an immacurc cell will form.
In che cell cracing p ro ced u re the fate ot m igrating neu­
rons is followed by labeling them wich a chem ical marker,
such as critiated thym idine. In neurogenesis, a given cell
divides repeatedly to form a cell lineage. The cclls derived
trom a particular progenitor ccll can be traced by infecting
progenitor cells with a retrovirus that expresses a green fluo­
rescent protein. The virus transfers trom a progenitor cell to
its offspring bu t not to other cells. Grow ing cells containing
the fluorescent protein can be viewed directly and co n tin u ­
ously by time-lapse videomicroscopy (O kad a et al. 1999).
Recently, there has been an increase in the use ot geneti­
cally manipulated animals to scudy chc developmenc o f che
nervous system. In the tran sg en ic p ro ced u re a foreign gene
is introduced inco chc zygote o f an anim al, usually a mouse.
Since the gene is passed on ro che offspring, many m ice with
chc same generic m odification can be produced. The goal is
со introduce a gene th at affects che expression o f a particu­
lar procein in a defined cvpe o f neuron.
 The transgenic procedure reveals che roles o f particular
proteins in developmenc and o f m echanism s chac govern
the expression o f proteins. The procedure is lim ited by avail­
ability o f recom bination agents chac affect expression o f
particular genes.
In che g en e k n o ck o u t p ro ced u re a gene product is
removed or a gene is introduced chat expresses a toxin chac
inhibits production o f specific proteins. This procedure
may prevent specific cells trom developing. For example,
retinas o f a transgenic mouse containing a toxin-producing
gene linked to the red opsin gene were devoid o f cones.
Anim als with an inactivated gene may develop com pensa­
tory m echanism s thac mask the normal effects ot che gene.
Also, cransgenecic knockout animals may die before che
effeccs ot transgenic procedures can be investigated
(G oldow iz et al. 1 992). It is not practical or desirable to
apply these procedures to primates.
In the tran sfeccio n procedure, D N A is introduced into
a virus, such as che herpes virus, chac has been rendered non-
coxic. The virus, which is known .us a v ecto r, is introduced
inco a sclecccd region o t che nervous syscem or inco cell cul-
cures, where it is taken up by cell nuclei. The ideal vector
infects only cells o f a specified type that can express the
D N A carried by the vector. The D N A expresses a marker
agent, which is usually a fluorescent protein, as described in
Scction 5.4.2a. This procedure can be used in prim ates to
reveal w hich genes are involved in regulating cell grow th. Ic
can also reveal genes chac alter chcir expression in response
to neural activity.
Marked viruses thac pass across synapses allow one со
trace neural con nection s (Callaway 2 0 0 5 ).
Optic vesicle
Growth of lateral portions
Side views w ith ectoderm removed
Ectoderm
Optic stalk
8 v 9
"5
Sections corresponding to the side views
(■■Ku>c6.9. D ev elo p m en t o f th e hum an eye.
A natural m utation may also knock our a particular
gene. The study o f defects, such as albinism , can reveal
mechanisms underlying development.
These anatom ical, genetic, physiological, and behavioral
procedures have accclcratcd the growth o f knowledge abouc
che developmenc and diseases o f che nervous syscem.
6 .3 D H V F . L O P M E N T O F T H F , E Y E A N I)
V IS U A L P A T H W A Y S
6 .3 .1 D E V E L O P M E N T O F T H E EYE
6 .3 .1 a G e n e ra l D e v e lo p m e n t
The retina develops from chc o p tic v csiclc, an oucgrowch o f
the forebrain, as shown in Figure 6.9. After m aking concacc
wich chc overlying cccodcrm , chc vcsiclc invaginaccs со form
che opcic cu p, which is actached to the brain by the o p tic
stalk . The lining o t the opcic cup forms chc recina, and the
oucer surface o f che cup form s the pigm ent epithelium . The
overlying ectoderm is induced to form the lens and cornea.
The ventral surface o f both cup and stalk invaginate to form
chc o p tic fissure. The sides o t the fissure fuse, and axons
from the retina begin to enter the optic stalk, which becom es
chc opcic nerve.
The volume o f chc eye o f chc adulc human is abouc chrcc
times that o f the eye o f che neonate. The eye grows propor-
cionacclv less chan chc bodv as a whole, which increases in
volume abouc 20-fold. The corneal surface increases about
50% , while chc area o f chc recina approximaccly doubles
Optic cup
Indentation
Fissure of the
optic cup
Retina
Pigment epithelium
Optic stalk
a
\
Groove Groove
Lens vesicle
io6)
from 5 9 0 m n r со 125 0 m n r (Scam m on and W ilm er 1950).
The axial length o f the eye increases from about 15.5 mm at
birth to its adult value o f 2 4 .5 mm, w hich is reached ac
about the age o f 13 years. A bout h a lf the increase occurs in
the first 2 years (Larsen 1971). This means chac an infancs
eye requires about 8 5 diopters o f refraction to focus an
image, com pared with about 6 0 diopters for an adult eye
( I .otmar 1976). Also, the small size o f an infancs eye means
that Г o f visual angle corresponds to betw een 0 .1 8 and
0.2 mm on the rccina, com pared wich 0 .2 9 mm on che
adult retina (H am er and Schneck 1 9 8 4 ). Thus, for a given
stimulus, rhe recinal image in rhe infanceye is considerably
smaller chan that in the adult eye.
The lens o f chc human eye has adiam ecer o f abouc 9 mm
and a thickness o f about 4 mm. It is composed almost
entirely o f protein m olecules in long fiber-like cells arranged
in tightly packed and interlocking concentric layers, like the
layers o f an onion. See Section 9 .2 .2 for more details abouc
the lens. The inner layers develop first to form the lens
nucleus. As the lens grows, the outer epithelium adds new
layers to form the lens cortex and then the outer lens cap­
sule. D uring the first 5 postnatal years the equatorial diam ­
eter o f the lens increases about 2 mm. After that, the lens
grows throughout life ac a rate o f about 2 0 nm per year
(O yster 1999, p. 5 0 4 ).
The developm ent o f the visual fields is discussed in
Section 7 .2 .4 .
6 .3 .1 b G e n e tic C o n t r o l o f Eye D e v e lo p m e n t
It has been escimared char ac lease 2 ,0 0 0 genes arc involved
in the grow th o f an eye. They form a com plex hierarchical
conrrol netw ork. C ertain hom eocic genes express transcrip­
tion factors that initiate the genetic expression ot proteins
responsible for the developm ent o f the eye. For example,
the gene eyeless initiates eye form ation in the fruit fly. Eyes
do not develop when the gene is absent (Q u m n g c t al.
1994). W h en the gene was turned on in a leg, wing, or
antenna, a com pound eye developed in that location
(H aider et al. 1 9 9 5 ). However, in som e parts o f the
flvs body the eyeless gene has other functions. O th er genes,
such as dachshund, also initiate eye developm ent in the
fruit fly.
A gene sim ilar to the eyeless gene occurs in many other
phyla, including cephalopods (squid and octopu s), fish,
birds, and mammals. In m ice, the gene is known as Pax-6.
This gene is active throughout m orphogenesis. It isexpressed
first in the optic sulcus and then in the eye vesicle, lens,
retina, and cornea. It is remarkable that the Pax-6 gene from
a mouse im planted in to the leg o f a fly produces a com ­
pound eye (H aider et al. 1 9 9 5 ). In humans, the gene is
know n as /in iridia (O liver and Gruss 1997).
C o n n exin genes encode the proteins thac link gap junc­
tions betw een cells. Signals passed over gap ju n ction s coor­
dinate developm ent in com plex structures. For example,
knockout o f the gene Cx50 expressed by the lens results in
reduced growth o fth e lens and eye (W h ite 2 0 0 2 ).
The com m unality o f gene expression through many
phyla has led som e evolutionary biologists to propose that
all eyes had a com m on ancestor and evolved only once. But
the eyeless gene also occurs in animals that lack eyes and has
other functions even in animals thac possess eyes. If che dis­
tinct types o f eyes in different phyla evolved independently,
as seems likely from o ther evidence, the preexisting eyeless
gene was probably recruited in each case because o f its
general ability to initiate activity in a com plex netw ork o f
genes, nor only that responsible for eye development
(Travis 1997).
6 .3 .1 c E m m etrop ization
In many vertebrates, including primates, the eyes o f n e o ­
nates are too short in relation to their optics. As a result, che
eyes of human neonates are hypermetropic when the
intraocular muscles are paralyzed with acycloplegic drug so
that the lens is focused at infinity. This m eans that the image
o f a distant o b ject lies beyond the retina. W hen the muscles
are not paralyzed, the eyes o f human neonates tend to be
myopic (H ow land 1 9 9 3 ). The normal adult eye is em m e­
tropic, so that the image o f a distant o b ject is focused on the
retina w ithout accom m odative effort.
The developm ent o f emmetropia with age is know n as
em m etro p izatio n . In the first 3 years the refractive power
(curvature) o f rhe human cornea decreases by about 4 .8
diopters from an initial mean value o f 53 diopters. In the
first 12 years the axial length o f the eye increases by about
9 mm trom an initial mean value o f 15.5 mm. Sim ilar
changes occur in rhesus monkeys (Bradley cc al. 1999).
These changes are partly under genetic control and partly
under visual control (T ro ilo and Wallman 1 9 9 1 ).
The axial length of the eyes o f young cats and chickens
adapts ro com pensate for a refractive error induced by lenses
(W allm an and Adams 1987; Schaeffel et al. 1988). Eye
growth increased with hypermetropia induced by negative
lenses and was inhibited by myopia induced by positive
lenses. However, the em m etropization mechanism is more
responsive to myopic defocus than to hyperm etropic d efo ­
cus. For example, equal alternating periods o f myopic and
hyperm etropic defocus produced hypermetropia, showing
th at myopic defocus had a greater effect (W inaw er et al.
2 0 0 5 ).
U nder normal circum stances, animals are exposed to
objects at many distances and the eyes becom e em m etropic
for viewing at infinity. C ats raised in cages thac restrict
vision to near distances were more myopic than normal cats
(Belkin et al. 1977). W ild soet and Schm idt (2 0 0 1 ) exposed
chicks to a M altese cross on an opaque surface at one focal
distance tor 4 days. A + 2 5 D lens induced myopia o t 7 D.
The myopia was reduced to 1.7 I) when the surface was
made transparent so that the animals could see more
distant o bjects. Thus, the growth o f t h e eye adjusts to the
range o i depths in the environm ent.
O n e can ask w hether active accom m odation is required
for em m etropization. W ild soet and Schm idt (2 0 0 1 ) dis­
abled accom m odation by sectioning the ciliary nerves. Now
myopia induced by stim uli at several distances was the
same as that induced by a stimulus at one distance. They
concluded that active accom m odation is involved in
em m etropization. Schacffcl c t al. (1 9 9 0 ) found chat dis­
abling the accom m odative system did nor affect how ch ick ­
ens adapted со imposed myopia. However, chey used
unrestricted vision and lower power lenses.
Em m etropization requires a stimulus that indicates
the sign o f defocus o f the image (see Section 9 .8 ). This
could be chrom atic aberration. There is evidence that
chrom atic aberration is involved in em m etropization.
M yopia produced by form deprivation was more severe in
chickens raised in m onochrom atic light than in those raised
in white light (Schm id and W ild soet 1 9 9 7 ). However,
chickens raised wich a positive lens in m onochrom atic light
showed the same corrective elongation o f the eye .is animals
raised in w hite light (Schaetfel and Howland 1991;
W ild soet et al. 1 993). Presumably, cues to the sign o f
defocus other than chrom atic aberration were sufficient
(Section 9 .8 .2 ).
Since defocuscd images induce com pensatory eye
grow th, stim uli with high spatial frequencies are not
required (Schaetfel and D icth er 1 999). For chickens, spatial
frequencies o f about 1 cpd were m ost effective in p rom ot­
ing proper eye growth (Schm id and W ild soet 1997).
W hatever their spatial frequency, images o f low contrast
do n o t prom ote em m etropization. Schm id et al. (2 0 0 6 )
exposed 8-day old chickens to 1.6 cpd square-wave gratings
tor 5 days. The gratings varied in contrast but had the same
mean lum inance. C o n trast o f less then 4.2 % produced
marked myopia, as indicated by the eyes refractive error
and axial dim ensions. Som e myopia was evident with c o n ­
trasts o t less than 4 7 % .
Visual experience is also involved in em m etropization
in primates. However, the m agnitude ot adaptation to lenses
in primates is not as large as that in chickens. Four infant
monkeys fitted with a + 3 D or - 3 D lens in fronc ot one eye
and norm al vision in the o ther eye adapted fully to the
anisom etropia. N one o f the monkeys adapted to 6 D o f
anisom etropia. Som e, bu t n o t all monkeys showed consid­
erable adaptation to 6 D lenses worn over both eyes (Sm ith
and Hung 1 9 9 9 ). See also Sm ith et al. (1 9 9 4 ) and Hung
et al. (1 9 9 5 ).
A ccom m odative error due to interactions between lens
accom m odation and convergence o f the eyes has been
im plicated in the developm ent of myopia in humans.
M yopic children show enhanced accom m odative conver­
gence (Jia n g 1995). A child who is esophoric must relax
accom m odation to maintain single vision. 'Ih c resulting
image blur during near work could induce axial growth o f
the eye and hence myopia (Gw iazda et al. 1 9 9 9 ). Schor
(1 9 9 9 ) has developed a model o l these processes.
Even in adults, excessive near work, such as reading,
increases myopia (Section 9 .6 .2 ). There is also evidence that
the axial length o f the human eye decreases with advancing
age to com pensate lor a decrease in the depth o f t h e ante­
rior cham ber and o fth e refractive power o f the cornea and
lens (G rosvenor 1987).
A change in the axial length o fth e human eye ofbetw een
2 and 2 0 um, corresponding to a change o fb etw een - 0 .0 3 6
and - 0 .0 1 5 diopters, occurs as em m etropcs or myopes
accom m odate (D rexler et al. 1998). This change seems to
be caused by contraction o f the ciliary muscles. Long-term
changes in axial length in those engaging in near w ork could
arise from the cumulative effect ot these changes.
In addicion, there is evidence th at loss o f contrast in the
image over long periods increases the axial length o t che
adult eye (Hartmann and Schaetfel 1 9 9 4 ). W hen the eyelids
o f a young m onkey were sutured so that only diffuse light
entered the pupil, the eye developed an increased axial
length and a consequent axial myopia (W iesel and Raviola
1979; Tigges c t al. 1 9 9 0 ). O th e r investigators could not
replicate this effect in monkeys (von N oordcn and Crawford
1 9 7 8 ), but W allm an et al. (1 9 7 8 ) obtained sim ilar effects in
chickens.
H oyt et al. (1 9 8 1 ) found axial myopia in infants to be
associated with prolonged early eyelid closure due to third
nerve palsy and o ther causes. They suggested th at the effect
m ight arise from m echanical or thermal effects o f eyelid
closure, since patients with corneal opacification did not
have myopia.
In contrast to the general finding that form-deprivation
induces elongation o f the eye (m yopia), som e studies have
reported hypermctropia after less severe deprivation or in
association with strabismic amblyopia (see K iorpes and
W allman 1995). M yopia is discussed further in Sections
9.2.1 and 9.6.2.
Schaetfel and Howland (1 9 8 8 ) and Flitcroft (1 9 9 8 )
have developed m odels o f em m etropization. The topic has
been reviewed by Young and Leary (1 9 9 1 ) and Schaetfel
and Howland (1 9 9 5 ).
6 .3 .2 D EV E L О P M E N T О F
T H E R E T IN A
6 .3 .2 a S tru c tu r a l D e v e lo p m e n t o f th e R e tin a
The precursors o f retinal cells develop from the inner layer
o f che optic cu p — an outgrow th o f che forcbrain. Ganglion
cells differentiate first, followed by cones, horizontal cells,
bipolar cells, and lastly rods. C ells develop first in the cen ­
tral retina. A t first, the cells are not confined to their proper
layers in the retina. In che visual corcex, radial glial cells
guide cells to their proper locations (Section 6 .4 .6 ).
But chere are no radial glial cells in the developing retina.
The differentiation and distribution o f retinal cell types is
controlled by che following mechanisms:
1. Early cclls produce m olecular markers. For example,
before ganglion cells develop in the mouse, two
m em bers o f chc Eph family o f receptors (E ck and Elk)
.ind their ligands are discribuced over the retina. Eck
receptors are distributed in a high temporal со low nasal
gradient, and cheir ligand form s a reciprocal gradient.
Elk receptors arc distributed in a high vencral со low
dorsal gradienc and cheir ligand forms a reciprocal
gradienc (M arcu sec al. 1 996). Thus the temporal-nasal
and vcncral-dorsal recinal coordinaces are specified by
orthogonal reciprocal m olecular gradients. Also, in
chickens, EphB recepcors are expressed in a high vencral
со low dorsal gradienc in chc plexiform layer o f the
developing recina. M acching ligands are discribuced in a
reciprocal gradienc (Braisced ec al. 1997).
W c will see lacer chac Eph recepcors and cheir ligands
are involved in guiding axons through the chiasm , the
I.G N , and the visual corcex.
2. The dendritic fields o fe a c h type o f ganglion cell form
into a regular mosaic (G alli-Resca 2 0 0 2 ). For chis со
happen, che dendrices from sim ilar cells must recognize
and repel each ocher on concact. This causes chem со tile
che recina wich licde overlap. Extra cells added in a ccll
culture repelled the dendrices ot similar neighboring
cclls to form smaller rcccptivc fields. W h en ganglion
cells were removed trom a region, che dendrices o f
sim ilar neighboring cells moved inco che gap, although
there seems to be an upper lim it to the size ot ganglion-
ccll dendricic fields (see I.in cc al. 2 0 0 4 ). The dendricic
fields o f different cvpcs o f cell did not repel each other
and therefore overlapped. The end result is that each
type o t ganglion cell receives an efficient and com plete
sampling o f che visual field.
3. Incorrecdy positioned cells are eliminaced (see C o o k
and Chalupa 2 0 0 0 ).
The development o f die human retina has been recorded
from 13 weeks o f gescacion. At this age, the mosaic o f foveal
cones is identifiable and has a density o f abouc 14,000 cones
per m n r (Hendrickson and Yuodelis 1984; Diaz-Araya and
Provis 1992; Hendrickson and Drucker 1992). By 2 4 weeks
o f gestation, cone density in the central retina is approxi­
mately 3 8 ,0 0 0 per m n r, compared wich an adulc value ot over
100,000 per mm2. C o n e density is inversely related to cell-
soma diameter. The increase in cone densicv in the fovea is
due со migracion o f cells coward che fovea from a circumfcr-
cncial region o f undilferentiaced cells, rather than to cell
division within the ccncral region (Diaz-Araya and Provis
1992).
O n e week after birch, che human peripheral recina
resembles chac o f che adult, but che macular region covering
abouc 5" o f chc central retina is verv immature. There is a
foveal depression, but all cell layers extend across it rather
than being parted as in the adult retina. The principal
m echanism for form ation o f the foveal depression is m igra­
tion o f ganglion-cell bodies in the inner retinal layers away
from the center (K irby and Steineke 1992).
At 2 6 weeks o t gescacion che inner segments o f rods and
cones arc rudimentary. There are no outer segments until 3 6
weeks o f gestation. Foveal cones ot the one-week-old intanc
have inner and outer segments that are only about one-six-
ceench the length o f adult segments. In the neonate periph­
eral recina, the inner and outer segments o f rods and cones
are 3 0 to 50% o f adult length. The outer segments o f cones
continu e to elongate over a period o f up to 5 years. Foveal
cones becom e narrower with age, trom 5 to 7.5 m icrons
wide at birth to 1.8 to 2.2 m icrons in the adult (Yuodelis
and H endrickson 1986). The decrease in diam eter means
th at a foveal cone subtends between 1.5 and 2.2 arcmin at
the nodal point in the neonate eye and about 0 .5 arcm in in
the adult eye.
The larger receptor aperture in the intanc eye severely
reduces che etfeccive contrast o f high spatial-frequency
images (Banks 1988). The retina o f an 11-m onth-old infant
is sim ilar to that o f che adulc in boch che periphery and
fovea (A bram ov et al. 1982). The retina o f the monkey
shows a sim ilar developm ent, but the fovea is more advanced
at birth than in the human (Sam orajski et al. 1965;
H endrickson and Kupfer 1976).
The visual field is smaller in human infants under 8
weeks o f age than in the adult (Scctio n 7 .2 .4 ), but to whac
extent this is ilue to optical factors rather uhan maturation
o f chc recina is noc known (Schw artz et al. 1987).
6 .3 .2 b Fu n ctional D ev e lo p m e n t o f Recina
G anglion cclls develop first, then cones, am acrine cells, and
horizontal cells. Bipolar cells, rods, and glial cclls develop
last ( Robinson 1991).
In all vertebrate species that have been exam ined, waves
of action potentials spread over the developing retina and
produce correlated firing o f neighboring ganglion cclls.
These discharges occur before retinal receptors have devel­
oped. M am m alian ganglion cells show spontaneous neural
activity• well before birth. This activity/ occurs in the rat retina
by at least em bryonic day 17 (G alli and Matfei 1988).
O p tical imaging using a calcium-sensitive dye in n e o ­
nate ferrets revealed that waves o f spontaneous firing o f
ganglion cells spread over each o f a varying mosaic o f local
areas o f the retina at intervals ot at least 5 0 s (Feller ec al.
1 9 9 6 ; W ong et al. 1995; W ong 1999). These waves o f activ­
ity occur when rctinocortical connections are being formed
and cease jusc before the eyes open (W ong and O akley
1996).
In rabbits, early retinal discharges arc blocked specifi­
cally by acetylcholine antagonises. Since acetylcholine
occurs only in scarbursc am acrinc cclls, the spontaneous
firing must originate in this subclass o f am acrinc cells, which
synapse with ganglion cells and ocher am acrinc cclls (Z heng
et al. 2 0 0 6 ). D ifferent functional classes o f ganglion cells
develop their own firing patterns. After postnatal day 4 ,
cholinergic synapses are reduced and G A B A ergic synapses
becween the am acrinc cells swicch from being excitatory to
being inh ibitory (Z h en g e t al. 2 0 0 4 ).
In m ice, selective application ot antagonists tor differ­
en t types o f neurotransm itter revealed that early cholinergic
retinal synapses are replaced by glutamacergic synapses
betw een bipolar cells and ganglion cclls (W ong and Wong
2 0 0 1 ). Before the eyes open, waves mediated by acetylcho­
line are replaced by waves mediated by glutamate. These
waves involve asynchronous bursts o f activity in O N and
O F F ganglion cclls. They presumably help to segregate
these functionally distinct pathways (Kerschensteiner and
W ong 2 0 0 8 ).
In the adult mammalian retina, O N and O F F bipolar
cells and the distinct ganglion-cell dendrites into which they
teed are segregated in distinct strata in the inner plexiform
layer. Tootle (1 9 9 3 ) claim ed th a t ganglion cells in the devel­
oping retina o fth e cat and rabbit are initially either O N or
O F F types. However, m ore recent evidence shows that
immature ganglion cclls in the ferret retina show both O N
and O F F responses to a flash o flig h t (W ang c t al. 2 0 0 1 ).
Initially, O N and O F F bipolar cells are n o t segregated, and
ganglion-cell dendrites ram ify throughout the plexiform
layer. Later, O N and O F F ganglion cells occur in distinct
sublaminae ot the inner plexiform layer. Thus the develop­
m ent o f synaptic connections in the ferret retina involves
both the growth and the pruning ot dendrites. Segregation
o f O N and O F F ganglion cells in the mouse retina requires
visual stim ulation (T ia n and Copenhagen 2 0 0 3 ).
In m ice, ganglion cells begin to respond to light stim u­
lation o f t h e receptors by postnatal day 10, just before the
eyes open. In the cat, electrical stim ulation induces spikes in
about a third o f ganglion cells by em bryonic day 30
(5 weeks before b irth ). By em bryonic day 5 5 , alm ost all
ganglion cells are capable o f generating repetitive discharges.
Discharges are abolished by application o f tetrodotoxin,
which indicates that they are mediated by sodium
ions(Skaliora et al. 1 993).
Presumably, this early spreading activity helps in the
developm ent o f t h e tangential retinal netw ork even before
the development o f structures responsible for activating the
optic nerve. Spontaneous waves o f retinal activity are also
required for the developm ent o f precise visual pathways. In
m ice lacking this spontaneous activity, retinal projections
ro the superior colliculus failed to form rhe precise mapping
found in norm al m ice (M cLaughlin et al. 2 0 0 3 ). Also, the
deficient m ice lacked fine-scale retinouopic mapping in the
L G N (G ru bb et al. 2 0 0 3 ). W e will see in Section 6 .6 .2 that
spontaneous retinal activity is also Involved in the develop­
m ent o f the visual cortex.
In the cat, betw een the tim e o f eye opening at postnatal
day 7 and postnatal day 2 1 , the interm ittent bursts o f spon­
taneous activity in ganglion cells change to a more regular
spontaneous discharge. Just after eye opening, only a few
ganglion cells respond to light, buc by poscnacal day 10 they
all respond (T oo tle 1993).
The inner retina o f m ice, and probably all mammals,
contains a netw ork o f ganglion cells containing the p h o to ­
pigm ent melanopsin (Section s 5 .1 .4 g ). These cells project
to chc suprachiasmacic nucleus, w hich concrols chc circa­
dian rhyrhm (see Section 5 .3 .1 ). G anglion cells containing
melanopsin respond ro light from chc day o f birch. Thus,
chis system develops before the system responsible for regis­
tering visual images. The density o f ganglion cells co n tain ­
ing melanopsin declines as the retina matures (Sekaran et al.
2 0 0 5 ). There is evidence that prim ates possess a similar
system (H ao an d Rivkces 1999).
The developm ent o f functional retinal synapses can be
followed by im m unocytochem ical labeling o f the synaptic
glycoprotein, S V 2. This protein is correlated with the pres­
ence o f synapses, as revealed by the electron m icroscope
(O kada et al. 1994). Synaptic developmenc follows a foveal
со peripheral progression and occurs tor rods before cones
ac chc same retinal eccentricicv. M ocilicy ofd endricic filopo-
dia associated with synaptogcnesis can be observed by
time-lapse confocal m icroscopy after transfection wich a
fluorescent procein.
6 .3 .3 G R O W T H O F T H E O P T IC N ER V E
AND TR A C T
6 .3 .3 a S tr u c tu re o f chc O p t ic N e rv e and T ra c t
G anglion-cell axons grow over the recina coward chc optic
disk. They are guided by a variety o f chem ical growth fac­
tors. These include adhesion molecules, such as intcgrin
and calm odulin in che excracellular macrix, and adhesion
molecules on che growing ganglion-cell axons (Z elin a cc al.
2 0 0 5 ).
Ac che opcic disk chc ganglion-ccll axons leave chc recina
со form che opcic nerve. In th ecac, axons begin со grow inco
che opcic nerve by abouc chc 30ch em bryonic day (Shacz and
Srecavan 1986; O kada ec al. 1994) (Porcraic Figure 6 .1 0 ).
They then progress through the opcic chiasm to the lateral
geniculate nucleus (L G N ).
The m orphogen S o n ic hed gehog plays a crucial role in
recinal developmenc. In che recinal periphery, where icscon-
cencration is low, it attracts growth cones o f ganglion-cell
axons. In che central recina, where concencration is high, ic
inhibits m ovem ent o f growth cones. The centrally directed
growth o f ganglion-ccll axons is disrupted when the expres­
sion o f S o n ic hedgehog is disrupced (K olpak ec al. 2 0 0 5 ).
This m orphogen is also involved in che dcvclopm cnc o f che
chiasm and cerebral corcex (Section 6 .4 .7 ).
W h en ganglion-ccll axons arc w ithin about 5 0 p of
che head o f che opcic nerve chey are guided inco che nerve

Figure6 .№. Carla J. Shan. B o m in N e w Y o rk C it y in 1947. She o b taine d
а В .Л . in c h c m is try fro m R a dclitfe C ollege in 1969 and a P h .D . in
n e u ro b io lo g v fro m H a rv a rd M e d ic a l S chool w ith D . H u b e i and T .
W iese l in 1976. She c o n d u cte d p o s td o c to ra l w o rk w ith Pasko Rakic
a t H a rv a rd M e d ic a l S chool. In 1978 she jo in e d the fa c u lty at S ta n fo rd
U n iv e rs ity , D e p a rtm e n t o f N e u ro b io lo g v , w here she bccam c professor
o f n e u ro b io lo g v in 1989. In 1992. she m oved to the D e p a rtm e n t o f
M o le c u la r and C c ll B io lo g y a t Berkeley, w here she bccamc professor
o f n e u ro b io lo g v and an in ve stig a to r o t th e H o w a rd H ughes M e d ic a l
In s titu te . In 20 0 0, she bccam c N a th a n M arsh Pusey Professor o f
N c u ro b io lo g y in the D e p a rtm e n t o f N e u ro b io lo g v a t H a rv a rd M e d ic a l
School. H o n o rs in c lu d e th e G o lg i A w a rd fro m I'id ia in 1992, the
Silvo C o n te A w a rd fro m the N a tio n a l F o u n d a tio n fo r B ra in Research
in 199Л, th e C h a rle s A . D a n a A w a rd fo r P ionee ring A c h ie v e m e n t in
H e a lth and E d ucatio n in 1995, the A lc o n A w ard fo r O u ts ta n d in g
C o n trib u tio n s to V is io n Research in 1997, and th e Bernard Sachs
A w ard fro m the C h ild N e u ro lo g y S ociety in 1999. She was elected to
the A m e ric a n A cad cm v o f A rts and Scicnccs, in 1995 to the N a tio n a l
A ca d cm y o f Scicnccs, in 1997. D r Shatz was president o f the S o cicty fo r
N euroscience, 1 9 9 4 -9 5 .
by the growth factors lam in in and n ctrin -1 (D cin er ct al.
1997). As rhe axons advance along the optic nerve they
change their responsiveness to nctrin-1 Irom attraction to
repulsion. This allows them to advance into the netrin-1
free regions o l the optic nerve (Shcw an c t al. 2 0 0 2 ).
Axons in the optic nerve form into bundles, or fascicles,
that are enclosed by interfascicular glial cclls. G row th cones
arc distributed at random am ong older axons both within
fascicles and in different parts of the optic nerve. In the
monkey, growth concs becom e conccntratcd in the outer
layers o f the optic nerve by em bryonic day 4 5 . However,
even in the late em bryo, growth cones penetrate between
older axons in deeper fascicles o f the optic nerve far
from the outer pial m em brane o t glial cclls (W illiam s ct al.
1 9 9 1 ).
In the optic nerve, ganglion-cell axons reach the optic
chiasm , where they undergo hemidccussation (see Section
6 .3 .4 ).
After leaving the chiasm , ganglion-cell axons enter
the optic tract, which term inates in the I.G N and other
subcortical ccntcrs. The inner layers o f the optic tract o fth e
cat consist ot crossed and uncrossed axons from the co n tral­
ateral nasal and ipsilatcral tem poral hemiretinas. Axons in
these layers therefore show a sharp hem idccussation. The
superficial layers consist mainly o f fine axons from the
whole contralateral retina and the ipsilateral temporal
retina. Thus, these layers contain axons from the temporal
retina th at have crossed che chiasm . Axons in rhe superficial
layers arise late in developm ent, when signals that direct
axons from the tem poral retina to take an uncrossed course
arc weakened (Reese et al. 1991).
Secondary axons grow from rhe L G N along the optic
radiations to layer 4 o f the visual cortex. C ells trom each
pare o f the retina co n n ect with specific locations in the
L G N and cortex. See H olt and Harris (1 9 9 3 ) tor a discus­
sion o f retinal markers that determ ine che mapping o f visual
inputs.
6 .3 .3 b C o m p e titiv e Survival o f G an g lio n C clls
G anglion-cell axons grow toward their target areas in sub­
cortical nuclci such as chc superior colliculus and LG N . The
destinacion of a given axon seems со be determ ined by the
rccinal region from w hich ic originaccs. Thus,ganglion cclls
from a transplanted area ot the protoretina in the toad still
grow toward the destination appropriate to the original site
(Fraser 1991). We will see later thac other factors determ ine
the precise way in which ganglion cclls make synaptic co n ­
tacts with target cells in the LG N.
G anglion-cell axons start to grow into chc opcic nerve ot
the cat on the 19th em bryonic day. By the 39th day, the
nerve contains about 6 0 0 ,0 0 0 axons. By two weeks after
birth, the number o f axons has declined to the adult value
of about 1 6 0,000 (Lam ct al. 1 9 8 2 ; Ng and Stone 1982;
W illiam s e ta l. 1986).
In the monkey, by the 95 th em bryonic day, the optic
nerve contains about 2.85 m illion axons com pared with 1.6
m illion in chc adult. Axons arc lost m ost rapidly between
the 95th and 120th em bryonic days, which is just when
retinal terminals segregate inco d istin ct layers in the LG N
(R ak ic and Riley 1983). The surplus o f optic nerve axons is
due со overproduction of ganglion cells rather than to
axonal branching o f existing neurons (Perry ct al. 1983;
Sefton 1986). In both normal cats and in cats with one eye
removed there is elose agreem ent between the num ber o f
ganglion cells and the num ber o f optic nerve fibers ac each
scage o f developm ent (C halupa c t al. 1984). A sim ilar loss
of mocor axons innervacing muscles has been noced during
early dcvelopmcnc (C ow an 1973).
C ells in che LG N w ith which ganglion cells make syn­
aptic concaccs secrcce che neurocrophic growch taccor
(Section 6 .4 .3 d ). C om petition for this grow th factor deter­
mines which opcic-nerve axons survive and which die. The
growch factor binds to receptor molecules on the surface o f
the growing axon (see Allendoerter et al. 1994). Signals are
then transported rapidly down the axon to chc ccll soma,
where they regulate the genetic expression o f proteins
required for cell growth and survival (Spencer and W illard
1 9 9 2 ). In the absence o l che growch factor the neuron dies.
D eath o f ganglion cells in tissue culture is prevented when
the culture contains target cells o r a grow th factor derived
from target cells. In the growing visual system, ccll death is
prom oted by removal o f che growch factor (see R a ff ec al.
1993). Deach is prom oted in cells wich severed axons
because chey arc cu t o ff from che growch factor (Bray
e ta l. 1 992)."
G anglion cells in tissue culture respond to the neu-
rotrophic growth factor only when they are in an active
state (M eyer-Franke cc al. 1 9 9 5 ). C cll growch and survival
chus depend boch on che growch faccor and activation o f
the ccll. Som e growch faccors are highly specific, and ensure
that only appropriate synaptic contacts survive (Korsching
1993). A sim ilar com petitive m echanism operating at the
cortical level is described in S ection 6.7.2d .
Removal o f one eye reduces che num ber o f cells com per­
ing for thalam ic connections. W hen hamsters and rats had
one eye removed in ucero, the optic nerve from the remain­
ing eye had about 2 0 % m ore axons than a norm al optic
nerve (Sengelaub and Finlay 1 9 8 1 ; Jeffery and Perry 1982).
In cats with one eye removed prenatally, che rem aining eye-
had about 1 8 0 ,0 0 0 ganglion cclls com pared with 1 5 0,000
in a norm al eye, and the receptive fields o f cortical cells were
smaller in m onocularly enucleated cats than in norm al cats
(C h alu p aecal. 19 8 4 ; Scone and Rapaport 1 9 8 6 ). Ganglion
cells o f an eye in which action potentials were blocked by
tetrodocoxin died ac chc norm al rate, bur cells o f che n on ­
treated eye died ac a reduced race (Schcecz ec al. 1995).
In chc developed retina o f the monkey, the density o f
ganglion cells has been reported to be 3 0 0 times higher in
the foveal region than in che far periphery (Perry and Cow ey
1 9 8 5 ). However, m ore recently, the density o f ganglion
cells has been estim ated to be 1,0 00 tim es higher in the
fovea (W asslc e t al. 1 990). The processes responsible for the
developmenc o f chis differential density are noc fully known.
The loss o f ganglion cells and their segregation in to areas o f
different dcnsicy is accom panied by differencial growth o f
the retinal surface.
6 .3 .3 c M vW clination
M yelin is a fatty substance chac forms an insulacing sheath
around each axon o f the voluntary nervous system. In the
central nervous syscem, myelin sheachs are form ed from a
type o f glial cell known as o lig o d cn d ro cy tcs. Th e produc­
tion o f oligodendrocytes is jointly concrolled by a growch
faccor and electrical activity in the axons (Barres and Raff
1993). G anglion-cell axons begin ro myelinate after the
period o f axonal loss and the process mostly occurs poscna-
rally. A xon diam eter and condu ction velocity are correlated
with the thickness ot the myelin
< sheath. W hen mvclination
/ ac chc same cime. A xons from che cemporal rccina ac firsc
is prevented by X-ray irradiation, axons do n o t increase in
diamecer, showing thac growth o f axon diam eter depends
on some factor derived from the myelin sheath (C oleilo
e t al. 1994).
In chc human visual system, myelination proceeds from
che brain coward the eye. Axons arising from the fovea
myelinate before chose arising from the peripheral retina.
M vclination o f subcortical visual pathways is com plete by
chc chird postnatal m onth (Yakovlev and I.ccours 1967)
and chac o f the geniculocortical pathways by the seventh
m onth (M agoon and R obb 1981). M yelination o f the cere­
bral cortex system is n o t com plete until early adulthood.
In the peripheral nervous system, myelin sheaths arc
form ed from Schwann cells. D eveloping and regenerating
peripheral axons express a receptor for B D N F that controls
myelinacion (Cosgaya ec al. 2 0 0 2 ). Sec Sherm an and Brophy
(2 0 0 5 ) for a review o f m echanism s o f myelinacion.
6 .3 .4 S E G R E G A T IO N O F A X O N S
A T T H E C H IA S M
6 .3 .4 a G en eral D ev elo p m en t o f th e C h iasm
W h en ganglion-cell axons reach che chiasm , they segregate
into those from che ccmporal hemirccinas chat remain on
the same side, and those from the nasal hem iretinas that
decussate to chc concralaccral side. Two m echanism s have
been proposed со account for chis segregation. In the firsc,
growing axons respond со structural o r chem ical signals as
they approach che chiasm . In che second, axons from the
cemporal retina grow at random to one side or che ocher,
and chose caking che wrong route are subsequently
elim inated.
Sretavan (1 9 9 0 ) injecced a fluorescent dye inco chc opcic
tracc (postchiasm ) o f em bryonic mice (Portrait Figure 6 . 11).
The dye rctrogradcly labeled axons in che opcic nerve (prc-
chiasm ) according to whecher they were destined to cross or
remain on chc same side. C han and G uillery (1 9 9 4 ) labeled
recina! regions o f em bryonic racs. These procedures revealed
thac ganglion-cell axons have a recinocopic order as chcv
leave che retina, alchough axons from differenc classes o f
ganglion ccll inccrminglc. W h en axons rcach chc chiasm
chey lose their recinocopic order. Axons from dorsal and
vencral retinal regions inccrminglc wich chose from nasal
and tem poral regions (W alsh 1986). Thus, che partition
mechanism chac decides whecher a given axon dccussaccsor
not has n othing to do with the relative positions o f axons in
chc opcic nerve (D ragcr 1985).
D uring the first stage o f developm ent in che em bryonic
mouse, axons from the vcntroccm poral rccina chac are des­
tined со be uncrossed arrive at the chiasm before other
axons and grow directly inco che ipsilaceral opcic tract w ith­
out approaching the m idline (M arcus and Mason 1 9 9 5 ). In
later stages, crossed and uncrossed axons arrive at the chiasm

F »fp r< 6 . П . D arisf W. Sretavan. H e o b ta in ed hiv B .S c . in ncurophyM oIogy
from M c G ill U niversity4 and a P h .D . from S tan fo rd U n ivcrsitv
4
with
C a rla Shat/ in 19 8 5 . A fter a p o std o cto ra l fellow ship at R ockefeller
U n iv ersity he jo in ed th e d ep a rtm en t o f o p h th alm o lo g y am i physiology
in the U n iv ersity o f C a lifo rn ia a t San Fran cisco in 1 9 9 4 , w here lie is
now an associate protestor.
tollow the same route as those trom the nasal retina as they
grow coward che m idline o f rhe chiasm , buc at chis poinc che
temporal fibers bend sharply toward the ipsilateral side.
Thus, in che mouse, chere is an age-dependenc change in che
process o t segregation at the chiasm .
Axons from the tem poral hem iretina o f che monkey
took an ipsilateral route through the chiasm by em bryonic
day 3 6 (M eissirel and Chalupa 1 9 9 4 ). This is before cross­
ing axons trom the nasal hem iretina reach the chiasm . Thus,
the first uncrossed axons do n o t require pioneer crossed
axons trom the opposite eye. They are presumably guided
by a specific chem ical. By em bryonic day 4 2 , there was a
clear segregation o t crossed and uncrossed axons in the
optic tract. The early uncrossed axons occupied the lower
region. These pioneer uncrossed axons may be lost at a later
age, since the deeper layers o f the adult optic tract consist o f
crossed fibers.
As retinal axons approach the chiasm they defasciculate
and spread out. Radial glial cells replace the interfascicular
glial cclls. G row th concs accum ulate in subpial regions
am ong the endfeec o f che radial glial cells (C olello and
Guillerv 1 9 9 2 ). However, chis ordering is lost in the m id­
line o f the chiasm (C olello and C olem an 1 9 9 7 ). As axons
leave the chiasm they4 becom e bundled again to form the I *
optic tract.
The growth ot pioneer axons along the optic nerve and
tract o f cats and mice can be observed wich cime-lapse video
m icroscopy after the axons have been labeled with fluores­
cent dyes. Periods o f advance, during which growth cones
are elongated and have tew filopodia, arc interspersed with
pauses in which growth cones spread out and project filopo­
dia. As the axons reach "decision regions" in the optic
chiasm or I.G N , the periods o f advancc arc short and the
pauses are prolonged for one hour or more. During pauses,
growth concs enlarge and develop a com plcx structure.
Filopodia "seek o u t" the appropriate pathway in the chiasm
or the correct target cclls in the I.G N (Bovolcnta and
M ason 1987). The growth cones o f uncrossed axons becom e
highly branched wich filopodia. They then turn toward the
ipsilateral opcic tracc before reaching che chin raphe, or
seam, o f cells along the chiasm atic m idlinc (Sretavan and
Rcichardt 1 9 9 3 ;G o d e m e n ce ta l. 1 9 9 4 ; M arcus e ta l. 1995).
They are deflected by a chem ical signal, which forbids them
from crossing the m idline (G o d em e n te t al. 1990).
Removal o f one eye in feral m icc and ferrets, before
axons reach chc chiasm , reduced che num ber o f uncrossed
axons trom the surviving eye in the optic tract. Uncrossed
axons accumulated at the chiasm (see Taylor and Guillerv
1 9 9 5 ). M onocular enucleation in the neonate, alter axons
have reached the L G N , increased the num ber o f uncrossed
axons (C h an and G uillery 1 9 9 3 ). This suggests that a chem ­
ical signal that guides uncrossed axons through the chiasm
is activated by crossed axons trom the other eye as they pass
through the chiasm . M onocular cnucleacion did noc affect
the routing o f uncrossed axons but it did abolish the pause
in axon growth at chc chiasm (Sretavan and Rcichardt
1993).
O th er evidcncc suggests that axons arising from the
nasal and temporal retina interact at the chiasm . Culcurcd
nasal growth concs o t the chick retina are ju st as likely to
grow in a culture o f nasal axons as in a culcure o f cemporal
axons, whereas tem poral growth con cs grow only in a cul­
ture o f temporal axons (B onhoeffer and H u f 1985).
Temporal growth cones in culture collapse when they co n ­
tact nasal axons. This suggests that nasal (crossed) axons
produce an inh ibitor specific to temporal growth concs
(R aper and Grunew ald 1990).
In marsupials, uncrossed axons do not approach the
chiasm m idline. Instead, they remain grouped in the lateral
region o t the chiasm . This is also true o t at least one placen­
tal mammal, the tree shrew (Jeffery c t al. 1998).
Injection ot a m onoclonal antibody tor glial cells
revealed a palisade o f radial glial cells straddling the chias­
matic midline o f the em bryonic mouse. G row ing ganglion
ccll axons enter the radial palisade and co n tact glial cclls,
trom which they pick up cell surface molecules with oppos­
ing effects on crossed and uncrossed axons (C olello and
Cauillery 1992). Also, in the em bryonic mouse, a V-shaped
pattern o f specialized neurons ( C D 4 4 neurons) develops in
the neuroepithelium at the site o f the future chiasm a day or
two before ganglion-ccll axons arrive at the site. These neu­
rons express neurocrophins and cell surface molecules,
which either prom ote or in h ib it axon growth (Sretavan
et al. 1994). Their effects on grow ing axons can be
seen when retinal cells are cocultured with cells trom the
chiasm atic m idline o f em bryonic m icc (W a n g e t al. 1995).
Alter a specific antibody had removed these epithelial neu­
rons, subsequently arriving ganglion-cell axons failed со
decussate (Sretavan et al. 1 9 9 5 ). Specific inhibitory m ole­
cules have also been revealed in cultures o f growing gan­
glion cells Irom the em bryonic rat, an animal in which only
a few axons trom the ventrotem poral margin ot the retina
project ipsilaterally (W izenm ann c t al. 1993).
6 .3 .4 b M o le cu la r R o u tin g M ech an ism s
in the C h iasm
In many animals, including insects, fish, and mammals, the
retinas, optic stalk, and various regions o fth e growing ner­
vous system express proteins known as S lit 1, S lit2 , and
SIic3. The axon receptors for these ligands are known as
R o u n d a b o u t, or R o b o receptors. In fru it flies {Drosophila),
S lit expressed by m idline glial cclls repels ganglion-cell
axons that have inappropriately crossed the m idline (Kidd
c t al. 1999). In zebra fish lacking R obo receptors, axons that
enter the wrong pathway at the chiasm are n o t corrected, as
they are in anim als with R obo receptors ( Fricke e t al. 2 0 0 1 ;
Hutson and C h ien 2 0 0 2 ).
S lit also prevents ganglion cclls from innervating inap­
propriate brain areas in zebra fish. In m ice, S litl and S lit2
provide repulsion signals that d irect axons along their
appropriate paths before they enter and after they leave the
chiasm . They also torm an inhibitory system that guides
axons to their destinations in the diencephalon (m idbrain),
as described in Section 6 .4 .3 b . In m ice deficient in both
S litl and Slit 2 , growing axons are m isrouted in several
pathways, including the optic nerves, corpus callosum,
and thalam ocortical tracts (Bagri et al. 2 0 0 2 ; Plump et al.
2 0 0 2 ). The Slit-R ob o system is also involved in the migra­
tion and differentiation o f cortical cclls, as we will see in
Section 6 .4 .7 a .
F.phrin ligands and their F.ph recep to rs are involved in
the developm ent o f several parts o f the nervous system,
including the retina (Section 6 .3 .2 ), I.G N (Section 6 .3 .5 ),
corpus callosum (Section 6 .4 .6 d ), chiasm (Section 6 .3 .4 b ),
and visual cortex. А -class ephrin ligands interact with
Л -class Eph receptors. В -class ligands interact with B-class
receptors. Both ligands and receptors are bound to ccll
m em branes. For example, in the frog Xenopus, ganglion
cells destined to remain uncrossed at the chiasm express
EphB. Tli is receptor protein binds with the ligand ephrin-B,
which is expressed in the chiasm during metam orphosis,
when uncrossed axons reach the chiasm.
The ligand ephrin-B2 is strongly expressed in radial glial
cells in the chiasm m idline in the mouse when the chiasm is
form ing during em bryonic days E 1 4 -E 1 6 . It repels
ganglion-cell axons that express the receptor EphBl into
the ipsilateral pathway. These ipsilateral axons arise in the
ventrotem poral retina. Ipsilateral projections are eliminated
when ephrin-B2 is blocked and are severely reduced in mice
lacking F.phBl (W illiam s ct al. 2 0 0 3 ). The closely related
receptor, Ep hB 2, is less elfective in directing axons into the
ipsilateral pathway (Petros c t al. 2 0 0 9 ). In the mouse,
only about 3% o f axons project ipsilaterally. After em bry­
onic day F. 16, the chiasm expresses less ephrin-B2, and most
arriving axons decussate. The developing chiasm does not
express ephrin-B in animals, such as zebra fish and chickens,
that have few if any uncrossed axons (Nakagawa et al.
2000 ).
Crossing at the chiasm is not merely a default route
taken by axons in the absence o t repulsion by o f ephrin-B2.
Tine ccll adhesion m olecule N r-C A M is expressed by co n ­
tralaterally projecting ganglion cells (W illiam s et al. 2 0 0 6 ).
It attracts axons in to the crossed pathway. W h en N r-C A M
is disabled, m ore axons p roject ipsilaterally. After the criti­
cal period, N r-C A M attracts these axons and all other axons
into the crossed pathway.
Recently, genes th at determ ine the routes taken by gan­
glion cell axons through the chiasm have been discovered.
Zinc finger ( Zic) genes are involved in the developm ent o f
left-right asymmetry o f the body plan. In m ice, the tran­
scription factor Z ic 2 is expressed only in ganglion cells des­
tined to p roject ipsilaterally. These are the 3% o f ganglion
cclls in the ventrotem poral retina that also express E p h B l.
The expression o f Z ic2 ceases once the ganglion cclls have
passed through the chiasm . The proportion o f ganglion
cells expressing Z ic2 in toads, m ice, ferrets, and chickens
correlates with the size o fth e ipsilateral projection (H errera
et al. 2 0 0 3 ).
The transcription factor Islet-2 (Is l2 ) is expressed only
in ganglion cells destined to project contralaterally. These
cells occur in all parts o f cach retina o f the mouse. M ice
lacking the Ы 2 gene have an increased num ber o f cclls
expressing Z ic2. Consequently, there is an increase in gan­
glion cclls projecting ipsilaterally (Pak c t al. 2 0 0 4 ). It thus
seems that the expression o f Isl2 in crossing ganglion cells
regulates the num ber o f ipsilateral axons.
B rain F a cto r 1 (B F 1 ) is expressed in the developing
nasal retina and B rain F a cto r 2 ( B F 2 ) is expressed in the
tem poral retina. These proteins are also known as Foxgl
and Foxdl respectively. They guide the developm ent o f
retinal axis polarity. The same proteins are also expressed in
the chiasm . In m ice lacking B F 2 (F o x d l) the normally
uncrossed axons in the chiasm cross over. Also, E p h B l and
the transcription factor Z ic2 are boch m issing in m ice lack­
ing B F 2 (H errera et al. 2 0 0 4 ).
The m orphogen Sonic-H edgchog (Sh h ) is also involved
in axon segregation at the chiasm . It is expressed at the dien­
cephalon m idline. Its receptor, B oc, is present in ganglion
cells destined to project ipsilaterally. A t the chiasm , Shh
acts on ganglion cells containing Boc to prevent them from
crossing (Fabre et al. 2 0 1 0 ).
In summary, ganglion cells in the temporal retina des­
tined to p roject ipsilaterally express E p h B l, Z ic2, Brain
Factor 2 , and Boc. G anglion cells in the nasal retinal
destined to p roject contralacerally express Isl2, Brain
Factor 1, and N r-C A M .
It has been reported that many axons from the temporal
hem iretinas o f the fetal rat, ferret, and cat take the wrong
route at the chiasm and are subsequently elim inated (Jeffery
1984, 1 990). This provides a second mechanism lor axon
segregation at the chiasm . However, there is som e uncer­
tainty about this m echanism , since o ther evidence from
m ice, ferrets, and cats suggests thac during early fetal stages
all axons from the temporal hem iretinas take the ipsilaceral
rouce but, at a later stage, decussate and remain decussated.
The lace decussation could occur because the chem ical
signal forbidding decussation o f temporal axons fades or
because late-arriving axons arc insensitive to that signal (see
Sretavan 1 9 9 0 ; Reese and Baker 1992; Baker and Reese
1993). Decussated tem poral axons o f cats arc o f a specific
type, but their function remains obscure.
In all mammals, axons from the nasal retinas fullvdecus-
4
sate. In fetal monkeys, the adult pattern o f hcmidecussation
is evident before the developm ent o f ocular dom inance col­
umns and before the period o t ganglion-cell death (Chalupa
and I.ia 1991).
Axons o f ganglion cells em erging from the chiasm form
the optic tract. Crossed and uncrossed axons form pairs.
Axons segregate according to the type o f ganglion cell (par-
voccllular, magnocellular, W -cclls). Axons o f each type
acquire a retinotopic order. Those from the upper and lower
halves o f the retina segregate in to anterior and posterior
segments o f the tract respectively. Segregation o f dorsal and
ventral regions is controlled by factors carried on glial cells
(Reese et al. 1 9 9 4 ). These processes arc controlled by
regulatory genes that express patterns o f proteins in overlap­
ping longitudinal dom ains in the forebrain (M arcus e t al.
1999).
G A P -4 3 (neurom odulin), a m em brane protein
secreted by growing axons, may be involved in guiding
axons as they leave the chiasm . D isruption o f the gene for
G A P -4 3 in rat em bryos caused many axons to grow in
random directions as they left the chiasm (K ruger e t al.
1998). They form ed abnorm al connections in the I.G N
and superior colliculus (Sretavan and Kruger 1998; Zhu
an d ju lien 1 999).
Thus, three transform ations o f axons occur in the region
o t the chiasm. (1 ) A xons torm into crossed and uncrossed
pairs. (2 ) They segregate according to cell type. (3 ) Each cell
type reestablishes a retinotopic order. W ith in this transi­
tion zone the glial cclls change from an interfascicular
organization to the radial organization typical o f the dien­
cephalon (Reese c t al. 1994). Ganglion ccll axons then enter
rhe lateral geniculate nuclei, where they segregate into dis­
tin ct laminae.
The developm ent o f the chiasm has been reviewed by
G uillcry et al. ( 1 9 9 5 ), Jctfcry ( 2 0 0 1 ), and Petros c t al.
(2 0 0 8 ). A bnorm alities o f dccussation o f axons at the chiasm
are discussed in Section 3 2 .6 .2 .
6 .3 .5 D E V E L O P M E N T O F T H E LGN
6 .3 .5 a L G N L a m in a tio n
The structure o f the lateral geniculate nucleus (L G N ) was
described in S ection 5.2.1.
In the ferret, which has stereoscopic vision, inputs to
the L G N are mapped rctinotopically at birth. However,
segregation into d istin ct lam inae is not com plete until one
or two weeks after birth (Jeffery 1 9 8 9 ). In the neonate, che
ipsilateral inputs arise from rhe temporal hem iretina, as in
the adult. Initially, contralateral inputs arise from the whole
retina. O n ly later do they arise from the nasal hem iretina
(Jeffery 1990). The same is true o f retinotectal projections
to the superior colliculus o f the rat (Land and Lund 1979).
In the ferret, inputs from O N -cen tcr and O F F -cen ter
receptive fields segregate into distinct layers in the third
postnatal week.
In the cat, afferents from the contralateral nasal retina
invade the L G N by the 32n d day o f gestation. This is about
10 days after the firsc ganglion cells develop and about
5 weeks before birth. Afferents trom the ipsilateral tem po­
ral hem iretinas invade the L G N about 3 days later than
those from the contralateral nasal hem iretinas (Shatz 1983).
This may be a consequence o f the recent evolution o f the
nondecussating pathway. Visual effects o f this asymmetry
arc discussed in S ection 22.6.1. Regions o f the I.G N receiv­
ing from the central retina (m edial parts o f each lam ina)
develop before those receiving from the peripheral retina
(lateral parts o f each lamina) (Sretavan and Shatz 1987). In
the cat, inputs from the cwo eyes ac first interm ingled and
becom e alm ost fully segregated into distinct layers by about
the 54th day o f the 64-day gestation.
D endrites in the L G N o f neonate cats have many spines
and growth cones. A bout 4 m onths after birth, growth
cones disappear, chc num ber o f spines decreases, and den­
dritic arborizations becom e rescricted со the laminae ot the
eye o f origin (D e C ourcen and Garey 1 9 8 2 ). In humans,
sim ilar changes excend over a longer period (G arey 1984).
C orticogenicu latc and geniculocortical interconnec­
tions also develop in the prenatal and postnatal periods in
the cat. These interconnections developed even after retinal
afferents were removed as they started to invade the L G N
(G uillcry c t al. 1985).
Injection o t radioactive tracers into the eyes o f monkey
fetuses revealed that all I.G N cells are formed by the 64th
day o f the 169-day gestation. Their segregation into six lam ­
inae occurred betw een the 6 4 th and 110th day (Rakic
1 9 7 6 ) (P ortrait Figure 6 .1 2 ). Huberm an et al. (2 0 0 5 a )
found that, in che macaque monkey, inputs were extensively
interm ingled in all layers except parvocellular layers 5 and 6
on day 69. Segregation was com plete by day 7 8 in all chc
parvocellular layers and, by day 8 4 , it was also com plete in
the m agnocellular layers 1 and 2. The L G N ot che nconacc
m onkey has che same general m orphology and laminar
structure as that o f the adult.

Figure6.12. Pasko Rnkic. B o rn in R u m a, Yugoslavia. H e ob tain ed an M .D .
and P h .D . trom B elgrad e U n iv ersity an d jo in ed the facu lty a t the
H arvard M ed ical S ch o o l in 1 9 6 9 . In 1 9 7 9 he m oved to Yale U niversityd
S ch o o l o t M cd icin c, w here he is now D u b c rg Professor o f N cu roscicn cc
and d ircccor o f t h e Kavli In stitu te fo r N cu ro scicn cc. H e rcccivcd the
G era rd , B ristol-M yers, Lashlcy. Pasarow, and Fyssen awards and is a
m em ber o f the N atio n al A cad cm y o t Scien ces.
G anglion cclls in chc eye o f the em bryonic monkey
diverge inco m agnocellular and parvocellular types soon
after chcir lasc m itotic division. The two types o f axon p roj­
e ct to discincc alternating L G N laminae. Innervation o f
parvoccllular laminae begins before innervation o f m agno­
cellular laminae (M eissirel et al. 1997). In the neonate
monkey, m agnocellular and parvoccllular neurons arc
clearly distinguishable on the basis o f their responses to
visual stim ulation, although immature cclls have a lower
spontaneous rate o f firing and longer latency than do those
of- adult cclls.
In a study o f 5 3 human brain s,cells in the parvocellular
layers o f the L G N were found to reach almosc cheir adulc
size by age 6 m onths, while cells in the magnocellular layers
continued to develop rapidly up to age 12 m onths. After
that, both types o fcell developed slowly to reach their adult
size at about 2 years (H ickcy 1977).
Prenatal segregation o f inputs into eye-specific laminae
in the L G N involves an inicial coarse segrcgacion inco sim i­
lar cell types: X , Y, and W types in the cat and m agnocel­
lular and parvoccllular types in primates (Casagrande and
C o n d o 1988).
In the cat, this segregation is followed by growth o f ter­
minal arborizations and elim ination o f inappropriate axonal
side branches (Sretavan and Shatz 1986a). In each LG N
lamina, inputs from one eye elim inate inappropriate
synaptic con tacts from the other eye (Shatz 1990b ). In the
m acaquc, Snider ct al. (1 9 9 9 ) found no cvidcncc o f
retraction o f inappropriate axonal side branches in the
neonatal L G N . They concludcd that formation ofeye-sp c-
cific projections depends on selective loss of whole axons.
Three m echanism s could be involved in the formation
o f eye-specific L G N laminae.
1. Time o f arrival o f afferents G anglion-cell axons from the
contralaccral cvc arrive before chose from the ipsilateral
eye. This idea has noc been tested.
2. Axon guidance The early postnatal developm ent o f
eye-specific laminae in the ferret L G N depends on
gradients o f guidance molecules. Nasotemporal
gradients of EphA receptors expressed by L G N axons
interact with a high laterovcntral to low mediodorsal
gradient o fth e ligand ephrin-A in the L G N . Axons
from the contralateral eye express a high level o f EphA
(see Section 6.3.2a) which causes them to be repelled by
the high concentration o f cphrin-A in the A laminae.
O n the other hand, the low concentration o f EphA in
ipsilateral axons causcs them to be attracted to the low
concentration of ephrin-A in the A l laminae.
O vcrcxprcssion o f EphA forces chc axons inco the
wrong lamina (H uberm an ec al. 2 0 0 5 b ).
The human em bryonic retina is different. Instead o f a
nasotem poral gradient o f EphA it expresses a high level
o f EphA in che center, w hich decreases toward the
nasal and temporal poles. The ligand, cphrin-A , is
expressed in a com plem entary gradient. This evolution
o f distinct nasal and temporal gradients is associated
with the evolution o f frontal vision and
hemidecussation. The human L G N expresses a single
high lateroventral со low m ediodorsal gradienc o f
ephrin-A ligands and a com plem entary gradient o f
EphA, as in lower mammals (L am b o t et al. 2 0 0 5 ).
3. Neural activity Tin's mechanism o f lam ination in chc
L G N is discussed in the next section.
6 .3 .5 b L G N L a m in a F o rm a tio n and N eu ral A ccivicy
W h ile eve-specific laminae in the L G N are form ing, burses
ofsynchronized nerve impulses arise in che recina (M eister
ec al. 1991; M ooney ec al. 1 9 9 6 ). They are gcncraccd by
waves o f high-frequency accivicy cransmicced over che recina
by acecylcholine released from scarbursc am acrinc cells.
In the second postnatal week in the mouse the retinal activ­
ity arises from glutam atcrgic synaptic transmission.
M ice with a genetic defect in cholinergic synaptic trans­
mission in the early postnatal period do not develop eye-
specific laminae in che L G N (T o rb o rg ccal. (2 0 0 5 ). Insccad,
inputs from the two eyes segregate in to coarse patches
(M uir-R obinson et al. 2 0 0 2 ).
G anglion cells in the cat retina generate action poten­
tials by em bryonic day 30. The subsequent increase in
sodium -m ediated action potentials coincides with the
period o f innervation o fth e L G N by ganglion cells (Skaliora
et al. 1 993). Spontaneous retinal activity subsides after the
eye-specific layers have formed in the L G N .
In the tree shrew, L G N laminae do n o t develop follow­
ing bilateral cnucleation (Bru nso-B echtold and Casagrandc
1985). In the cat, inputs from one eye are n o t sufficient for
developm ent o f L G N laminae. W hen Srctavan and Shatz
(1 9 8 6 b ) removed one eye in cars at em bryonic day 23,
before axons had reached the L G N , axons of the remaining
eye developed a norm al m orphology and loss o f axonal
branches, but projected diffusely rather than being confined
to norm al eye-specific laminae.
W hen sodium -m ediated action potentials in ganglion
cells o f the cat were unilaterally blocked by tetrodotoxin
betw een em bryonic day 4 5 and birth, eye-specific L G N
lam ination was disrupted. There was a proliferation o f inap­
propriate dendritic growth across normally be eye-specific
layers (Sh atz and Stryker 1 9 8 8 ). D end ritic m orphology was
affected less by bilateral blockage o f action potentials than
by unilateral blockage (D alva c t al. 1994).
In the ferret, eye-specific laminae in the L G N develop
during the prenatal period. D uring this period, spontane­
ous discharges in ganglion cells produce excitatory postsyn­
aptic currents in both N M D A and n o n -N M D A synapses
in the L G N (M oon ey et al. 1 9 9 3 ). W h en this neural activ­
ity was pharm acologically blockcd in one retina som e axons
from the active eye invaded laminae that norm ally received
inputs from the inactive eye (Penn ec al. 1 9 9 8 ). However,
only a few axons invaded rhe laminae o f rhe inactive eve.
/ 4
Thus, the projection ot m ost axons to the L G N of the ferret
does not depend on spontaneous retinal activity (C oo k
et al. 1 999).
In monkeys, segregation o f I.G N laminae was severely
disrupted by prenatal removal o f one eye, although some
segregation o f m agno- and parvocellular regions was still
evident (R akic 1 981). O n ce established, L G N lam ination
is im m une to effects o f postnatal visual experience. M onkeys
deprived ot vision in one eve trom birth to 2 7 weeks devel­
oped a substantially norm al L G N . This was so in spite o f
the fact that this type o f deprivation leads to a reduction in
the num ber o f binocular cells in the visual cortex (Blakem ore
and V ital-D urand 1986a).
Thus, segregation o f eye-specific lam inae in rhe LG N
during the prenatal and early postnatal period depends on
nerve impulses arising in the retina. These inputs are also
required for the postnatal m aturation o f L G N synapses.
However, at that stage, inputs arising from visual experience
in normal anim als are more effective than electrically evoked
potentials in nonseeing kittens (K alil 1990).
By the Hebbian rule (Section 6 .5 .1 ), synapses firing in
synchrony in a given region reinforce cach other and sup­
press activity at synapses firing out o f phase with the dom i­
nant input. Spontaneous activity is synchronized within
one eye bur nor between eyes. It is assumed that these pat­
terns o f synchrony drive similar axons into their own layers
and impel them to form their own connection s with
relay cells.
The segregation o f laminae in the L G N o f neonatal fer­
rets was n o t affected when the synchrony o f spontaneous
discharges was disrupted by pharmacological depletion o f
am acrine cells (H ubcrm an et al. 2 0 0 3 ). Perhaps the activity
from the tw o eyes remained sufficiently different to pro­
m ote segregation. Segregation was disrupted when all
spontaneous retinal activity was blocked.
C om petitive synaptic interactions generated by sponta­
neous neural discharges arc probably also responsible tor
the fact that ganglion cclls with O N -cen reran d O F F -cen ter
receptive fields segregate into d istinct layers in the L G N
and csrablish distinct con nection s with relay cclls (H ahm
et al. 1 9 9 1 ). The segregation o f inputs trom O N -ccn ter and
O F F -cen te r ganglion cells in the ferret I.G N coincides with
the onset o t distinct spontaneous firing patterns from the
two types o f receptive fields. D uring the first 2 postnatal
weeks, both types o f ganglion ccll fire in a sim ilar way. But,
as G A B A inhibitorycircu icsd evelop in the retina, the firing
rate o t O N -ccn tcr ganglion cells declines relative to that ot
O F F -cen te r cells. This difference in firing rate allows
H ebbian synapses (N M D A synapses) for the two types o f
ganglion cell to form d istin ct layers. Segregation did not
occur after blockage o f N M D A receptors (Fischer K F et al.
1 9 9 8 ). Blockage o f N M D A synapses in early developm ent
seems to have two effects. It removes the basis for com peti­
tive access to L G N neurons and it prevencs the removal o f
inappropriate synaptic connections (see Section 6.4.4b ).
The developm ent o f d istin ct tem poral patterns o f sponta­
neous activity through the growth o f specific inhibitory
circuits at specific times may be involved in other develop­
mental processes.
6 .3 .5 c F u n c tio n a l D e v e lo p m e n t o f th e L G N
W ich in the first 4 postnatal weeks, cclls in the LG N o f k it­
tens showed low rates o f m aintained discharge to illum ina­
tion, weak and long-latency responses to flashed scimuli,
and an absence ot surround inhibition. By 4 weeks, the spa­
tial characteristics o f the receptive fields achieved their
adult form . After 4 weeks the tem poral response o f cells
becam e m ore biphasic, and there was a large decrease in
response latency and response duration (C a i c t al. 1997).
C ells o f che X-cype showed mature response properties
before Y-tvpc cells (D aniels ct al. 1978). Early geniculate
responses were mainly cxcitatory. Inhibitory circuits
matured later (R am oa and M cC o rm ick 1994).
The spacial resolution o f a ccll in chc L G N is indicated
by rhe highest spatial frequency o f a drifting high-concrasc
grating that evokes a response in the ccll. Blakem ore and
Vital-D urand (1 9 8 6 b ) reported that the spatial resolution
ot L G N cclls with receptive fields at an eccentricity ot more
than 10" was much the same in the neonate m onkey as in
the adult. However, for the foveal region, L G N cclls in the
neonate m onkey resolved only up to about 5 cpd compared
with 35 cpd in the adult.
In a more recent study, M ovshon et al. (2 0 0 5 ) found
that L G N cells in neonate m onkeys responded vigorously to
stimulation but showed less spontaneous activity than cells
in the adult monkey. The characteristic spatial-frequency
tuning o f m agnocellular (M cells) increased from 2 to 4 cpd
during the first 4 weeks. T h e spatial-frequency tuning o f
parvocellular cells (P cells) remained constant at 2.3 cpd
during the first 4 weeks and doubled by the age o f six months.
Thus, initially, M cells developed more rapidly than the P
cells. For both types o f cell, an increase in spatial-frequency
tuning represents a decrease in the size o f excitatory recep-
tive-fields. During the first m onth, responses o f L G N neu­
rons were attenuated at low spatial frequencies, which
indicates that their receptive fields had developed the
center-surround organization o t cells tound in the adult.
The tem poral tuning function o f an L G N cell is indi­
cated by its response to temporal m odulations o f a grating o f
optim al spatial frequency. Hawken et al. (1 9 9 7 ) found that
the temporal resolution o f M cells in the neonate monkey
was low but rapidly improved over the first 2 months.
M ovshon e t al. (2 0 0 5 ) found that the overall shapes o f
temporal tuning functions in neonate monkeys were sim i­
lar to those o f adult monkeys. The m ajor change was an
increase in the frequency o f tem poral responses. At 1 week,
M cells had a median tem poral-frcquency tuning o f
2 3 .4 Hz com pared with the adult value o f 4 9 .7 Hz. The
corresponding values for P cells were 8.1 Hz and 22 Hz.
The contrast sensitivity ot L G N cells can be measured
by recording responses to gratings o f optimal spatial and
tem poral frequency as a function o f contrast. M ovshon
c t al. found that the contrast sensitivity o f M cells (as
indicted by the slope ot the contrast response tunction)
increased from 129 to 2 2 9 during the first 24 weeks. For P
cells the increase was from 2 4 to 34.
Movshon e t al. concluded that changes in the size o f
rcccptivc-ficlds account for changes in spatial resolution o f
L G N cells, and that changes in synaptic functions account
for changes in temporal resolution. They also concluded that
visual performance in young primates is lim ited by the imma­
turity o f the visual cortex rather than o f the retina or LG N .
The developm ent o f the L G N was reviewed by
Casagrandc and Brunso-Bechtold (1 9 8 8 ). The evolution o f
the mammalian visual pathways was reviewed by H enry and
Vidyasagar (1 9 9 1 ).
6 .4 D E V E L O P M E N T O F T H E B R A IN
6 .4 .1 G EN E R A I. D E V E L О P M E N T О F T H E
N ER V O U S SYSTEM
Em bryonic developm ent o f the vertebrate nervous system
starts with successive cell divisions o f the fertilized egg
accom panied by differentiation o f cells into general types
laid o u t in specific regions.
Each cell nucleus contains tw o com plete sets o f ch ro ­
mosomes. Each set contains the D N A com prising the
genetic code. A t the initiation o f protein synthesis a partic­
ular D N A sequence, known as a p ro m o to r, binds to a set o f
tran scrip tio n fa cto rs and R N A p olym erase. W h en the
polymerase has been phosphorylated it begins transferring
inform ation from the DNA to form a m essenger
rib o n u cle ic acid (m R N A ). The construction o f a particu­
lar m R N A is term inated by another D N A sequence.
Tit is process is known as tra n scrip tio n . Each m RN A co n ­
tains a linear sequence o t co d o n s. Each codon specifies a
particular am ino acid. The m RN A s emerge from the
nucleus and move to the site in the cell where protein syn­
thesis occurs. Proteins destined to be inserted into the cell
membrane are assembled in R ib o so m e s distributed on an
en d op lasm ic reticu lu m . Proteins destined to remain
w ithin the cell are assembled in unattached ribosomes,
known as free ribosom es. Ribosom es read the codons in
order and assemble polypeptides, which build up into the
protein m olecule (U em ura c t al. 2 0 1 0 ). W hen the last
codon (the stop codon) has been read, the com pleted pro­
tein m olecule is released from the ribosom e. This process is
known as tran slatio n (Husi et al. 2 0 0 0 ; Steward and
Schum an 2 0 0 3 ).
D evelopm ent depends on interactions betw een many
genes arranged in a hierarchy. At the top o f the hierarchy are
the master genes, o r hom eogenes. lhey produce h om eo-
p ro tcin s containing core sequences o f am ino acids, known
as h o m co b o x sequ en ces. These sequences are the same in
invertebrates and in vertebrates, including humans. They
arc said to be conserved over long periods o f evolution.
H om coproteins are transcription factors that bind to spe­
cific sequences o f genes and thereby control the production
ot m orphogens. M orp h o g cn s torm gradients in the devel­
oping em bryo that determ ine its m orphological structure.
The result is that hom eogenes specify the general body plan
o f the animal and the general structure o f particular organs
(G ehring 1 9 8 7 ). O n ce the general structure has been
form ed, other transcription factors, acting at particular
tim es or in particular locations, turn on genes that control
the developm ent o f particular body structures. Thus, che
final structure depends on the hierarchical sequence
and spatial interaction o f many transcription factors
(Section 6 .6 .1 ).
Patterns o f cell differentiation in the em bryo arc deter­
mined by gradients o f m orphogens. A m orphogcn is a pro­
tein produced in a restricted region o f em bryonic tissue
from w hence it diffuses to form a long-range concentration
gradient. Three families o t m orphogens have been identi­
fied: W ingless ( W N T ) , Hedgehog (H g ), and the trans­
form ing growth factor (T G F ) . The position o f a ccll on a
morphogcn gradient determ ines the type o f cell into which
it will differentiate.
 In chc developing nervous system, a gradient o f the
W N T m orphogen decermines the anccrior-postcrior axis
o f chc neural plate. The Hg m orphogen specifies chc dorsal-
vencral axes o f the neural tube. Pyramidal neurons develop
from the dorsal telencephalon, and inhibitory inccrncurons
develop from che vencral telencephalon. W h en the H g m or­
phogen is inhibited in em bryonic cultures in vitro, all the
cells in che neural plate develop into pyramidal neurons.
The cells then differentiate in to various types o f pyramidal
cells, presumably under checoncrol o f local factors (Gaspard
ec al. 2 0 0 8 ). There is evidence chac hom coprotcins also act
as m orphogens (Brunec ec al. 2 0 0 7 ).
M orphogens bind со recepcor m olecules on em bryonic
cells. I l l is triggers a cascade o f m olecular signals chac pro­
duce changes in gene expression. Ac a later stage, che same
m orphogens help со concrol chc growth o f axons and
cherebv4 decermine che basic scruccurc o f che nervous svscem
4

and sense organs (sec Sanchcz-C am acho cc al. 2 0 0 5 ).

The nervous system develops from che neural cube, as
described in Section 6.4.2. C cll division (m itosis) is accom ­
panied by differentiation of cells into differenc cypes and
migration o f cclls from che layers in which chcy were formed
со layers in which chey will ultimacely function. N euronal
m ig ration involves chc whole ccll, including che cell
nucleus. O n ce che cell nucleus reaches ics destination the
axon grows to form synapses wich dendrites on ochcr neu­
r>go««6.ij. R oger Sperry. H e was born in H a rtfo rd , C o n n e c tic u t, in 1 9 1 3 .
H e received his В .Л . in English trom O b erlin C o lleg e in 1 9 3 5 and a
P h .D . w ith Paul A . W eiss a t th e U n iv ersity o f C h ica g o in 1 9 4 1 . A fter
a p o std o cto ral year w ith K arl S. L ash lcy at H arvard, h e held academ ic
ap p o in tm en ts in th e D ep artm en t o f P sychology at th e U niversity
o f C h icag o . In 195-t he becam e professor o f p sy ch o bio logy a t the
C alifo rn ia In stitu te of T ech n ology. H e w on a m u ltitu d e o f academ ic
awards and was awarded the N obel Prize in Physiology in 1 9 8 1 . H e
died in 1 9 9 4 .

rons in che same layer, in differenc layers, or in discincc

regions. The tip o f chc axon forms a grow th co n e, which
extracellular substrate through w hich the axons are
navigates through intervening tissue. In grow th co n e navi­
growing. W h en sim ilar molecules mutually attract cach
gation the cell body is stationary. Som e axons, such as chose
ocher, che binding is said со be h o m o p h ilic. C A M s also
in che opcic tract, grow through considerable distances. The
provide craccion for movemenc of the growch cone over
human brain contains about 10i: neurons, and each neuron
che subscrace. Thus, an adhesive subscrace form s a
form s synapses with hundreds o f others. It has been esti­
"highway" along which growch cones advance. Some
mated that halt o f an anim als genes are devoted to che
C A M s bind axons cogccher inco bundles. The axons
growch o f che nervous syscem.
fascicu lacc со form nerves, such as che opcic nerve.
Paul W eiss (1 9 3 9 ) cham pioned che view chac axon
Axon growch also depends on mechanical interactions
growch is largely determ ined by physical properties o f the
betw een cells or betw een cells and o ther structures.
surrounding tissues rather chan by chem icals produced by
C A M s arc discussed in Scction 6.4.3b.
chc target site (W eiss and Taylor 1 944).
His student, Roger Sperry, had different ideas. H e devel­ 2. L ocal guidance molecules These ligands are secreted by a
oped the ch en io a ffin ity th eo ry , according to w hich specific fibrous matrix known as the ex tra cellu la r m a trix or bv *

con nection s between nerve cells are determ ined by m olecu­
lar markers (Sperrv 19 6 3 ; Freeman and G uidon 2 0 0 2 )
(Porcraic Figure 6 .1 3 ). W e will see chac boch factors are
involved in chc developm ent o f t h e nervous system. Also,
we now know that spontaneous and stimulus-induced
activity in growing neurons is involved in form ing and
m aintaining correct connections in the nervous system.
Ligand m olecules expressed by growing cells bind with
recep to r m olecules expressed by other cells. Three broad
types o f m olecular markers are involved in guiding axons to
their destinations.
1. Cell adhesion molecules (С/I Ms) Som e C A Ms expressed
by growing axons bind with sim ilar C A M s on the
astrocytcs. Four major fam ilies o f local guidance ligands
have been identified: netrins, slits, sem aphorins, and
cphrins. Each ligand attaches to specific rcccptor
m olecules on the m em branes o f axons growing through
thac local region. This produces signals in che growch
cone chat keep the axons on track. At ch oice points,
such as the optic chiasm , some axons grow in one
direction while others grow in another direction. Som e
guidance* molecules attract axons inco chc corrccc
channel, while others repel axons away from the
in corrcct channcl. C cll adhesion ligands can also
provide directional inform ation at choice points. The
cffcct thac a given ligand has on a growing axon depends
on chc cvpc o f recepcor expressed by chc axon. The same
 ligand can be an attractant for one type o f axon and a axis o f the em bryo. The anterior-posterior axis and che
repellent for another type. Also, the receptor expressed dorsoventral axis o fth e growing neural tube are determ ined
by a given growing axon may change over time. Thus, a by m orphogens derived from the neighboring notochord
given axon may be attracted by a given ligand at one (presumptive backbone). The neural tube is lined with a
location and repelled by the same ligand when it ncuroepithclium o fm u ltip o ten tstem cells thac arc destined
reaches another location. These guidance m olcculcs are to form the brain, spinal cord , oculom otor nerves, retina,
discussed in Section 6 .4 .3 . and iris.
Stem cells in the neural tube migrate back and forth
3. Long-range guidance molecules These ligands diffuse
between the inner and outer surface o f the tube. During
through em bryonic tissue from their p o in t o f origin to
intervals between m igrations they divide. D uring migra­
form chem ical gradients that guide the axons to their
tions they synthesize D N A . This cyclic m ovem ent is known
destinations. They arc known as n cu ro tro p h in s. There
as the elevator m ovem ent. The ventral neural tube forms
arc tour m ajor families, each with distinct receptors.
m otor neurons that emerge trom the ventral nerves o f the
M orphogens also help to guide growing axons to their
spinal cord and brainstem . The dorsal part form s sensory
destinations. N curotrophins are discussed in Sections
neurons that em erge from dorsal sensory nerves.
6 .4 .3 and 6 .4 .7 .
Som e stem cells m igrate to the outer layer o fth e tube as
they differentiate into neuroblasts, which form neurons, or
O n ce axons have reached their destination they form appro­
into glioblasts, w hich form glial cells. The rem aining stem
priate synapses with the dendrites ot other neurons (see
cells divide at ditferent rates in different parts o f the tube to
Section 6 .4 .4 ).
form the forebrain, m idbrain, hindbrain, and spinal cord.
T h e basic structures and m echanism s o f the visual
The shapes ot brains ot different vertebrate species can be
system begin to develop in the early em bryo and becom e
modeled by a com puter sim ulation o f differential growch
fully functional several m onths after birth. Initially, devel­
rates in the neural tube (Fujita 1990). The neural crest
opm ent o f the visual system is genetically programmed.
form s above the neural tube. Neural crest cells form che
However, even before birth , spontaneous discharges from
autonom ic nervous system, m ost sensory nerves, and the
the retina affect the form ation o f neural connection s in the
cornea, sclera, and ciliary muscles o f rhe eye.
visual pathways and brain. After birth, stimulus-dependent
The brain has three main subdivisions— hindbrain
neural activity determ ines the precise com bination o f path­
(rhom bencephalon), m idbrain (m esencephalon), and fore-
ways from the two eyes and the fine-tuning o f the whole
brain (prosencephalon). The hindbrain contains the fourth
visual svstem.
i ventricle, brainstem nuclei, and cerebellum. The midbrain
G enetic and experience-dependent processes do noc
contains the third ventricle and the colliculi. The forebrain
operate independently. G en etic processes set the stage for
derives trom the anterior region o f the neural tube. It is
neural activity, and neural activity affects the expression o f
subdivided into che diencephalon and celencephalon. The
genes. Activity-regulated gene expression determ ines the
diencephalon concains the thalamus and hypothalamus,
type and level o f protein synthesis, which in turn affects the
and gives rise to che opcic vesicles chac form che recina.
establishm ent and refinem ent ot neuronal circuits, as we
The ventral telen cep h alo n forms che subcortical basal
will see in S ection 6 .6 .1 .
ganglia (caudate nuclei, putam en, and globus pallidus). The
Visual m echanism s are modified by growth processes
dorsal telen cep h alo n forms the 6-layered n eo co rtcx , the
extending throughout infancy. These growch processes
3-laycrcd archicortex (hippocam pus), and the olfactory
include: ( l ) changes in the size and shape o f the eyes and
cortex. In mammals, the tw o cerebral hemispheres ot the
their scccing in chc head, (2 ) modificacions o f accom m oda­
ncocortex expand over the diencephalon and m idbrain.
tion and vergence, (3 ) changes in the size o fth e retina, (4)
Each hemisphere contains a cerebral ventricle. The n eocor­
myclinacion o f che visual pachways and visual corcex, and
tex form s alm ost 8 0 % o f che human brain.
(5 ) changes in the distribution o f dendrites and a reduction
In mammals, mosc G A B A inhibicory incerneurons o f
in the density o f synapcic concaccs.
che neocorcex develop in che subcortical ventral forebrain
C ontem plation o f the myriad o f com plex factors thac
and migrate tangentially to populate the entire cortex.
rcgulacc chc developmenc o f the visual system induces a
However, retroviral labeling in tissue cultures o fth e em bry­
sense of awe.
onic forebrain o f humans, revealed that 65 % o f interneu­
rons originate in the dorsal telencephalon. O n ly 35 % o f
6 .4 .2 G R O W T H O F C O R T IC A L A R EA S interneurons originate in the ventral forebrain (Lecinic
ec al. 2 0 0 2 ).
6 .4 .2 a D iffe re n tia tio n o f t h e M a in A reas
The morphogen H g expressed by the S o n ic hedgehog
Th e vertebrate central nervous system starts with the estab­ gene {Shh ) determ ines the differential rates of growth o f
lishm ent o f the neural plate, w hich invaginatcs to form the different parts o f the brain (B ritto et al. 2 0 0 2 ). For example,
neural tu b e that runsdorsally along che ancerior-poscerior Hg expressed by the neural tube governs the expansion o f
the early forebrain and m idbrain, including che cerebral
vesicles. D efective signaling results in reduced cell prolifera­
tion and collapse o f the ventricles (Tannahill cc al. 2 0 0 5 ).
The sonic hedgehog gene probably played a decisive role in
the evolution o f the vertebrate brain.
In mammals lacking the Sonic hedgehog gene, the cere­
bral hemispheres fail со separate— a condition known as
holoprosencephaly. I he tw o eyestalks fuse to produce one
cyclopean eye in the center of the forehead— a condition
known as cyclopia (M in g c r al. 2 0 0 2 ; C ordero ec al. 2 0 0 4 ).
Holoprosencephaly is the m ost com m on congenital fore­
brain defect in humans. Ic occurs in 1 in 16,000 neonates
but probably occurs in 1 in 2 5 0 em bryos. M ilder forms
show as a facial deform ation. In its excreme form ic is fatal.
The Hg m orphogcn is also involved in regulating ccll
division and survival in chc em bryonic axial skeleton, spinal
cord, recina, optic nerve, hippocampus, and cerebellum
(C h ian g ec al. 1996). Thus, che m orphogcn produced by
the Son ic hedgehog gene acts at different times and in dif­
ferent places со perform che same basic funccion o f regular-
ing cell division and survival.
The W N T m orphogens expressed by the gene fV ntl are
also involved in the general growth o f the nervous system
and in chc form ation o f differenc corcical areas (see C ian i
and Salinas 2 0 0 5 ).
The neocorcex o f mammals is enlarged relative со ocher
parts o f the brain, mainly because o f an expansion o f the cor­
tical surface (H olm an 1985). The neocorcex o t primates has
about five times the volume o f that o f insectivores, after allow­
ance has been made for general increase in brain size (Barcon
and Harvey 2 0 0 0 ). O n average, there are over 13 billion neu­
rons in the adult human neocorcex (Braengaard et al. 1990).
The mammalian neocorcex concains areas for cach sen­
sory m odality as well as mocor areas and areas associated
wich a variety o f cognitive and em otive functions. All co rti­
cal areas have six layers with an average total thickness o f
about 0 .2 6 cm , which is sim ilar in all mammals wich brain
volumes greater than about 3 c m ' (H ofm an 1 9 8 9 ). C ells in
che deepest layer (layer 6 ) p roject со che chalamus, chose in
layer 5 p roject to subcortical nuclei other than the thala­
mus, and chose in upper layers 2 and 3 projccc со ocher co r­
tical areas. Layer 4 is the main recipient layer. All cortical
areas have the same basic cellular consticuencs and show
evidence o f colum nar organization.
Across vercebrace species, brain weighc increases as a
power funccion o f body weighc (H ofm an 1989). The cere­
bral cortices ot small mammals, such as the mouse, are
sm ooth, or lisscnccphalic. If brains o f increasing size were
to remain similar in appearance, the surface area would
increase as the tw o-thirds power o f the volume. In fact, the
area o t the mammalian cerebral cortex increases alm ost in
proportion to its volume. This means thac che brains o f
larger mammals must fold in order со tie in to an econ om i­
cally sized skull— chey becom e gyren ccph alic. Thus, with
species ot increasing size the cerebral cortex becom es
increasingly folded into gyri (convolutions) and sulci
(grooves).
D uring the first h a lf o f the gestation period the human
cerebral cortex has very few gyri or sulci. A m ong the first
sulci to appear are the parieto-occipital and calcarine sulci
(Polyak 1 9 5 7 ). As the cortex grows, convolutions becom e
increasingly com plex.
Ac birch, che human brain as a w hole isonlyone-quarcer
o f ics macurc volume (Sauer ec al. 1 9 8 3 ). The volume o f the
adult human brain can vary becween abouc 1180 and 1625
c m 3, and that o f the n eocortex betw een about 5 7 4 and 8 2 9
cm \ w ithout any correlated variation in incelligence (Filipek
et al. 1 9 9 4 ). The human brain represents about 2% ot the
total body weighc buc accouncs for abouc 20 % o f the oxygen
consum ption ot the body.
The relative sizes and locations o f different regions o f
the neocortex are under the control o t several genes. For
exam ple, E M X I and PAX6 are expressed by neural progen­
itor cells in opposing gradients over the neocorcex before
thalam ic afferents invade che cortex (Bishop ec al. 2 0 0 2 ).
W e will see later that finer subdivisions o f the cortex are
determ ined by activity in afferent neurons.
The mammalian visual cortex, described in Section 5.5,
is part o f the convoluted surface o f che neocorcex. Before
birth in primates, and particularly in humans, the visual
cortex grows more rapidly than other parts o f the brain. At
birth it has reached about h alf its mature volume, which it
reaches abouc 4 m onths after birch. The adulc visual corcex
occupies abouc one-thirriech o f rhe cortical surface. The
visual cortex o f the human neonate is between 1.4 and 1.7
mm th ick, compared with betw een 2.1 and 2.5 mm in che
adulc (W ong-R ilcy e ta l. 1993).
The num ber o f ganglion-cells, n, and therefore che
num ber o f relay cells in the L G N , increases as the size o f the
eye increases. To m aintain con stan t visual resolution, the
num ber o f cortical processing units (hvpercolumns) should
increase in proportion to n. But ro m aintain constant angu­
lar resolution, the num ber o f cells in each hypercolumn
should increase by n vl. Therefore, the overall num ber o f
cortical cells should increase in proportion to n times « ' : ,
or n ' Stevens (2 0 0 1 ) found chac, over 2 3 primates includ­
ing humans, the num ber ot neurons in V I was proportional
to che 3/2 power o f the number o f L G N cells.
In the human visual cortex, cell density is over 1 m illion
per m m ' at 2 weeks o f gestation. Ic decreases со abouc 9 0 ,0 0 0
per m m ' at birth and to about 4 0 ,0 0 0 per m m ' at age 4
m onths. C ell density then remains stable (Lcuba and Garey
1987). 'I his loss o f cell density is due to overall growth, since
there seems со be no loss o f neurons in chc visual corcex
with aging.
6 .4 .2 b In trin s ic S p e c ific ity o f C o r tic a l A reas
D uring developm ent, che types o f cell inco w hich a cell may
develop becom e progressively restricted. The zygote is a
non-self-renew ing to tip o te n t cell because ic gives rise со
every cypc o f cell but docs n o t renew (unless ic forms frater-
nal cwins). C ells in differenc regions o f che em bryo becom c
specialized со produce the cells appropriace со chac region.
They are referred со as self-renewing m u ltip o te n t stem
cells, or siinplv stem cells. They divide со form ocher m ulti-
p o ten t cclls o r differentiate inco more specialized p ro g en i­
to r cells. 'I he progenitor cells for che ccntral nervous syscem
becom e further specialized into n cu ro b lasts, which form
neurons, and g lio b la sts, which form oligodendrocytes and
ascrocyccs (Delaunay ec al. 2 0 0 8 ).
These processes are controlled by various Sox tra n scrip ­
tio n factors. For example, chc S o x B l cranscription factors
induce seem cells со produce ocher stem cells rather than
differentiate, while m em bers o t chc SoxE group determ ine
the cvpe o f cell chat a seem cell form s (sec W egner and Scolc
2 0 0 5 ).
The human genom e concains chousands o f D N A
sequences chac produce RN A s chac do noc code for pro­
teins. These include transfer RN A and ribosom al R N A ,
which have imporcanc functions. However, ic had been
thought th at mosc noncoding RN A s are m olecular fossils
wich no function. Ic is now em erging chac many large n on­
coding RN A s inceracc wich cranscripcion faccors to control
em bryonic cell differentiation, including neural differentia­
tion (Guccman et al. 2 0 0 9 ).
N oncoding R N A s wich only 2 2 nucleotides arc known
as m icroR N A s, or m iR N A s. Their expression varies from
tissue to tissue and over che developmental sequence. They
bind со m R N A s and regulate chc cranslacion process chac
produces proteins (G u o cc al. 2 0 1 0 ). Som e m iR N A s pro-
m occ replication o f stem cells, while ochers prom ote differ­
entiation o f seem cells (M elto n cc al. 2 0 1 0 ). They are also
involved in neurogcnesis in chc subvencricular zone o t the
mamm alian brain (Seccion 6 .4 .2 d ). Also, m iR N A s are
cransporced со specific comparcmencs o f che dendritic fields
o f developing neurons, where they help to regulate den­
dritic growth responsible for synapcogenesis and synaptic
plascicity (see Seccion 6.6.1b ).
Studies involving che use o t tissue culture, cell lineage,
and ccll transplantation have shown that che em bryonic
nervous syscem exhibits laminar and regional specificities.
These arise from fam ilies o f procein m olecules (m orp h o­
gens) expressed ac specific tim es by specific groups o f genes.
The proceins in chc corcical place form densicy gradiencs
and spacial patterns before thalam ocortical atferencs arrive.
G enes expressing m orphogens are curned on by cran­
scripcion faccors known as hom eoproceins expressed by
mascer genes, known as hom eogenes (see Seccion 6 .4 .1 ).
There are at lease 25 hom eoproceins expressed in rhe em bry­
o n ic forebrain. In addition, several nonhom eogcne cran­
scripcion faccors are expressed in specific regions and layers
o f the developing cerebral corcex (B u lfon e ec al. 1995).
Particular progenitor neural cells are genetically
programmed со produce proceins specific to a particular
cortical area at a ccrtain period, in che absence o f influences
trom the surroundings o f the cells. For example, progenitor
cclls from chc presumpcive lim bic syscem express a specific
genetic factor after they have been isolated in vitro (see
Section 6 .6 .1 ). In vertebrates, n eu rogen ic genes similar со
those concrolling neurogcnesis in invereebraces, co n tro l the
specification o f different cortical areas and ccll types.
A second m echanism o f cell differentiation depends on
asymmetric ccll division in which daughter cclls express d if­
ferent quantities o f regulatory proteins to form a chem ical
gradient (Lew is 1996). C hem ical gradients over growing
axons arc reciprocally m atched to gradiencs in receptor
regions. This is known as the “handshake” m odel ot
developm ent.
6 .4 .2 c In flu e n c e o f T h a la m o c o r tic a l In p u ts
For some progenitor cells, there is a critical period during
which they can adopt the m orphological and chem ical fea­
tures characteristic o f a cortical area into w hich chey have
been transplanted (see Levitt e t al. 1997). Thus, the detailed
structure o f intracortical connections, in parcicular che
recepcive-field structure o t neocortical sensory areas, seems
to be determ ined by thalam ic sensory inputs rather than by
intrinsic properties ot progenitor cells.
Frost and M etin (1 9 8 5 ) induced visual atferencs o f neo-
nace hamscers eo innervate rhe growing somatosensory
cortcx. Visual stim ulation in the mature animals revealed
cells in che somaeosensory corcex wich well-defined recino-
copically organized receptive fields resem bling those in the
norm al visual cortex. Late em bryonic cells destined ro form
pare o f the visual cortex ot the rat, acquire somatosensory
inputs when transplanted into the developing som atosen­
sory area. Consequently, a piece ot transplanted visual
cortex formed chc arch itectonic features characterised o f
the som atosensory cortex. Thus, somatosensory inputs to
the foreign piecc o f visual co rtcx determ ined the character­
istics o f that piece o f cortex (Schlaggar and O ’Leary 1991).
Visual atfcrents o f neonate ferrets have been induced
to innervate the auditory thalamus and cortex. Visually
responsive cells in the auditory cortcx formed a retinotopic
map. They showed orientation and direction selectivity and
simple and com plex receptive field organization, although
their receptive fields were larger than those o f cells in the
visual cortcx. The cells were less sensitive than cclls in the
visual corcex (R o e ec al. 1992). Ferrers reared with a rewired
auditory cortex in one hemisphere and a norm ally wired
cortex in the other hemisphere responded to visual stimuli
directed to the rewired auditory cortex. However, the co n ­
crasc sensitivity o f che rewired auditory cortex was lower
chan that ot the normal visual cortex (von M elchner et al.
2000 ).
Thus, che rcccptive-ficld structures o f diticrcnc areas o f
the neocorcex are determ ined by the identity o f cells that
migrate into them trom the thalamus rather than by the
identity o f cells ascending from the ventricular zone.
However, the co rticoco rtical and efferent con nections o f
the visual cortex are n o t much affected by cross-modal
m anipulations (see Sur et al. 1 990). Thus, the efferent co n ­
nections o f the visual cortex arc specified before the devel­
opm ent o f cortical layers or thalam ic inputs.
Adult fish and am phibians arc able to restore cortical
con n ection s after rhe optic nerve has been cur (Sperry
1951). G anglion-cell axons regenerate and find co rrect co n ­
nection s in the tectum . This docs not involve the creation
o f new ganglion cells {Beaver et al. 2 0 0 1 ). If the cu t ends of
am phibian optic nerves are grafted onto rhe ipsilateral optic
tract they torm con nection s with the ipsilateral tectum .
After recovery, the animals exh ibit reversed optokinetic
nystagmus and m irror-im age reversal ot movements in
response to prey (Sperry 1 945). The adult visual tectum o f
fish and am phibians treat the crossed inputs as if they
originated in the eye that norm ally innervates that cortical
hemisphere.
6 .4 .2 d N c u ro g c n c s is an d R e p a ir in A d u lt
N e rv o u s svstem s
Ncurogcncsis can be detected in the central nervous system
by first labeling neurons with a neuron-specific marker and
then applying an agent (B rd U ), w hich labels D N A during
cell division. C ells carrying both labels m ust be dividing
neurons.
T h e retinas o f adult fish, am phibians, and birds contain
mulcipotent stem cells that are capable o t regenerating dam­
aged recinal neurons (Fischer and Reh 2 0 0 1 ).
M ultipotcnt stem cells occur in various regions o f the
brains ofad ulrrodcnrs, including the hippocam pus(Tashiro
et al. 2 0 0 6 ), spinal cord, olfactory bulb (Livnch et al. 2 0 0 9 ),
and chc lining o f the ventricles. A pplication o f growth fac­
tors induces these cells to differentiate into neurons or glial
cells in vivo and in vitro (Reynolds and Weiss 1 9 9 2 ; M cKay
1997). Neurogenesis is inhibited by the transcription factor
Sox9. A noncoding RN'A (m iR -1 2 4 ) regulates the expres­
sion ot S ox9 (C h e n g e t al. 2 0 0 9 ). Neurogenesis is controlled
by the balance o f these two factors.
Pharm acological suppression ot neurogenesis in the
hippocampus o ft h e adult rat impaired associative learning
(Shors et al. 2 0 0 1 ). Stem cells in the ventricular lining o f
the brain o fth e adult mouse rarely divide in norm al animals
but divide rapidly after spinal cord injury (Johansson e t al.
1999). It seems that m icroglia guide m igrating stem cclls to
a damaged area (Aarum et al. 2 0 0 3 ).
There has been a debate about whether ncurogcncsis
occurs in the neocortex o f adult subhuman primaces (R akic
19 8 5 ; Bourgeois et al. 1 994). Gould et al. (1 9 9 9 ) produced
evidence that, in adult macaques, new neurons are con tin u ­
ally produced in the subventricular zone of the pretrontal,
posterior parietal, and inferior Temporal areas, bur not in
the striate cortex. However, neither Kornack and Rakic
(2 0 0 1 ) nor Koketsu et al. (2 0 0 3 ) could find any newly p ro ­
duced neurons in the neocortex o f the macaque. Like other
investigators, they found new neurons only in rhe hip­
pocampus and olfactory bulb. O th er evidence, reviewed by
Au and Fishell ( 2 0 0 6 ), argues against neurogenesis in the
primate neocortex.
There has also been some dispute about whether neu ro­
genesis occurs in postnatal humans. Shankle et al. (1 9 9 8 )
analyzed some earlier anatom ical data and concluded that
the num ber o f cortical neurons more rhan doubles between
the ages o f 15 m onths and 6 years. However, Korr and
Schm itz (1 9 9 9 ) questioned the assumptions underlying
their analysis and concluded that it provides no evidence ot
postnatal ncurogcncsis in the hum an cerebral cortcx.
Stem cells from the human em bryonic torebrain propa­
gate in vitro and differentiate to form neurons or glial cclls,
but it is n o t known w hether stem cells are present in the
central nervous systems o f adult humans (C arpenter et al.
1999; Korr and Schm itz 1999).
Severed neurons in the central nervous system (C N S )
in many lower vertebrates, including new ts and salaman­
ders, regenerate and find their way back to their original
destination. Also, the central nervous system o f very young
mammals and birds is capable o f substantial repair after
damage. However, damaged neurons in the C N S o f adult
mammals do n o t regenerate. Severed axons form character­
istic retra ctio n b u lbs surrounded by glial scar tissue and
the debris o f myelin sheaths. O n the other hand, severed
4
axons in the peripheral nervous system (P N S ) o f adult
vertebrates, including mammals, may regenerate.
Several factors could account for rhedifference between
the regenerative capacities o f C N S and P N S neurons in
mammals. Th e myelin sheaths o f PN S neurons are derived
from Schwann cells, while those o f the C N S are derived
from oligodendrocytes. After neuronal damage, the debris
of myelin sheaths in the C N S remains for a much longer
tim e than myelin debris in the PN S. It seems that the myelin
scar tissue surrounding severed C N S axons produces chem ­
icals that inhibit regeneration. These chem icals may include
guidance m olecules such as nctrin and ephrin that repel
axon growth (see Case and Tessier-Lavigne 2 0 0 5 ).
The cerebral cortex is reviewed in M ountcastle (1 9 9 8 ).
6 .4 .3 M E C H A N IS M S O F A X O N G U I D A N C E
This section reviews the m echanism s that guide, accelerate,
or retard the growth o f axons in the central nervous system.
Axon growth occurs at the growth cone at the tip o f the
axon.
The direction o f axon growth is partly determ ined by
the physical structure o t the extracellular matrix. Also, car­
tilage and other tissues form barriers chat guide axonal
growth. Extracellular spaces in em bryonic neural tissue
form channels through which neurons migrate or axons
grow. However, we will see that growing axons are mainly
controlled by a variety o f protein ligands secreted by cclls in
the extracellular matrix or by the area toward which the
axon is growing. Som e cclls act as guide-post cclls that guide
axons at each o f a series o f choice points or indicate where
synapses should form . O th ers provide a scaffold along
which growing axons progress. See C hao e t al. (2 0 0 9 ) for a
review o f the role o l cell interactions in axon guidance.
Each ligand from a guidepost or scaffold cell binds with
a specific receptor on the axon. The bound receptors
undergo a conform al change thac activates a procein kinase
enzyme. This results in the receptor being tagged with a
phosphate group. Som e ligands bind che axon со che extra­
cellular matrix. Som e attract the growth cone while others
repel it. Som e accelerate axon growch while ochers cermi-
nace ic. Som e phosphorylaced receptors trigger a cascade o f
chem ical events chac spreads down che axon со che cell
nucleus. There, the signals evoke genes to express proteins
required for cell grow th. The proteins are conveyed along
tubules in the axon to where thevф are needed. M olecular
signals in growch cones has been reviewed by Huber ec al.
(2 0 0 3 ).
The variety and com plexicy o f chese processes is bewil­
dering. Tliis chapccr provides only an outline o t som e ot
chese processes.
6 .4 .3 a T h e G ro w th C o n c
Grow ing axons and dendrites form grow th co n es trom
which extend weblike la m ellip o d ia and finger-like
filo p o d ia. These extensions are several m icrom eters long.
They form and retract on a m inute-by-m inute time scale, as
depicted in Figure 6 .1 4 (Portera-C ailliau et al. 2 0 0 3 ).
Filopodia control che race and direccion o f axon growch
and branching. Pioneer axons have several radiacing filopo­
dia chat dececc m olecular markers in che surroundings.
Axons growing along a pach marked ouc by pioneer axons
have fewer filopodia. W h en an axon encouncers an obstacle,
ics grow th co n e collapses and lateral elements develop from
the axon and from trailing axons in the same fasciculated
bundle. Som e elem ents develop into new growth cones
(D avenport et al. 1 9 9 9 ). These events can be observed by
time-lapse photography o f fluorescent growth cones
(H alloran and Kalil 19 9 4 ; Mason and W ang 1997).
Filopodia also form on growing dendrites during synapto-
genesis. This topic is discussed in Section 6.4.4.
Exposure o f one side o f a growth cone to attractive cell
adhesion m olecules produces an increase in calcium ions on
that side. Thus the initial signal is an asymmetrical release o f
calcium ions in chc growth cone. Neuronal growth stops it a
blocking agent depletes the store o f calcium ions (Takai
et al. 1 9 9 8 ). The role o f calcium in neural developm ent was
reviewed by W ong and G hosh (2 0 0 2 ).
Tojim a et al. (2 0 0 7 ) observed the effects o f an asym­
metrical release o f calcium ions into growth cones on an
attractive substrate ( L I , N G F, or M A G ). W ith in a period
1 mn
A В
Fi&«rc6 .14. M obility o f dendriticJU opodia. (A ) A pyram idal n eu ron in the
visual c o rtc x o f a 2-day-oId m ouse im aged by tw o -p h o to n m icroscopy.
'Ih c in set area is show n m agnified in (b ). ( B ) Fram es from a tim e-lapse
video show ing the m in u tc-to -m in u tc m ovem en t o f filop od ia on a single
d en d rite. Ih c filopodia tend to clu ster around the grow th co n c a t the
tip o t the d en d rite. < г « .т P o m r * Л . 200 * )
o f 1 m inute, vcsiclcs rapidly migrated along m icrotubulcs
into that region o f che growth cone m em brane where cal­
cium ions had been released. This produced some curning
in chat direction. They suggested chac insertion o f new
material in to the mem brane produces an asymmetrical dis­
tribution o f chem icals and causes the m em brane to expand
asymmetrically. D uring chc initial period chcrc were no
changes in the dynamics o f m icrotubules or in the num ber
or length o t filopodia. Calcium ions released asymmetri­
cally into growth cones on a repulsive substrate (lam inin)
had no effect on vesicle transport. Thus, in the initial period,
asymmetrical insertion o f material inco che cell mem brane
is involved in grow ch-conc actraction but noc in growth-
cone repulsion. A few minuces after reception o f signals,
growth cones com e under the control o f cytoskclctal
dynam ics, as we will now see.
Filopodia and lamellipodia contain actin filam ents,
w hich arc assembled by polymerization o f actin m onom ers
at the distal end o f che growth cone. Filam ent assembly is
controlled by agents known as actin n u clcators (Pak cc al.
2 0 0 8 ). Tlie filam ents self-assemble into meshlike patterns
in lam ellipodia, inco linear bundles chac extend along
filopodia, or into arclike structures. The actin filam ents flow
ac a vclocicy o f abouc 100 jun/min со chc proximal region o f
che growing con e, where the polymer chain is disassembled
into m onom ers, which arc rccvclcd. The proccss is known
as che accin tread m ill. The turnover tim e o f actin filaments
in hippocam pus neurons is about 4 4 scconds (Star c t al.
2 0 0 2 ). Th e net rate o f growth cone advance is determ ined
by chc balance betw een actin fiber assembly ac che tip o f the
cone and actin fiber m igration away from the cone. W hen
the growch co n c advances, polymerization o f accin filamencs
increases and retrograde actin flow decreases. The opposite
effects accom pany conc recraccion. Accin circulacion is
attenuated during cone advance because the actin filaments
becom e anchored to the cytoplasm ic dom ains ot cell sur­
face m olecules, such as N -cadherin, which in turn are
anchored by their extracellular dom ains to the fibrous extra­
cellular matrix (Lin and Forscher 1995; Sutcr cc al. 1998).
The rate ot growth cone advance is correlated with the
m echanical coupling betw een N-cadherin receptors
(catenins) and retrograde actin flow (Bard e t al. 2 0 0 8 ).
This know n as the m o lecu lar clu tch m echanism .
If the growth cone becom es attached to the extracellular
matrix on one side, it grows in that direction. W h ile the
shaft o f the growing filopodia is attached to the extracellu­
lar matrix, lam ellipodia (veils) develop that control the
direction o f growth cone advance (Stcketec and Tosncy
2 0 0 2 ). Thus the m olecular clutch m echanism regulates the
form ation and m ovem ent o f filopodia and lam ellipodia and
determ ines the direction o f axon growth. This activity can
be observed in living neurons by coupling a green fluores­
cent protein (G F P ) to proteins that bind the niicrotubules
to the substrate (Stepanova et al. 2 0 0 3 ). The processes are
depicted in Figure 6 .1 5 . Axon growth differs from chc pro­
cess ot m igration o f neurons described in Section 6.4.5b.
Behind the actin filaments, a parallel bundle o f m icro -
tu bu les form s as a cytoskeletal netw ork chat extends down
the length ot the axon. Substances required tor axon growth
are transported along the niicrotubules in in tracellu lar
vesicles to the tip ot the growing axon or dcndrice
(M artenson c t al. 1 993).
Each m icrotubule is form ed in the growth co n c by
polym erization o f tubulin m olecules into a linear array.
G rowth
M ic ro tu b u le s ^ ^D isa sse m b ly f jj^ e n ts
P rolein
"7
C ell adhesion m olecule
E xtracellular matrix
F i*m с 6.i*. A dvance o f л g r v w ih м н е, C c ll ad hesion m olecu les em bedded
across rhe ccll m em brane o f t h e grow th c o n c a ttach to j»lvcoprotcins
o n chc extracellular m atrix. P rotein m olecules link the ccll adhesion
m olecu les to accin filam ents in chc g row th co n e. A s che grow th c o n c
advances, th e retrograd e flow o t th e filam en t netw ork is atten u ated and
the m icro tu b u lcs m ove forw ard w ith the grow th co n e. ( К с Л гд м a tr<>rn I
(Ч нясЬо 1^ $ )
As the axon grows, the m icrocubulcs extend into the lam el­
lipodia and filopodia. They then consolidate to torm a new
segment o f the growing axon or new dendritic spines. W hen
a growth cone retracts, the niicrotubules depolymerize and
retract. The m icrotubulc cvtoskelcton determ ines the final
shape o fth e dendritic spine.
Tim e-lapse m icroscopy in cultures o f cortical neurons
from mature m ice revealed that niicrotubules rapidly
polymerized and extended inco dendritic spines and filopo­
dia and then, after a few m inutes, depolymerized and
retracted (H u et al. 2 0 0 8 ). They extended into only a small
percentage o f spines at a given time. O n e and som etim es
two m icrotubulcs moved into a spine from either the proxi­
mal or the distal end o fth e dendrite. This would allow them
to deliver proteins from the soma or from the end o f the
dendrite. The num ber and duration o f intrusions increased
when the cell culture was stimulated with K C I and decreased
when activity was reduced by tctrodotoxin. These activity-
dependent intrusions could be involved in torm ing and
m aintaining spines in learning and synaptogenesis.
Inhibition o t m icrotubule dynamics reduced the num ber ot
dendritic spines (G u c t al. 2 0 0 8 ).
M icrotubules control the movements o f actin filaments.
Extracellular m olecules no longer attract or repel growth
concs when m icrotubulc activity is pharmacologically
blocked. Furtherm ore, application o f a drug that stabilizes
niicrotubules on one side ol a growth cone causes the cone
to grow in that direction (Buck and Zheng 2 0 0 2 ). W c shall
see that the activity o f actin filam ents and m icrotubulcs is
governed by gradients o f many intracellular and extracellu­
lar proteins. Som e are actraccants, while others are repel­
lents (sec D ent and G ertier 2 0 0 3 ).
Thus, che speed and direccion o f a growth conc is u lti­
mately determ ined by the magnitude and asymmetry o f
cytoskeletal dynamics controlled by receptors on the sur­
face o f the grow th cone. However, these processes take time
to develop. W e will now see chat the initial response o f a
growth cone is influenced by asymmetrical expansion o fth e
outer m em brane o f the growth conc.
6 .4 .3 b C e ll A d h e s io n M o le c u le s ( C A M s )
Axons grow along a substrate formed by pioneer cells, radial
glial cells, astrocytes, and the extracellular matrix. Each
growth cone possesses a rich array o f cell adhesion m ole­
cules (C A M s). These are receptors that bind with ligands
expressed by glial cells on the extracellular matrix. Som e
receptors anchor che growch cone to the substrate by bind­
ing to ligands secreted by the substrate. O th er receptors
respond to ligands that determ ine which pach the growing
axon will take.
The ligands produced by glial cells on rhe extracellular
matrix arc g ly co p ro tein s. They include n c trin , lam in in ,
i n Jfl«i
fib ro n e ctin , and ten a.vein secreted by astrocytes (a type
o f glial cell) (Sanes 1 9 8 9 ; D ityatev and Schach ncr 2 0 0 3 ).
The extracellular matrix is substantially rcduccd after
growth ot the nervous system is com plete.
A ctivation o f cell-surface receptors by glycoproteins
controls the polymerization and backward circulation o f
actin filam ents from their assembly point at the tip o f
the growth cone to the place where they are disassembled
(Luo 2 0 0 2 ).
Som e glycoproteins on the extracellular matrix are
attr actants. O thers are repellents and create exclusion zones
from w hich axons are deflected (P in i 1 9 9 3 ). Som e glyco­
proteins attract some axons and repel others (see Tcssier-
Lavigne and G oodm an 1 996). A ttractants prom ote actin
polym erization, while repellents decrease it. A ntibodies o f
glycoproteins in h ib it axonal growth (C oh en c t al. 1986).
Filopodia o f a growth cone observed under the m icroscope
in vitro collapse com pletely when chem ical repellents arc
applied (Fawcett 1993).
G lycoproteins may also have enzymatic or proteolytic
properties that m odify the extracellular medium in which
growth concs move (P ittm an 1985).
The type o f glycoprotein m ost active in a given cortical
region may change over time (C oh en e ta l. 1986). F.xposurc
to a growth factor can alfect subsequent responses to the
same growth factor (D iefenbach c t al. 2 0 0 0 ). Also, as an
axon grows trom one cellular environm ent into another, the
type o f extracellular glycoprotein to which it responds
changes because ot intrinsic changes within the growth
co n e (sec Dodd and Jcssell 19 8 8 ; S o n g c t al. 1997). Thus,
growth cones encounter a com plex spatiotem poral pattern
o f chem ical influences as they m igrate through the extracel­
lular matrix (see Letourneau et al. 1 9 9 4 ).
Som e extracellular glycoproteins, such as lam inin and
fibronectin, appear only during neurogenesis in mammals
but remain in animals, such as fish and frogs, which are able
to regenerate the optic nerve. O th er molecules, such as
tenascin, remain in the adult mammalian brain. Interactions
betw een extracellular m olecules and ccll adhesion m ole­
cules are involved in long-term potentiation (Section
6 .4 .4 f) underlying learning in the adult brain (see Jon es
1 9 9 6 ; M ueller 1 999).
Specific glycoproteins bind to specific ccll adhesion
m olecules (R eichardt 1 992). The receptors tall into at least
three families: cadherins, integrins, and immunoglobu­
lins. Each m olecule has an extracellular dom ain and a cvto-
plasmic dom ain linked by a transm em brane segment. The
extracellular dom ain determ ines specific connections o u t­
side the axon, and the cytoplasm ic dom ain interacts with
the cells cytoskelcton to determ ine the shape and m otility
o fth e growing cell. Integrins are localized on regions o fth e
cell m em brane that are d istin ct from the regions containing
cadherins and im m unoglobulins (N akai and Kam iguchi
2002 ).
C a d h e rin s are a supcrtamily ot transm em brane pro­
teins that m ediate a wide range o f cellular interactions
during neurogenesis and in the adult brain. Their role in
cortical synaptogcnesis is not fully understood but they
presumably help to label cortical dom ains so that growing
axons recognize them.
Three subfamilies ot cadherins have been identified, but
there arc probably many m ore. The extracellular dom ain o f
acadherin m olecule varies w ithin subfamilies and the intra­
cellular, or cytoplasm ic dom ain varies between subfamilies.
Each type o f cytoplasm ic dom ain triggers a distinct type o f
reaction in the cell. Wu and M aniatis (1 9 9 9 ) identified 52
human cadherin genes in three clusters, each with a co n ­
stant region, coding a cytoplasm ic dom ain, and a variable
region, coding extracellular domains. They speculated many
types o f cadherins are created in neurogenesis by rearrange­
m ent o f variable D N A regions relative to constant regions,
in the same way that the im m une system generates a m ulti­
tude o f T -cell receptors and im m unoglobulins. The great
variety o f cadherins and their extracellular binding
m olcculcs could ensure that synapses arc formed between
specific cells.
N -cadherins provide a signal that stops thalam ocortical
axons when they reach cortical layer 4 . Som e cadherins arc
expressed in the cerebral co rtcx o f mice lacking thalam ocor­
tical projections (M iyashita c t al. 1999). Thus, these intrin­
sic m olecular markers specify the basic organization o f the
visual cortex independently o f visual inputs.
The differential expression o f o ther cadherins and other
genetic growth factors is n o t evident until after thalam ocor­
tical axons have invaded the developing co rtcx (Nakagawa
ct al. 1999). These factors arc responsible lor the influence
o f thalam ocortical inputs on the developm ent o f the visual
cortex. In animals blind from birth, auditory and tactile
inputs invade the visual cortex and m odify its basic archi­
tecton ic structure (see Section 8 .1 .4a). Th e role ofcadherins
in synaptogenesis is discussed in Section 6.4.4.
Integrins are the second family o f transm em brane
receptors on growing neurons. There are at least 25 integ­
rins. Each is a receptor for specific sim ilar (hom ophilic
binding) or dissimilar (hcterop hilic bind ing) molecules on
the extracellular matrix or on adjacent ccll membranes.
Thus, the cell adheres to another ccll or to the extracellular
m atrix, and signals carricd to the interior o f the ccll guide
its growth.
Cell-surface receptors carry signals from the extracellu­
lar binding site to the cytoplasm ic dom ains inside the cell
(C hallacom be c t al. 1996). These signals converge onto
sm all protein m olecules that belong to a superfamily known
as G T I ’ases. Som e o f these m olecules help axons adhere to
the substrate. O thers stimulate axonal growth by decreasing
the retrograde flow o f actin while others inhibit growth by
increasing actin flow. Som e induce the growth cone to co l­
lapse. Signals also travel to the soma o t the growing neuron,
where they control gene expression o f proteins involved in
m orphogenesis (Palecck et al. 1997; Luo 2 0 0 2 ).
Immunoglobulins are a third family o f cell adhesion recep­
tors on growing neurons. A subgroup ot immunoglobulins.
known as M A G occurs in myelin and glial cells. M A G pro­
m otes axonal growth in the em bryo but inhibits growth
postnatally. This sw itch is accom panied by a decrease in
A M P receptors (C ai e t al. 2 0 0 1 ). Thus, M A G is responsible
for the inability o f mature axons to regenerate.
Signals conveyed by different receptors may interact.
For example, signals conveyed through cadherins interact
with those conveyed through integrins (Lilicn e ta l. 1999).
6 .4 .3 c S h o r t-R a n g e G u id a n c e M o lc c u lc s
Short-range guidance m olecules that determ ine the direc­
tion o f axon growth originate w ithin the tissue through
which the neuron is growing. A growth conc is very sensi­
tive to side-to-side differences in concentration o f guidance
molecules. Such differences alter the side-to-side balance ol
filopodia and hence determ ine which way the axon grows.
Long-range agents originate lrom a more distance source.
They arc discussed in the next section.
There are four main fam ilies o f short-range guidance
molecules. These arc:
1. Ephrinsand their Eph receptors.
2. N etrins and their U N C 5 receptors.
3. Scm aphorins and their neuropilin receptors.
4 . Slits and their roundabout (R o b o ) receptors.
G row ing axons com e under the co n tro l o f different short-
range guidance molecules at different times and at different
positions along the growth path. Particular m olecules are
delivered from the endoplasm to the ccll m em branes o f par­
ticular growing neurons by a process o f exocyto sis. W h en
they arc no longer required, they arc returned to the end o­
plasm by a process o f cn d o cy to sis.
R eceptor molecules span the ccll m em brane to form an
extracellular com pon ent and an intracellular com ponent.
At certain tim es, growth cones secrete proteases that cleave
these com ponents and thereby release the intracellular com ­
ponent into the ccll interior, where it travels to the ccll
nucleus and regulates the expression o f particular genes.
This m echanism is discussed in m ore detail later.
Ultimately, guidance m olecules direct growth cones by
controlling the dynamics o f the m icrotubules and actin fila­
ments in the growth cone, as described in Section 6.4.3a.
Thcv/ do this through
w the mediation o f the Rho family
/ ot
guanosine triphosphatases (R h o G T P a s e s ) (see O ’D onnell
c t al. 2 0 0 9 ).
E p h rin s consist o f cphrin-A and cp hrin-B ligands,
which bind selectively to p ro tein ty ro sin e kinase recep ­
to rs, known as F.phA and EphB respectively. Because both
the ligand and its receptor are anchored to ccll membranes,
they arc able to guide particular cells to particular locations.
Ephrin/Eph com plexes transm it signals both into and o u t
o f the cell, a process known as forw ard and reverse sig n al­
ing. There are several numbered subtypes o f each receptor-
ligand class. They are involved in the developm ent o f many
body tissues in vertebrates, including the neuromuscular
system and the visual system (W ilkin son 2 0 0 1 ). They are
involved in the developm ent o f the retina (Section 6 .3 .2 ),
chiasm (Scctio n 6 .3 .4 ), and L G N (Scctio n 6 .3 .5 ).
In fish, Ephrins are involved in guiding axons growing
from cach sensory area of the thalamus to their proper des­
tinations in the tectum . For example, in zebra fish they
guide visual afferents to their target cells in the tectum
(Brennan c t al. 1997).
The neurocpithelium and radial glial ccllso f the chicken
tectum express a high dorsal to low ventral gradient o f
ep h rin -B l ligand during the tim e when afferent axons are
grow ing into the tectum . This gradient m atches a com ple­
m entary gradient o f Eph receptors in the afferent axons.
These two interacting gradients guide axons to their desti­
nations in the tectum along the ventral-dorsal axis. A gradi­
ent o f the ligand ep hrin -B 2 in deeper layers o f the tectum
may control developm ent o f lam inar patterning in the
tectum (Braisted c t al. 1997).
The ligands ephrin-A 2 and ephrin-A5 form an anterior-
posterior gradient w ithin the chickcn tcccum. A com ple­
m entary gradient o f EphA receptors derived from the retina
helps to guide axons to their destinations along the anterior-
posterior axis (H ansen et al. 2 0 0 4 ). In low concentration,
EphA receptor m olecules are attractants. In high co n cen ­
tration, they are repellents.
Axon tracing in normal and m utant mice has revealed
that ephrins control the cortical area ro which axons from
different sensory areas o f the thalamus project. The ephrins
occur in the internal capsule in the ventral telencephalon
through which the growing sensory axons pass on their way
from the thalamus to the cortcx. In this region, a rostral-low
to caudal-high gradient o fep h rin -A 5 ligands m atches co m ­
plementary gradicntsofEphA receptors in the thalamic axons
(D ufour c t al. 2 0 0 3 ). This process results in an anterior-
posterior mapping o f the growing axons. This same region
contains a gradient o t the genetic transcription factor
( Ngn2), w hich specifies the responsiveness o f axons to guid­
ance factors (Seib t c t al. 2 0 0 3 ).
EphA receptors are also involved in establishing the
retinotop ic mapping in the superior colliculus o t the mouse
(Brow n c t al. 2 0 0 0 ).
D onoghue and R akic (1 9 9 9 ) used D N A probes to
exam ine the distribution o f ephrins in slices o f macaque
visual cortex at days 6 5 ,8 0 , and 95 o f the 165-day gestation
period. They found that som e m em bers o f the EphA/
ephrin-A class o f molecules are expressed in different pat­
terns in the em bryonic cortical plate, co rtical lam inae, and
cv toarchitccton ic cortical zones before the arrival o f thal-
am ocortical afferents. For example, when cells arc prolifer­
ating in the ventricular zone and m igrating ro rhe cortical
plate (day 6 5 ), EphA 6 is expressed in the region o f the
cortical plate corresponding to chc future visual cortcx, and
EphA 3 is expressed in the region corresponding to layer 4
o fth e future extrastriate cortex.
O th er EphA/ephrin-A m olecules are expressed or
becom e differentially distributed in the cortical plate only
after the arrival o f thalam ocortical axons (day 8 0 - 9 5 ) . For
exam ple, ephrin-A5 becom es concentrated posteriorly and
ephrin-АЗ anteriorly during this period. In som e cases, cells
that becom e linked by Eph receptors and ephrin ligands
break apart in about 3 0 m inutes and then repel each other.
The break occurs because the ephrin molecules are cleaved
by a transm em brane protease that is coexpressed with
cphrin-A 2 (H atto ri et al. 2 0 0 0 ).
The ephrin-B I ligand appears in the cortical neuroepi­
thelium at the onset o l neurogenesis and declines when it is
com plete. The ligand is expressed on radial glial cells and
form s a high-to-low gradient between the ventricle and pial
surface (Stuckm ann ct al. 2 0 0 1 ). EphB receptors also regu­
late the developm ent o f dendritic spines and synaptogencsis
(see Section 6 .4 .4 b ).
Interactions between glial cells and neurons mediated
by EphA 4 and its ligand ephrin-АЗ are involved in the reg­
ulation of dendritic spines. The mapping o f visual inputs
o n to the visual cortcx is degraded in m ice that arc geneti­
cally deficient for ephrins-A 2, -A 3, and -A 4 (G ang et al.
2 0 0 5 a ). Ephrin-A s and retinal activity contribute to the
developm ent o f topographic maps in both the colliculus
and visual cortcx o f m ice (Pfeitfenbcrger et al. 2 0 0 6 ).
There is thus a considerable econom y in the way the
same m olecular markers are involved in different wavs i at
different stages o f developm ent and in different locations.
N ctrin sa rc ligands produced by thecxtracellular matrix.
W e have already seen that they act locally to bind the growth
cone to the extracellular m atrix. But netrins also diffuse sev­
eral m illim eters from their point o f origin and serve to
guide growing axons. Netrins act as attractants for some
axons and as repellents for o ther axons, depending on the
receptors in the growth cone. Also, for a given growing
axon, nctrin can change from an attractant to a repellent.
For example, N ctrin-1 attracts ganglion-cell axons into the
optic nerve and then acts as a repellent to prevent them
from leaving the nerve. This change can be initiated by
decreased neural activity at A M PA synapses. Increased
neural activity induces the opposite change (M in g et al.
1997). Nctrin-1 also prom otes the growth o f thalam ocorti­
cal axons. Asymm etric binding o f N ctrin -1 to the growth
cone induces axon turning. Like other ligands, they
stimulate genes in the growth co n e to express proteins
(see Barallobre et al. 2 0 0 5 ).
S cm a p h o rin s are a large family o f cell-surface and extra­
cellular diff usible proteins that repel or attract growth concs
by activating rhe membrane receptor n eu rop ilin . Sem a-
phorin 3 released from the marginal zone of the developing
cortex regulates the growth o f pyramidal cells toward the cor­
tical white matter by acting as a repellent. But semaphorin-3
from the pial surface o f the cortex attracts dendrites o f pyra­
midal cclls. Thus, the same ligand-rcceptor pair has op p o­
site effects on opposite ends o f pyramidal cells. The
difference is due to an asymmetrically localized enzyme in
growing pyramidal cclls (Pollcux et al. 2 0 0 0 ). W e will see in
Section 6.4.5a that scm aphorins arc also involved in guid­
ing em bryonic neurons to their target layer in the cortex.
S lits are large secreted proteins that occur in various
regions o f the growing nervous system o f many animals,
including insects, fish, and mammals. There are three main
S lit ligands (S lit 1, Slit 2, Slit 3 )c a c h w ith a Roundabout, or
R o b o , axon receptor. They form a general inh ibitory system
that prevents ganglion-cell axons from invading inappro­
priate areas o f the thalamus, hypothalamus, superior co llic­
ulus, chiasm , and corpus callosum (N iclou et al. 2 0 0 0 ;
Ringstcdt c t al. 2 0 0 0 ). The different types o f Slit ligands are
expressed in different places and at ditferent tim es during
developm ent (Erskine c t al. 2 0 0 0 ). Their role in the devel­
opm ent o f the optic chiasm was discussed in S ection 6.3.4.
6 .4 .3 d L o n g -R a n g e and A x o n G u id an ce
As an axon approaches to w ithin about 3 0 0 jun ot its target
ccll in the thalamus or co rtex the action o f glycoproteins
secreted by the extracellular matrix is switched off, and
the growth cone com es under the control o f diffusible
n cu ro tro p h in s secreted by the target cell (see K orsching
1993; Lindsay et al. 1 9 9 4 ; C hao 2 0 0 3 ). It is n o t known
w hether this change is mediated by the neurotrophins o r by
an intrinsic tim ing mechanism in the growing axon.
N eurotrophins arc a family o f four related proteins:
nerve grow th fa c to r (N G F ), b rain -d eriv ed n eu ro tro p h ic
fa cto r (B D N F ), and neurotrophins N T -3 and N T -4 / 5 .
The N G F is restricted to specific areas ot the central ner­
vous system while the o ther factors arc more widely distrib­
uted. N eurotrophins peak in the neonatal period ot neural
developm ent.
Rita Levi-M ontale ini and Stanley C o h en , in the labora­
tory o f V icto r Hamburger in St. Louis, discovered the first
neurotrophin, the nerve grow th facto r. They were led to
the discovery by noting that deletion o f target tissue reduced
the survival o f m otor and sensorv neurons. I.cvi-M ontalcini
and C ohen received the Nobel Prize in 1 9 8 6 (see Robinson
2001 ).
N eurotrophins are produced by neurons, glial cells, and
fibroblasts. Som e neurotrophins are released into the extra­
cellular m atrix, w hile others remain bound to ccll m em ­
branes (K atz and Callaway 1992). Agents secreted by
neurons modulate the secretion o f ncurotrophins. O t par­
ticular im portance is the fact that rhe production o f B D N F
in particular synapses can be m odulated by stimulus-
induced synaptic activity (see Section 6.5.1c).
G row ing axons produce one or more cell-surface pro­
teins, each o f which is a receptor for one or m ore neurotro­
phin. These are the n eu ro tro p h in recep tors. There are two
main types— chc cvrosinc recepcor kinases, or T rk re ce p ­
tors, and the p 7 5 receptor (Barbacid 1994; Lewin and
Barde 1 996).
Trk receptors are high-affinity receptors, which means
that each one binds with a specific neurotrophin. They are
expressed by trk genes at the appropriate tim e during devel­
opm ent. ТгкЛ binds with N G F , T rkB binds with B D N F
and N T 4 , and T rk C binds with N T -3 . After binding, the
Trk receptor undergoes dim erization (b o n d in g o t tw o simi­
lar m olecules) and autophosphorylation. These changes ini­
tiate an intracellular signal cascade in the axon, which
spreads to rhe ccll nucleus. The cascade involves the tyrosine
receptor kinases and the R h o family o f guanosine triphos­
phatases (R h o G T P a se s) (Thrcadgill c t al. 1 9 9 7 ). So-called
truncated T rk B receptors on astrocytes lack the intracellu­
lar tyrosine kinase dom ain and respond by releasing calcium
ions trom intracellular stores (R ose et al. 2 0 0 3 ).
The p75 recepcor is a low affinity recepcor chac binds
with all neurotrophins (Rodriguez-Tdbarct al. 1990) Newly
formed neurotrophins arc known as p ro n eu ro tro p h in s
because they possess a term inal fragm ent o f am ino acids
know n as che “p ro reg ion ." In m ature n eu ro tro p h in s, the
prorcgion is removed. Proneurotrophins bind selectively to
p 75, while mature neurotrophins bind to Trk receptors
(see Lu 2 0 0 3 ). W e will see that the tw o types o f neurotro­
phin have very different effects. Failure to distinguish
betw een these opposed effects probably explains some
con flictin g results.
Trk receptors are influenced by signals em anating
trom o ther receptors and also influence the responses ot
o ther receptors (C h a o 2 0 0 3 ). For exam ple, activation o f
the p 75 receptor can increase the affinity ot Trk receptors
for specific neurotrophins (B en cd etti c t al. 1 9 9 3 ). This is
only one o f many cases ot cross talk between receptor
systems.
This section is concerned with signals initiated by neu­
rotrophins chac guide growing axons to their destination. In
addition, signals triggered by neurotrophins spread to the
cell som a, where chey concrol ccll differentiation and sur­
vival. N eurotrophins are also involved in activity-dependent
synaptic plasticity during the critical period, as we will see
in Sections 6 .5 .1 c and 6.7.2. They are also active in the adult
nervous system, especially in areas that arc involved in learn­
ing, such as the hippocampus. For example, B D N F pro­
m otes long-term potentiation (I.T P ) in the hippocam pus
by increasing the density o f synaptic vesicles (T yler et al.
2001 ).
Som e neurotrophins attract axons growing toward a
particular target cell while others prevent axons from grow­
ing into particular regions (C h ao 1992; Lindsay ec al. 1994).
N eurotrophins activate intracellular pathways that regulate
rhe dynam ics o f the accin cytoskeleton w ithin the filopodia
o f growth cones. For example, neurotrophins binding to
che rcccpcor p75 reduce che accivicy o f the protein RhoA.
This increases the length o f filopodia on growth cones
(G eh ler c t al. 2 0 0 4 ). Thus, active RhoA inh ibits the growth
o f filopodia.
The neurotrophins B D N F and N T -3 and the p75 neu­
rotrophin receptor are expressed in the cortical subplate o f
the visual co rtcx when thalam ocortical axons invade che
cortical plate. The neurotrophins acting on the p 75 recep­
tor increase the form ation o f filopodia on neurons growing
in the subplate (M cQ m llen et al. 2 0 0 2 ). M ice lacking the
gene for N T -3 or for p75 show a reduction in thalam ic
inputs to the visual cortex (M a et al. 2 0 0 2 ).
It seems that neurotrophins' are sufficient to guide axons
to their destinations in chc tectum o f am phibian larvae,
such as the axolotl. Axons reach their destination when
forced to travel an unusual route in the absence o f nerve
impulses (H arris 1984).
In both infant and adult m ice, the brain-derived neu-
rotrophic factor (B D N F ) acting through TrkB receptors
and sodium ion channels on dendritic spines can depolarize
the cell m em brane within milliseconds. This initiates a train
o f action potentials sim ilar to those initiated by neurotrans-
m itters (Blum et al. 2 0 0 2 ). There is som e evidence that
grow th cones are also attracted by neurotransmitcers
secreted by target cells (Z h eng et al. 1994).
Fitzsim onds and Poo (1 9 9 8 ), M cA llister et al. (1 9 9 9 ),
and R cichardt (2 0 0 6 ) reviewed neurotrophins.
6 .4 .3 e P ro te in S y
ф
n th e sis an d N e u ro n a l G ro w th
O ver a period o f minutes, nerve growth faccors send signals
to genes in the cell nucleus, which lead to transcription o f
m RN A s. The niR N A s are carried to the growth con c, where
they express specific proteins required tor cone growth and
guidance.
W hen growth is com plete, genes expressing relevant
proteins are switched off. For example, rhe lk l-2 protein
produced by the bcl-2 gene fosters the growth o f ganglion-
ccll axons in chc retina. Loss o f Bcl-2 suppressed axon
growth while excess production o f Bcl-2 in adult m ice
allowed severed ganglion ccll axons to regcneracc (C hen
ecal. 1997).
The G A P -4 3 procein, also known as neurom odulin, is
present in developing and regenerating growth cones. It
interacts with extracellular growth factors and binds with
calm odulin (Vancura and Jay 1 9 9 8 ; Zhu a n d ju licn 1999).
G p ro tein s (guanine nucleotide-binding proteins) are
attached to the inside o f the ccll m em brane. They route sig­
nals received from many types o f m em brane-spanning
receptor molecules со several distinct intracellular path­
ways. These pathways form a com plex n etw ork o f in te ra c t­
ing p ro tein m o lecu les w ithin the ccll chac regulate cellular
processes such as genetic transcription, ccll m otility, and
secretion. *lhe network consists o f local m odules devoted
to specific functions (M aslov and Sncppcn 2 0 0 2 ).
'I he m otility o f growth cones is controlled by guanosine
triphosphatases (G T P a s e s ), including R ho, and Rac.
Rho G T P ases prom ote the protrusion o f lam ellipodia and
hence the advance o f the growth cone. Rac-type G TPases
prom ote cel! retraction (D eM ali et al. 2 0 0 3 ). These p ro ­
cesses are involved in both developm ent and learning
(Neves et al. 2 0 0 2 ).
It was explained in Section 6 .4 .3 a that the growth and
guidance o f filopodia on growth cones depends on the
extension o f actin filam ents. The protein B -actin is rapidly
produced in the growth cone when it is stimulated by
growth factors, For example, asymmetrical stim ulation o f
cultured em bryonic spinal neurons from the trog Xenopus
with B D N F produced an asymmetrical accum ulation o f
m R N A tor B-actin . The consequent asymmetrical expres­
sion o f B -actin induced the growth co n e to turn in the
direction o f greater stim ulation (Yao et al. 2 0 0 6 ).
Asymm etrical stim ulation o f growth cones in em bryonic
retinal cells by netrin had a similar effect (l.cu n g e t al. 2 0 0 6 ).
Thus, newly synthesized B -actin at the site o f signal recep­
tion controls the direction in which growth cones grow.
Protein degradation (proteolysis) is an im portant m ech­
anism o f axon growth. Proteolysis involves the attachm ent
o f a chain o f polypeptide u b iq u itin molecules to proteins
by a process known as poly-ubiquitination (H crshko et al.
1 9 8 0 ). Tliis marks the proteins for destruction by the p ro -
tc a s o n ic — a protein disposal unit in each cell. A ttachm ent
o f a single ubiquitin m olecule (m on o-u biq u itin ation ) to
proteins is involved in controlling the strength o f synapses
(Hegde and D iA n to n io 2 0 0 2 ; D iA n to n io and H ickc
2 0 0 4 ).
G uidance m olecules and signals they produce create the
com plex central nervous system. The com plexity depends
on genetic regulation ot their expression at different phases
o f developm ent, and context-sensitive interactions between
the different guidance systems (Yu and Bargmann 2 0 0 1 ;
D ontchev and Letourneau 2 0 0 2 ). But we will now see that
the fine structure o f the cortex also depends on activity-
dependent changes occurring at Hebbian synapses.
6 . 4 . 3 f A c tio n P otentials
W e will see in S ection s 6.6.1 and 6 .6 .2 that synaptic activity
involving release o t neurotransm itters is n o t required tor
initial form ation o f thalam ocortical con nection s or o f co r­
tical layers. However, neural activity is required for the
refinem ent and m aintenance o f cortical synapses (Section
6 .6 .3 ). For example, blockage o f sodium -dependent excit­
atory activity by tetrodotoxin ( T T X ) disrupted synaptic
developm ent (Shatz 1990a). However, T T X did nor affect
the growth o f axons to their destination.
Depolarization o f the presynaptic membrane by neural
activity releases calcium ions. These ions initiate release o f
neurotransmitters and prom ote rhe production o f the
enzyme calcium /calm odulin-dependent p rotein kinase II
(C aM К 11) (Section 5.5.2c). See Catrcrall and Few (2 0 0 8 ) for
a review ot the role o t calcium channels in neural plasticity.
Application o f C aM К 11 to cultured slices o f the rat hip­
pocampus prom oted the growth o f filopodia and form ation
o f dendritic spines (Jou rd ain e t al. 2 0 0 3 ). O n the other
hand, a m odest release o i calcium ions activated ca lcin cu -
rin p hosphatase, which repelled growing axons in the
em bryonic spinal cord ot Xenopus (W en et al. 2 0 0 4 ). The
tw o processes therefore provide a mechanism for axonal
guidance.
O th er members o f the calm odulin kinase family
(C aM К I and C aM К IV ) also control the growth and
branching o f growth cones. Inhibition o f C a M K I causes
growth cones to collapse (W ayman c t al. 2 0 0 4 ).
Neural activity not involving neurotransm itter release is
involved in axonal guidance. Spontaneous fluctuations in
intracellular calcium ions occur throughout the cell bodies
o f developing neurons, including the dendrites and growth
cones. These fluctuations increase in frequency when a
growth cone halts its advance at a choicc point. Also, the
frequency o f fluctuations is inversely related to the rate o f
axonal growth. Suppression o f calcium transients prom otes
axon growth in am phibians and in mammals (Tang et al.
2 0 0 3 ). Waves o f calcium ions spread over the em bryonic
cortex through electrical coupling over gap ju n ction s rather
than by synapses (Section 6 .6 .2 ). Electrical coupling
betw een gap ju n ction s is prom inent betw een neurons
during the developm ent o f the nervous system. Specific
types o f gap junction that occur only in early development
are crucial for neuron differentiation and synaptogenesis
(M axeiner et al. 2 0 0 3 ). Spontaneous neural activity in the
developing I.G N was discussed in S cctio n 6.3.5b .
In amphibians, axon growth may depend on spontane­
ous neural activity involving potassium ions rather than
sodium ions. W hen M cFarlane and Pollock (2 0 0 0 ) blocked
potassium channels, developing ganglion cells o f the trog
Xenopm grew aberrantly in the optic tract and optic tectum .
Thus, different forms o f neural activity may be involved in
different groups o f animals.
6.4.4 S Y N A P T О G E N E S I S
6 .4 .4 a Form ation o f Synapses
The various types o f synapse were described in S ection 5.5.2.
Presynaptic boutons, containing ncurotransm itter vesicles,
occur on axons. M ost excitatory postsynaptic elements
occur on dendritic spines. The postsynaptic m em brane co n ­
tains the postsynaptic density, consisting o f receptors and a
com plex o f proteins. Typically one bouton makes synaptic
contact with one spine, but some boutons con nect with
more than one spine (K n o tt et al. 2 0 0 6 ).
M ature spines are a few m icrons long but vary in shape
and volume. 'Ih eir volume can vary between 0.0001 and
1 [im. Synapses may change in efficiency o f transmission, as
wc will see in Scction 6.5. By shape, spines fall into three
categories: thin spines, stubby spines, and spines with
bulbous heads (mushroom spines). Rearrangem ents o fth e
actin cycoskclccon cause spines to change their shape.
Synapses can also occur on dendritic shafts, especially in
young animals. Several lines o f evidence suggest that spine
and shaft synapses arc separate and serve different functions
(see A oto ct al. 2 0 0 7 ). However, neural activity causes some
shaft filopodia to be converted into synapse-bearing
dendritic spines (Portera-C ailliau et al. 2 0 0 3 ).
D uring early developm ent, axonal boutons and den­
dritic spines grow and retract over a period o f minutes. This
process can be triggered by synaptic activity Filopodia
occur in large numbers on young dendrites. As synapses
mature, the number o l filopodia decreases, but only it the
synapses are active (Frcdj c t al. 2 0 1 0 ). Som e but nor all o f
the filopodia are replaced by mature dendritic spines. New
spines can also form w ithout passing through a filopodial
stage (M arrs et al. 2 0 0 1 ). O nly a fraction o f nascent syn­
apses stabilize into mature synapses (N iell ct al. 2 0 0 4 ).
Electron m icroscopy o f the hippocam pus ot neonate
rats has revealed that filopodia and lamellipodia on den-
dritic spines are highly m obile and seek out con tacts with
axons or with axonal filopodia (Fiala c t al. 1998). However,
there is a rapid turnover o f filopodia in the neonate cortex.
They have a half-life o f only minutes. Som e filopodia
develop into dendritic spines and synapses that have a halt-
life o f days or more, by postnatal day 12, synapses develop
on dendritic spines. Tim e-lapse m icroscopy in the optic
tectum o f the zebra fish has revealed that alm ost all gluta-
m atergic synapses form from dendritic filopodia. Inh ibitory
synapses torm on sm ooth dendrites o f interneurons.
Local calcium -ion transients occur w ithin seconds after
a filopodium has contacted an axon. The higher the fre­
quency o f these transients the more stable is rhe synaptic
co n tact (l.ohm ann and B on h oeticr 2 0 0 8 ). These calcium
transients help filopodia to distinguish betw een glutamater-
gic and G A B A ergic axons (Lohm ann and Bonhoeticr
2 0 0 8 ).
Grow ing axons in the developing visual cortcx have “hot
spots” that release the neurotransm itter glutam ate under
the influence o t spontaneous neural activity or, later, under
the influence o f visual stim ulation. Orav ct al. (2 0 0 6 ) found
that the m otility o f filopodia and dendritic spines was
reduced when slices o f m ouse cortex were bathed in A M PA
or N M D A during the period o f synaptogenesis. The degree
o f spine m otility did not depend on the types o f receptors
that the neurotransm itters activated. Inhibition o f the
m obility o f actin filaments responsible for spine m otility
causes the grow th-cones o f spines to round up and becom e
more stable and regular (Fischer et al. 2 0 0 0 ; G od a and
Davis 2 0 0 3 ). Low -frequency stim ulation, w hich induces
long-term depression o f synaptic activity, also stabilizes
actin activity through the m ediation o f N M D A receptors
(Star et al. 2 0 0 2 ). This is a m echanism for experience-
dependent m odulation o f actin filam ent dynamics and
dendritic spine form ation.
Synaptogenesis observed in time-lapse m icroscopy can
o ccu r in a period o f 1 to 2 hours (O kab e et al. 2 0 0 1 ). A
yellow fluorescent protein is expressed in pyramidal cclls o f
the visual cortex in a strain ot transgenic mice. G rutzendler
ct al. (2 0 0 2 ) used a scanning m icroscope to observe the fine
structure ot particular cells over m onths through a window
in the skull o f these mice. In 1-m onth-old m ice, rapid exten­
sion, retraction, and elim ination ot dendritic filopodia
could be seen over an observation period o f 4 hours. O ver
the first 4 weeks m ost filopodia were elim inated. O nly
rarely were they seen to convert into spines. Also, during
the first m o nth , the num ber o f spines decreased. O th ers
have reported a similar early pruning ot spines.
In adult animals the spine and synapse population stabi­
lizes. Som e stability o f synaptic connections in the adult is
required tor long-term memory. However, synaptogenesis
occurs in the cerebral cortex o f adult animals. O ver a period
o f 1 m onth, 96 % o f spines in adult m ice remained in the
same locations and few new spines developed. However,
many adult spines showed marked changes in length or in
head diameter. These changes were seen over a 3-day obser­
vation period. Changes in spine length and volume are co r­
related with changes in postsynaptic density and also with
the cfficicncy and filtering properties o f synaptic transmis­
sion (M urthv et al. 2 0 0 1 ). G rutzendler ct al. observed cells
m ainly in cortical layers 1 and 2, while synaptic plasticity
has been studied mostly in layer 5. Perhaps synapses in layer
5 o f the visual cortex or in other cortical areas arc less stable
over time.
The growth o f new dcndriric spines in the barrel cortcx
(serving tactile inputs from the whiskers) o l adult m ice over
a one-m onth period has been observed by in vivo imaging
coupled with serial-section electron m icroscopy (K n o tt
et al. 2 0 0 6 ). Newly developed spines were thin and usually
lacked synapses, bur all spines that persisted tor more than 4
days were larger and had synapses, indicated by the presence
o f a postsynaptic density. M ost o f the new synapses co n ­
tacted with existing presynaptic boutons, which already had
.it least one synaptic con nection with other parent dendrites
(m ultisynaptic boutons). K n o tt et al. concluded that, in the
adult cortcx, spine growch precedes synapse form ation.
New synapses are formed on new spines, m ost o f which
grow toward preexisting presynaptic boutons. The topic o f
form ation and plasticity o t dendritic spines has been
reviewed by Alvarez and Sabatini ( 2 0 0 7 ), Parrish c t al.
( 2 0 0 7 ), and H oltm aat and Svoboda (2 0 0 9 ).
In cultures o f pyramidal cclls from chc hippocam pus o f
adulc rats, sm all dendritic spines form ed,changed in size, or
were elim inated over a tim e span o f hours, even when
N M D A synaptic activity was blocked. But these changes
were amplified in the presence o f normal synapcic accivicy
(Yasumatsu et al. 2 0 0 8 ). Large spines were stable and did
noc change in size, even in chc presence o f synapcic accivicy.
Tli is suggests that small dendritic spines and che synapses
chat torm on them are involved in new learning, while large
spines carry mature synapses responsible for m aintaining
long-term memories.
Initial co n tact betw een an axon and dendritic filopodia
is followed by a rapid rise in calcium ions in the growth
conc. The conc then slows down and rounds off. C ell adhe­
sion m olecules bind the pre- and postsynaptic membranes.
O n the presynaptic m em brane, calcium channels and the
m achinery o f synaptic vesicles develop.
Packets o f immature synaptic vesicles tagged with green
fluorescent protein (G F P ) have been seen traveling along
the presynaptic axon toward a newly formed synapse, where
they are involved in the creation o f the m achinery o f the
presynaptic m em brane (Ahm ari et al. 2 0 0 0 ). O n the post­
synaptic side, receptors and the m olecular and structural
com ponents o t the postsynaptic density develop.
Synaptogenesis has also been studied in the adult brains
of monkeys. Tim e-lapse m icroscopy revealed changes in
presynaptic boutons on axons (S te ttle r e t al. 2 0 0 6 ). C clls in
V I o f adult macaque monkeys were stained with green fluo­
rescent protein and observed by tw o-photon m icroscopy in
the living brain at 1-week intervals. Figure 6 .1 6 shows an
example o f a pyramidal cell in the superficial layers o f t h e
cortex. Presynaptic boutons can be seen on the branching
long-range horizontal axons. Synapses on axonal shafts
betw een boutons are rare. The size ol a presynaptic bouton
is related to the size o f t h e postsynaptic density and to the
number o f synaptic connections. O bservations of the same
cells at weekly intervals revealed that som e boutons were
elim inated and others added, with che total num ber rem ain­
ing more or less constant. D uring 1 week, abouc 7% o f the
Figure6. 16. . /p y ra m id a l ccll in I '/ o fth e yttacaquc. Til с ccll was labeled wich
green flu orescent p rotein and chc im age co n stru cted from a stack o f
views through a d ep th o f 3 0 0 fim by tw o -p h o to n m icroscopy in the
living brain, ( lic e Metier ct d. 2 0 0 6 »»uli paiumiun h o e Klvcvjer)
boutons were replaced. Large-scale changes in chc axonal
branching pattern were not observed, but small side
branches bearing boutons appeared and disappeared from
one week to the next.
6 .4 .4 b M o lecu lar Factors in Synaptogenesis
C ell adhesion molecules (C A M s) embedded in the pre-
and postsynaptic m em branes play a m ajor role in synapto­
genesis. For example, n eu ro lig in s are cell adhesion proteins
that becom e localized on the postsynaptic m em brane of
developing excitatory synapses. They are ligands tor neur-
exins, which are proteins localized on the presynaptic m em ­
brane. The two molecules engage in reciprocal signaling
(G ra f et al. 2 0 0 4 ). Neuroligins induce differentiation o f the
presynaptic m em brane, while neurexins induce differentia­
tion ot the postsynaptic m em brane. However, the develop­
ment o fth e postsynaptic mem brane lags behind that o fth e
presynaptic m em brane. Addition of neuroligin to a culture
containing pre- and postsynaptic neurons induced che
developm ent o t synaptic vesicles in the presynaptic m em ­
brane (Sch ciffelc ct al. 2 0 0 0 ). Removal o f neuroligin
arrested developm ent ot the presynaptic membrane.
Activation o f ncurexin by neuroligin also helps со bind che
pre- and postsynaptic m em branes and activate presynaptic
C a channels chac crigger the release o f ncurotransm ittcr
(M issler et al. 2 0 0 3 ).
There are over 1,000 varieties o f ncurexin and many
neuroligins. Thisdiversicy helps in the developmenc o f dis­
tinct types o f synapse. For example, overexpression ot
neuroligin-1 in cultured neurons increased responses o f
excitatory synapses, while overexpression ot neuroligin-2
increased responses o f inhibitory synapses (C hubykin et al.
2 0 0 7 ). B o th effects depended on synaptic activity, which
suggests that neuroligins contribute to activicy-dependenc
strengthening o f neural circuits.
O cher families o f cell adhesion molecules are involved
in synaptogenesis and they too occur in many form s (see
W ashbourne ec al. 2 0 0 4 ). For example, chc cell adhesion
protein N -cad h erin accumulates at nascent synapses that
form at filopodia-axon concacc points. Ic binds wich
eaten ins, which link with the actin cvtoskelcton and c y to ­
plasmic signaling pachways chat control gene expression.
These m echanism s allow cadherins to influence the struc­
ture o f both che presynaptic and postsynaptic membranes
of developing synapses (see Bam ji 2 0 0 5 ). A t the same time,
cadherins respond to activity occurring across the synapse.
In mature synapses cadherins are required for long-
term potentiation (L T P ), control the m orphology o f den­
dritic spines, and help in che final stabilization o f mature
synapses.
The ligand ephrin-B secreted by the presynaptic m em ­
brane and its F.phB receptor on the postsynaptic mem brane
are involved in the development o f excicacory synapses on
dendritic spines (Penzes et al. 2 0 0 3 ). M ice lacking F.phB
recepcors have reduced filopodia m otility and reduced
numbers o f synapses (Kayser c t al. 2 0 0 6 , 2 0 0 8 ). Also, the
ligand ephrin-B secreted by the postsynaptic mem brane is
involved in the developm ent o f synapses on dendritic shafts
but not on spines (A oto et al. 2 0 0 7 ).
Exposure to an enriched visual environm ent improves
the m aturation o f basic visual functions, such as visual
acuity. This effect has been shown to depend on visually
evoked expression o f molecules such as the insulin growth
factor (IG F -1 ) and brain-derived neurotrophic factor
(B D N F ). Blocking the expression o f B D N F in the retinas
o f neonate rats retarded the dendritic segregation in gan­
glion cells, which reduced visual acuity (I.and i e t al. 2 0 0 9 ).
C h o n d ro itin -su lp h a te p ro teog ly can s (C S P G s ) are
im portant com ponents ot the extracellular matrix. In the
critical period o f neuronal plasticity their expression is co n ­
trolled by visual experience. Toward the end ot the critical
period, C S P G s form p crin eu ro n al n ets round neurons in
the visual cortex. These nets inhibit axonal and dendritic
growth and thereby stabilize neuronal patterns in the adult
cortex (Pizzorusso ct al. 2 0 0 2 ). Proteoglycans work in co n ­
junction with the Sonic Hedgehog m orphogcn in co n tro l­
lingcell division (C h an ct al. 2 0 0 9 ).
6 .4 .4 c R o le o f A stro cy tes in Svnaptogcncsis
A strocytes, a type o f glial cell, constitute more than h alf the
cells in the human brain. They provide m etabolic supporc
and clear surplus ions and neurotransm itter molecules from
the synaptic cleft. A strocytes form a reticular netw ork
linked by gap ju n ction s (Section 5.5. I f ) . The role o f radial
astrocytes in guiding the m igration o t neurons to their
proper cortical layers is discussed in Section 6.4.5. The
period o f synaptogenesis in the developing central nervous
system coincides with rhe period when astrocytes develop.
A strocytes are also involved in synaptogenesis.
A strocytes in slices o f living neural tissue taken from the
brainstem o f early postnatal m icc and stained with fluores­
cent protein were observed by time-lapse laser scanning
(H irrlingcr e t al. 2 0 0 4 ). O ver a period ot m inutes, astro­
cytes extended lam ellipodia m em branes and filopodia to
neuronal cell bodies and over active synapses. They are
well situated to regulate synapse form ation, stability, and
efficiency.
ф
D uring developm ent, astrocytes increasingly ramify
around dendritic spines at synapses. Spines on the dendrites
of' Purkinjc cells in the cerebellum were less m obile when
physically constrained by astrocytes (Dunaevsky et al.
2 0 0 1 ). However, astrocytes do m ore than physically restrain
spines. 'Ih e receptor EphA4 occurs on dendritic spines o f
pyramidal cells in the hippocam pus ot adult m icc (M urai
et al. 2 0 0 3 ). Its ligand, ephrin-A 3, occurs on the mem branes
o f astrocytes that envelop the spines. Activation o f
EphA4 by astrocytes causes spines to retract. M ice lacking
the gene for EphA 4 develop irregular spines on dendrites o f
pyramidal cells. Thus, m olecular signals passed between
astrocytes and neurons regulate the structure o f excitatory
synapses. Visual stim ulation o f N M D A synapses in the
tectum o f Xcnopus tadpoles produced rapid structural
changes in astrocytes (Trem blay et al. 2 0 0 9 ).
M uller and Best (1 9 8 9 ) transplanted living astrocytes
from neonate kittens into one hemisphere o f the visual
co rtex o f adult cats and dead astrocytes into the other hem i­
sphere. After 4 to 8 weeks o f m onocular deprivation, a
change in the ocular dom inance o f cells occurred only in
the hemisphere with living neonate astrocytes.
C ultured retinal ganglion cells have much higher synap­
tic activity when astrocytes are present. A strocytes increase
the influ xofcalciu m ions and the num ber ofvcsicles released
at the presynaptic m em brane. G anglion cells cultured tor
14 days with astrocytes produced many m ore synapses than
cells cultured w ithout astrocytes (U llian et al. 2 0 0 1 ).
During synaptogenesis, astrocytes produce a variety o f
cell adhesion molecules, including fib ro n ectin and glial
grow th fa cto rs (Lem ke 2 0 0 1 ) that arc required for cortical
plasticity.
A strocytes also secrete th ro m b o sp o n d in s at a high
level during developm ent o f the central nervous system.
These large protein m olecules attach to the extracellular
m atrix and bind to receptors on the mem branes o f neurons.
Addition o f throm bospondins to cultures o f ganglion cells
stimulated the proliferation o f synapses (C hristopherson
et al. 2 0 0 5 ). M ice lacking throm bospondins developed up
to 4 0 % fewer cortical synapses (see Ehlers 2 0 0 5 ).
C h o le stero l secreted by astrocytes is another critical
factor in synaptogenesis (M auch et al. 2 0 0 1 ). D uring the
period o f synaptogenesis the cholesterol available from neu­
rons must be supplemented by that provided by astrocytes
(see Pfrieger 2 0 0 2 ).
6 .4 .4 d Tlic R o le o f G A B A c r g ic N eurons
in Synaptogenesis
In early cortical developm ent, G A B A acts as an excitatory
(depolarizing) rather than inh ibitory transm itter. Excitatory
G A B A crgic interneurons form the first active neural n et­
work. Inhibitory G A B A crg ic synapses between interneu­
rons and pyramidal cells form later. The early excitatory
G A B A crgic netw ork in cooperation with activation o f
N M D A synapses influences ccll m igration and synaptogcn-
esis in many parts o f the nervous system (O w ens and
K ricgstcin 2 0 0 2 ; Bcn-A ri c t al. 2 0 0 4 ; Wang and K ricgstcin
2 0 0 8 ). W e will see in Section 6 .4 .5 b th at G A B A is involved
in form ation o f cortical layers.
The early excitatory G A B A system also controls activity-
dependent dendrite form ation in che developing cortex.
Introduction o f G A B A antagonists into cultures o f em bry­
onic n co cortex o t the rat reduced the growth o f dendrites
(M arie et al. 2 0 0 1 ).
 Also, the conductance o f existing recepcor sites
increases (B cn k c et al. 1 998). Neural activity associated
wich long-term depression (L T D ) triggers the
production ol the protein kinase R ap , which leads to
removal o fA M P A receptors from the postsynaptic
density. This involves the process o f cn d o cy to sis,
described in Section 6.5.1a.
It was explained in Section 5.2.2a that synapses in chc
L G N that transm it inputs from the retina involve chc
A M P A receptor subunit G lu R l. Visual activity is
required for the insertion o f G lu R l receptors in the
postsynaptic membranes o f these synapses (K ielland
ct al. 2 0 0 9 ).
T h e developm ent o f synapses involves reorganization o f
the cytoskeleton by regulation o f actin dynamics, as
described in Section 6 .4 .3 a . Accin dynamics involves
R h o G T P ases that are activated by stim ulation o f
N M D A synapses (Sin et al. 2 0 0 2 ).
O n ce a synapse has been modified by long-term
learning ic becom es m ore resistant to further
m odification. D uring learning, the N M D R receptor
subunit N R 2 a increases relative to che N R 2 b receptor
subunit (Q u in lan et al. 2 0 0 4 ). The N R 2a receptor has a
higher threshold than the N R 2 b receptor, so that its
increase renders the synapse m ore resistant со
m odification. These processes are discussed in more
detail in S cctio n 6.5.1a.
3. Increase in the area o f synaptic membranes A synaptic
m em brane may increase in area by increasing its
curvature or by increasing the num ber o f dendritic
spines contacted by axon term inals. Such changes have
been observed by the electron m icroscope in cultured
slices o f rat hippocam pus betw een 3 0 to 6 0 minutes
after bursts o f electrical stim ulation (Buchs and Muller
1 9 9 6 ; Toni et al. 1 999). The num ber o f rcccptor zones
on the postsynaptic m em brane may also be increased by
perforations in the mem brane (Edwards 1995).
4 . Changes in dendritic spines Laser scanning ot cultured
slices from rhe rat hippocam pus infected with a virus
expressing a fluorescent protein has revealed the fine
structure o f dendrites and dendritic spines. Tim e-lapse
imaging showed that, w ithin 6 0 s after 100 H z tetanic
scimulacion, new dendritic spines developed and
existing spines elongated. The effects were localized to
w ithin about 100 jmi and were abolished by an
antagonist for N M D A receptors (M alctic-Savatic c t al.
1 9 9 9 ). Low -frequency repetitive stim ulation that
induced long-term depression reduced the diam eter o f
spines and produced a small reduction in spine density
(Niigerl et al. 2 0 0 4 ; Zhou et al. 2 0 0 4 ). C ells in the
nucleus laminaris o f chc ch ic k s auditory system receive
inputs trom one ear on one set ot dendrites and from
the other car on another set. Electrical stim ulation o f
one set ot dendrites rapidly produced elongation ot that
set and retraction o f the other set (Sorensen and Rubel
2 0 0 6 ).
Changes in postsynaptic dendritic spines are produced
by
/ form ation o r contraction o f accin filaments in chc
spine. These changes have been observed w ithin
seconds o f synaptic activity (Fischer c t al. 1998).
A ctin-binding proteins released from the postsynaptic
density control synapcic accivicy and form ation and
contraction o f actin filaments. The crucial factor is the
equilibrium between filamentous actin (F-actin ),
which increases the efficiency o f synaptic efficiency,
and globular actin (G -accin ), which decreases synaptic
efficiency (O k am o to ct al. 2 0 0 4 ).
During long-term potentiation (L T P ),g lu tam ate
molecules secreted by endosomes are delivered to the
postsynaptic membrane. As L T P progresses,
endosom es migrate into the dendritic spines, which
enlarges the spines (Park c t al. 2 0 0 6 ). M orphological
changes in dendritic spines, produced by dynamic
changes in the actin cytoskeleton, arc associated with
increases in synapcic transmission and reduction in
response latency (Yustc and B onhoeticr 2 0 0 1 ). For
example, the actin-binding protein c o rta c tin , which is
conccntratcd in dcndritic spines, controls the size and
shape o f dendritic spines. Its removal leads to depletion
o f spines, and its ovcrcxprcssion causes spines to
elongate. Stim ulation o f N M D A synapses facilicaces
chc remodeling accivicy o t corcaccin and causes chc
protein to be redistributed to the dendritic shaft
(I lering and Shcng 2 0 0 3 ). See Pak and Sheng (2 0 0 3 )
and Jaworski et al. (2 0 0 9 ) for a discussion o f proteins
involved in shaping or elim inating dendritic spines.
In the mouse visual cortex, dendritic spines are highly
mobile during the critical period o f cortical plasticity,
especially in m ice deprived o f vision from birth
(M ajcw ska and Sur 2 0 0 3 ) . Tli с m em brane rcccptor
N o tch 1, w hich is activated by ligands on neighboring
cclls, inhibits neurice growch in chc visual corccx. This
recepcor is im plicated in experience-dependent
synaptic plasticity during the critical period (D ahlhaus
e ta l. 2 0 0 8 ).
As synapses mature chey becom e less dependent on
actin dynamics (Z hang and Benson 2 0 0 1 ).
Spontaneous release o f neurocransmitcer is required to
maintain dendritic spines on cortical neurons
(M cK in n ey e ta l. 1 9 9 9 ). Interactions betw een glial
cells and neurons are also involved in form ation and
stabilization o f dendritic spines (Section 6.4 .4 c).
O n e would cxpcct learning a specific task to produce
changes in specific regions ot the brain. Y an g eс al.

Figure & is. D evelopm ent o ft h e hum an visu alcortex. (A ) P h o to m icrograp h
o f a N issl-staincd scctio n throu g h the visual c o rtc x o f 17-w cck hum an
fetus. N eurons develop in chc ventricular z o n e , lin in g the cerebral
ventricle. T h ey m igrate throu gh the in term ed iate zon e and co rtical
subplatc со the co rtic a l plate, ju st below chc pial surface o f t h e brain.
T h e six layers o t the visual co rtex arc n o t yet visible, but develop in the
co rtica l plate. ( B ) P h o to m icro g rap h o f t h e visual c o rtcx o t th e hum an
n eon ate. T h e six layers arc form ed , and the subplate has transform ed
in to largely n eu ron -free w h ite m atter. ifUphnuJfam Yjnctal. permit*»
fru m tl*c»icr S o c n i c )
W h en lam ination o f the visual co rtcx is com plete, the
interm ediate zone and subplace form the neuron-free white
matter, and glial cells becom e stellate astrocytes.
6 .4 .5 b C c ll lin ea g e and M ig ra tio n
Cells derived trom a particular progenitor cell can be traced
by infecting the progenitor cell with a retrovirus thac trans­
fers only to the cell’s offspring. The virus expresses a green
fluorescent protein (G F P ), which can be viewed co n tin u ­
ously by time-lapse videomicroscopy (H atanaka and
M urakami 2 0 0 2 ).
Early in neurogenesis, progenitor cells in the ventricular
zone divide about tw ice a day, so that the num ber o f cells
more than doubles each day. A t first, most progenitor cells
divide symm etrically to produce m ore progenitor cclls that
remain in the ventricular zone. In the mouse, each initial
cell produces about 2 5 0 progenitor cells. If we assume that
each progenitor cell produces all the cells in one cortical
colum n then the final number o f progenitor cells deter­
mines the num ber o f colum ns. The gene Brain factor-1 co n ­
trols the duration o f the ccll division cycle and hence the
num ber o f times a progenitor cell divides symmetrically to
torm o ther progenitor cells (T ao and I.ai 1992). It is there­
fore responsible for the evolutionary expansion o f the
cerebral cortex.
D uring neurogcnesis, progenitor cclls in the ventricular
zone change to an asymmetrical, or stem -cell, mode ot divi­
sion. O n e daughter remains a progenitor ccll tethered to
the preplate, and the other differentiates into a neuron or
glial ccll, which undergoes no further division. Progenitor
cells may also generate in term ed iate p ro g e n ito r cells that
migrate to the subvcntricular zone before dividing symmet­
rically into tw o neurons that continue to migrate toward
the cortical plate (N o cto r et al. 2 0 0 4 ). The genes Brain
factor-1 and Sonic hedgehog determ ine when the transition
trom symmetrical to asymmetrical division occurs
(H anashim a ct al. 2 0 0 2 ; Palma e t al. 2 0 0 5 ).
Progenitor cells that migrate radially from the ventricu­
lar zone divide asymmetrically two or more times to form
radial clusters o f cells o f the same type, either excitatory
neurons or glial cells (M cC o n n ell 1995a). The radial clus­
ters from the set o f related progenitor cells form horizontal
rows o f “cousin” cells w ithin the cortical laminae.
The num ber o f times each progenitor cell divides
asymmetrically to form neurons determ ines the number
o t cells in each cortical colum n. The number is fairly co n ­
stant in mammalian species, since the thickness o f the
cortex does not vary. Late in neurogcnesis, progenitor cells
divide symmetrically into two differentiating cells, leaving
the preplate almost depleted o f progenitor cells (Caviness
c t al. 1995).
B o th G A B A and glutamate are strongly expressed in
the ventricular zone o f the developing cortcx. It seems
that they induce progenitor cclls to divide symmetrically
со produce other progenitor cclls rather than neurons
(Section 6 .4 .5 ). Ultim ately this increases the num ber o f
cells in the cortex (Haydar et al. 2 0 0 0 ).
Progenitor cells in the retina and central nervous system
that divide symmetrically have the m ito tic spindle parallel
to the neuroepithelium so that the cleavage plane is o rth og­
onal to the epithelium . This causes N um b protein m ole­
cules to be distributed equally to the daughter cells. In
progenitor cells that divide asymmetrically, the cleavage
plane has rotated so that it is parallel to the m em brane. This
causes Num b molecules to be distributed mainly *
to the
daughter cell that remains a progenitor cell. The o ther cell
differentiates into a neuron. Num b inhibits cell differentia­
tion by blocking the signals sent to the cell nucleus by the
protein N o tch . M utant mice lacking the gene for Numb
rapidly depleted their progenitor cells after the onset o f
neurogenesis (Petersen et al. 2 0 0 2 ). However, there is some
dispute on this question (sec Castaneda-Castellanos and
Kriegstein 2 0 0 4 ). Later in developm ent. Num b allows cell
differentiation (sec C ayouettc and R a ff 2 0 0 2 ).
The rotation o f t h e spindle axis during progenitor cell
m itosis in living slices o f mouse neural tissue has been
observed w ith time-lapse m ultiphoton m icroscopy co m ­
bined with nucleic acid staining (Haydar et al. 2 0 0 3 ). There
is evidence that the process is under m olecular control
(Sanada and Tsai 2 0 0 5 ). The centrosom e is also involved in
chc orientacion o f chc micocic cleavage plane (W a n g cc al.
2 0 0 9 ).
Nadarajah ec al. (2 0 0 1 ) observed cwo cypes o f radial ccll
m igration in slices ot em bryonic mouse brain: locom otion
and tran slocation . In locom otion , a radial glial ccll guides
the whole neuron to its final destination. In translocation,
the neuron extends a leading process along the glial cell over
which the nucleus o f rhe cell migrates. Som e cells migrate
by locom otion m ost o f the way to their destination and
then sw itch ro translocation. W h en cells reach their desti­
nation they must recognize stop signals, disengage trom the
glial ccll, and becom e organized into a cortical layer. We
will see in the next section that the glycoprotein rcclin
secreted by C ajal-R ctziu s cells is involved in this signaling
process (see Nadarajah and Parnavelas 2 0 0 2 ).
D uring cell locom otion , ccll adhesion molecules
(C A M s) on the soma o f the cell form gap ju n ction s with
C A M s on the radial glial ccll. Downregulation o f these
C A M s in the rat impaired m igration o f neurons to the co r­
tical plate (E lias c t al. 2 0 0 7 ). M igrating cells extend filopo­
dia, which rapidly extend and retract along the glial cell.
A cytoskeleton o f m icrotubules holds the soma o f the
m igrating cell in the lagging region ot the cell and projects
into che filopodia.
Neuroblasts m igrating from the ventricular zone to the
cortical plate o f che em bryonic corcex express several cypes
o f Cl A BA receptors. Introduction o f G A B A to tissue slices
o f im m ature corcical cissue prom otes the radial migration
oi neuroblasts. G A B A also acts as a stop signal to term inate
migration (see Reprcsa and Ben-A ri 2 0 0 5 ).
The centrosom e is an essential com ponent o f the m icro­
tubule cytoskeleton. Together with the G olgi com plex it is
rhe primary source o f m icrotubules. As rhe cell migrates,
the centrosom e moves forward ahead of the soma. It has
been suggested that the centrosom e transm its the pulling
forces generated by the cytoskeleton to the som a. W hen the
cell changes its direction o f m igration, the centrosom e
becom es reoriented (see H igginbotham and Glecson
2 0 0 7 ).
Vesicles move w ithin the m icrotubules during cell loco ­
m otion. There are accin filamcncs near chc soma o f migrac-
ing neurons but not in the filopodia. In this respect, cell
locom otion differs from axon growth.
Tim e-lapse im aging has revealed that m igrating neurons
first move rapidly away from the ventricular zone and then
halt in the sub ventricular zone for as long as 2 4 hours.
During this interval they becom e m ultipolar and extend
and retract processes in a highly dynamic manner. Som e
cells migrate back toward the ventricular zone before finally
m igrating to the cortical plate (K ricgstcin and N octor
2 0 0 4 ). These processes are depicted in Figure 6.19.
Som e progenitor cells and a few postm itotic differenti­
ating cells from the ventricular zone o f the dorsal forebrain
m igrate laterally, som etim es changing rheir direction o f
movement (O ’Rourke et al. 1 9 9 2 ; Kornack and Radic
Pia
f ig ur e i9 . C e ll m igration in the developing n co co rccx . (K<Jwn fom
X .».l <гл'л1| Jii«i Rtrnivcta* 20 01)
1 9 9 5 ; Reid et al. 1 9 9 5 ). The progenitor cclls divide sym ­
m etrically as they migrate to produce a series o f evenly
spaced nonm igratory daughter progcnicor cells.
The tim ing o f cell differentiation is controlled by inter­
actions betw een factors intrinsic to the developing cells and
extrinsic chem ical signals from ocher cells. For example,
stem cclls, which produced neurons or glial cclls in high-
densitycellculcures,diffcrcnciaccd into sm ooth muscle cells
when cultured at low density (Tsai and M cK ay 2 0 0 0 ).
Presumably, this effect depends on differential rates o f d if­
fusion o f a chem ical across ccll m em branes. The effect o f a
given chem ical agent depends on when it is applied. For
example, sites on progenitor cells receptive to an epidermal
growth factor increase in num ber during embryonic- devel­
opm ent. W h en a retrovirus introduced extra receptor sites
in the early stages, the progenitor cells behaved like chose in
later stages and differentiated in to glial cells rather chan
inco neurons (Burrows ec al. 1997).
A progen icor cell in its early phase o f cell division, when
transplanted into an older host, behaves like the cells o f the
host (Gray and Sanes 1 9 9 1 ). A progenitor cell in its late
phase o f ccll division retains its initial idcncicy when crans-
planted. If ic was destined to migrate to layer 6, it continues
to do so when transplanted into che visual corcex o f an
animal ac the stage when cells were m igrating in to layers 2
and 3 (M cC o n n ell and Kaznowski 1 9 9 1 ). Thus, a young
progenitor cell is capable o f form ing several types o f cell
depending on its environm ent. As tim e passes, progenitor
cells lose their com petence со form a variecy o f cclls.
Axons growing in cultured slices o f immature visual
cortex from che fcrrcc arborized w ithin cheir appropriace
layer. Neural activity arising from outside the cortex is thus
noc required. However, inhibicion o f neural activicv in chc
now see thac selective ablation o f these structures in geneti­
cally m odified m ice severely disrupts cell m igration and
form ation o f cortical layers (X ie et al. 2 0 0 2 ).
G hosh et al. (1 9 9 0 ) used kainic acid to ablate subplate
neurons in the visual corcex o f fetal cats on em bryonic day
4 2 , when the first L G N axons had arrived in the subplate.
This prevented L G N axons trom innervating their normal
target cells in cortical layer 4 . The effect seems to be specifi­
cally related to the loss o f subplate neurons, because appli­
cation o f kainic acid directly to layer 4 did nor produce this
deficit. A blation o f subplate neurons in 1-week-old kittens,
just after the innervation o f'cortical layer 4 by I.G N axons
but before the form ation o f cortical columns, disrupted the
form ation o f orientation and ocular dom inance colum ns in
the region above the ablated area (G h osh and Shatz 1992b,
1944).
Subplate ablation in 1-week-old kittens impaired trans­
mission ofvisual inputs from the I.G N (Kanold et al. 2 0 0 3 ).
This loss o f cortical activity could have disrupted column
form ation because it removed the basis for com petitive
innervation o f cortical cells. However, the effects o f abla­
tion could also have arisen if chem ical markers that deter­
mine colum n form ation were located in che cortical
subplate.
A blation o f subplate neurons in cat fetuses disrupted
the developm ent o f axons from the visual cortex to the
L G N (M cC o n n ell et al. 1 9 9 4 ). The subplate therefore aids
in the developm ent o f both geniculocortical and co rtic o ­
thalam ic pathways.
The neurotransm itter glutamate acting on N M D A
receptors serves as an actraccanc for cells m igrating inco che
corcicai place (B e h a rc ta l. 1 9 9 9 ). Thencurocrophins B D N F
and N T -3 expressed in che corcicai subplace increased che
tormacion ot filopodia on growing neurons (M cQ u illen
cr al. 2 0 0 2 ). M ice lacking che gene for N T -3 showed a
reduction in thalam ic inputs to the visual cortex ( M a c t al.
2 0 0 2 ). Loss o f subplate neurons produced an increase in
brain-derived neurotrophic factor (B D N F ) in the affected
region (L ein et al. 1 9 9 9 ). An oversupply o f B D N F in mice
produces an early m aturation of G A B A ergic inhibition and
an early onset and early closure o f the critical period for for­
mation o t ocular dom inance columns. Thus, subplate neu­
rons are involved in the m aturation o f cortical inhibition
(see S ection 6 .7 .1 ).
Subplate neurons and their axons can thus be regarded
as a tem porary scaffold for the initial developm ent o fg en ic-
ulocortical con nection s, their segregation in cortical layers,
and the subsequent developm ent o f cortical colum ns. After
cortical layers have form ed, m ost subplate cells die, along
with the lateral con n ection s o f L G N neurons w ithin the
subplate (Shatz ct al. 1 9 9 1 ; Bourgeois and Rakic 1996).
Thalam ocortical axons grow radially chrough deep corcicai
layers 5 and 6 со reach cheir descination in layer 4.
M agnocellular afferents term inate mainly in cortical
layer 4 A , but some term inate in layer 3 C . Parvocellular
afferents cerminace alm ost exclusively in layer 4 B . The ter­
m inal arbors o f both types o f cell increase in size and co m ­
plexity as they mature (Pospichal et al. 1994).
After thalam ocortical axons reach their destinations in
the cortex they lose cheir growch cones, branch, and form
synapses. These processes can be observed in cultured
explants from the em bryonic or postnatal co rtex o f the rat
(M olnar and Blakem ore 1999). Axon growth is arrested by
a m olecular stop-signal emitced by the cells o f layer 4 . The
stop signal seems to be the transmembrane glycoprotein
N -cadhcrin. W hen N-cadherin was blocked in living co rti­
cal slices from neonacal rats, thalam ocortical axons failed to
scop and concinucd со grow chrough layer 4 until chey
reached che corcicai surface. Also, blockage o f N-cadherin
actenuaccd the growth o f thalam ocortical axons through
layers 5 and 6 (Poskanzer et al. 2 0 0 3 ).
After the co rtical layers have form ed, the cells
in the various lavers develop at a uniform rate (Lund et al.
1977).
6 .4 .5 d L o ss o f S y n a p tic D e n s ity
In the rac, synapcic densicy in chc visual corccx increases up
со che third postnatal w eek. It then decreases to adult levels
by day 25. Activity-dependent release o f cell adhesion m ol­
cculcs at N M D A synapses has been im plicated in these
developm ental changes (Butler ec al. 1999).
In chc primace visual corccx and in the cortcx as a whole
there is a rapid increase in the density and total num ber o f
synapses and in the thickness o f layers just before and after
birth (R akic et al. 1 9 8 6 ). In che macaque monkey, synaptic
density wichin the visual corcex increases exponentially to
the third postnatal m onth, after w hich ic decreases, ac firsc
slowly and chen more rapidly со reach ics adulc value after
about 5 years (Bourgeois and R akic 1993).
In humans, this increase is mosc rapid between the
ages o f 2 and 4 m onths bu t continues to about 8 m onths,
when mean synaptic density reaches about 2 5 ,0 0 0 per
neuron. After about 8 m onths a massive but slow loss o f
synapses occurs. Synaptic density reaches the adult level o f
about 1 0 ,0 0 0 synapses per neuron by abouc the age o f
11 years.
There is no evidence o f neuron loss during chis process
buc, because o f increasing brain volume, ccll densicy declines
and corcicai layers becom e thinner during rhe firsc few post­
natal m onths in boch monkeys and humans ( O ’Kusky and
C o lo n n icr 1982;G arcy an d d cC o u rccn 1983; I luccenlochcr
and de C ourcen 1987; Zielinski and H endrickson 1992).
Loss o f synapses in chc visual cortcx is related to chc devel­
opm ent o fo cu lar dom inance colum ns in which inputs from
the tw o eyes com pete for synaptic access to binocular cclls.
It is thus part o f the process by w hich neural networks
develop in response to maturational and environmental
demands.
 6 .4 .6 D E V E L O P M E N T O F C O R T IC A I
C O N N E C T IO N S
6 .4 .6 a Interlayer C o r tic a l Synapses
The basic m orphology o f chc cerebral corcex is determ ined
genetically. However, we will see chat the detailed pattern­
ing o f dendrites depends on sensory inputs and interactions
betw een neighboring cells.
Spiny stellate cells of cortical layer 4 are the primary
recipients o f visual atferencs. In the cat, che projeccions o f
layer 4 cells to cortical layers 5 and 6 are com plete by post­
natal day 15. C o n n ectio n s w ithin layer 4 , w hich are che
m ost com plex, take 2 0 days to mature. C o n n ectio n s from
layer 4 to layers 2 and 3 take even longer со mature.
Callaway ( 1998b ) labeled neurons for cytochrom e o xi­
dase in living brain slices from V I o f prenatal macaque
monkeys (P ortrait Figure 6 .2 0 ). C onn ection s between the
main cortical layers developed with a high degree o f selec­
tivity, suggesting that these connections are genetically co n ­
trolled. In cultured blocks o f cortex from 10-day-oId rats,
axons grew m ost effectively on a m em brane prepared from
the cortical layer containing their target cclls. Presumably,
target cells produce a layer-specific growth factor (C astellan i
and Boltz 1 9 9 7 ). For exam ple, layer 6 neurons form co n ­
nections in layer 4 but bypass layer 5. The appropriate co n ­
nections develop in vitro, which shows that extrinsic
influences are n o t involved. However, the connection s were
less specific when intrinsic spontaneous activity was sup­
pressed by cecrodotoxin (Danczker and Callaway 1998).
Thus, although layer-specific connections arc determ ined in
part by m olecular markers on target cells, local spontaneous
neural activity must also be involved.
Figure6.Ю. E ihu an lM . C allaw ay. H e o b ta in ed his P h .D . from the
C a lifo rn ia In stitu te o f T e ch n o lo g y in 1 9 8 8 and did p o std o cto ral work
a t th e R ock efeller U n iv ersity and D u ke U niversity. H e is now professor
in the system s n eu rob iolog y lab oratories a t the Salk in stitu te for
B io log ical Stu d ies, La Jo lla , C a lifo rn ia .
C o n n ection s betw een cclls w ithin chc main cortical
layers show evidence o f early exuberance followed by elim i­
nation o f superfluous connections. The evidence reviewed
in Section 6.4.4a suggests that N M D A receptors are-
involved in elim inating surplus synapses.
6 .4 .6 b Inccrcolum n C o r tic a l Synapses
Fibers of pyramidal cells running parallel to the co rtical sur­
face link cortical cells with similar orientation cuning in
layers 2 to 6 (Section 5 .5 .6 ). Long-range fibers extend up to
6 mm and form fine branches distributed in repeating clus­
ters corresponding to the repeating orientation-selective
colum ns (G ilb ert and W iesel 1979; Rockland and Lund
1982; Luhm ann c t al. 1986).
In the cat, crudclv cluscered horizoncal connections
develop from layers 2 and 3 before the arrival o f co n n ec­
tions from layer 4, but the fine-tuning o f horizontal co n n ec­
tions occurs only after the arrival o f inputs from layer 4
(Callaway and Katz 1992).
Hata et al. (1 9 9 3 ) traced the developm ent of horizontal
connections by analyzing correlations betw een spike trains
recorded simultaneously at different lateral locations in the
visual cortcx o f kittens, a procedure developed by Pcrkcl
et al. (1 9 6 7 ). D uring the first 2 postnatal weeks, these co n ­
nections were wholly excitatory. Inhibitory linkages devel­
oped by the fourth week. Also, the connection s were
widespread betw een cells with very different orientation
preferences and did not show the clustered distribution evi­
dent in the adult. By week 7 , the con nection s becam e co n ­
fined to a radius o f about 6 0 0 ц т and со cells wich similar
oriencation tuning. A t the same time, the clustering pattern
emerged. Hata ec al. also found chac correlaced firings devel­
oped first in layer 4 but, by postnatal week 7 , the frequency
o f firing in layer 4 declined to the low level typical o fth e
adult and was overtaken by firing rates in other layers.
The refinem ent o f lateral connection s involves che
growch and elim ination of synaptic con n ection s rather than
cell death (Callaway and Katz 1990).
The clustering of lateral connections is less precise in
cats binocularly deprived during chc first few weeks o f life
(Callaway and Katz 1991). Ruthazer and Stryker (1 9 9 6 )
observed significant clustering o f laccral connection s in chc
cat by postnatal day 21. C lustering was further refined
during days 34 to 3 6 , when cclls acquired their orientation
tuning.
Dalva and Katz (1 9 9 4 ) studied the developm ent o fc o n -
nections in cultured slices of visual cortex from the ferret.
The slices were perfused with a form o f glutam ate that
remains inactive (caged) until activated by ultraviolet light.
By recording from a given cell .is neighboring cells were
activated by an ultraviolet laser they were able to map out
patterns of lateral connections. They confirm ed that local
connections are overproduced before birth and are subse­
quently reduced as long-range connections develop.
 W hen action potentials in the visual cortex o f ferrets
were silenced by infusion o f tetrodotoxin from postnatal
day 2 1 , the horizontal con n ection s did not develop the
adult clustering pattern (Ruthazer and Stryker 1996). It
seems that the initial clustering depends on spontaneous
neural activity at the level o f the L G N or cortex, but that
the fine-tuning o f the clustering pattern depends on cortical
neural activity arising from visual experience. However,
Butler et al. (2 0 0 1 ) found that the developm ent o f lateral
and interlayer con nection s from pyramidal cells in different
layers o f the ferret visual co rtex are affected in different ways
by rhe absence o f cortical neural activity. Thus, one can n ot
generalize over different classes o f connections.
B u rk h alteret al. (1 9 9 3 ) used a fluorescent dye to observe
the developm ent o f lateral connections in a series o f post­
m ortem human visual cortices from 2 4 weeks o f gestation
to 5 years postnatal. Lateral connections first emerged at 3 7
weeks o f gestation, after the developm ent o f radial co n n ec­
tions at right angles to the cortical surface. As in the cat,
lateral con nection s showed first in layer 4 B, bu t also in layer
5 and then in layer 6. Fiber density increased rapidly, lead­
ing to the form ation o f a uniform plexus at 7 weeks postna­
tal. The patchiness typical o f lateral con n ection s in the adult
cortex emerged after the 8th postnatal week. Longer-range
lateral con nection s in layers 2 and 3 did not emerge until
the 16th postnatal week and reached their adult form by
the 15 th m onth. These long-range con nection s were patchy
to begin with and rem ained patchy. Layer 4 B is associated
with rhe m agnocellular system, and layers 2 and 3 w ith the
parvocellular system. This suggests that, in the co rtex, the
m agnocellular system develops before the parvocellular
system.
I .ong-rcrm changes in synaptic conductivity along these
lateral pathways in the ca ts visual co rtex have been induced
by pairing synaptic responses with con d ition in g shocks o f
depolarizing current (H irsch and G ilbert 1 9 9 3 ). The results
suggest that these pathways are involved in stimulus-
dependent changes in cortical responses. Long-range lateral
con nection s could serve a variety o f functions, as listed in
Section 5.5.6.
N eurotrophins are involved in the developm ent o f col­
lateral con nection s betw een cortical cells receiving visual
inputs (spiny stellate cells in layer 4 ) and betw een cclls in
layers 3 and 5. They are also involved in development o f
con nection s betw een cortical output cells (pyramidal cells)
and cells in layers 2, 3 , and 5. Also, B D N F regulates the
expression o f one o f the receptors for the ncurotransm itter
dopam ine (Section 5 .5 .2 g ) in the central nervous system
(G uillin et al. 2 0 0 1 ).
6 .4 .6 c Transcorcical C o n n e c tio n s
In the cat, the projections of transcortical axons from area
17 to area 18 are established before birth. However, these
axons are evenly distributed between the various cortical
layers before the age o f about 2 0 weeks. Later, they arise
mainly in layers 2 and 3. D uring the same period, cells p ro ­
jectin g from area 17 to area 18 form into clusters through
the elim ination o f projections Irom intercluster zones (Price
et al. 1994}. These gross macurational changes do n o t depend
on visual experience, since binocular deprivation up to 2 8
weeks ot age did n o t stop them (Price and Blakemore 1985).
However, binocular deprivation and blockage o f afferents
from the L G N reduced the density and precision o f the pro­
jections from area 17 to area 18 (C aric and Price 1999).
6 .4 .6 d D e v e lo p m e n t o f th e C o r p u s C a llo su m
The structure o f the corpus callosum was described in
Section 5.3-5. In the cat, transcallosal connections are pres­
ent at birth, bu t rhe zone in each hemisphere from which
they originate (callo sal efferen t zone) and the zone to
which they project (callo sal term in al zo n e) are spread out
over areas 17 and 18. O nly later do they becom e restricted
to the boundary region between areas 17 and 18.
Before the arrival ot axons at the m idline, radial glial
cells in each hemisphere migrate through the dorsal septum.
M igrating cells differentiate in to astrocytes under the influ­
ence o f a fib ro b la st grow th fa c to r (F G F ). They form two
m idline populations o f astrocytes, one above and one below
the corpus callosum , known as the in tcrh cm isp h eric
brid ge. In m ice, the bridge forms 2 days before the appear­
ance o f pioneer callosal axons and fades after the corpus
callosum is formed (Silver et al. 1982). 'Ihese are the first
astrocytes to develop.
M ice lacking the gene for rhe fibroblast growth factor
exhibit callosal dysgenesis (Sm ith et al. 2 0 0 6 ).
G row ing transcallosal axons in vivo and in vitro are
guided through the intcrhcm ispheric bridge between the
two populations o f glial cells. The glycoproteins nerrin and
S lit2 secreted by the extracellular m atrix are involved in the
guidance o f these axons (Serafini c t al. 1 9 9 6 ; Shu T and
Richards 2 0 0 1 ; Shu T et al. 2 0 0 3 ). A lso, Fph receptors and
their ephrin ligands occur in the developing corpus callo ­
sum. The corpus callosum does not develop, or develops
incompletely, in m ice lacking one or m ore o f these recep­
tors (M endes et al. 2 0 0 6 ).
After the glial bridge has been cut, the axons that would
have crossed form into a pair o t neuronal knots (neurom as)
next to the central fissure. However, the axons begin to cross
it the bridge is repaired at an early enough stage (Silver and
Ogawa 1983).
The glial bridge does n o t form in mammals with co n ­
genital absence ot the corpus callosum. In acallosal humans
an aberrant longitudinal bundle o f axons w ithout organized
term inations forms in the w hite m atter ot both hemispheres
(Loeser and Alvord 1 9 6 8 ). This is known as P ro b s t’s
bu n d le. It consists o f axons that were prevented from cross­
ing in the fetus. Instead they turn in a sagittal direction in
the ipsilateral hemisphere. In acallosal m ice, many axons in
Probscs bundle cerminace ipsilaterally in chc same regions
as intrinsic association axons (O zaki c t al. 1 9 8 9 ). Callosal
agenesis is often associaced wich disorders such as hydro-
cephalus, m icrogyria, abnorm al cerebral fissures, or absence
o f cranial nerves.
The firsc axons Co cross chc m idline arise from the cingu-
lacc gyrus, in the archicortcx. These pioneer axons probably
guide axons from che neocorcex со cheir descinacions (Rash
and Richards 2 0 0 1 ).
In che cerminal zone, developing callosal afferents
migrate along radial glial fibers, which guide chem со their
destinations in chc various layers o f rhe corcex (N orris and
Kalil 1 9 9 1 ). A xon growch cones advance rapidly within the
callosal cracc wich only b rief pauses wich excensions o f
filopodia. They then extend radially through the cortical
layers until chey reach chc targee region. Ncxc, chcv pause
and produce transitory branches and show repeated cycles
o f advance and withdrawal as i f sensing ouc cheir environ-
menc (H alloran and Kalil 1 9 9 4 ).
D uring che firsc poscnacal week o f che cac, chc callosal
cerminal zone in each hemisphere becom es restricted to the
boundary becween areas 17 and 18— che region corre­
sponding to the vertical m idline o f the visual field. During
chc firsc 3 poscnacal monchs, chc callosal ctfcrcnc zone
becom es less densely populated and also restricted to the
m idline region (In n ocen ti 1 981).
C'allosal connections develop at about the same time as
ocular dom inance colum ns (Aggoun-Aouaoui ec al. 1996).
In macure cacs, cells in areas 17 and 18 chat receive callosal
con nection s occur in periodic stripes that stain with cy to ­
chrom e oxidase (Boyd and M atsubara 1994).
Ic has been suggested that callosal connections that sur­
vive are chose receiving correlaced inpucs from correspond­
ing regions near the vertical meridians o f the two eyes. These
arc binocular con n ection s. Cacs reared wich severe scrabis-
mus would lack correlaced visual inpucs Irom che cwo eyes
and should cherefore lack chc basis for chc scleccivc survival
o l callosal conneccions. For less severe strabismus, callosal
zones should be displaced inco chc concralaceral hemisphere
lor divergenc squinc and inco the ipsilateral hemisphere lor
convergent squinc. Ic has been claim ed chac, in scrabismic
cats, the efferent and recipient zones o f callosal connections
are discribuccd со an abnorm al degree beyond che midline
region (Lund ct al. 1 9 7 8 ; Innocenti and Frost 1979; Lund
and M itchell 1979a).
However, Berm an and Payne (1 9 8 3 ) found chat the cal­
losal term inal zones o f cxocropic or esocropic cacs were in
their norm al positions. Furtherm ore, Bourdet ct al. (1 9 9 6 )
found thac cacs raised wich even severe surgically induced
convergent or divergenc strabismus did noc show an abnor­
mal distribution o l callosal zones. A ccording to this evi­
dence, balanced binocular inpucs from corresponding
regions in chc cwo eves are noc required lor che chinning
and regional rescriccion o f callosal neurons. See Boire ec al.
(1 9 9 5 ) for a discussion o f chis issue.
Three paccerns o f conneccions in chc corpus callosum o f
the rac were described in Section 5.3.5. Symmetrical co n ­
nections link cells in the two eyes on opposite sides o fth e
m idline and are therefore capable o l registering binocular
disparities chac span chc m idlinc. Nonsymmecric co n n ec­
tions link cortical cclls that receive inputs from neighboring
locations on chc same side o f chc m idlinc in chc cwo rccinas.
A second cype o f nonsym m etric con nection s link cclls with
an input from a region in one eye wich cells in che opposice
hemisphere with an input from the same region in the same
eye. See Section 5-3.5 for more details. These m on ocular
co n n ectio n s cannot register disparity bu t presumably serve
to create a unified visual field.
D uring early developm ent, chc eyes are noc well aligned
so that there is little correlated activity arising Irom corre­
sponding regions in the cwo rccinas. Buc chere is good co r­
relation betw een inputs to the two hemispheres from
regions in the same eye. Thus, the developm ent o f m onocu­
lar connections could be guided by correlated inputs from
the same region in one eye rather chan from corresponding
regions in the tw o eyes. Even in strabism ic animals, one
would not expect these callosal zones со be alfecccd by
strabismus.
The developm ent o f callosal conneccions becween co r­
responding locations in the two eyes could be guided by
correlated accivicy arising from chc cwo eyes after chc eyes
have becom e aligned. W e will sec in Seccion 8 .2 .2 b chac
unbalanced visual inpucs produce an asymmccrical cransfer
o f signals through the corpus callosum .
Early binocular cnuclcacion in racs and cacs reduced chc
num ber o f cells in areas 17 and 18 receiving callosal co n n ec­
cions (Olavarria and van Sluyters 1995). In enucleated rats,
che mirror-image paccern o f conneccions in the medial
region o l the callosum was the same as that in norm al rats.
However, the nonsym m etric paccern o f conneccions
becween inpucs Irom che same side o l che m idline, which
occurs in che laceral region o f normal racs, was replaced by a
symmetric pattern (Olavarria and Li 1995).
In a subsequent paper Olavarria and H iroi (2 0 0 3 ) found
that these changes occurred only when the rats were cnuclc-
accd bccwccn poscnacal days 4 and 6. This evidence suggescs
that the symmetric pattern o l connections is the basic one
but that it is replaced by a nonsym m etric pattern in che lac­
eral region o f the callosum during postnatal days 4 and 6.
The basic sym m etrical pattern does not require visual inputs
and presumably develops under the guidance o f m olecular
markers. The nonsym m etric paccern requires visual inpucs
and presumably depends on correlaced visual inpucs.
F.tfeccs o f binocular deprivacion on che developmcnc o f
che corpus callosum vary with the type o f deprivation.
Binocular lid suture produced a greater reduction o f cal­
losal con nections than bilateral enucleation { Innocenti and
Frosc 1 9 8 0 ) or dark rearing (Frost and M oy 1989).
Thus, stim ulation chrough sutured eyelids is worse chan no
stim ulation.
 Innocenti and Frost found chat binocular enucleation These spatiotem poral m echanism s determ ine how an array
produced a wider than normal distribution o f callosal co n ­ o f initially identical prim ordial cells develops in to a well-
nections, while lid suture and dark rearing produced a dis­ ordered pattern o f diverse cell types.
tribution that was slightly narrower than normal. This Interactions betw een com plem entary m orphogen gra­
suggests th at either light o r spontaneous retinal activity dients also serve to guide growing axons to their destina­
control the width o f callosal connections. tion. Som e m orphogens act as attractants and others as
repellents. Som e are attractants at low concentration and
repellents at high concentration. For example, a low ante­
6 .4 .7 С E L L D 1F F E R E N T I AT I О N
rior to high posterior gradient o f a receptor molecule in
6 .4 .7 a M o rp h o g e n s and C c ll D ifferen tiation axons from retinal ganglion cells interacts wich a com ple­
mentary gradient ot a ligand in the optic tectum o f birds.
M orp h og en s are proceins produced in a restricted region
This ensures that each ganglion ccll connects w ith che
o f em bryonic tissue from w hence they diffuse to form a
appropriace cell in the tectum . N ote that a single gradient is
long-range concentration gradient. Three families have
n o t sufficient. For example, i f the receptor m olecules were
been identified: W ingless ( W N T ) , 1 ledgehog (H g ), and a
evenly distributed over ganglion cells all their axons would
third family. M orphogens operate at all stages o f develop­
all be attracted to one end o f the tectal gradient. C o rrect
m ent. They determ ine the basic anterior-posterior axis ot
mapping o f cells from one region o n to cells o f another
the early em bryo and the ventral-dorsal axis o f the neural
region requires an interaction o f counterbalanced forces o f
tube. Ac a later stage they help to form the basic structure ot
attraction and repulsion. C ell m igration may also depend
the retina, chiasm , and cerebral cortex.
on m echanical rather than chem ical interactions between
M orphogens bind to receptor m olecules on em bryonic
cells o r between cells and other structures.
cclls. The local concentration o f the m orphogen and the
type o f receptor m olecule determ ines w hich o f several types
o f cell a prim ordial cel! differentiates into. M orphogens and 6 .4 .7 b D e v elo p m en t o f C o r tic a l C c ll Types
cheir receptors induce changes in the genetic transcription
C o rtical neurons differ in the structure o f their dendritic
m echanism s in the cell nucleus.
arborizations and these differences are reflected in differ­
A concentration gradient o f one m orphogen may be
ences o f function. 'Ihere are tw o basic types o f excitatory
superimposed on that o f another m orphogen to create a
neurons in the co rtex; spiny stellate cells, m ost o t which
com plex pattern o f cellular environm ents. D ifferent m or­
radiate dendrites in all directions, and pyram idal cells that
phogens may trigger different responses in the same recep­
have triangular cell bodies w ith a single long apical dendrite
tors. O n e m orphogen may in h ib it the effect o f another
and several shorter basal dendrites (see Figure 5 .2 0 ).
m orphogen. Thus, a cell’s fate may depend on the com bined
Progenitor cells in the neocortex that express the gene
effects o f more than one m orphogen. Th e effect o f a m or­
EtnxJ give rise to excitatory neurons (pyramidal cells and
phogen may also be modified by the presence o f nonprotein
spiny stellate cells), C ajal-R ctziu s cells, and glial cells.
molecules.
G A B A ergic interneurons have a distinct lineage (G orski
T h e m orphogens and receptor molecules genetically
et al. 2 0 0 2 ).
expressed by a given cell change over time. After a cell has
D uring development, many pyramidal cells lose their
differentiated, its response to m orphogens is turned off.
apical dendrite and becom e transformed in to stellate cells.
This turning o ff can be achieved by endocytosis and subse­
Tliis can be observed in vivo and in cell cultures (Threadgifl
quent degradation o f receptor molecules or by production
et al. 1 9 9 7 ). It seems to be controlled by neurotrophins
o f antagonistic m olecules. C ell differentiation is also influ­
expressed in the extracellular matrix. This process could be
enced by interactions with neighboring cells.
under genetic control but it could also be influenced by
There are n o t enough m orphogens to determ ine the
neural activity. M ore research is required on this question.
m illions o f type o f cell. I lowever, the type o f cell that an
In Section 6.4.5a it was explained how N um b protein
undifferentiated cell develops in to depends on the follow­
m olecules determ ine w hether progenitor cells in many
ing faccors.
body tissues o f both invertebrates and vertebrates differen­
tiate or remain undifferentiated.
1. Location on superimposed m orphogen gradients.
The N o tch / D elta system is another signaling pathway
2. The types o t receptor molecules. involved in the developm ent o f several body tissues in inver­
tebrates and vertebrates. The N otch family o f cel I-surface
3- The age o f the cell.
proteins are receptors for D elta ligands attached to the
4. The cell’s neighbors. m em brane o f a neighboring cell. A ctivation o f a N otch
receptor by ccll-to-ccll co n tact sends a signal to the cell
5. Spontaneous o r stimulus-evoked activity.
nucleus that controls the expression o f several genes. In the
6. Epigenetic m echanism s (sec Scction 6.6.1) developing cerebral cortex, cells m igrating along radial glial
discussed in Section 6 .6 .3 . Their role in chc developm ent o f
ocular dom inance colum ns is discussed in Sections 6.7.1
and 8 .2 .3 .
6.5.1 T H E HEBBIAN SYNAPSE
6.5.1 a B a sic M ech a n ism o f the H c b b ia n Synapse
H cb b (1 9 4 9 ) proposed that synaptic contacts strengthen
when sim ultaneous activity in pre- and postsynaptic cells is
correlated, and weaken when it is uncorrelated (Portrait
Figure 6 .2 1 ). Ariens-Kappers c t al. had proposed a similar
idea in 1936. Synapses behaving in this way are called
Hebbian synapses. They were described in Section 4 .3 .4 f.
See C itri and M alenka (2 0 0 7 ) for a review o f synaptic
plasticity.
Long-term potentiation was first reported by Terje
Lom o in 196 6 (sec L o m o 2 0 0 3 ). Bliss and Cardncr-M edw in
(1 9 7 3 ) provided experim ental support tor the H ebbian
mechanism o f synaptic plasticity. They reported chat repeti­
tive activation ot cells in preparations in vitro o t the
dentate nucleus o f adult rabbits produced long-lascing aug­
m entation o t synaptic transmission. Subsequently, most
work on synaptic plasticity has been conducted on chc
hippocam pus— a region ol the old cortex, or paleocortex.
Figure 6 . 21 . D on ald O. H cbb. B orn in C hevter, N ova S c o tia , C an ad a, in
1 9 0 4 . H e o b ta in ed а В .Л . in psychology from D alhou sie U n iv ersity
in 1 925- H e was л sch o o ltea ch er for several years b efore o b ta in in g a
P h .D . w ith K arl Lashlev in psy chology a t H arvard U n iv ersity in 1 9 3 6 .
In 1 9 3 7 he becam e a fellow o f chc M o n trea l N eu rological Institu te
w ith \Xr. Penficld, and in 1 9 3 9 he o b ta in ed an acad cm ic ap p o in tm en t
at Q ueens* U niversity in C an ad a. In 1 9 4 2 he m oved to th e Ycrkcs
L ab o ra to ry in Flo rid a, and in 194~ he was appointed professor o t
psychology a t M c G ill U n iv ersity in M o n treal. A fter his retirem en t in
1 9 7 2 he retu rned to D alh o u sic U n iv ersity as professor em eritus.
H e died in 1 9 8 5 .
im plicated in spatial m emory (Fa/.eli 1992; Sherry c t al.
1 9 9 2 ). However, synaptic plasticity has been observed in
many cortical areas, especially during early development.
For example, synaptic con n ection s can be rcversiblv
strengthened or weakened in brain slices o f chc cac visual
cortex. Tli is was done by correlating postsynaptic responses
generated by stim ulation o f w hite maccer wich dcpolariza-
cion or hyperpolarizacion o f che poscsynapcic mem brane by
currenc delivered chrough che recordingeleccrode (Fregnac
ec al. 1 9 9 4 ).
C onsider cwo presynapcic cells converging on che same
synapse or on neighboring synapses on a single neuron.
W h en aecivicy in the presynaptic cells is synchronous, it is
more highly correlated with activicy in chc poscsynapcic cell
chan when che inpucs are asynchronous. This is because che
poscsynapcic m em brane sum maces pocencials from converg­
ing synchronous inputs more effectively chan from asyn­
chronous inpucs. The ouccom e is chac correlaced accivicv in
cwo or m ore converging inpucs leads со long-term p o te n ­
tiation (L T P ) o f the transmission efficiency o f that path­
way. W h en converging inputs are persistently uncorrelated,
the synaptic strength o f che one more highly correlaced wich
che poscsynapcic pocential eventually increases, while the
other suffers lon g-term depression (L T D ).
Changes in synaptic strength on a given neuron are
mainly confined to chc local group o f synapses on chc
neuron on which the inputs converge. Unstim ulated syn­
apses on cclls w ithin about 7 0 jun o f an active Hebbian syn­
apse may also m anifest L T P (Engert and BonhoefFer 1997).
However, L T P also involves a general change in che
incrinsic excicabilicy o f all che synapses on a neuron (see
Zhang and Linden 2 0 0 3 ).
The crucial events underlying neural plascicicy ac
Hebbian synapses involve che coaccivacion o t che N M D A
and n o n -N M D A recepcors (A M P A , kainace, and meca-
bocropic receptors) that were described in Section 5.5.2).
Two or more cypes o f recepcor on chc same poscsynapcic
m em brane are said со be colocalized . Each receptor co n ­
sists o f several glycoprotein m olecules surrounding a pore.
The glycoproteins round each pore differ to form distinct
receptor subunits, which help to determ ine chc specificicy
ot responses со diverse inpucs со a given synapse. The dis-
cincc subunics differentiate during early developmenc,
apparencly in response со specific presynaptic inputs (Shcng
e ta l. 1 9 9 4 ; G ottm an n et al. 1997).
The response o f n o n -N M D A receptors depends only
on presynaptic release o f the neurocransmicccr glucamacc.
By concrast, the response of N M D A receptors to glutamate
is blockcd by m agnesium ions unless the poscsynapcic
m em brane is depolarized. The postsynaptic m em brane is
depolarized by chc accivacion o f fasc accing n o n -N M D A
recepcor sices (parcicularly A M PA sices) on che sam e posc­
synapcic m em brane. Backpropagating action potentials
w ithin the postsynaptic dendrites may also be involved, as
described in Section 6.5.2.
 Electric shocks delivered at a frequency o f 5 H z to the
white m atter underlying both the hippocam pus and the
visual cortex produced a long-term increase in synaptic
conductance, except when an antagonist inhibited N M D A
receptors (K im u ra e t al. 1 9 8 9 ). Inhibition o f N M D A syn­
apses in neonatal rats triggered a wave o l ccll death in the
hippocampus and in the parietal and frontal lobes
(Ikonom idou et al. 1999).
D uring I.TP, the release ot glutamate by the presynaptic
m em brane follow ing removal o f magnesium ions by posc-
svnaptic depolarization triggers a voltage-dependent
response in the N M D A receptors. Tli is produces a graded
release ot postsynaptic calciu m ion s into the cell. W hen the
concentration o f calcium ions exceeds a critical level it trig­
gers an accum ulation ot activated enzymes, known as
p rotein kinases, in cytoplasm ic structures abutting the
postsynaptic receptors (Lism an 1989; Asztely and
Gustafsson 1 9 9 6 ; D i C risto c t al. 2 0 0 1 ). These include
с A M P-dependent protein kinase (P K .C ) and calcium/
calm odulin-dcpcndcnt protein kinase 11 ( C a M K I l).
W h ile m ost protein synthesis occurs in the cell soma,
C a M K Il is synthesized in the dendrites, because dendrites
contain m R N A for the expression o f this protein (M iller
c t al. 2 0 0 2 ) (see Section 6 .4 .4 ). Sec Wayman c t al. (2 0 0 8 )
tor a review o f the role o f calm odulin-kinases in synaptic
plasticity.
There are tw o isoform s o f C a M К 11. The first, C a M К I la ,
responds to activity at N M D A receptors and high calcium
levels. 'I he secon d ,C aM К 11 responds to activity at A M PA
synapses and low calcium levels. The ratio o f a to (6 isoforms
is inversely regulated by neural activity (Thiagarajan et al.
2 0 0 2 ). This may help in the hom eostatic regulation o f
C a M K Il activity.
Calcium /calm odulin kinase 11a acts as a m olecular
switch. A transient rise in calcium ions during synaptic
activity moves it into its active, phosphorylatcd state.
Activated C aM К I la is translocated from the dendritic
cytoplasm to the synaptic density o t the postsynaptic m em ­
brane. Tli is process has been observed in vivo over a period
o t m inutes in specific synapses ot zebra fish by tagging
C a M K Il with a green fluorescent protein (G leason c t al.
2 0 0 3 ).
The protein kinase molecules remain active for
about 6 0 minutes after the trigger stimulus has ceased
(Otm akJcov c t al. 2 0 0 4 ). This m aintained activity is due
to protein phosphatases attached to the protein molecule
that allow ic to autophosphorylate (C olbran 2 0 0 4 ).
Experience-dependent cortical plasticity in the visual cortex
is absent in m ice lacking the gene responsible for autophos­
phorylation o f C aM К 11 (Glazew ski et al. 2 0 0 0 ; Taha ec al.
2 0 0 2 ). There is con flictin g evidence about w hether inhibi­
tion o f C a M K Il reverses L T P after ic has been induced
(C h en ec al. 2 0 0 1 ).
Accivation o f C a M К 11 increases the perm eability o f the
cell m em brane со calcium ions. Furrherm orc, introduction
o f C a M K Il into in vitro hippocam pal cclls enhanced
synaptic transmission and axonal growth (Shirke and
M alinow 1997; Jourdain ct al. 2 0 0 3 ). Ac neighboring syn­
apses, lacking N M D A activation, C a M K Il weakens synaptic
transmission (Prate ct al. 2 0 0 3 ). This double action generates
structural rearrangements in synaptic connectivity.
Stim ulation that produces concentrations o f calcium
ions below the critical level triggers long-term depression
(L T D ) o f synaptic conductance (Singer 1990; Kirkwood
and Bear 1 9 9 4 a ; Ghosh and Greenberg 1995; Scanziani
et al. 1996). The critical level ot stim ulation tor the transi­
tion betw een L T P and L T D is itse lf increased after a period
ot increased activity and decreased after a period ofdecreased
accivicy (Kirkw ood cc al. 1 9 9 6 ). The low level o f calcium
ions associaccd wich L T D may arise because o t lasting depo-
larizacion o fth e postsynaptic m em brane after the poscsyn-
apcic spike For a review o t chis and relaced copics see
Karmarker cc al. ( 2 0 0 2 ) and M oncgom crv and Madison
(2 0 0 4 ).
The A M PA recepcors on che postsynaptic membrane
are activated by glutamate. They m ediate the responses o f
the major fasc-acting excitatory synapses in chc brain. The
receptors consist o f subunits G lu R l to G lu 4. D uring LTP,
C a M K Il binds со N M D A rcccpcors on chc poscsynapcic
membrane. This accivaces G lu R l recepcor molecules
(Carroll ec al. 1998). Ic also leads со the insertion o f new
A M PA receptors into the mem brane (Lism an and
Zhabocinsky 2 0 0 1 ). The A M PA recepcor molecules are
cransporccd to the postsynaptic m em brane from secretory
structures w ithin the ccll known as en d osom es. The end o­
somes contain a reserve o f A M PA receptor molecules
(P ark er al. 2 0 0 4 ).
Sensory experience during che critical period o f devel­
opm ent o f the mouse barrel cortex (an area serving tactile
inputs from the whiskers) increased the delivery o f G lu R l
receptor m olecules to the postsynaptic mem brane o t
A M PA synapses (Takahashi c t al. 2 0 0 3 ).
G lu R l receptor molecules have long cytoplasm ic tails
(C -cails) chac can be identified in living neural cissuc by tag-
gingchem with a green fluorescent protein (G F P ). Subunits
G lu R 2 and G lu R 3 o f A M PA reccptors consist o f molecules
with short cytoplasm ic tails. Kopec e t al. (2 0 0 7 ) revealed
that G lu R l recepcors play a dual role in LTP. The C -cails o f
the reccptors play an essential role in increasing the size o f
dendritic spines, while chc rcccpcors’ ion channcl increases
synaptic efficiency.
After rcduccd synapcic accivicy, chc num ber o f AM PA
recepcor molecules is reduced, w hich leads со L T D
(K irkw ood cc al. 1 9 9 6 ; Zhu cc al. 2 0 0 2 ).
Thus, che crucial evenc in L T P is an increase in AM PA
recepcors on che postsynaptic m em brane by protein kinases
produced by activacion o f N M D A recepcors. The crucial
evenc in L T D is a decrease in A M PA rcccpcors on che posc­
synapcic m em brane (see Song and Huganir 2 0 0 2 ). The
cwo processes acc cogether in a given region. Also, LT P at
inhibitory synapses is involved in che production o f L T D ac
excitatory synapses (Kom atsu and Yoshimura 2 0 0 4 ).
D uring I.TP, Л М Р Л receptors move from the endo-
somcs to the synaptic m em brane. D uring L T D , Л М РА
receptors arc removed from the postsynaptic m em brane.
"The molecules destined for removal becom e attached to
u b iq u itin , a process known as u b iq u itin a tio n . The marked
proteins arc brought into a pit that closes ro form a capsule
in the cytoplasm o f the cell (Scctio n 5.5.2a). This process is
known as e n d o cy to sis. In the capsule, the molecules are
assembled into a lvsosom
/ c where thevi are broken down
(Hegde and D iA n ton io 2 0 0 2 ). U biqu itin ation , and hence
turnover o f proteins on the postsynaptic density, increases
with increased synaptic activity and is mediated by a family
o l protein kinases (Pak and Sheng 2 0 0 3 ).
O th er types o f receptor, such as N M D A and G A B A
receptors on postsynaptic m em branes, show the same
dynam ic balance betw een mem brane insertion and endo-
cytosis (sec C arroll and Ztikin 2 0 0 2 ). Endocytosis o f recep­
tor m oleculcsdoes m ore than regulate synaptic transmission.
For example, endocytosis o f ncurotrophins atfects a cell’s
trophic functions (C arroll e t al. 2 0 0 1 ).
Postsynaptic m em branes in the immature cortex lack
A M PA receptors. In the absence o f A M PA receptors, acti­
vation o f N M D A receptors is blocked by magnesium ions.
For this reason im m ature synapses have a high threshold
and are called sile n t synapses. D uring the first postnatal
m onth, neural activity and neurotrophin activity cause
N M D A synapses ro acquire A M PA receptors and rhe
response threshold declines (Feldm an and Knudscn 1998;
Rumpel et al. 1 9 9 8 ; Petralia et al. 1 999).
A ctivity-induced m odifications o f synaptic strength
becom e consolidated into perm anent patterns only after
several repetitions o f a stimulus. For an hour ot so after ini­
tial induction o f LTP, introduction o f new stimuli can cause
a reversal to the original state (see Z hou and Poo 2 0 0 4 ).
During learning, the N M D R reccptor subunit N R 2a
increases relative to the N R 2 b receptor subunit (Q uinlan
et al. 2 0 0 4 ). The N R 2a reccptor has a higher threshold than
the N R 2b receptor, so that its increase renders the synapse
more resistant to m odification.
The basic activity-induced postsynaptic changes at a
Hebbian synapse may be summarized as follows. Excitatory
inputs that coactivatc N M D A and A M PA receptors above
a critical level increase the number and efficiency o f A M PA
receptors on the postsynaptic m em brane. Excitatory inputs
below the threshold for activation o f N M D A synapses
decrease the num ber and efficiency o f A M PA receptors.
This form s a m echanism for detecting coincid ent and co r­
related activity in inputs converging on a cell. O f particular
im portance for this book, these processes provide a m echa­
nism for establishing use-dependent neural netw orks sensi­
tive to binocular disparity. Berns et al. (1 9 9 3 ) developed a
com puter m odel o f this process. O th er structural changes
underlying learning were described in Section 5.6.8.
6 .5 .1 b M e ta b o tro p ic R eceptors and
Synaptic plasticity
M etabotropic glutamate receptors are often adjacent to
NMDA receptors on the postsynaptic membrane.
M etabotropic receptors involve a cascade o f second messen­
gers (Section 5 .5 .2 d ), which are im plicated in long-term
potentiation (B o rto lo tto et al. 1994; Riedel 1 9 9 6 ; Benquet
et al. 2 0 0 2 ). W h en a m etabotropic glutamate agonist is
applied to the visual cortex, the response o f N M D A syn­
apses is potentiated (W ang and Daw 1996). The second
messengers o f m etabotropic receptors may also be involved
in memorv consolidation.
M etabotropic receptors are particularly prevalent
during the critical period for form ation o f ocular dom i­
nance colum ns (Reid 1995). There is evidence th at they
provide an alternative to N M D A receptors in induction o f
L T P in the neonate (Section 6 .6 .3 ) However, m etabotropic
receptors are not involved in the long-term depression o f
responses o f cortical cells to stim ulation o f a visually
deprived eye (sec Section 8.2.6b ).
6.5.1 с O t h e r Factors in Syn aptic Plasticity
The brain-derived ncurotrophic factors B D N F and N T 3
and their associated Trk receptors are implicated in activity-
induced L T P at Hebbian synapses (K angand Schum an 1995;
Patterson et al. 2 0 0 1 ; G ottm ann et al. 2 0 0 9 ). Responses aris­
ing Iroin release o f neurotransmitters are amplified by action
potentials initiated in postsynaptic dendrites by BD N F.
Pairing a weak burst o f presynaptic stimulation with a brief
application o f B D N F to the postsynaptic dendrite induced
immediate and robust L T P (Kovalchuk et al. 2 0 0 2 ).
Production o f B D N F increases in the neighborhood o f
neuronal activity and ncurotrophins enhance release o f
ncurotransm itter in presynaptic neurons containing the
receptors for B D N F (Thoenen 1995). To be effective in
controlling activity-dependent plasticity, the effects o f
B D N F m ust be restricted to active synapses. U nlike other
ncurotrophins, the B D N F m olecule has a very limited
range o f diffusion. Also, the effects o f B D N F are spatially
restricted because the TrkB receptor molecules for B D N F
form on the postsynaptic mem branes o f activated synapses
(sec Nagappan and I.u 2 0 0 5 ).
Introduction o f B D N F potentiated the response o f
in vitro N M D A receptors and rapidly elevated their intrac­
ellular calcium levels (Jarvis et al. 1 9 9 7 ). A dm inistration o f
N G F or B D N F to slices o f cm brvonic
i rat brain increased
the amplitude o f stimulus-evoked synaptic responses and
B D N F increased the frequency o f spontaneous responses
(C arm ign o to et al. 1 9 9 7 ). M utant m ice,deficient in B D N F ,
showed shrinkage ot cortical neurons and retraction of
dendrites (G orski et al. 2 0 0 3 ).
The inhibitory neurotransm itter G A B A , and the neu­
rotransm itter norepinephrine are o ther factors implicated
in chc developm ent o f che visual corcex. This topic is dis­
cussed further in Section 8.2.4.
Astrocytes arc also involved in transmission at N M D A
synapses. G lutam ate released at n o n -N M D A synapses stim ­
ulates neighboring astrocytes to release the am ino acid
D -sc rin e into the synaptic gap o f N M D A synapses. The
gene for D -serine is active in these astrocytes. Application
o f an enzyme that degrades D -serine reduced transmission
at N M D A synapses in rat brain slices (W olosker e t al.
1999). Also, clam ping the release o f D -serine from astro­
cytes blocked L T P in neighboring cells in the hippocampus
(H enncberger ec al. 2 0 1 0 ).
6.5.2 SPIKE T IM IN G -D E P E N D E N T
PLA STICITY
Tem poral relationships betw een pre- and postsynaptic
events are im portant in I.T P and L T D . This is known as
sp ike tim in g -d ep en d en t p lasticity , or S T D P (Karm arkcr
c t al. 2 0 0 2 ).
In slices o f pyramidal cells from the rat neocortex, back-
propagatingaction potentials were initiated in the postsyn­
aptic neuron by stim ulating the cells soma. A t about the
same tim e, the presynaptic neuron was stim ulated. The
response ot the synapse was increased (L T P ) when, over
many repetitions o f the stimulus sequence, the presynaptic
stimulus preceded the postsynaptic stimulus by 10 ms. The
response o f the synapse was depressed (L T D ) when the pre-
synaptic stimulus followed w ithin 4 0 ms o f the postsynap­
tic stimulus (M arkram et al. 1 9 9 7 ).
In a similar experim ent using slices o f cells from rhe rat
hippocampus, postsynaptic spikes that followed presynap­
tic activation within 2 0 ms induced LTP. Spikes chac
preceded prcsynaptic spikes by up to 2 0 ms induced L T D
(B i and Poo 1998).
Spike tim ing influences the developm ent o f the tuning
o f cells in the developing nervous syscem. For example,
repetitive exposure ot the tectum o t Xenopus tadpoles to a
bar moving in a given direction led to the developm ent o f
cells tuned to direction o f m otion (M u and Poo 2 0 0 6 ).
Spike tim ingcan also produce changes in the tuning func­
tions o f cells in the adult visual cortex. For example, repetitive
pairing o f visual stimuli in different orientations induced a
shift in orientation tuning o f neurons in the visual cortex o f
the cat (Yao and Dan 2 0 0 9 ). Pairing a b rief flickering grating
with stimulation o fth e visual cortex o f the cat shifted the ori­
entation preference o f cells in a direction that depended on
the order o f the paired stimuli (Schu ett et al. 2 0 0 9 ).
A ctivity-induced synaptic plasticity also depends on
stimulus-induced spiking patterns. For example, after a pair
o f pre-and postsynaptic spikes, succeeding spikes w ithin up
to several tens o f m illiseconds had no effect (Froem ke and
D an 2 0 0 2 ).
‘Ihe effectiveness o f presynaptic potentials preceding
postsynaptic potentials by 10 ms increased as the repetition
race was increased to 50 H z. Thus a reasonable repetition
rate is required to depolarize the postsynaptic membrane
to the level necessary for I.T P (Sjostrom et al. 2 0 0 1 ).
It seems that single backpropagating potentials do not
remove che m agnesium -ion block at N M D A synapses.
A temporal integration o f voltage is required. The depen­
dence o f neural plasticity on both spike tim ing and spike
frequency is com plicated by the fact that a given presynap­
tic potential may be both preceded by and followed by p ost­
synaptic potentials (see Sjostrom 2001 for a discussion o f
this issue).
Although backpropagating accion potentials reach
proximal synapses (those near the som a), they are strongly
accenuaced when they reach the distal synapses.
Backpropagating action potentials in pyramidal cells in
layer 5 o fth e rat neocortex increased the am plitude o f post­
synaptic potentials in distal synapses when the tim ing o f the
two events was similar to the tim ing requires for induction
o f L T P (Stu art and Hausser 2 0 0 1 ).
Lisman and Spruston (2 0 0 5 ) raised some o bjection s to
the view that backpropagating potentials provide the only
postsynaptic potentials required for L T D . They pointed
out that the evidence was based on the use o f artificially
induced backpropagating potentials in the presence o f weak
excitatory potentials. G olding et al. (2 0 0 2 ) found that
strong synaptic stim ulation induced L T P in distal synapses
in hippocam pal cells when tetrodotoxin blocked backprop-
agatingaction potentials. They produced evidence that L T P
in distal synapses depends on depolarization induced by
regenerative neural spikes generated locally w ithin small
dendritic dom ains. A zouz and Gray (2 0 0 0 ) and Letzkus
et al. (2 0 0 6 ) produced further evidence that spike tim in g -
d ep en d en t plasticity depends on faccors operating locally
within the dendritic tree o f the neuron.
Pyramidal cells with cell bodies in cortical layer 5 o f the
neocortex receive excitatory inputs trom proximal synapses
in layer 5 and from distal synapses in layers 2 and 3. Inputs
trom distal synapses are attenuated relative to those trom
proximal synapses because they have further to travel before
reaching the soma (W illiam s and Stuart 2 0 0 3 ). Also, the
amplitude o f backpropagating potentials is attenuated in
distal synapses.
Using patch-clam p recordings and tw o-photon imag­
ing, Sjostrom and Hausser (2 0 0 6 ) found that a given stim u­
lus generated I.T P in proximal synapses and L T D in distal
synapses o f the same pyramidal cell. The gradient o f plastic­
ity between L T P and L T D was a function o f the degree o f
backpropagation o f potentials along the axon. Boosting
backpropagation to the distal synapses changed the L T D
into LTP. Thus, the magnitude o f backpropagation from
layer 5 regulates the sign and magnitude o f plasticity in
superficial co rtical layers. Inputs to proximal synapses in
pyramidal cells o t cortical layer 5 are mainly local, while
inputs to distal synapses in superficial layers are from higher
co rtical centers. Thus, inputs trom local centers could
regulate the sign and degree o f cortical plasticity in synapses
activated by higher centers.
The above mechanism does n o t work for all neurons.
For example, for neurons in the hippocampus, potential
amplitudes arc the same for proximal as tor distal synapses
because distal synapses have a com pensatory increase in
the density o f glutam ate receptors (W illiam s and Stuart
2 0 0 3 ).
A ctivation o f cholinergic and adrenergic neurom odula-
tor receptors can also determ ine w hether a given relative
tim ing o f presynaptic and postsynaptic firing produces LT P
or L T D (Seo l et al. 2 0 0 7 ). Thus, chc behavior o fth e animal,
as it affects the activation o f neurom odulators, can control
corcicai plascicicy.
Long-term depression chac depends on advanced post-
synapcic accivicy is anci-H ebbian because ic dececcs differ-
cnees rather chan coincidences. Ic could form che basis tor
predictive coding in which postsynaptic activity arising
trom higher centers and generated in advance o t scimula-
cion gaces che sensory inpucs according to whecher chey
conform со what is anticipated. For reviews o f spike
cim in g-d cpcn d cn c plascicicy see Bi ( 2 0 0 2 ), Kepees ec al.
(2 0 0 2 ), and Dan and Poo (2 0 0 6 ).
6.5.3 PRES YN AP TIC PROCESSES
IN L T P A N D L T D
Up to now, only postsynaptic changes at Hebbian synapses
were considered. Buc L T P and L T D also involve changes in
che presynapcic neuron.
'Ih c usual mechod ofm easuringneurocransm iccer release
is со record postsynapcic potentials elcctrophysiologically, a
method chac does n o t clearly distinguish becween prc- and
postsynaptic changes. Patch clam p recordings trom the pre­
synapcic m em brane ofcu lcu red hippocam pal synapses have
revealed that repetitive correlated firing ot pre- and post­
synapcic neurons resulcs in rapid and persiscenc enhance-
menc o f presynaptic excitability, lowered spiking threshold,
and reduced variability o f spike frequency (Ganguly et al.
2 0 0 0 ). Long-term potentiation is noc induced by eicher
poscsynapcic depolarizacion alone o r by presynapcic s im u ­
lation alone (O tsu et al. 1 995).
Pharm acological m ethods allow one со visualize chc
release ot neurotransm itter trom presynaptic vesicles at
individual synaptic boutons (M algaroli e ta l. 1995). A fluo­
rescent marker ot presynaptic activity has revealed enhanced
neurotransm itter release after L T P (Z akharenko c t al.
2 0 0 1 ). Inhibition o f the presynaptic enzym e, calcium -
calm odulin-dependent kinase II (C a M K Il), abolished
these changes wichouc afFeccing poscsvnapcic LTP.
Changes in the presynaptic neuron require a retrograde
messenger from the postsynaptic m em brane. O n e possibil­
ity is the diffusion o t nieric oxide from the postsynaptic
m em brane (M oncague ec al. 19 9 4 ; Wu cc al. 1 9 9 4 ). There
has been a dispute about the role o f nitric oxide in synaptic
plascicicy. In some scud ics, L T P was prevenced by inhibicion
o f nitric oxide synthesis (Schum an and M adison 1991).
However, ocher invcscigacors have rcporccd chac sensory-
dependent plasticity resulting from m onocular depriva­
tion in kiccens is noc affected by inhibicion o f nicric oxide
synchesis (Reid ec al. 1996a). M ore recent evidence sug­
gests thac cherc is more chan one way со synchesize nicric
oxide. A nim als in which the genes for both types o f
synthesis arc deleted do noc show synapcic plascicicy
(H olsch er 1 9 9 7 ).
Ephrin-B ligands and cheir EphB recepcors are also
implicated in presynapcic changes. Introduction o f the
ligand ephrin-B produced an increase in the density o f pre­
synaptic vesicles (D alva e t al. 2 0 0 0 ). Inactivation o f E p hB2
receptors in cortical-cell cultures decreased the frequency
o f synapcic evencs (Kayser ec al. 2 0 0 6 ).
Ic is now known that N M D R receptors occur on the
presynaptic mem branes o f both excitatory and inhibitory
cortical cells. Their activation by glutamate modulates neu-
rotransm itter release in many pares o f che nervous syscem
(see M acDerm occ et al. 1 9 9 9 ). This m odulation occurs on a
second-by-second basis and is shore lascing.
Sjostrom ec al. (2 0 0 3 ) produced evidence that presyn­
aptic N M D A receptors are involved in some forms o f LTD .
They proposed thac presynapcic N M D A recepcors detect
activity in the presynaptic neuron by responding to the glu­
tamate neurotransm itter released from the presynaptic
m em brane. O th er receptors on the presynapcic mem brane
( С В 1 receptors) d etect activity in the postsynaptic m em ­
brane by responding со cn d o ca n n a b in o id s released from
che poscsynapcic m em brane.
Repeated coactivacion o f N M D A and C B 1 recepcors
induced L T D in pyramidal cells in che rac visual corcex. For
che cwo recepcors со be coaccivaced, accivacion o fth e p ost­
synaptic m em brane muse precede chac o f chc presynapcic
membrane. O therw ise, cndocannabinoids would n o t reach
the presynaptic m em brane while neurotransm itter was
being released. Thus, this process is a form o f spike tim in g -
d ep en d en t plasticity. The critical tim ing was found to vary
with che availabilicy o t cndocannabinoids.
A similar process produced L T D ac inhibicory synapses,
which released excitatory pyramidal cells from inhibition
and thereby enhanced L T D in pyramidal cells (Chevaleyre
and Castillo 2 0 0 4 ).
Thus, boch presynapcic and poscsynapcic processes are
involved in L T P and L T D . Boch depend on C a M K Il and
on correlaced accivicy ac N M D A synapses. However, more
recenc evidence shows that the presynaptic mechanism
operates only before the critical period o f cortical neuro­
plasticity. C orlew et al. (2 0 0 7 ) demonstrated a rapid loss o f
presynaptic N M D R recepcors in che visual corcex o f m ice ac
the onset o f the critical period. Before the critical period,
induction o f spike tim ing-dependent L T D depended on
accivacion o f presynapcic N M D R recepcors. D uring and
after che cricical period, L T D depended on activation o f
inputs representing a particular stimulus feature. They
called this branch-spikc plasticity. Since different branches
o f a neuron could be sensitive to different stimulus features,
the neuron could com bine inform ation about different
features.
G row ing axons are controlled by a variety o i protein
ligands' secreted by the extracellular matrix. D uring early
developm ent, dendrites o f mature synapses in the brain
becom e wrapped in a dense mesh formed from the extracel­
lular matrix. This stabilizes synapses by hindering the diffu­
sion o f A M PA receptor molecules and other mem brane
proteins betw een cclls. Frischknecht et al. (2 0 0 9 ) proposed
that inhibitoryJ effects o f the extracellular matrix form den-
dritic com partm ents th at contain specific surfacc proteins.
This would allow for the delivery o f A M PA receptors to
particular synapses in a dendritic tree and thereby produce
changes in particular synapses.
6 .6 N E U R A L A C T IV IT Y A N D
С О R T 1 С A L D КV E L О P M К N T
6 .6 .1 N E U R A L A C T IV IT Y AN D G EN E
E X P R E S S IO N
6 .6 . Ia Neural C o n tr o l o f G e n e Tran scrip tion
Tlie human genom e contains about 2 5 ,0 0 0 genes arranges
along the D N A double helices o f the chrom osom es. They
code the basic catalog o f all proteins. After fertilization, the
zygote divides in to pluripotcnt identical cells. A fter that,
different tissues becom e progressively specialized for spe­
cific functions. Therefore, specific genes must be activated
in different tissues and at different times so as to provide the
relevant proteins. Neural plasticity, including learning, also
requires proteins to be expressed by specific genes in
specific neurons at specific times.
M olding o f gene expression in different tissues and at
different times during developm ent is known as epigenesis.
In the last 3 0 years there has been an explosive increase in
knowledge ofepigenesis (H irabavashi and G o to h 2 0 1 0 ).
C hrom osom es do n o t consist only o f D N A . In each
chrom osom e, the D N A helix is wrapped round a core co n ­
sisting o f four types o f historic proteins, Н 2 Л , H 2 B , H 3,
and H 4 . Each repeating D N A unit o f 147 base pairs wraps
round four pairs o f histone m olecules to form a disk-shaped
nucleosonic. The nuclcosom cs form an array, like beads on
a string.
H istone molecules con tain lysine and arginine am ino
acids that protrude from the nuclcosom c. These am ino
acids may be modified by phosphorylation or by addition
o r removal o f one o r m ore methyl or acetyl groups. These
m odifications either activate or suppress transcription o f
particular genes. For example, histone d cacctylascs
(H D A C s) remove acetyl groups from histone molecules.
Tliis opens up specific nuclcosom cs to transcription factors,
which facilitates transcription o f specific genes. O th er
enzymes add methyl groups, condense the nucleosom es,
and suppress gene expression.
G en e transcription is also controlled by m ethylation o f
cytosine. This is one o f the four nucleosides that form the
base pairs o f the D N A genetic code.
M ethylation may be short-lived or may persist and be
passed on to other cclls in the same cell line of the develop­
ing anim al. M ethylation o f histones and cytosine is specific
to the particular type of cell. Barski e t al. (2 0 0 7 ) produced
a map o f m ethylation o f histones in the human genome.
The com plete pattern o f m ethylation o f cytosines in the
human genom e has been mapped in tw o types o f cell— stem
cells and fibroblast cells (L ister et al. 2 0 0 9 ). This type o f
work will ultim ately reveal the epigenetic maps o f a wide
variety o f cell types.
Epigenesis affects basic developmental processes. For
example, animals possess two sets of chrom osom es, one
from each parent. In mammals, about 100 genes are
expressed from the genom e derived from only one or the
other parent. This is known as genom ic im printing.
M ethylation o f histones and cytosine determ ines which o f
a pair o f genes is expressed (C icco n e et al. 2 0 0 9 ).
The m ost remarkable thing for the subject o f this book
is that m ethylation o f histones and cytosine during devel­
opm ent is controlled by the activity o f cells. In the develop­
ing visual system, gene expression in particular neurons is
governed by visual experience. For example, neural responses
activate histone dcacctylascs that regulate the expression o f
proteins required for m aturation o f synapses in early devel­
opm ent (see A khtar et al. 2 0 0 9 ). This explains why visual
experience in neonates has dram atic effects on the develop­
m en t o f the visual system.
Neural activity at N M D A synapses also affects how the
nuclei of neurons in the hippocampus are folded (W ittm an n
ct al. 2 0 0 9 ). The pattern o f folding affects how calcium sig­
nals from active neurons gain access to the nucleus so as to
m ethylate particular histones. Thus changes in the geom etry
of the nucleus constitute another epigenetic mechanism.
As a given type o f ccll divides, the pattern o f methyl.»-
tion and acctylation is conveyed to the genom e of the new
ccll. The process takes time so that there is a period during
which signals impinging on the cell can m odify the pattern
o f m ethylation and acctylation (S ch arf et al. 2 0 0 9 ). This
process o f changing m ethylation is responsible for the d if­
ferentiation o f cells from stem cells to precursor cclls to spe­
cialized mature cells. O n ce a nerve cell has matured it does
n o t divide again. However, neural activity still controls
m ethylation o f D N A and the expression o f proteins
required for learning in the adult animal (sec M iyashita
et al. 2 0 0 9 ; G upta et al. 2 0 1 0 ; F en g eraL 2 0 1 0 ; M iller et al.
2 0 1 0 ).
Epigenetic processes during developm ent affect the
phenotype but do not affect the D N A genetic code.
However, chere is a grow ing body o f evidence chac
som e patterns o f m cthylation or acetylation o f histones in
germ cells mutate and are inherited across generations.
Unlike D N A m utations, epigenetic m utations are revers­
ible. They could control the race o f mucacion o f particular
D N A genes or patterns ol genes (see Jablon ka and Lamb
2 0 0 5 ).
6 .6 .1 b N e u ra l C o n t r o l o f G e n e T ra n sla tio n
The epigenetic m echanism s discussed so tar affect gene
expression by controlling transcription o f inform ation со
m R N A s in che cell nucleus. Epigenesis also involves control
o f how m R N A s translace inform ation to produce proteins.
This p o sttran scrip tion al co n tro l is achieved by m icroRN As
(m iR N A s). They are small noncoding RN A s, w hich means
that they do not express proteins. M ore than 2 0 m iRN A s
have been discovered (S cctio n 6 .4 .2 b ).
Neural activity releases calcium ions that produce a cas­
cade o f m olecular signals, including C R E B , chat pass to the
cell nucleus. The signals lead to the transcription ot m RN A s
and m iR N A s. In neurons, m R N A s and m iR N A s are trans­
ported along niicrotubules to local sites (Section 6.4.3a).
The m iR N A s modulate the activity o f m R N A s and thus
regulate protein translation in dendrites and synapses. Local
control o f protein synthesis is more efficient than control in
the cell nucleus because it can be guided by local activity in
cellular subcom partm ents. Also, local control allows tor the
coordinated expression o f functionally related proteins
when and where they are needed (M ikl et al. 2 0 1 0 ; Szaro
and Strong 2 0 1 0 ; W ang e t al. 2 0 1 0 ).
Specific m iR N A s operate in con cert with a G T P asc
protein ro control activity-induced growth o f dendrites in
cortical neurons (V o et al. 2 0 0 5 , 2 0 1 0 ). C o n tro l is medi­
ated by regulation o f t h e activity o f the actin cytoskeleton
(Siegel e t al. 2 0 0 9 ). M iR N A s also influence cell diflerentia-
tion and form ation o f cellular networks (see Fineberg
e t al. 2 0 0 9 ).
6 .6 .1 c A ctiv ity -R e g u la te d G e n e s
Sensory signals release ncurotransm ittcr at central synapses.
This induces an influx o f calcium ions, which triggers a cas­
cade o f signals that pass to the cell nucleus where they
induce particular genes to produce transcription factors.
These are known as im m ed iate-early genes, but a better
name would be activ ity -reg u lated genes. Transcription
factors are proceins ch.it bind to specific D N A sequences
and thereby transfer (transcribe) genetic inform ation from
D N A ro messenger ribonucleic acids (m R N A s) required
for the production o f specific proteins.
The first activity-regulated gene to be discovered was
c-fos, which encodes the Fos transcription factor. The co n ­
centration o f Fos increases in an area o f the chick s brain
when the chick is being imprinted on its parent (see Suge
c t al. 2 0 1 0 ). Many other activity-regulated genes have now
been found (see Flavell and G reenberg 2 0 0 8 ).
M em brane depolarization increases calcium ions and
activates members o f the C R E B (calcium /cA M P response
elem ent binding proteins) family o f transcription factors.
These factors lead to che production o f the brain-derived
neurotrophic factor (B D N F ) and molecules involved in
activation o f N M D A synapses and activity-dependent
growth o f dendrites ( Wayman e t al. 2 0 0 6 ). C o rtical plastic-
icy depends on activation o f C R E B and coactivator
molecules (T O R C ’s) (L i e t al. 2 0 0 9 ).
C ats that were dark-reared during the critical period for
ocular dom inance form ation showed decreased production
o f B D N F in the visual cortcx. Blockage o f visual inputs
trom one eye during the critical period reduced B D N F pro­
duction in eye-specific LG N lam inae and in eye-specific
ocular dom inance colum ns in the visual cortex (Lein and
Shatz 2 0 0 0 ).
The concentracion o f some transcription factors in che
visual cortcx can vary over a few hours, depending on the
strength o f stim ulation (W est et al. 2 0 0 2 ). For example, che
concentration o f the transcription factor o f the gene zif268
decreased in the contralateral visual cortex ot rats when
inputs from one eye were blocked by tetrodotoxin o r occlu­
sion (W orley c t al. 1991). In monkeys, ocular dom inance
colum ns serving an eye with a sutured eyelid contained less
o f this transcription factor relative to colum ns serving che
open eye (Chaudhuri e t al. 1995; K am in skaet al. 1996).
A ctivation o f N M D A synapses by glutamate stimulates
im m ediate early genes to express proteins in developing
synapses (Kaczm arek and Chaudhuri 1 9 9 7 ; Scheetz et al.
2 0 0 0 ). For example, the immediate-early gene Arc, pro­
duces a protein in dendrites only when the neuron is excited
(Lyford et al. 1995). This protein controls the num ber o f
AM PA receptors in the postsynaptic m em brane o f N M DA
synapses and thus influencessynaptic plasticity. M onocularlv
deprived m ice lacking Arc did not show a shift in ocular
dom inance o f binocular cells in the visual cortex (M cC u rry
et al. 2 0 1 0 ). A ctivation o f Arc in the developing visual
cortex leaves a lasting trace that can be observed in tissue
sections. Tagawa et al. (2 0 0 5 ) used these traces to observe
the developm ent o f contralateral and ipsilateral projections
to the visual cortex o f normal m ice and m ice subjected to
m onocular deprivation.
M ajdan and Shatz (2 0 0 6 ) assayed levels o f m RN A s in
the visual cortex o f norm al and m onocularlvi enucleated
mice. A large set o f genes was maximally activated during or
just after the critical period o f cortical plasticity. They called
these ag e-sp ecific genes. The expression o f m ost o f these
genes was downregulated in che contralateral cortex serving
the enucleated eye but was normal in the ipsilateral cortex.
A few genes were upregulated in the contralateral cortex.
Thus, age-specific genes are responsible tor creating che
proteins required for the basic structures o f neurons and
synapses.
 M ajdan and Shatz also identified 11 genes th at were
down regulated by m onocular enucleation, not only during
the critical period but also throughout development.
Furtherm ore, these genes were still regulated in the visual
cortex o f dark-reared m ice. They called them the com m on
set genes. They arc associated with the signaling systems
responsible tor visually driven cortical plasticity. For exam ­
ple, the gene R d t f which is responsible for rhe production
o f neurotrophins, was one o f the m ost robustly regulated
genes in this set. N eurotrophins are required for cortical
plasticity during the critical period.
New neurons are produced in the hippocam pus o f adult
mice. But whether particular hippocam pal cells survive
and form synapses depends on neural activity at N M D A
synapses (Tashiro et al. 2 0 0 6 ).
In conclusion, age-specific genes are regulated by visual
activity only during periods in which the structures that
they are responsible for arc developing. O n ce the structures
are grown, age-specific genes are turned oil. O n the other
hand, the com m on set genes are regulated by visual activity
at all ages. However, their capacity to influence m ajor struc­
tures in the visual cortex is lim ited after the age-specific
genes have com pleted their work.
The broad topic o f structural changes underlying
m em ory in adult animals was discussed in Section 5.6.8.
This topic was reviewed by Bailey and Kandel (1 9 9 3 ) and
Edwards (1 9 9 5 ). For reviews o f neural plasticity in the
visual cortex see Rauschecker (1 9 9 1 ).
In summary it can be stated that sensory experience and
behavior affect the way genes arc expressed in the nervous
system. The pattern o f gene expression recursively affects
sensory processing and behavior. Behavior in a particular
environm ent over generations exposes a species to selective
pressure to improve the sensory-m otor m echanism s that
enable that species to operate in that environm ent. The
selective pressure is removed or modified it a species enters
a new environm ent, acquires a new sensory system, or
begins to behave in a different way. Given that parents pass
on patterns o f behavior to the next generation, the linkage
betw een behavior and genetic expression will be indirectly
inherited. See Borrelli et al. (2 0 0 8 ) for a review o f epige­
netic processes responsible for neural plasticity.
6.6.2 SPONTANEOUS NEURAL ACTIVITY
M am m alian ganglion cells generate spontaneous neural
activity well before birth and before maturacion o f retinal
receptors (see Section 6 .3 .2 ).
The local waves o f spontaneous firing in the retina pro­
duce near-neighbor correlations o f firing o f cells in the
developing L G N and visual cortex (H anganu et al. 2 0 0 6 ).
Spontaneous neural activity arising in the retina is involved
in guiding afferent axons through the subplate to their
target cclls in the visual cortex (Scctio n 6 .4 .5 ). Blockade o f
retinal activity disrupted the segregation o f visual afferents
into ocular dom inance colum ns (Stryker and Harris 1986).
M utant m ice lacking the acetylcholine receptor for genera­
tion o f retinal activity in chc first postnatal week showed
reduced grating resolution and imprecise mapping o f visual
inputs in the visual cortex (Rossi c t al. 2 0 0 1 ; G ang et al.
2 0 0 5 b ).
In addition со rccinal accivicy, neuronal accivicy occurs
spontaneously over dom ains o f becween 5 0 and 100 pm in
slices o f corcex trom the neonate rat. In each dom ain, waves
o f intercellular calcium propagate from a central trigger
cell. Propagacion occurs over gap ju n ction s between neu­
rons and betw een glial cells. Synapses are not functional at
this stage (Yuste et al. 1 9 9 5 ). D om ain activity is elicited by
infusion o f inositol triphosphate— a molecule involved in
the second-messenger system ot m etabotropic glutamate
synapses (K andler and Katz 1998). The cortical neuronal
dom ains are elongated in a radial direction, which suggests
thac chey aid formacion o f corcicai columns.
G araschuk et al. (2 0 0 0 ) used a tw o-photon scanning
m icroscope со observe slices o f rac neocorcex. Sponcaneous
oscillacions involving intracellular calcium ions spread over
the longitudinal axis o f the whole cortex at intervals o f
several minutes. These oscillacions depended on glucamace
rcccpcors, buc ic is noc d ear whecher they involved normal
synaptic transm ission. They could be involved in the growth
o f long-range horizontal cortical connections.
After synapses have m atured, a new type o f spontaneous
activity emerges, which depends on chem ical synaptic trans­
mission ( O ’D onovan 1999).
All neurocransmicccr release is scoppcd in che brain o f
m ice lacking che типе IS - / gene. By em bryonic day 18 che
brainscem lose ics neurons and che neocorcex resembled
chac o f neonaces. However, soon after birch, che corcicai
neurons ot che deteccive m ice dcgeneraced (Verhagc ec al.
2000 ).
Thalam ocortical projections and cortical topology were
normal in mucanc m ice lacking stimulus-evoked synapcic
activity, but retaining spontaneous neurotransm itter release
(M olnar ec al. 2 0 0 2 ). There was no loss o f cells in chis case.
Thus, ic seems that, at least in m ice, neural activity
involving release o f neurotransm itter is not required for ini­
tial form ation o f cortical layers. However, we will see that
neural accivicy is required for che refinemenc and maince-
nance o t cortical synapses.
6.6.3 HEBBIAN SYNAPSES AND VISUAL
D EV ELO PM EN T
O bservations o f in vitro slices o f visual co rtex trom rats and
m ice revealed chac long-term pocenciacion ac N M D A syn­
apses is involved in neural plasticity in the developing visual
cortex (Kirkw ood ec al. 1993; Weiss et al. 1 9 9 3 ; Kirkwood
and Bear 1994b).
Kirkwood ct al. (1 9 9 5 ) induced L T P in slices o f
rat visual cortex. Susceptibility to L T P peaked during the
mature in the first 4 weeks, bv which time the monkey
J 4
begins to show evidence of stereopsis.
A t 31/ 2 weeks, the singularities in the orientation
system show a tendency to lie in the centers o f the ocular
dom inance colum ns, and the iso-orientation contours run
orthogonally across the borders o f ocular dom inance col­
umns, which is the adult pattern. The full adult pattern o f
ocular dom inance is established in monkeys by the age of
six weeks (LeVay et al. 19 8 0 ; Tychsen and Burkhalter
1997).
The transition from a state o f uniform binocular inner­
vation in layer 4 C to one o f m onocular dom inance is
believed to involve a phase of exuberant proliferation and
hom ogeneous distribution o f synaptic terminals followed
by selective pruning or withdrawal ot inappropriately co n ­
nected dendrites. It has been suggested that pruning is
accom panied by an expansion and m aturation ot appropri­
ately connected dendrites. The process also involves a bal­
ance between excitatory and inhibitory connections, as
described in the next section.
A n ton in i and Stryker (1 9 9 3 ) used im m unohistochcm i-
cal procedures to trace growth processes at the cellular level.
They revealed that widely extending but immature branches
ofg en icu loco rtical afferents are elim inated at the same tim e
that other branches grow in length and com plexity and seg­
regate into patches according to their eye o f origin.
M echanism s involved in the developm ent o f ocular dom i­
nance colum ns are discussed in the next section.
Stim ulus-dependent changes in light absorption by rhe
cortical surface revealed that, in the first 31/2 weeks, ocular
dom inance colum ns o f the cortex o f the monkey increased
in width by about 20% . This is about tw ice the rate at which
the periodicity o f the distribution o f orientation prefer­
ences increases (Blasdel et al. 1 9 9 5 ). The area ot the visual
cortex in an adult car is more than double that at birth . The
area increases about 50% between postnatal weeks 3 and 10
(D u ffy e t al. 1 998).
O n e would therefore expect ocular dom inance colum ns
in the cat to increase in width betw een 3 and 10 weeks. But
2-deoxyglucose staining showed that colum n spacing did
not change after the age o f'3 weeks (R ath jen c t al. 2 0 0 3 ). It
is unlikely that ocular dom inance colum ns subdivide after
this age because the growth o f visual inputs is com plete by
the age o f 3 weeks. However, the 2-deoxyglucose procedure
reveals ocular dom inance colum ns only for the central
visual field. The central retina develops before the periph­
eral retina. Therefore the cortical region representing the
central field could develop first. R athjen et al. suggested
that ocular dom inance colum ns o f cats form in the part o f
the visual cortex representing the central visual field by the
age ot 3 weeks, but continue to form tor the peripheral
visual field after that age.
C ytochrom e oxidase is present in the cortical plate ot
the human brain by the 26th week o f gestation. W hen
this enzyme is stained, it provides a sensitive indicator ot
neural activity. Cytochrom c-oxidasc blobs are evident in
the human visual cortex by the 24 th postnatal day and arc-
well organized by the fourth m onth. C ytochrom e-oxidase
stripes in V 2 are weakly evident in the human neonate
(W o n g -R iley ct al. 1993). In contrast, both blobs and stripes
are clearly evident in the visual cortex o f the neonate
macaque, although the distribution o f the enzyme is not the
same «is in the adult (H o rto n 1984; Kennedy c t al. 1985;
H orton and H ocking 1996c).
The next section deals w ith factors that control the
developm ent o f ocular dom inance columns.
6.7.2 M E C H A N I S M S OF C O L U M N
DEVELOPMENT
6 .7 .2 a Io n o tr o p ic Sy n ap ses
Hebbian synapses d etect synchronous activity. In the devel­
opm ent o f ocular dom inance columns, the synchronous
activity is that betw een inputs arriving from the two eyes.
The following lines o f evidence suggest that the segregation
o f distinct ocular dom inance colum ns depends on N M D A
synapses activated by the ncurotransm itter glutamate
(C on stantin e-P aton c t al. 1 9 9 0 ). In the first place, the den­
sity o f N M D A synapses increases abruptly in all layers o f
the visual cortex o f kittens during the period when inputs
from the tw o eyes segregate into ocular dom inance co l­
umns. After this period, the density declines to the adult
level (Bode-G reuel and Singer 1989; Fox et al. 1989;
C z e p ita c ta l. 1994).
Synapses in the im m ature cat cortex lack AM PA recep­
tors. For this reason they have a high threshold and are
called silent synapses. During the first postnatal m onth,
active N M D A synapses acquire A M PA receptors, and the
response threshold declines (Feldm an and Knudsen 1998).
W h ile ocular dom inance colum ns are form ing, N M D A
synapses in the visual cortex o f the rat arc m ore numerous
and more active than those in the adult (C arm ign oto and
V icin i 1992). High activity o f N M D A synapses is therefore
associated with cortical plasticity.
Infusion o f an N M D A antagonist in the cat visual
cortex profoundly suppressed responses to visual stim ula­
tion (M iller et al. 1989a). Also, the experience-dependent
coordinated mapping ot ipsilateral and contralateral p rojec­
tions onto the tectum o f developing frogs (Xenopus) was
disrupted by application o f N M D A antagonists (Scherer
and Udin 1 9 8 9 ).
R oberts and R am oa (1 9 9 9 ) used histochem ical and
in vitro patch-clam p procedures to measure the postsynap­
tic receptor subunits o f N M D A synapses in the developing
visual cortex o f the ferret. Before the period o f ocular-
dom inance plasticity, there was a preponderance o f N R 2B
receptor subunits. After eye opening, subunits N R l and
N R 2A increased rapidly, bur N R 2 B increased beyond its
initial level only after day 30. This is the period o f greatest
ocular dom inance plasticity, when the animal is m ost sensi­
tive to m onocular deprivation. A t the same time there was a
decrease in the decay tim e o f receptor mediated synaptic
currents.
G lutam ate synapses chat are selectively sensitive to the
synthetic ligand Л М Р А are also particularly numerous at
the tim e o f maxim um cortical plasticity in cats (D ud ek and
Bear 1989).
C o rtical plasticity has been m ost extensively studied in
ocular dom inance induced by early m onocular deprivation,
as discussed in Section 8.2.4b.
6 .7 .2 b M c ta b o tr o p ic Sy n ap ses
Ionotropic synapses (N M D A , A M P A , and kainatc) are
ligand-gated glutamate synapses. M ctabotropic synapses
operate through the G -p rotein , second messenger system,
as described in Scction 5.5.2d. This system has eight main
types o f receptors (m G lu R s) on the postsynaptic m em ­
brane. They are identified by the agonists th at trigger them.
D uring developm ent, the receptor types becom e differen­
tially distributed over the cortical layers. In cats, type 1
receptors occur in all cortical layers except layer 4 , and this
distribution docs n o t change with age. Type 5 receptors
becom e concentrated around the layer 4/5 border during
the first 5 postnatal weeks. Initially, receptor types 2 and 3
are evenly distributed but disappear from layer 4 between
postnacal weeks 4 and 6. These changes in receptor distribu­
tion must be influenced by visual stim ulation because they
are postponed by dark rearing (Section 8 .1 ). The disappear­
ance o f receptor types 2/3 from layer 4 is correlated with
the segregation o f ocular dom inance colum ns (Beaver and
Daw 1 9 9 9 ). A ctivation o f these receptors increases the level
o f A M P receptors on the postsynaptic mem brane (Reid
e t al. 1996b). The A M P channel is closely associated with
cortical plasticity.
Evidence reviewed in Section 6.6.3 shows that
m ctabotropic synapses are involved in cortical plasticity
before the N M D A system matures. However, pharm aco­
logical blockade o f m G luR s receptors had no effect on the
developm ent o fo cu lar dom inance colum ns in m icc(H cn sch
and Stryker 1 9 9 6 ). It therefore seems that, by the time
ocular dom inance colum ns develop, the involvement o f
m ctabotropic receptors in visually induced plasticity has
been replaced by that o f N M D A receptors.
6 .7 .2 c O t h e r N e u r e tra n s m itte rs
All intracortical excitatory synapses and cortical synapses
receiving inputs from the sense organs involve the neu-
rotransm icter glutamate. But the cortex also receives inputs
from a variety o f subcortical areas. Each o f these inputs
involves a distinct ncurotransm ittcr, such as acetylcholine,
noradrenaline, dopam ine, and serotonin (Scctio n 5.5.2g ).
C o rtical cells contain a variety ot receptors tor each o t these
transm itters. They are called neurom odulators because they
modulate responses o f cells to glutamate. Application o f the
neurom odulators acetylcholine and noradrenaline to che
4
visual cortex o f anesthetized neonate kittens facilitated
stimulus-induced changes in ocular dom inance and orien­
tation selectivity (G reuel et al. 1988). Also, noradrenaline
is involved in the adaptive response o f cortical cclls to
m onocular deprivation (Section 8 .2 .7 h ).
D uring early developm ent, the visual cortex and ocher
cortical sensory areas o f the rat display a prom inent but
transient pattern ot acetylcholinesterase. This enzyme indi­
cates activity at acetylcholine synapses. The activity appears
mainlvв in laver
« IV, where thalam ocortical axons terminate.
It may help togu id e incom ing axons. Binocular enucleation
results in an alm ost com plete loss ot this enzyme, which
dem onstrates that it depends on afferent neural activity
(R obertson et al. 1987).
In the visual cortex o f kittens betw een 3 0 and 8 0 days o f
age, cells receptive to serotonin are concentrated between
cytochrom e oxidase blobs (K ojic et al. 2 0 0 0 ). Application
o t serotonin increases synaptic plasticity in these interblob
regions bu t decreases it in the blobs. These location-specific
effects o f serotonin may therefore prom ote the develop­
m ent o f cortical colum ns. Serotonin is expressed by neurons
originating in the raphe nucleus (Section 5.5.2g ).
6 .7 .2 d C o m p e titio n fo r N eu ro tro p h in s
The development o fo cu la r dominance columns depends
on com petition between visual afferents for access to a
neurotrophic growth factor produced by cortical cells.
A ctivation ot Trk receptors in the cell m em brane by
neurotrophins is required tor cell survival. A dm inistration
ot the neurotrophins N G F or B D N F activates Trk recep­
tors and thereby reduces neuronal death, or ap o p to sis
(H ofer and Barde 1 9 8 8 ). Proneurotrophins activate the
rcccptor p 75, which prom otes cell death (C h ao 2 0 0 3 ).
Thus, two forms ot the same neurotrophins have opposite
effects.
O n ce afferents reach their target cells they com pete for
neurotrophins that determ ine w hether a given cell survives.
They also modulate axonal and dendritic arborization.
A cell gains com petitive advantage in accessing neurotro-
phin by virtue o f both spontaneous and stimulus dependent
activity in the ccll. W hen activity in a developing cortical
neuron was pharm acologically suppressed, fewer synaptic
boutons developed on that neuron (Burrone et al. 2 0 0 2 ).
Thus, axons form synapses preferentially on more active
neurons. U niform suppression o f activity in a set o t cortical
cells had no effect. Suppression o f activity at a mature
synapse resulted in a com pensatory increase in synaptic
efficiency.
N euronal activity increases the local production o f neu­
rotrophins, which enhance transm itter release in presynap­
tic neurons containing the appropriate receptor molecules
eyes o f m onocularly deprived kittens, but only during the
critical period o f colum n form ation (H ata et al. 2 0 0 0 ).
Infusion o f neurotrophins N G F, B D N F , or N T -4/ 5 also
counteracted effects o f m onocular deprivation in the rat
visual cortex (I.odovichi c t al. 2 0 0 0 ). Form ation o f ocular
dom inance colum ns was also disrupted by inh ibition o f the
ligand T rkB lor these neurotrophins (C abelli e t al. 1997). It
seems that neurotrophins chat activate TrkB during the c r it­
ical period prom ote connections between cortical cells even
though there is no correlated activity from the eyes.
The fourth neurotrophin, N T -3 , or its ligand TrkA , has
no effect on colum nar developm ent because it is expressed
at an earlier stage.
Ultim ately, plasticity and consolidation o f ocular d om i­
nance colum ns depend on proteins produced by specific
genes. Neural activity induces immediate-early genes to
produce m R N A transcription molecules, which induce
genes to produce specific proteins. For exam ple, membrane
depolarization and the consequent increase in calcium ions
activates mem bers o f the C R F .B family o f transcription
factors. These factors induce genes to produce the brain-
derived neurotrophic factor (B D N F ) and m olecules that
activate N M D A synapses. These molecules are required for
ocular dom inance plasticity.
O th er studies on the role o f neural growth factors in the
developm ent o f ocular dom inance colum ns arc discussed in
Section 8 .2 .3 .
6 .7 .2 e B a la n c e b etw ee n E x c ita tio n an d In h ib itio n
Th e balance betw een excitation and inhibition spreading
over the cortical surface may be a m ajor factor in colum nar
developm ent. H ensch and Stryker (2 0 0 4 ) pharm acologi­
cally modified cortical inhibition in kittens tor 1 m onth,
starting 2 weeks after birth. Local application o f diazepam,
which enhances inhibition, produced three effects in the
neighborhood o f the infusion site. These were (1 ) reduc­
tion in the binocularity o f cells, (2 ) widening o f the ocular
dom inance colum ns, and (3 ) sharpened segregation o fth e
colum ns. An agent that reduced in h ibition produced local
narrowing o f the columns.
Hensch and Stryker concluded that G A BA -m ediated
inhibition controls local com petition between inputs from
the eyes for access to binocular cells. Increased inhibition
increases com p etition, which reduces the num ber o f b in ­
ocular cells and widens the colum ns. Increasing inhibition
has the same effect as early strabismus, which decorrelates
rhe visual inputs. T h e role o f inhibition in cortical develop­
m ent is discussed further in Section 8.2.4a.
6 .7 . 2 f M o d e ls o f D e v e lo p m e n t
o f O c u la r D o m in a n c e
M odels o f the developm ent o f ocular dom inance columns
fall into tw o types. Those o f the first type stress the role o f
com petition o f afferent axons from the two eyes for access
to cortical cclls (E llio tt e t al. 1997; Harris e t al. 1 9 9 7 ; von
der M alsburg 19 79; F.lliott and Shadbolt 1996, 1999,
2 0 0 2 ). The input that is m ost active gains access to the
cortical cell.
Bienenstock e t al. (1 9 8 2 ) and Swindalc (1 9 8 2 ) devel­
oped m odels based on the idea o f com petition between
inputs from the two eyes plus excitatory and inhibitory
interactions between cortical cells. The model developed by
Bienenstock et al. emphasizes com petition in che temporal
dom ain rather than in the spatial dom ain and has been
im plem ented by Blais et al. (1 9 9 9 ).
M odels o f the second type stress the role o f the correla­
tion o f sim ultaneous patterned inputs from the two eyes
(see G o o d h ill 1993). N eighboring regions o f a typical visual
scene tend to be m ore sim ilar in lum inance, color, orienta­
tion, and m otion than do nonneighboring regions. Because
o f this, stim uli falling on the same retina arc correlated to an
extent that decreases with increasing distance between
them . B u t inputs from neighboring regions in the two reti­
nas also tend to be correlated. Correlated inputs torm stron­
ger synaptic connections than do inputs that are not
correlated. Thus, cortical binocular cells will have com pet­
ing tendencies to co n n ect with neighboring cells from the
same retina as opposed to corresponding cells from the two
retinas. O cu lar dom inance colum ns represent a com p ro­
mise betw een these tw o tendencies. A stronger correlation
betw een inputs from the two eyes leads to narrower
columns.
M iller et al. ( 198 9 b ) developed a model that takes
account o f four factors thac influence the developm ent o f
ocular dom inance columns. These are: (1 ) the initial pat­
terns o f cell connectivity, (2 ) patterns o f correlated activity,
(3 ) interactions betw een neighboring cortical cells, and (4)
constraints on synapric strength. Erw in and M iller (1 9 9 8 )
modeled the developm ent ot both ocularly matched orien­
tation colum ns and ocular dom inance colum ns o n the basis
o t correlated inputs.
W oodbury c t al. (2 0 0 2 ) introduced a threshold fu nc­
tion for activation o f cortical cells in to M illers m odel. This
allowed the model to simulate the increasing topographic
refinem ent o t the cortical map in addition to the develop­
m ent o f cortical colum ns.
Nakagama and Tanaka (2 0 0 4 ) developed a model o f the
coordinated developm ent o fcy to ch ro m e oxidase blobs and
ocular dom inance colum ns. The m odel is based on corre­
lated activity betw een inputs from various types o f ganglion
cells in the tw o eyes. As the strength o f correlation increases,
the blobs merge across ocular dom inance colum ns, as in the
cat’s visual cortex. The m odel also predicts the effects o f
m onocular and binocular deprivation on che form ation o f
ocular dom inance colum ns.
W iem er et al. (2 0 0 0 ) applied an algorithm developed
by K ohonen (1 9 9 5 ) to simulate the developm ent o f
the representation o f orientation, ocular dom inance, and
 Ruthazer c t al. (2 0 0 3 ) induced dual innervation o f one
optic tectum o f tadpoles o f the frog Xenopus. They used
time-lapse images from the tectum o f che living tadpoles to
observe the changes in the branching o f retinotectal axons.
O cu lar dom inance bands appeared som e weeks after abla­
tion o f one tectum . They observed that correlated neural
activity in axons from the same eye shaped the m orphology
o f axonal arbors, which produced ocular dom inance bands.
The process involved elim ination ot inappropriate branches
plus selective stabilization o f appropriate branches. Both
processes required neural activity at N M D A synapses.
Hem isphereccom y perform ed on epileptic human
patients produces hem ianopia (loss of vision in one hem i-
field). M uckli e t al. ( 2 0 0 9 ) reported the case o f a 10-year-
old girl with congenital absence o f the right cortical
hemisphere and m ost o f the right eye. Remarkably, she had
close to norm al vision in both hemifields and good bilateral
m otor coord ination. Thus afferents from the nasal h alf o f
the left eve must have been rerouted at the chiasm to follow
an ipsilateral route to the in tact left hemisphere. Responses
in V I to stim uli presented to the left eye recorded by fM R I
revealed that the maps representing che ipsilaceral and
contralateral visual fields in V I were m irror symmetric and
overlapping, resembling the con d ition in albinism.
However, in extrastriate regions in V 2 and V 3 there was an
alternation o f dom inance o f contralateral and ipsilateral
inputs. M uckli et al. suggested that the initial mapping in
V I resulted from gradients o f Ephrins in che retina but chat
rhe later maps arose from com petition betw een neural
activity arising from the tw o retinas.
6 .7 .3 c T ra n sp la n te d T h ird Eye
In a frog em bryo, an eye bud can be transplanted from
another em bryo to form a third eye (C onstantine-Paton
and Law 19 7 8 ; Law and C onstantine-P aton 1981). The
opric nerves o f rhe natural eye and those o f a nearby trans­
planted eye grow to innervate the same tectum , where they
form 200-um -w idc ocular dom inance colum ns resembling
those ot mammals. The initial projection o t inputs to the
appropriate region o f the tectum is presumably due to
chem oaffinity. However, the subsequent segregation into
ocular dom inance colum ns results from conHicc between
two eye-specific topographic mappings. Each eye seeks
со preserve connecced neighborhoods and со m inim ize
con tacts with inputs from the other eye. The width o f
connected neighborhoods could be related to regions o f
dendritic arborization. A ction potentials in the optic nerves
arc required for che form ation o f ocular dom inance co l­
umns in three-eved frogs (R eh and C onstantine-Paton
1985). Thus, colum n form ation could depend on local
synchrony o f spontaneous neural firing.
6 .7 .3 d C o n s tr u c tio n o f a C o m p o s ite F.ye
Fawcett and W illshaw (1 9 8 2 ) constructed a com posite eye
trom two nasal halves or two tem poral halves trom opposite
sides o f the head o f Xenopus larvae. As wich double inner­
vation from a transplanted eye, the inputs from the co m ­
posite eye formed roscrocaudaJ eye-specific colum ns in che
tectum .
6 .7 .3 c A b la tio n o f th e T e m p o ra l R ccin a
Ide e t al. (1 9 8 3 ) removed the temporal tw o-thirds o f an eye
bud o f the em bryo o f the frog Xenopus. The remaining nasal
portion grew in to a normal-appearing eye. In the mature
frog, each h alf o f the retina projected to the entire contral­
ateral tectum in stripes alternating with stripes trom the
other h alf o f the retina. In chis case, the inputs were from
the same eye o f the same anim al so that the factor determ in­
ing segregation o f inputs was neither eye o f origin nor
animal o f origin. The crucial factor was probably the greater
synchrony of firing betw een near-neighbor inputs, since
abolition o f neural activity by application o f a neurotoxin
prevented the induction o f ocular dom inance colum ns in
goldfish (M eyer 1982).
6 .7 .3 f S u m m ar v
All the evidence reviewed in this section supports the amaz­
ing conclusion that ocular dom inance colum ns appear in
animals that do not norm ally possess them . N ot only thac,
buc che colum ns con tain binocular cells with m atching
tuning function in chc m onocular receptive fields. Again,
this occurs in animals that do not normally possess
binocular cells. This means chat the m echanism s required
tor the developm ent o t ocular dom inance colum ns and bin­
ocular cclls were already present before stereoscopic vision
evolved. These facts have a profound significance for under­
standing how stereopsis evolved. This topic is discussed in
Section 33.8.
 7
D E V E L O P M E N T OF P E R C E P T U A L F U N C T I O N S

7.1 Procedures 368 7.3.6 Vergence 379

7.2 Development o f visual functions 369 7.4 Development o f visual depth perception ISO
7.2.1 Acuity and color sensitivity $69 7.4.1 Perception o f distance 380
7.2.2 Orientation sensitivity 372 7.4.2 Perception o f 3-D form 383
7.2.3 Flicker and motion sensitivity* 373 7.5 Development o f binocular vision 38$
7.2.4 Development o fth e visual liclds 375 7.6 Development o f stereoacuity 386
7.3 Growth o f the oculomotor system
0
176 7.6.1 Preverbal stereo tests 386
7.3.1 Accommodation 376 7.6.2 Standard stereo tests 387
7.3.2 The pupillary response 377 7.6.3 VEPs and development o f stereopsis 388
7.3.3 F.vc alignment 377 7.6.4 Stereoacuity in the aged 389
7.3.4 Pursuit eye movements 378 7.7 Development o f auditory localization 389
7.3.5 The saccadic system 379

7 .1 PROCEDURES no longer evident. The stimulus is then changed in a

Th e developm ent o f visual perception has been studied by
the follow ing procedures.
1. Reaching The experim enter records the accuracy with
which infants reach for objects in different directions or
at different distances.
2. Avoidance behavior The in fa n ts reactions are recorded
as it is presented with a stimulus such as a visual c liff or
an approaching o b ject.
3. Preferential looking Som e stim uli are naturally attractive
to infants. For instance, infants spend more time
looking at chc m ore brightly colored o f two stim uli or
the one chat moves, flashes, or has higher contrast. They
may also prefer a 3 -D display to a flat display. The
preferential-looking procedure was introduced by Fantz
(1 9 6 5 ). The infant is shown tw o stim uli side-by-side,
and a record is kept o f the tim e the infant spends gazing
at each. The person w atching the infant’s eyes does not
know w hich stimulus has been presented and follows a
forced-choice, bias-free procedure in deciding w hether
the infant is looking at one stimulus o r the other (Teller
1979).
4 . Dishabituation This is a variant o f preferential looking,
The infant is shown a stimulus until signs o f interest are
defined way, and the extcnc to which interest is
restored is determ ined by observing the in fan ts eye
movements or bv indications o f arousal such as
increased heart rate. The scimulus is chen changed
in the reverse direction. As a con trol, each stimulus is
flashed o ff and on again.
5. Operant conditioning The preceding procedures use a
built-in response and require a m inim um o f
prelim inary training. In operant con d ition in g, the
su bject is first trained to respond to a reinforced
stimulus while a stimulus differing in som e crucial
respect is not reinforced. A subject who learns
to make differential responses to the stimuli
is deem ed to have the capacity to discrim inate
them . It is difficult to design stimuli thac
differ in the factor being studied and not in
irrelevant factors.
6. Pursuit eye movements The ability o f an infant to
d etect a stimulus may be revealed by m oving the
stimulus and observing w hether che in fan ts eyes track
it. O p to kin etic nystagmus (O K N ), is present in che
neonate (Sh ea et al. 1980).
7. Physiological procedures These include recording the
electroretinogram , visual evoked potentials, and the
fM R I.
 7 .2 D E V E L O P M E N T O F V IS U A L
F U N C T IO N S

7 .2 .1 A C U IT Y AN D C O L O R S E N S IT IV IT Y

7 .2 .1 a D ev elop m en t o f C o n tr a s t Sensitivity

'Ihe concrasc-sensicivity function is che reciprocal o f

contrast threshold plotted againsc the spatial frequency
o f a grating with a sinusoidal m odulation o f luminance
(Section 3 .2 .5 ).
C o n trast sensitivity can be measured in monkeys by
training them to discrim inate betw een a grating and a blank
field. Tli is procedure revealed chat sensitivity to spacial fre­
quencies below 5 cpd approached adulc levels by the 20th
week, and that sensitivity со higher spacial frequencies
improved until the 2 8 th week, when the concrasc-sensitivity
function acquired its adult form (B o o th e ec al. 1980).
Preferential looking has been used со measure the con-
A nthonyM . N orcia. H e received his В .Л . in psychology from
trast-sensicivicy function o f infants betw een ages 1 and 3 ih c U niversity o f M in n eso ta am i his P h .D . in p sy ch ology from I.eland
m onths (Atkinson et al. 19 7 7 ; Banks and Salapatek 1978) S tan fo rd J r U niversity. H e is now a se n io r scien tist at th e S m ith -
and 4 and 6 m onths (Pctcrzell cc al. 1995). O ne-m onth-old K cttlcw cll Rye Research Institu te in San Francisco.

infants showed little evidence o f the drop in sensitivity

below 1 cpd th at is evident in older children and adults.
W ith increasing age, che peak o f che sensicivitv funccion
shitted со higher spatial frequencies.
Infant concrasc sensicivicy has also been measured by use
o f visual evoked potencials (V E P s) (P irch io et al. 1978;
Norcia et al. 1 9 8 6 ,1 9 9 0 ). Norcia ec al. (1 9 9 0 ) tesced infants
betw een the ages o t 2 and 4 0 weeks. The high-frequency
lim it improved from 5 cpd at o n e monch со 16.3 cpd ac 8
m onths to 3 2 cpd tor adults. They obtained higher contrast
sensitivities in infants chan did Pirchio ec al. or invescigacors
using behavioral procedures. For example, the co n trast scn-
sicivicv o f 10-week-old infancs was close со adulc levels wich
spacial frequencies below 1 cpd ( N orcia et al. 1988) (Portrait
Figure 7 .1 ). Sensitivity to higher spatial frequencies took
longer со reach adult levels. Like che behavioral studies,
evoked pocencials showed a devclopmencal crend coward
greater contrast sensitivity and extension ot sensitivity to S patial frequency (cpd)
higher spacial frequencies, as shown in Figure 7.2.
ri*»r« ?.2. C ontrast sensitivity from evoked potentials. M ел n с о n t rast -
M ovshon and Kiorpes (1 9 8 8 ) concluded chac group
sensitivity I u n ctio n s for ten I0-\vcck-old in fan ts and live ad ults. Error
averaging o f daca in earlier scudies produced che erroneous bars in d icate 9 5 % co n fid en ce lim its. (R««Jr.>wn fr»m 198$)
conclusion chac the contrast-sensitivity funccion o f young
infants does not show che low-frequency falloHFat low spa­
tial frequencies. Their reanalysis o f che earlier data revealed Ac all ages, concrasc sensicivicy and gracing acuicy are
thac che fallotf in scnsicivicy ac low spacial frequencies, typi­ higher in the foveal region than in che periphery (Courage
cal o f che adulc, is presenc even in 1-monch-old infancs. and Adams 1996). Ac ages betw een 10 and 3 9 weeks, grat­
Using preferencial-looking and opcranc procedures, ing acuity and contrast sensitivity, revealed by V E P s, were
Gwiazda ec al. (1 9 9 7 ) found chac betw een ages o f 2 and 4 abouc 2.3 times higher for a grating in the central 2° o f chc
m onths there was a one octave loss o f scnsicivicy tor a 0.38 visual field chan for one in an annulus becween 8 and I6 r in
cpd gracing, coupled wich again in sensicivicy ac higher spa­ chc periphery (Allen cc al. 1996).
cial frequencies, as shown in Figure 7 .3 . They proposed that In 241 children, contrast sensitivity had not reached
che loss for che low spacial frequency is due со developmenc adult levels by age 7 years (Scharrc c t al. 1990). Gwiazda
ot laceral inhibicion. et al. (1 9 9 7 ) confirm ed this result.
 I I l l l l l l l I i I I II III i I A -L L L U i

0.1 1 10 100
S patial frequency (cpd)

_L ± _L
F ip u t 7.X Contrast um itivity in an infant a t fo u r agcr. (A d a p t e d fru m G v w d a « a
4 6 8 10 12 14
1* 7 ) Age of infants (months)

»‘i£ur*7.i. S ttw p V E P g ra tin g a c u ity a t a fu n ction o f a g e. M ean gracing acu ity

for 1 9 7 in fan ts w ith 9 5 % co n fid cn cc bands derived from the sweep
V E P p ro ced u re. ( A i L f u d f«om N o r t t o n d T>t ct 1УЙ5)
7 .2 .1 b D e v e lo p m e n t o f G rating A cu ity

G rating acuity is the highest spacial frequency o f a sinusoi­

dal lum inance grating with maximum contrast that can just counrerphase-m odulated grating. They obtained estimates
be resolved. It is the upper lim iting spatial frequency o f the o f grating acuities o f 13 arcm in (4 .6 cp d ) at 1 m onth and
contrast-scnsitivity function or the angular subtense o f one 3 arcm in (2 0 cpd) at about 12 m onths, as shown in
period o f a grating with the highest detectable spatial fre­ Figure 7.4. The mean adult acuity with this procedure was
quency. G rating acuity improves as the retina, lateral genic­ about 3 2 cpd (N orcia et al. 1 9 9 0 ). These acuities are much
ulate nuclei, and visual cortex mature. Three behavioral better than those reported from behavioral studies or other
criteria have been used to assess grating acuity in young evoked-potential studies referenced in their paper. The
infants. frequ ency-sw ept V E P provides a finer determ ination
because it is fast and therefore immune to adaptation. It is
1. The occurrence o f optokin etic nystagmus in response to also immune to effects ot probability summation (Section
a moving grating, 13.1.1). G rating acuity obtained by this m ethod was only
slightly better with binocular viewing chan with m onocular
2. The pupil response to a grating presented against a
viewing» and was similar in the two eyes (H am er et al.
background with the same space-average lum inance.
1989).
3 . A ch ild ’s tendency to look at a patterned stimulus. The mean grating acuity o t 106 infants below the age
o f 5 m onths, assessed by preferential looking, differed
These procedures do not always produce th e same betw een che cwo eyes by 1 octave. Although che results were
results. However, behavioral procedures have indicated that very variable, this difference fell to about 0 .5 octaves by age
acuity fo r high 'C on trast gratings improves from approxi­ 9 m onths. The superiority o f binocular over m onocular
mately 100 arcm in at 1 m onth, to 2 0 arcmin at 3 m onths, to acuity was evident after age 6 m onths (B irch 1985) (Portrait
10 arcmin at 12 m onths, and to th e adult value o f 1.5 arcmin Figure 7 .5 ).
(4 0 cp d ) at 5 years o f age (D obson and Teller 1978; Jacobson
et al. 19 8 2 ; Mayer and D obson 1982; Banks and Stevens
7 .2 .1 c D e v e lo p m en t o f V c r n ic r A cuity
19 8 5 ; C o ck er et al. 1 994).
M aurer c t al. (1 9 9 9 ) tested grating acuity in 28 infants Vernier acuity is a hyperacuity because it is finer chan chc
immediately after their vision had been restored by removal
• 4
mean spacing o f retinal cones. U nlike resolucion acuicy, it is
o f cataracts between 1 week and 9 m onths o t age. Their noc subject со che N yquist lim it (Section 3.1 .3 b ). Several
acuity was no better than that o f neonates bu t showed signs investigators have inquired w hether chis superioricy o f
o f im provement after only 1 hour and continued to improve hyperacuity is present in young children.
over a 1 -m onth rest period. Thus patterned visual inputs are M anny and Klein (1 9 8 5 ) measured vernier acuity in
necessary tor the postnatal developm ent o f acuity. infants from 1 to 14 m onths o f age. They firsc used a prefer-
N orcia and Tyler (1 9 8 5 ) recorded evoked potentials ential-looking procedure, in w hich the child’s direction o f
trom the scalps o f intants in response to a frequency-swept, gaze was recorded while one o f two horizontal lines was

370 • BASIC M E C H A N I S M S

M aterial c h r a n e n y a u to r s k y m pravom
к ju.c7.5- E ileen Bin//. B o rn in N e w Y ork in 1952. She o b ta in e d а B .A .
fro m chc U n iv e rs ity o f C o n n e c tic u t in 1974 and a P h.D . fro m the
U n iv e rs ity o f C a lifo rn ia at Santa B arbara w ith J. M . Foley in 1979.
A fte r p o s td o c to ra l w o rk a t M I T she m oved to the R etina F o u n d a tio n
o f the S outhw est, w here she is n o w se n io r research scientist and a d ju n ct
p ro lcsso r o f o p h th a lm o lo g y a t the U n iv e rs ity o f Texas S outhw estern
M e d ic a l C enter.
rcplaccd with a line wich a vernier offset. They also used a
tracking procedure in which the infants’ eyes were observed
as the vernier target moved from placc to placc. In both pro­
cedures, the experim enter could not see the stimulus but
had to infer ics posicion by w atching chc infancs eyes.
Vernier acuity improved to a mean value o f abouc 2 arcmin
ac age 11 m onths, com pared with a mean adulc value o f
abouc 0 .2 5 arcm in. A cuity was higher and less variable wich
chc cracking procedure chan wich chc cw o-choicc proce­
dure, perhaps because che cracking procedure included a
mocion signal and an accom panying sound.
Sh im ojo ec al. (1 9 8 4 ) used prefcrenci.il looking со mea­
sure vernier and gracing acuities o f infancs aged 2 со 9
m onths (P ortrait Figure 7 .6 ). For vernier acuity, infants
were shown a square-wave vertical grating o f 1.1 cpd and
chc same gracing wich a horizontal offset. The offset grating
oscillated up and down in cime wich a beep sound. This was
designed со encourage chc infancs со acccnd со chc scimulus.
Ic was assumed chac che m ocion would be detected only
when chc off sc с was dccccccd (sec Skoczenski and Aslin
1 9 9 2 ). For gracing acuity, a square-wave vertical gracing of
variable spatial frequency was presented on a gray field.
Vernier acuity was inferior to grating acuity at 2 m onths o f
age, buc by 9 m onths, vernier acuity was 2.5 arcmin while
gracing acuicv was only 5 arcm in. Vernier acuity developed
in parallel with stereoacuity as reported in Held cc al.
(1 9 8 0 ). Sh im ojo and Held (1 9 8 7 ) reporced sim ilar crends.
O n e problem is chac vernier acuicv for otfsccs o f multiple
D E V E L O P M E N T O F P E R C E P T U A L F U N C T IO N S
ShinsukcShim ojo. B o m in T o k y o in 1955. H e o b ta in e d his B .A .
in e xp e rim e n ta l psych o lo g y fro m the U n iv e rs ity o f T o k y o in 1978 and a
P h.D . fro m M I T in 1985. A fte r a p o s td o c to ra l fe llo w s h ip at the S m ith *
K e ttlc w c ll Eye Research In s titu te in San Francisco* he was associate
professor o l psych o lo g y in T o k y o u n til 1997. H e is n o w professor in
th e b io lo g y d iv is io n o f c o m p u ta tio n & neural systems in the C a lifo rn ia
In s titu te o f Technology-
bars may he degraded by crow ding relative to chac for a
single bar.
Zankcr ec al. (1 9 9 2 ) used a cw o-choicc prefcrcncial-
lookingprocedure in which che child chose becween a single
vcrcical bright bar containing tw o offset segments and a
straighc bar. Vernier acuicy increased from abouc 2 5 arcmin
ac 2 m onths o f age to chc adulc value o f abouc 0.2 arcmin ac
5 years o f age. Gracing acuity developed more slowly from
about 8 arcm in at 2 m onths to abouc 1 arcm in ac 5 years.
Gracing acuicy was beccer chan vernier acuicy during che
firsc year, after which vernier acuity becam e progressively
better than gracing acuicy.
In spice o f variacions in scimuli and procedures, all invcs-
cigacors agree chac vernier acuicy changes from being worse
со being superior со gracing acuicy. The change occurs
becween 3 and 12 months.
C ark cct c t al. (1 9 9 7 ) measured vernier and resolution
acuities in children aged from 3 со 12 years. The vernier
stimulus was a bright vertical line with several offsets along
ics length. The resolution scimulus was a vertical dashed line
with variable density o f dashes. Vernier acuicy was always
superior со resolution acuicy and improved more rapidly
wich age. Becween age 3 and 12, vernier acuicy improved
from 15 arcsec со 6 arcsec— 2.5 rimes. M ean dashcd-line
resolution improved from 7 0 arcsec со 4 8 arcsec, a much
smaller difference. Carkccc cc al. concludcd chac, ac all ages
in cheir sample, vernier acuity was finer than expected from
chc densitv o f retinal concs.
• 371
Material chraneny autorskym pravom
 7 . 2 . Id Causes o f Visual Im m aturity*
Th e visual perform ance o f human neon arcs may be lim ited
by any o f the following factors.
Л . Preneural factors.
1. The optical quality an d aperture o f the eye. The growth
o f the eye s accom m odation mechanism is controlled
by image blur in the process ot em m etropization (see
Section 6.3.1c).
2 . The capacity o f the retina to sample the image. The
sam pling capacity o f the retina depends on the
photon-capture efficiency o ft h e receptors and
receptor spacing.
3 . Instability o f gaze an d convergence.
B. N euralfactors.
1. Noise in the sensory transduction process (see
Skoczenski and N orcia 1 998).
2 . Immature stimulus tuning ofreceptive fields o f
ganglion cells an d cortical cells.
3 . L ack o f inhibitory cortical connections. This would
produce spatial blurring o fth e image.
4 . Immature cortical synapses.
5 . Low cortical magnification (extent o f cortical tissue
devoted to each visual angle).
6 . Inability to attend to the stimulus.
Skoczenski and Aslin (1 9 9 5 ) measured the effects o f
adding Gaussian noise on vernier acuity in 3-m onth-olds,
5-m onth-olds, and adults. They concluded that reduction
in intrinsic blur due to optical o r retinal neural factors
accounts for im provem ent in vernier acuity betw een 3 and
5 m onths, but that later im provem ent depends also on the
developm ent o f postretinal m echanism s for processing high
spatial frequencies.
Banks and Ben nett (1 9 8 8 ) estim ated the contrast sensi­
tivity and grating acuity for two idcal-obscrvcr models, one
based on preneural characteristics o f the neonate human
fovea and one based on the characteristics o f the adult fovea.
This analysis predicted a difference in chc grating acuities o f
the infant and adulc o f 2 octaves com pared wich an actual
difference o f 3 .5 to 4.5 octaves. They concluded that imma­
turity o f preneural structures does not fully account for the
poor visual perform ance o f the neonate (sec also Jacobs and
Blakem ore 1 9 8 8 ).
An idcal-obscrvcr model predicts chac vernier acuicy is
inversely proportional со the square root o f photon capture,
while tw o-spot resolution is inversely proportional to the
fourth root o f photon capture (G eisler 1984). Banks and
Ben nett argued that an im provem ent o f photon capture
with age would explain why vernier acuity improves more
rapidly than resolution acuity. However, C arkcct et al.
(1 9 9 7 ) found that developm ental changes in both vernier
and resolution acuities were larger than could be accounted
for by improved photon capture. They concluded that the
developm ent of central neural processes is involved in
im provem ent o f acuity. W illiam s and B oothe (1 9 8 1 ) had
reached the same conclusion in their studies with monkeys.
Using a sim ilar analysis, W ilso n (1 9 8 8 ) concluded that pre­
neural factors play a greater role in lim iting visual perfor­
m ance in neonates than was found in the Banks and Bennett
study.
Adult amblyopes, especially strabismic amblyopes, are
like young children. They have low vernier acuity relative to
resolution acuity because o f deficits in central processing
(Section 8 .4 .2 ).
Such analyses are valuable but can be no better than the
в
set o f assumptions and the data on which they arc based.
7 .2 .1 e D e v e lo p m e n t o f C h r o m a tic S e n sitiv ity
In the first m onth or two, infants are very poor at discrim i­
nating betw een ditferent colors or betw een achrom atic and
chrom atic stim uli, especially at the blue end o f t h e visible
spectrum (Varner et al. 1985; Adam s et al. 1991). By 12
weeks, m ost infants can discrim inate hues over the whole
spectrum.
Banks and Bennett (1 9 8 8 ) proposed that poor color
discrim ination in infants is due ro poor visual sensitivity
rather than to a specific im m aturity o f the color system,
such as an absence o f different cone types. M orrone et al.
(1 9 9 3 ) found no V E Ps to chrom atic stim uli before 7 to 8
weeks o f age. However, Allen et al. (1 9 9 3 ) found that the
ratio ot lum inance sensitivity to chrom atic sensitivity, as
indicated by V E Ps, was the same for 2- to 8-week-old infants
as for adults. They found the same constant ratio when they
reanalyzed the data o f M orrone et al. Brown ct al. (1 9 9 5 )
also found a constant ratio after using optokinetic nystag­
mus to com pare color and lum inance contrast sensitivities
in infants and adults. Brown (1 9 9 0 ) reviewed color sensi­
tivity in infants.
7 .2 .2 О R IE N T A T I О N S E N S I T I V I T V
Braddick c t al. (1 9 8 6 ) found no evidence o f cortical cclls
tuned to orientation in the human neonate, as indicated
by V E Ps generated by changes in the orientation o f a grat­
ing. Evidence o f orientation tuning showed at the age o f
6 weeks. M anny (1 9 9 2 ) measured V E Ps in 3-m onth-old
infants exposed ro a 1-cpd grating changing in orientation
at a rate o f 18 Hz. The visual cortex responded to a change
o f orientation o f 1.33". Th e V E P in adults showed a similar
sensitivity but, when the spatial and tem poral frequencies
o f rhe stimulus were optim ized for adults, their sensitivity
increased to 0.5 3U.
 Binocular cells have che same oriencacion preference for
stimuli presented separately to the two eyes. This does not
seem to depend on visual experience because the receptive
fields o f binocular cells had m atching orientations in kit­
tens raised so thac both eyes did n o t see ac chc same cime
(G o d eck ean d Bonhocffer 1996).
Behavioral cescs revealed thac 6-week-old infancs could
discrim inace becween lines in opposice oblique oriencacions
(M aurer and M arcello 1 9 8 0 ; Held 1981). Lacer ex p erim en t
showed chac human neonaces could discriminace becween
oblique gracings. W h en newborn infancs were shown cwo
opposice oblique scacic gracings side-by-side chey preferred
looking ac che one chac chey had noc seen previously
(Atkinson ec al. 1 9 8 8 ; Slaccr cc al. 1988). In ocher scudics,
3-m onch-old infancs could discriminace becween gracings
cilced 4 5 “ and 15”, and 4-m onch-old infancs could discrim i-
nace becween gracings cilced 45° and 22° (Bom ba 1984;
T em poral frequency (Hz)
Bornscein ecal. 1 986).
The older liceracure on che developmenc o f che ability со r.A«.<?.7. Tem poral contrast sen sitivity am i age. The s tim u lu s was a u n ifo rm
categorize oriencacions was reviewed in Howard (1 9 8 2 ). flic k e rin g h e ld . (лЛ лр | с (! from Я л*си |;л!сс! 1997)

Л prefcrencial-looking procedure revealed chac infancs

under 14 weeks o f age could dccccc a pacch differing in
lum inance concrasc from ics surround buc could noc dccccc
a pacch concaining oblique lines sec in a surround o f lines in
a differenc oriencacion (Ackinson and Braddick 1992). They
concluded chac, alchough neonaces can discriminace
becween sidc-by-side gracings chac differ in oriencacion, chc
abilicy со group and segmenc embedded cexcures differing
in oriencacion cakes abouc 14 weeks со develop.
Adulcs are able со dccccc aligned concour elemencs
embedded in a random array o f elemencs (Seccion 4.5.2b ). In
a group of 4 0 0 children, chis abilicy improved becween che
ages o f 5 and 14 years (Kovacs 2 0 0 0 ). This suggests chac che
long-range connections in chc visual corcex chac are needed
for chis cask concinue со develop during chis age period.
7.2.3 F L I C K E R AND M O TI ON SENSITIVITY
7 .2 .3 a D e v e lo p m e n t o f F lick e r Sensicivicy
The cricical flicker frequ en cy , or C F F , is che highesc fre­
quency o f flicker o f a high-concrast stimulus that produces
a modulated response in che visual syscem. The C F F , as
indicaced by che elcccrorecinogram (E R G ), is adulc-like in
human neonaces (H orsccn and W inkelm an 1962). The
C F F , as indicaced by che corcical visual evoked pocencial
(V E P ), increases rapidly after chc lsc m onth and is adulc-
like by 5 m onchs (Apkarian 1993). This suggescs thac che
early limicacion is due со poscrccinal faccors. The adulc C F F
decermined psychophysically is abouc 5 0 Hz (Wacson
1 9 8 6 ). Using preferential looking, Regal (1 9 8 1 ) found thac
che C F F for a uniform field reached adulc levels o f over 50
H z by about the 12th week.
The tem p oral concrasc-sensicivicy fu nccion ( T C S F ) is
the contrast required for dececcion of flicker as a function o f
temporal frequency. The adult T C S F is typically bandpass
for a uniform field and for a low spatial-frequency grating
flickering in councerphase. Ic is low-pass for a high spatial-
frequency grating.
Rasengane ec al. (1 9 9 7 ) used a preferencial-looking pro­
cedure со measure che T C S F for a uniform field. Peak scn-
sicivicy increased from between 1 and 2 Hz ac 2 m onths, to
4 Hz ac 3 monchs, со 8 Hz ac 4 monchs, as shown in
Figure 7 .7 . Thus, peak sensicivicy shifted to higher frequen­
cies with increasing age, causing the function to change
from low-pass со band-pass. The C F F increased from 13 Hz
ac 2 monchs со 2 2 H z ac 4 monchs, scill well below che adulc
value. N one o f che infants responded со 3 2 H z, che highesc
frequency cesced. Nevercheless, while sensicivicy со high
flicker races macurcs ac an early age, sensicivicy со lower can -
poral frequencies was found noc со reach adulc levels
uncil 7 years (Ellem bergec al. 1 9 9 9 ).
The form ot che T C S F depends on che spacial frequency
o f che flickering scimulus. Swanson and Birch (1 9 9 0 ) found
chac concrasc sensicivicy, assessed by preferential looking,
increased becween che ages o f 4 and 8 m onchs for a 1-cpd
gracing flickered ac becween 8 со 17 Hz buc did noc change
for races o f 2 со 4 H z. Thus che T C S F ас 1 cpd changed
from being low-pass ac 4 monchs со being more band-pass ac
8 monchs. Ac 0.25 cpd che T C S F remained band-pass.
Harcmann and Banks (1 9 9 2 ) found a sim ilar change in che
T C S F from low-pass со band-pass for a 0.5-cpd gracing
becween che ages o f 1.5 and 3 monchs.
'" .2 .3 b D ev e lo p m e n c o f M o tio n Sensicivicy
O pcokinecic nyscagmus (O K N ) in human neonaces shows
chac chey are sensicive to uniform mocion. O K N is under
subcorcic.il control in chc young infant (Scccion 2 2 .6 .1 ).
This response indicated that the chreshold for detection o f
uniform mocion was conscanc ac abouc 3 7 s for infants
between 12 and 18 weeks o f age (B an ton and Bcrtenthal
1996).
N eonates responded to loom ing optic flow with a back­
ward m otion o f the head. The magnitude ot head m otion
increased with increasing velocity o f optic flow (Jou en
c t al. 2 0 0 0 ). This response is also probably under su bcorti­
cal control.
O cher experimencs on m ocion sensitivity in infants used
preferential looking, w hich must surely involve cortical pro­
cesses. To establish that infants are sensitive to visual m otion
one must dem onstrate that they respond specifically to
m otion rather than to flicker or change ol position. Aslin
and Shea (1 9 9 0 ) found that 6-week-old infants could discin-
guish bee ween stationary stripes and stripes moving at 9°/s
relative to a stationary surround. At 12 weeks, chey could
distinguish stripes moving at 4°/s. The velocity threshold
did not vary with stripe width, which indicates that the
infants were judging m otion rather than simple flicker
(num ber o f edges passing a given location in unit tim e). ri*u«c-.x. Ja n ette A tkinson. B o rn in C h e sh ire , F.ngland, in 1943- She

D annem iller and Frccdland (1 9 9 3 ) showed that
14-week-old infants detect m otion in standing-wave line
stim uli. These stimuli allow sensitivity4 to m otion to be dis-
tinguished from sensitivity to changes in position (sec also
Bcrtenthal and Bradbury 1 992).
W accam-Bcll (1 9 9 2 ) used preferential looking со mea­
sure che maximum displacem ent {dt/i) ° f a random-doc
paccern that allowed subjects to discrim inate betw een direc­
tions o f m otion and betw een coherent and incoherent
m otion. Betw een 8 and 15 weeks ot age, the oldest age-
tested, d n increased for both casks. The same developmen-
cal crcnds were evidenc in che m agnitude ot che visual evoked
pocencials criggered by m ocion o f checkerboard pacterns
(W actam -Bcll 1 991). The results suggesc chac scnsicivicy со
low velocities (small d ) develops before scnsicivicy со
high velocities (large d ).
O ne-m onch-old infants discriminaced becween inco-
herenc and coherent m otion o t random -dot patterns but,
even at 3 m onths o f age, detection required that 50% o f the
dots moved coherently compared with only 5-7% tor adults
(W attam -Bell 1 994).
Brosseau-Lachaine et al. (2 0 0 8 ) used a pretercntial-
looking procedure to measure the ability o f infants between
the ages o f 2 and 10 m onths to detect radially moving
random dots as a function o f the percentage o f randomly
moving dots. Sensitivity to radial optic flow improved
during the first tew m onths. Im provem ent was more rapid
for expanding than for contracting flow. Forward self-m o­
tion produces expanding flow. W e saw in Section 5.8.4c
that there are m ore cells sensitive to radial expansion
than there are cells sensitive to contraction in the medial
superior temporal cortex ( M S T ) and the parietal lobes o f
monkeys.
o b ta in e d a B.Sc. in psych o lo g y fro m B ris to l U n iv e rs ity in 1965 and я
P h .D . fro m C a m b rid g e U n iv e rs ity in 1971. A fte r p o s td o c to ra l w o rk at
Johns H o p k in s U n iv e rs ity she was a research associate a t C a m b rid g e .
From 1983 to 1993 she was senior external scientist o l th e M e d ic a l
Research C o u n c il at C a m b rid g e . She has been a professor
a t U n iv e rs ity C ollege . L o n d o n , since 1993- W in n e r o l the
K u rt-K o H k a m edal, 2009.
Infants aged 8 - 1 0 weeks responded to second-order
m otion defined by a grating ot random flicker sweeping
over a stationary random -dot display (Atkinson 2 0 0 0 ,
p. 8 1 ) (P ortrait Figure 7 .8 ).
H am er and N orcia (1 9 9 4 ) used VF.Ps to measure dis­
placement thresholds for a high-contrast, 1-cpd grating
oscillating from side to side at 6 H z. In 12-wcck-old intants
the threshold was 10 times che adult value, even though
contrast sensitivity was already h a lf the adult value. The
oscillation threshold was still over four times that o f che
adult in 1-year-old
*
intants.
Sensitivity to relative m otion, especially shear, as
assessed by preferential looking, continued to develop
betw een 12 and 18 weeks o f age (B anton and Bertenthal
1 9 9 7 ).
Alm ost all o f 2 6 infants between the ages o f 4 and 5
m onths showed a V E P response to a transition trom coher­
ent m otion to incoherent m otion. O nly h a lf the infants
showed a response to a transition trom a patterned array to
a random array o f segments (W attam -B ell et al. 2 0 1 0 ).
A lm ost all adult subjects responded to both stimuli.
This suggests chat mocion dececcion develops before form
detection.

7 .2 .3 c D e v e lo p m e n t o f D ire c tio n -o f-M о tion
Sensitivity4
An isotropic random -dot pattern is useful for studying dis­
crim ination o f m otion directions because, in this scimulus,
a change in m otion direction does not change elem ent ori­
entation. Also, a change in stimulus location is difficult со
detect.
There is evidence that detection o f the dircccion o f
m otion develops later than detection o f m otion. Thus,
although 1-monch-old infants could discrim inate between
stationary and m oving random -dot patterns in a preferen-
tial-looking procedure, they could noc discrim inate bccween
opposed directions o f m otion over a wide range o f veloci­
ties (W attam -B cll 19 9 6 a ). Psychophysical evidence indi­
cated that 3-m onth-old infants are sensitive to opposed
directions o f m otion (D ob k in s and Teller 1996).
O n ly 25% o f 121 infancs under 7 weeks o f age showed
VF.P responses со random -dot displays moving at I Г /s that
reversed their direction o f m otion four times per second. At
11 weeks, 8 0 % o f the infants showed responses. All the
5-week-old infants showed VHP responses со stationary
patterns thac reversed in orientation (Braddick c t al. 2 0 0 5 ).
Thus, cortical m echanism s for detection o f a change in
m otion direction develop later than those for detection o f
m otion or change in orientation.
The above studies used a change in m otion direction o f
180°. They could therefore not determ ine the threshold
change in direction. O n average, adults detected a difier-
encc o f 1.8' in the direction o f m otion o f a random -dot dis­
play moving at the optim al velocity o f 6 4 7 s (D e Bruyn and
O rban 1 988).
B an ton et al. (2 0 0 1 ) presented infants with a large ran­
dom -dot array m oving vertically at 1 Г /s. A 7.4° circular
region moved at the same velocity in a different direction.
The stimulus was moved suddenly every 5 0 0 ms to engage
the in fan ts attention. A preferential-looking procedure
revealed that 6-wcck-old infants did not discrim inate dif­
ferences in m otion direction. A difference o f 22° was dis­
crim inated at 12 weeks and a difference o f 17° at 18 weeks.
N eonates must detect m otion direction in chc subcorci-
cal areas that control optokinetic nystagmus (O K N )
because, in the neonate, O K N evoked by m onocular tem -
poronasal m otion is stronger than that evoked by nasotcm -
poral m otion. (Seccion 2 2 .6 .1 ). The direction o f O K N in
1-m onth-old infants was changed by a change o f 45° in the
direction o f m otion o f a plaid pattern (M anny and Fern
1990).
In humans, the directional asymmetry o f O K N declines
over the first 2 4 m onths because o f the growth o f cortical
inputs to the O K N system (Lew is et al. 2 0 0 0 ). B irch c t al.
(2 0 0 0 b ) found that cortical potentials did not show any
directional asymmetry in neonates, which supports the
n otio n that the neonate visual cortex is not sensitive to
direction o f m otion. D irectional asymmetry o f cortical
responses was evident in 2 -m onth-old infants, buc che
responses becam e symmetrical by the age o f 8 m onths. The
cortical asymmetry persists in adults wich early onset stra­
bismus (N orcia e t al. 1991).
This evidence suggests that a subcortical direction-se-
leccive mechanism underlying O K N develops before the
corcicai direction-selective mechanism chac is required for
visual discrim inations. This idea is supported by the finding
thac O K N in 6-week-old infants was evoked by a random -
doc display containing only 2 0 % o f moving docs. By co m ­
parison, infants required a much larger percentage o f
moving dots before chey could make a forced-choice dis­
crim ination becween a display with no relative m otion and
one with relative m otion (M ason cc al. 2 0 0 3 ). Developmenc
o f mocion sensitivity was reviewed by W attam -Bcll (1 9 9 6 b ).
D evelopm ent o f sensicivicy со mocion in depch is discussed
in Section 7.4.1c.
7 .2 .4 D EVELOPM EN T OF TH E
V IS U A L F I E L D S
The visual field is plocced by firsc gcccing chc animal being
tested to prefixate a central flashing targec. The experi­
m enter then observes w hether the eyes move to a Hashed
target presented at different eccentricities. For details, see
Sireteanu (1 9 9 6 ). The extent o f the visual field may be influ­
enced by optical factors as well as by retinal factors.
The size o f the visual field increases with age. In kitcens,
the visual field reaches its adulc excenc by abouc 10 weeks o f
age (Sircccanu and M aurer 1982). In humans under 2
m onths o f age, the region o f binocular overlap is smaller
than that o f the adult, especially along the vertical meridian
(Schw artz c t al. 1 9 8 7 ). Th e horizontal excenc o f chc region
ot overlap in 3-m onch-old human infancs has been esci-
maced as 60 " and chac in rhe 4 -m onth-old infant as 8 0 ”
(Finlay et al. 1982). The adult level o f about 90° is reached
betw een 6 and 12 m onths o f age (M oh n and van Hof-van
D uin 1986; Lewis and M aurer 1992).
Visual funccions in chc cemporal h alf o f che m onocular
visual field (nasal hem iretina) develop before those in the
nasal hemificld (tem poral hem iretina). For example, visual
acuity revealed by preferential looking was higher in the
temporal than in the nasal visual field o f infants between 2
and 11 m onths o f age (Sireteanu e ta l. 1994). For som e time
after firsc opening cheir eyes, kitcens oriented coward stimuli
in the tem poral visual field o f an eye, but ignored stim uli in
the nasal field (Sireteanu and Maurer 1982). Similarly,
human infants below 2 m onths o f age looked towards an
isolated light presented 3 0 u in to the tem poral m onocular
field buc noc cowards a light only 15" inco rhe nasal field
(Lewis and Maurer 1992). A similar procedure revealed
chac after che age o f 2 m onths boch hem ifields and the b in ­
ocular field expand rapidly uncil the age o f 8 m onths and
then more slowly until the age o f 12 m onths (M ohn and
Van Hof-van D uin 1986).
 A lthough the nasal hemifield remains smaller than the
temporal hem ifield, the tw o hemifields becom e more sim i­
lar in size with increasing age. Even in the adult monkey,
there are m ore cortical cells with a dom inant input trom the
contralateral eye (nasal hem iretina) than cells with a dom i­
nant ipsilateral input (tem poral hem iretina) (LeVay et al.
1985). The cortical magnification factor (linear extent ot
cortex devoted to unit visual angle) is proportional ro the
density o f ganglion cells ( Rovam o and Virsu 1979). Because
ganglion cells are denser in the far nasal retina than in the
temporal retina (C u rcio et al. 1 9 9 0 ), the magnification
factor is also higher for the nasal retina. The mature nasal
hem iretina is also m ore sensitive than the tem poral hem iret­
ina. Thus, decreases in vernier acuity and grating acuity with
increasing eccentricity o f the stimulus are steeper tor the
temporal than tor the nasal hem iretina (Fahle and Schm id
19 8 8 ; Grigsby and Tsou 1 994). R eaction tim es are shorter
for scimuli presenced to the nasal hem iretina (Payne 1967).
O ther aspects o f hemifield asymmetry are discussed in
Section 12.3.4.
For a review ot the developm ent o f spatial vision see
M ohn and Van Hof-van D uin (1 9 9 1 ).
7 .3 GROW TH OF TH E O CU LO M O TO R
SYSTEM
7 .3 .1 A C C O M M O D A T IO N
The developm ent o f the eye in relation to the developm ent
o f accom m odation was discussed in Section 6 .3 .1 . The pres­
ent section is concerned with che developm ent ot accom ­
modation in human infants.
The relaxed accom m odation o t an eye can be measured
with a retinoscope, w ith the ciliary muscles paralyzed by a
cycloplegic drug (Section 9 .2 .4 ). In a second m ethod, which
docs n o t require a drug, refraction is measured while rhe
child views adim m ed retinoscope light that is a poor accom ­
modative stimulus (M oh in d ra 1 975). There arc reports thac
human intants are about 2 diopters hyperm etropic relative
to the average adult. However, retinoscopy in infants is
unreliable, so the hypcrm etropia may be an artifact (Banks
1980). Severe untreated hypcrmetropia in infants can lead
to amblyopia (Ingram and W alker 1979).
The accom m odation response o f an eye can be measured
while a large pattern is moved to different distances. The
infrared optom eter is the m ost precise m ethod for measur­
ing changes in accom m odation (Section 9 .2 .4 ). However, it
can n ot be used in infants because the observer must m ain­
tain fixation. W ith infants, refraction is measured with
dynam ic retinoscopy, which gives the sign o f the refractive
error but takes time to operate; or by photorefraction,
which measures the instantaneous refractive state ot both
eyes (H ow land and Howland 1 9 7 4 ). The size o f the retinal
image must be kept constant to ensure that any lack o f
accom m odation is not due to the stimulus falling below the
resolution threshold.
N eonates showed signs o f changing accom m odation to
binocularly viewed large conspicuous objects nearer than
about 75 cm (Brookm an 1 9 8 3 ; Howland et al. 1987;
H ainline et al. 1 9 9 2 ). Beyond 8 weeks, accuracy (gain) o f
accom m odation increased. Adult levels were reached
betw een 16 and 2 0 weeks (H aynes et al. 1 9 6 5 ; Brookm an
1 9 8 3 ). Banks (1 9 8 0 ) concluded that accuracy o f accom m o­
dation is poor in infants, largely because o f their poor reso­
lution. The fluctuations ot steadv-statc
# accom m odation in
infants o f betw een 8 and 3 0 weeks o f age were larger than
those in adults (Candy and Bharadwaj (2 0 0 7 ).
After 8 m onths the gain o f accom m odation was greater
with binocular than with m onocular viewing (Turner et al.
2 0 0 2 ). The binocular advantage increased to adult levels by
about 8 years (Bharadwaj and Candy 2 0 0 8 ). Thus, the co n ­
tribution o f binocular disparity to accom m odation cakes
tim e to develop. By 6 m onths, che range o t accom m odation
is similar со that o f the adult (Braddick et al. 1979).
There are several reports that children below 4 years
tend to be astigm atic, with a vertical axis o f astigmatism.
This is “against the rule" astigmatism. However, there is dis­
pute on this point (see Saunders 1 9 9 5 ). In older children
and adults, astigmatism tends to be along a horizontal axis.
This is “with the rule astigmatism" (D obson et al. 1984;
G w iazd aet al. 1 9 8 4 ; Howland and Sayles 1984).
D epth o f field is the range o f discances w ithin which an
o b ject is in focus for a given state o f accom m odation. D epth
o f field is inversely proportional to pupil diam eter and to
the size o f the eye (Section 9 .6 .4 ). D epth o f field is greater
in intants than in adults. This is because the pupils o t intants
under 2 m onths o f age arc, on average, betw een 1 and 2 mm
smaller than those ot adults, and because the eves
* ot intants
arc smaller than the eyes o f adults (see B oothe et al. 1985;
G reen et al. 1980). Thus, image quality is less affected by
m isaccom m odation in the infant eve* chan in che adult eve.
*
In any case, image quality is not as im portant tor the infant
because high spatial-frequencies can n ot be resolved.
Accom m odative convergence is present in 2-m onth-old
infants; younger infants have n o t been tested (Aslin and
Jackson 1 9 7 9 ) (P ortrait Figure 7 .9 ).
W ith increasing age, the unaccom m odated eye increases
in focal length, causing the eyes o f older people to becom e
m ore farsighted, a condition known as p resbyop ia (Evans
1 9 9 7 ). There are no age-related changes in the refractive
index o f the lens (Glasser and C am pbell 1999).
Between the ages o f 10 and 5 0 years, the range o f accom ­
m odation declines from 10 diopters to about 1 diopter at a
constant rate o f about 0 .2 diopters per year (Sun et al. 1988;
Kragha 1 9 8 9 ). W h en tension is applied to the ciliary body
o f an excised eye, the focal length o f a young lens changes
significantly buc that o f a lens older than about 6 0 years
shows little or no change (Glasser and C am pbell 1998).
It seems that lens hardening rather than changes in the
F ifufc?.* R ichard N Ad in. B o r n i n M i l w a u k e e , W i s c o n s i n » in 1 9 4 9 . H e
r c c c i v c d b is В . Л . i n p s y c h o l o g y f r o m M i c h i g a n S t a t e U n i v e r s i t y in
197 1 an d h is P h .D . in c h ild p s y c h o lo g y a t th e U n iv e rs ity o f M in n e s o ta
in 1 9 7 5 w i t h P h i l i p S a l a p a t c k . F r o m 1 9 7 5 t o 1 9 8 4 h e w a s a m e m b e r o f
t h e f a c u l t y i n p s y c h o l o g y a t I n d i a n a U n iv e r s ity » B l o o m i n g t o n . In 1 9 8 4
h e m o v e d t o t h e U n i v e r s i t y o f R o c h e s t e r » w h e r e h e is n o w a p r o f e s s o r
o f b r a in a n d c o g n itiv e s c ie n c e s and a m e m b e r o f th e C e n t e r fo r V isu a l
Scicn cc.
ciliary musclcs is chc m ajor cause o f the age-related loss o f
accom m odative range.
Lens hardening increases rhe dam ping cocfficicnc o f the
lens 20-fold betw een the ages o f 15 and 55 years (B eers and
H eijde 1 996). This should reduce the speed o f accom m oda­
tion. Schaeffel e t al. (1 9 9 3 ) found great variability in sub­
jects’ speed o f accom m odation bur that the maximum speed
declined betw een the ages o f 5 and 4 9 years. Sun e t al.
(1 9 8 8 ) reported chat the rime constant o f accom m odation
doubled betw een the ages o f 13 and 4 0 years. However,
these studies took no account o f the decrease in the range o f
accom m odation with increasing age.
H eron et al. (2 0 0 1 ) made measurements w ithin the
effective range o f accom m odation. They found chat reac­
tion tim e, response time, and response frequency to unpre­
dictable + 1.05-diopter step changes in distance showed no
systematic changes over che same age range. They concluded
chac, for small scimuli wichin chc amplicude range o f accom ­
m odation, chere is licde change in che dynamics of accom ­
m odation, at lease up со chc age o f 4 9 years.
Similarly, M ordi and Ciuffreda (2 0 0 4 a ) found no
changes in chc cimc conscanc or peak velocicy o f accom m o­
dation becween che ages o f 21 and 5 0 years, when measure­
ments were confined to the effective range. Hut they did
find an age-dependent increase in latency and a decrease in
the am plitude o f m icrofluctuations o f accom m odation.
The increasing hardness of the lens should increase the
phase lag o f accom m odation. Phase lag in response to a
r.*w « -.ia R ich or AHeld. B o r n in N e w Y o r k in 1 9 2 2 . H e o b t a in e d a
B . S c . i n e n g i n e e r i n g f r o m C o l u m b i a U n i v e r s i t y in 1 9 4 4 a n d л P h . D . in
p s y c h o l o g y f r o m S w a r t h m o r e C o l l e g e in 1 9 4 8 . A f t e r p o s t d o c t o r a l w o r k
at H a r v a r d U n i v e r s i t y h e j o i n e d t h e p s y c h o l o g y d e p a r t m e n t at B r a n d c i s
U n i v e r s i t y in 1 9 5 3 - I n 1 9 6 3 h e b e c a m e p r o f e s s o r o f e x p e r i m e n t a l
p s y c h o l o g y at M I T . A l t e r r e t i r i n g in 1 9 9 4 h e b e c a m e p r o f e s s o r e m e r i t u s
a t M I T a n d d i r e c t o r o f r e s e a r c h in t h e d e p a r t m e n t o f v i s i o n s c i c n c c at
th e N ew E n g la n d C o lle g e o f O p to m e t r y .
target oscillating in depth through 0 .5 2 diopters betw een
0.05 and 1 Hz increased slightly, especially at higher fre­
quencies, as age increased from 18 со 4 9 years (H eron ec al.
1999).
7.3.2 THF . P U P I L L A R Y R E S P O N S E
The pupils o f normal adulcs conscricc abouc 29 % more wich
binocular illum ination chan wich m onocular illum ination
(ccn Docsschacc and A lpcrn 1967). Birch and Held (1 9 8 3 )
used chis facc со invescigace developmenc o f binocularicy in
infancs (Porcraic Figure 7 .1 0 ). The pupils responded more
to binocular chan m onocular illum ination by che age o f 4
monchs. The differential response was adulc-like by che age
o f 6 monchs. However, Shea ec al. (1 9 8 5 ) found reduced
buc significanc binocular lum inancc summation in chc
pupillary response o f 2-m onch-old infancs and in scere-
oblind adulcs (see also Sircccanu 1987). These rcsulcs sug-
gesc chac che developmenc o f che pupillary response is со
some cxcenc indcpcndcnc o f che developmenc o f stereopsis.
7.3.3 EYE A L I G N M E N T
D uring che firsc poscnacal m onch, kiccens have a large diver-
genc scrabismus, as indicated by chc divergence o f chc pupils
wich respecc со che opcic axes. Th e locations o f che opcic
axes arc indicaced by chc images o f a poinc o flig h c rcHccccd
from che corneas. By the end o f che second poscnacal m onth,
the optic axes becam e alm ost centered on the pupils.
Sherm an (1 9 7 2 ) concluded that divergent strabismus in
kittens changes in to a slight convergent strabismus.
O lson and Freeman (1 9 7 8 a ) measured che angle
between the visual axes o f kittens by plotting the receptive
fields o f cells in cortical area 17 with reference to p h o to ­
graphs o fth e pupils. They concluded thac the visual axes are
aligned wich the foveas even during the first two postnatal
m onths. This suggests chac the change in alignm ent o f rhe
pupils with the optic axes is accom panied by a medial migra­
tion o f the central retina. Ifw e assume thac each optic axis is
norm al со the pupil and passes through the entrance pupil,
chis process cncails a reduction in the angle betw een rhe
pupillary axis and the visual axis (angle lambda) Irom about
25° to 15°. Thus, as the eyes rotate inward during the firsc
two m onths, the central retina migrates medially. This
occurs in normally reared and dark-reared cats, except thac
norm ally reared cats reach a steady state m uch earlier than
dark-reared cacs (V on Griinau 1 9 7 9 ). Ic seems chac che basic
changes are macurational. Visual inputs are required only to
cerminace the changes.
O lson and Freeman tound that the inward torsional
angle between che slic pupils o f cats increased during che
first 2 months' to a value o f about 14°. In dark-reared ani­
mals this process continued through the 3rd m onth со reach
a mean value o l 24°.
The eyes ot human neonates tend to be divergent. It is
nor known w hether there is a medial m igration o f che fovea
in humans but the angle lambda has been estimated to
change from 7.9" at birth to 5.08° in the adult (London and
W ick 1 982).
Binocular alignm ent o f human eyes during and ju st after
saccadic eye movem ents improved from age 4.5 years to
adult levels ac 12 years (Vang and Kapoula 2 0 0 3 ).
7.3.4 PURSUIT EYE MOVEMENTS
Ultrasound im aging reveals a variety o f slow and fast eye
movements in the human fetus betw een 16 and 4 2 weeks ot
gestation (B irn h olz 1981).
O p to k in e tic nystagm us (O K N ) is an involuntary eye
movement evoked by movement o f the whole retinal image.
Pursuit movements (slow phases) are interspersed with sac­
cadic returns (fast phases). O pcokinecic nystagmus supple­
m ents the vcstibuloocular response and thereby stabilizes
the image as the anim al moves about. O pcokinecic nyscag-
mus is n o t under voluntary control. Ic is present in boch
fovcatc and afovcatc vertebrates and is controlled bv *
sub-
cortical nuclei with a cortical contribution only in higher
mammals, as we will see in Section 22.6.1.
G ratings m oving at up ro about 40°/sevoke optokinetic
nystagmus in neonate infants (K rem cnitzer c t al. 1979).
Von H ofsten and Rosander (1 9 9 6 ) measured O K N in
infants bccween 2 and 5 m onths ot age in response to a
vertical gracing filling chc visual field and m oving from side
to side at betw een 1 1 and 3 3 .4 % . O ver this period, gain
was fairly constant but phase lag decreased from 170 to 7 0
ms and latency decreased from 8 6 0 to 5 6 0 ms. Eye and head
tracking were reciprocally related.
M onocular optokin etic nystagmus (O K N ) o f human
infants below the age o f about 3 m onths is stronger in the
nasal direction than in the temporal direction. The same
directional asymmetry is typical o f animals lacking stereo­
scopic vision. The cime course for the developm ent o f sym­
m etrical O K N tor large, high-concrast stimuli is similar to
that for the developm ent o f stereopsis (W estall 1986;
Brown et al. 1 9 9 8 ). However, with fine gratings, some direc­
tional asymmetry o f O K N is evident in 24-m onth-old
infants (Lew is et al. 2 0 0 0 ). People lacking stereopsis retain
asymmetry o f O K N (sec Section 2 2 .6 .1 ).
O p to k in etic nystagmus must be suppressed when a
person fixates a stationary o b ject on a moving background
or when a person pursues an o b ject moving over a station­
ary background. Human adults can n ot suppress O K N
when there are no stationary objects in view but can readily
do so when a single stationary o b ject is presenc. O ne-m on th -
old infants showed no suppression o f O K N in the presence
o f a stationary o b ject, but 2-m onth-old infants showed
som e suppression o f O K N (Aslin and Joh n son 1996).
An eye m ovem ent in pursuic o f an objccc is known as
sm o o th pursuit. Sm ooth pursuit keeps the image o f the
o b ject on the fovea. Ic is therefore present only in animals
with fovcatc eyes and is necessarily under voluntary control,
especially when the o b ject moves with respect to stationary
objects.
It has been claim ed chat neonaccs show occasional pur­
suic eye movcmcncs to an o b ject moving at up to abouc
2 0 7 s (Krcm eniczer et al. 1 9 7 9 ). However, the o b jcct sub­
tended 10" and may have evoked O K N rather chan smooch
pursuic. In infants younger than 6 to 8 weeks, Aslin (1 9 8 7 )
did not observe sm ooth pursuic o f a 2°-wide vertical bar
m oving sinusoidally. Sm ooth pursuit ot a stcp-ram p o t a 2°
w hite square on a black background was slow and poorly
related to the velocity o f the target in 8-m onth-old infants
(Shea and Aslin 1990).
Von H ofsten and Rosander (1 9 9 7 ) measured sm ooth
pursuit eye movements o f infancs between the ages o f 2 and
5 m onths to sinusoidal or triangular m otion (0 .2 or 0 .4 H z)
o f a 10°-wide face on a w hite background. Pursuit gain (eye
velocity over stimulus velocity) increased over this period.
For sinusoidal m otion, phase lag was low, and by 5 m onths
pursuit began to lead the m otion o f the stimulus. For trian­
gular m otion, phase lag was large and did noc anticipate che
m otion o f t h e stimulus. The gain o f sm ooth pursuit does
n o t reach adult levels until mid adolescence (Salm an cc al.
2 0 0 6 a ).
In all the above studies the moving target was presented
on a blank background. U nder these conditions eye move­
m ents may be O K N rather than voluntary pursuit.
fusion involving preferential looking betw een a fusible pair
o i gratings and a rivalrous pair o l gratings. The few infants
that were noc ordhotropic during the first postnatal m onth
were exotropic. A lm ost all the infants were orthotrop ic by
the fourth m onth. Convergence began to show at 6 weeks,
but full convergence did n o t occur until betw een the 13th
and l 7 th weeks. The infants showed evidence of binocular
fusion betw een the 12th and 16th weeks. There was a high
correlation betw een the age o f onset o f convergence and
that o f binocular fusion.
Vergence accom m odation (accom m odation induced by
a change in vergence) has been investigated in infants by
placing a prism o f 2 , 15, or 2 0 diopters in fron t o f one eye
while the infants viewed a nonaccom m odative target co n ­
sisting o f a diffuse 2.7° patch o f light (B o bier e t al. 2 0 0 0 ).
Th e infants ranged in age from 1 to 3 m onths. A ccom m o­
dative changes were observed in som e o f the 3-m onth-old
infants. The mean stimulus C A / C ratio (accom m odative
change divided by prism power) was higher in the intants
than in adults. The response C A / C ratio (accom m odative
change divided by the vergence response) was not deter­
mined because vergence was n o t measured.
A ccom m odative vergence (vergence induced by a
change in accom m odation) has been investigated in infants
by measuring eye alignm ent with far and near targets viewed
binocularly and m onocularly (Aslin and Jackson 1979).
Accom m odative vergence was observed in 2-m onth-old
infants, bu t the m agnitude o f the response was not mea­
sured. Turner et al. (2 0 0 2 ) used the same procedure bu t
measured both accom m odation and vergence with a photo-
refractive technique. The infants ranged in age from 1 ro 54
weeks. Below the age ot 8 weeks, accom m odation changed
with target distance, but the response improved up to the
age o f 2 6 weeks. Changes in accom m odation could have
been evoked by image blur o r by the change in the angular
subtense ot the target. Vergence changes were not observed
below the age o f 8 weeks. After that age, vergence responses
improved up to the age o f 16 weeks. After the age o t 8
weeks, vergence responses were stronger with binocular
viewing than with m onocular viewing. This indicates some
contribution o f binocular disparity. However, m ost infants
older than 8 weeks showed some vergence responses with
m onocular viewing. This indicates the presence o f accom ­
modative vergence. However, it is not clear w hether m on­
ocular vergence was evoked by changes o f accom m odation
o r by the changing angular size o f the target.
Infants do noc need to move their eyes to d etect coarse
disparities. Birch et al. (1 9 8 3 ) found that infants over 6
monchs o f age, wich fully developed scereoacuicy, arc insen­
sitive to errors o f vergence o f up to 1.4°. C hildren had to
reach an average age o f 4.1 m onchs before they could distin­
guish depth in stereograms in which the disparity was
allowed to reach 1.4°. From this evidence, Birch et al. co n ­
cluded that the developm ent ofsrereoacu ity in the infant is
lim ited by the m aturation of disparity-detecting neurons
and not by the m aturation o f the vcrgcncc system. This
argum ent depends on the assumption that the younger
children would also tolerate vergence errors o f up to 1.4° if
the neural system were mature.
7 .4 D E V E L O P M E N T O F V IS U A L
DEPTH P E R C E P T IO N
7 .4 .1 P E R C E P T IO N O F D IS T A N C E
7 .4 .1 a A c c u ra c y o f R e a c h in g M o v e m e n ts
The earliest identifiable responses o t the arm are the neck-
tonic reflex evoked by rotation o f the head, the traction
reflex evoked by pulling the arm, and the grasp reflex evoked
by touching the palm o f the hand (T w itch ell 1 9 7 0 ). None
o f these innate reflexes is visually evoked.
W h ite et al. (1 9 6 4 ) outlined a normative developm en­
tal sequence o f visually guided reaching in infants. In chc
firsc monch, infants do not attend to objects w ithin arm’s
reach, and arm movements are unrelated to vision. In the
second m onth, infants attend to near o b jects and becom e
interested in their own arms. The first visually directed
swiping m ovem ents o f the arm develop in this period, but
the child grasps an o b ject only if the hand touches it. In chc
chird monch, arm swiping gives way со dirccced arm move­
m ents, and che child looks back and forth betw een object
and hand. By the fourth and fifth monchs chc com bined
action o f the arms com es under visual control and the child
is able to reach for and grasp an o bject. Reports that infants
only a few days old reach for visual objects and occasionally
grasp them have n o t been confirm ed (Bow er ct al. 1970b ;
Dodw ell et al. 1976).
Nine-week old intants cannot reach for an o b ject across
the body m idline. By 18 weeks, they behave like adults on
this task (Provine and W cstcrm an 1 9 7 9 ). Coordinated
bimanual reaching depends on che developm ent o f con tral­
ateral reaching.
Reaching movements chat are executed wichout visual
feedback once initiated, are called visually trigg ered m ove­
m ents. M ovem ents that are modified during execution by
visually perceived error are called visually guided m ove­
m ents. A successful reaching movement to an isolated
o b ject w ithout sight o f che hand requires intormacion about
the distance o f the objecr, which can be provided only by
accom m odation or vergence. A seen hand can be guided to
an o b ject by the use o f binocular disparity and lateral offset
betw een hand and objecc. In this case, absolute estim ates o f
discancc and direccion arc noc required for visual guidance.
There have been several studies on che developm ent o f
reaching in infants, and conclusions have been drawn about
the exten t to which reaching and grasping signify chac che
intanc has depch perception. For inscancc, 5-m onch-old
infancs moved the arm forward and made grasping
movements with the hand when a virtual o b ject was within this skill was more prccisc in 34-w eek-old infants (von
reach but not when it was o u t o f reach (G ord on and Yonas H ofstcn and Fazel-Zandy 1984).
1 9 7 6 ; B ech told t and Hutz 1 979). Infants 4 m onths old It is n o t clear in these studies to what extent perfor­
reached for the nearer o f two objects m ore consistently mance depended on disparity cues to relative depth between
when looking with tw o eves than with one (G ranrud 1986). o b ject and hand as opposed to vcrgcncc and m onocular
The superiority o f binocular reaching was correlated with a cues. N or is it clear to what extent infants judged the abso­
preference for looking at a random -dot stereogram with lute distance o f an o b jcct or the relative distance between
depth rather than at a random -dot surface. o b ject and hand.
In another study, 5 -m onth-old infants reached lor It is to be cxpcctcd that infants will be more likely to
an approaching o b je ct specified only by binocular inform a­ attend to an o b ject w ithin reach than to one beyond reach.
tion whereas 3.5-m on th-old infants did not (Yonas et al. Infants aged 6 to 2 0 weeks fixated on a solid o b jcct for
1978a) (P ortrait Figure 7 .1 1 ). Infants betw een the ages o f longer when it was 3 0 cm distant than when it was 9 0 cm
18 and 3 2 weeks directed ballistic arm movements to the distant (M cK enzie and Day 1972).
virtual position o f an o b ject viewed through prisms that Reaching in adults is discussed in S ection 3 4 .3 .
altered the angle o f vcrgcncc (von H ofstcn 1 9 7 7 ). In other
words, they moved their arms to where the eyes were co n ­
7 .4 .1 b C liff A v oid an ce
verged.
W h en reaching to grasp an o b ject, adults start to close M ost young mammals show an avoidance response when
the hand before touching the o b ject and start to close ear­ confronted with a visual clilf(G ib so n and W alk I9 6 0 ; W alk
lier for smaller o b jects. This skill could depend on an esti­ and G ibson 1 9 6 1 ) (P ortrait Figure 7 .1 2 ). In one study,
mate of the absolute distance ot the o b ject or of the relative 5-week-old kittens selected the shallower o l tw o steps
visually perceived distance betw een hand and o bject. (T im n cy 1981). In another study, 2-m onth -old human
Com pared with adults, infants betw een 5 and 9 m onths of infants discrim inated betw een the shallow and deep sides
age started to close the hand closer to the tim e o f contact. o f a visual cliff, as indicated by the heart rate (C am pos ct al.
Even 13-m onth-old infants did n o t react differently to dif­ 1970). However, both binocular and m onocular cues to
ferent sizes o f o b ject (von H ofstcn and R onnqvist 1988). depth were available in these displays, so one cannot
Infants 4 weeks old showed signs o f adjusting the orienta­ conclude anything about the developm ent of binocular
tion o f the reaching hand to the orientation o f a rod, but stereopsis in humans.

Fi*«rc7.i2. E leanorJ Gibson. B o r n E l e a n o r J a c k in P r e o r i a . I l l i n o i s , in

Figure*. II. Albert Yonas. B o r n in C l e v e l a n d . O h i o , i n 1 9 4 2 . H e o b t a i n e d
а В . Л . in p s y c h o l o g y f r o m c h c U n i v e r s i t y o f M i c h i g a n i n 1 9 6 4 a n d
a P h . D . in p s y c h o l o g y f r o m C o r n e l l U n i v e r s i t y in 1 9 6 8 . H e j o i n e d
th e fa cu lty o f th e In stitu te o f C h ild D e v e lo p m e n t at th e U n iv ersity
o f M i n n e s o t a i n 1 9 6 S , w h e r e h e is n o w p r o f e s s o r a n d d i r e c t o r o f t h e
C e n t r e f o r R e s e a r c h in L e a r n i n g .
1 9 1 0 . Sh e o b ta in e d а В .Л . at S m ith C o lle g e , and a P h .D . a t P rin ce to n
U n i v e r s i t y i n 1 9 3 8 . S h e h e ld a c a d e m i c a p p o i n t m e n t s a t S m i t h C o l l e g e
u n til 1 9 4 9 , w h e n she m o v ed to th e p s y c h o lo g y d e p a r tm e n t a t C o r n e ll
U n i v e r s i t y , w h e r e s h e r e m a i n e d u n t i l s h e r e t i r e d . S h e r e c e iv e d t h e A P A
D i s t i n g u i s h e d S c i e n t i s t A w a r d in 1 9 6 S . t h e G . S t a n l e y H a l l A w a r d in
1 9 7 0 , t h e 1 t o w a r d W a r r e n M e d a l in 1 9 7 7 , a n d t h e N a t i o n a l M e d a l o f
S c i e n c e in 1 9 9 2 . S h e d i e d in 2 0 0 2 .
angles and a second group со a crapezoid inclined ac the
same angles. Boch groups were chen cesced wich a froncal
square and a froncal crapezoid. The resulcs indicated chac the
infancs perceived che real shapes o i chc inclined scimuli—
chat chey had shape constancy.
Infancs seem со be capable oi recognizing a familiar
face when only a few days old (Slaccr and Kirby 1998;
Atkinson 2 0 0 0 , p. 5 3 ). However, che face was froncal, and
so ic is noc know n со whac excenc a face in an unfamiliar
oriencacion can be recognized by very young infancs.
Remarkably, infancs 2 со 3 weeks old were able со m im ic the
facial expressions o f another person (M eltzo ff and M oore
1977).
7 .4 .2 b P e rc e p tio n o f M o tio n -D e fin e d
C o n to u rs
A shape defined by random docs on a background o f
sim ilar docs is complecely camouflaged until che docs defin­
ing chc shape move wich respecc со chc ocher docs. This is
known as shape from m ocion. Kaufm ann-H ayoz ec al.
(1 9 8 6 ) found chac 3-m oncIvold infancs could discriminace
becween cwo m ocion-defined shapes. Also, after habicuat-
ing со a m ocion-defined shape, chey looked longer ac a novel
stationary lum inance-defined shape chan ac one sim ilar со
che habituated shape. To chis excenc, perception o f shape
was cue invariant. However, they showed no transfer when
chey were habicuaccd со a lum inance-defined shape and
cesced wich m otion-defined shapes. Perhaps che novelty
o f mocion overwhelmed any preference for one shape over
che other.
W hen a texturcd opaque surface moves over a station­
ary cexcured surface, elemencs o f che far surface are occluded
on rhe leading edge and emerge on the lagging edge. This is
the d e le tio n -a ccre tio n cu e to che depth order o f che cwo
surfaces (G ibson ec al. 1 9 6 9 ). G ranrud ec al. (1 9 8 4 ) pre-
senccd 5-m onch-old infancs wich acom puccr-gcncraccd dis­
play ot one random-doc surface moving over anocher. The
infants reached со che apparendv nearer surface, which sug-
gcscs chac chey used che accrecion-delecion cue.
An accrecion-delecion display like chac used by Granrud
ec al. concains a second cue со depch order. Ac che border
becween che cwo surfaces che cexcurc o f che nearer surface
has an associaced moving edge, while che cexcure o f the
more discan с surface has no associaced moving edge (Yonas
ec al. 1987a).
Cracon and Yonas (1 9 8 8 ) presenccd 5-m ondvold
infancs wich a display representing a near surface moving
over a more disranc surface. The only cue со depch order
was chac one surface had a moving edge associaced wich its
cexture elemencs. The cexcure elemencs o f boch surfaces
were kepc away from rhe moving edge so chac chere was no
accrecion-delecion (sec Figure 2 7 .1 1 ). The infancs showed
a reaching preference for che nearer surface defined in
chis wav.
ф
7 .4 .2 c P e rce p tio n o f R o ta tin g 3 - D S h ap es
D ynam ic changes in perspective (m otion parallax) p ro ­
duced by rotacing an objccc provide informacion abouc che
3 -D scructure o f the objccc (Seccion 2 8 .5 ). The kinetic
depth effect (K D E ) demonstrates the power o f this in for­
m ation. In one form o f chiseffecc, the silhouette o f a twisted
3 -D wire frame rear-projected o n to a screen appears flat
when the frame is stationary, but its 3 -D structure is per­
ceived when the frame rotates.
There is evidence that human infants are sensitive to
depth created by mocion parallax before becom ing sensicive
со scacic m onocular dcpch cues, such as perspective and
fam iliar size. H abituation tests revealed thac 4-m onch-old
infancs could noc distinguish becween a real cube and a
wedge-shaped objccc angled со projecc che same image as
chc cube. Adulcs could make chis discrim ination. However,
che infancs could distinguish betw een two o b jects thac were
rocacing abouc a vertical axis (O w sley 1983).
Kellman (1 9 8 4 ) habicuaced one group o f 4-m onch-old
infancs со a 2 -D image o f a 3 -D wire fram e rocacing abouc a
horizontal or a vertical axis. A second group o f 4-m onch-
old infancs was habicuaced со scacic views o f che o b ject caken
from che m otion sequence. The firsc group remained habit­
uated when tested with the sam e o b ject rotating about a
new axis bu t becam e dishabituated when presented with a
new rotacing objecc. The second group dishabituated to
both rotating displays. Thus, the addition o f m otion paral­
lax facilitates the perccpcion o f 3 -D form in 4-m onch-old
infancs, as ic does in adulcs (W allach and O ’C onn ell 1953;
Kellm an and Shore 1987). This facilicaeion could be due со
perccpcion o f che 2 -D kinetic feacures o f che rocacing shapes,
such as changing incerseccions, racher than o f cheir 3 -D
shape.
Arcerberry and Yonas (1 9 8 8 ) obcained similar resulcs
using a dynamic random -doc display in which che shapes o f
che cest objcccs (a cube and an indcnced cube) were defined
wholly by relative mocion o f che docs. However, ic is scill
possible that the 4-m onch-old infancs were responding со
differences in chc 2-D flow paccerns racher chan со che 3-D
shapes created by the m ocion. Two lurcher pieces o f evi­
dence suggest thac the infants were indeed responding to
3 -D shape. First, after habituating to a shape defined only
by m otion parallax, 4-m onth-old infants with high stereo
sensitivity remained habituated со che same scacionary
shape defined by disparicy. Infancs wich low stereo sensiciv­
icy did noc remain habicuaced со che shape (Yonas cc al.
1987b ). Second, 8-week-old infancs could discriminace
becween che cwo cubic form s only if chey saw che whole dis­
play racher chan only che region coneaining che greacesc d if­
ference in opcic flow (Arcerberry and Yonas 2 0 0 0 ).
Shaw ec al. (1 9 8 6 ) eliminaced che possibility o f subjects
using 2 -D flow. Infancs were habicuaced to a siihoucccc o f a
rocacing 3 -D objecc in which depth was specified only by a
cransformacion o f linear perspective. W h en cesced wich
years o r Liter. However, n o t all the previous investigators
used the rewards and attentional aids that Fox used.
The results o f these behavioral procedures do not allow
one to distinguish betw een the effects o f the following
developm ental factors.
1. Im provements in the sensitivity o f disparity detection
mechanism s.
2. Improved reliance on changes in vergence. This factor
could be removed by using b rief stimulus presentations.
3. Increasing interocular distance. The interocular distance
o f the neonate is only about tw o-thirds that in the
adult. O th er things being equal, the minimum
discrim inable binocular disparity is proportional to
interocular separation. This factor alone accounts tor a
3 0 % im provem ent o f stereoacuity with age. Also, as the
interocular distance increases, the mapping o f disparity
o n to the perception o f relative depth must be
recalibrated.
7 . 6 . 3 V E P s A N D D E V E L O P M E N T OF
STEREOPSIS
Th e logic for recording visual evoked potentials (V E P s)
from the surface o f the scalp to investigate binocular func­
tions is outlined in Section 13.1.8b. The relationship
betw een V E Ps and stereopsis is discussed in S ection 11.7.
Amigo c t al. (1 9 7 8 ) reported that binocular facilitation
o f the V E P first showed in infants at about the age o f 2
monchs but was still below adult levels at 5 m onths. They
concluded that the V E P could be used as a test o f cortical
binocularity. Pcnnc c t al. (1 9 8 7 ) obtained sim ilar results in
a longitudinal study o f three infants. However, Am igo et al.
tested at only one spatial frequency, w hich was 3 cpd for
adults and betw een 1 and 3 cpd for infants, according to
age. Pcnnc c t al. used a spatial frequency o t 0 .3 6 cpd. This
make it difficult to com pare ages because the spatial fre­
quency that evokes the best response may have been missed
(Section 18.6.3).
S h c a c t al. (1 9 8 7 ) recorded che VF.P in response to tem ­
porally modulated checkerboard patterns with low and
high spatial frequencies and found that m ost infants below
the age o f 10 m onths showed binocular sum m ation o f about
145% com pared with the adult value o f less than 100% .
They did n o t test infants under 2 m onths o f age.
T h e enhanced binocular V E P in intants could be due to
any o f the following factors.
1. It may be the summed response o f tw o m onocular pools
o f neurons (N uzzi and Franchi 1983).
2. Excitatory inputs to binocular cells increase during the
critical period for developm ent o f stereopsis (Leguire
e ta l. 1991).
3. D uring developm ent o f binocularity, inputs from
the two eyes increase their inhibitory interactions.
These inhibitory interactions reduce the level o f
binocular facilitation o f the V EP. M any people
with abnormal binocularity have an unusually
large interocular suppression, and it is argued that
lack o f binocular facilitation o f the VF.P is due to
abnorm al interocular suppression rather than to
loss o f binocular cells.
The first signs o f V E P s specifically related to depth in
dynam ic random -dot stereograms occurred in infants
betw een ages 10 and 19 weeks. This is several weeks after
the first V E P s evoked by a random -dot correlogram or by a
flickering checkerboard (Petrig et al. 1 9 8 1 ; Skart et al.
1993). Birch and Petrig (1 9 9 6 ) used the V E P and preferen­
tial looking to assess the developm ent ot binocular fusion ot
dynamic random dors and the developm ent o f stereopsis in
random -dot stereograms. Both measures revealed an abrupt
onset o f fusion and stereopsis between 3 and 5 m onths fol­
lowed by a rapid developm ent to near adult levels by 6 to 7
m onths.
In a test o f general binocularity but n o t specifically
stereopsis, V E Ps were recorded from the scalps o f infants
betw een the ages o f 4 and 3 6 weeks. They were shown
random -dot patterns alternating at a rate o f 1.9 Hz
betw een being correlated and uncorrelated in the two eyes,
and a control pattern, which alternated betw een two
uncorrelated states. The V E Ps o f m ost infants under 2
m onths o f age showed the same response to the test as to
the control stimulus. By the third m onth, all infants except
one with a strabismus showed a d istin ct tim c-locked
response to the test stimulus bur not to the control stimulus
(Braddick et al. 1980). A similar procedure used in a longi­
tudinal study, revealed thar the median age tor rhe first V E P
evidence o f binocularity was 91 days (Braddick et al.
1983).
There has been some dispute about when binocular
rivalry develops in the infant. Behavioral evidence suggests
that it develops by the age o f abou t 3 m onths (Section
7.6.1a). However, visual evoked potentials from the visual
cortex o f infants betw een the ages o f 5 and 15 m onths
showed no evidence o f rivalry in response to orthogonal
dichoptic gratings (Brow n et al. 1999) (see Section
12.9.2a).
Endo et al. (2 0 0 0 ) recorded trom single cells in V I ot
monkeys during the first 4 weeks o f life. The responses
showed evidence o t interocular suppression when the ani­
mals were shown dichoptic orthogonal gratings. Suppression
was stronger than that in adult monkeys. Endo et al. co n ­
cluded that young monkeys experience binocular rivalry
before the emergence o f stereoptic vision at betw een 4 and
6 weeks.
Visual evoked potentials in amblyopia are discussed in
Section 8.5.2.
 7.6.4 S T E R E O A C U I T Y IN T H E A G E D
Stereoscopic acuicy has been reported со remain constant
betw een the ages o f 8 and 4 6 years (I lo fstcttcr and Bcrtsch
1976). In several studies reviewed by O w sley and Sloane
(1 9 9 0 ) and Brown et al. (1 9 9 3 ) stereoacuity was found to
dcclinc in subjects over 5 0 or 6 0 years o f age. W right and
W orm ald (1 9 9 2 ) found that o f 7 2 8 people over che age o f
6 5 , only 2 7 % had full stereopsis and 29 % had no stereopsis
when tested with the Frisby stereotest.
In their own .study, Brown c t al. used a H ow ard-Dolm an
test to measure stereoacuicy in four groups o f subjects with
mean ages o f 2 4 ,4 5 , 5 6 , and 6 4 years. The mean stcrcoacu-
ity was about 16 arcsec for the first three groups and
declined to 2 7 arcscc for the oldest group o f subjects.
However, there was no significant effecc o f age after the
results o f tw o o f the 41 subjects were ignored.
Loss o f stereoacuity with age could be due со loss o f
optical quality o t the retinal image. Between the ages o f 2 0
and 7 0 people show a decline in the m odulation transfer
function o f che optics o t the eye, determ ined by a laser beam
reflected from the retina (G uirao et al. 1999). Reduced
retinal illum ination does not seem to be the cause o f the
reduction o f stereoacuicy wich age (Yap ec al. 1994).
There could be loss o f contrast sensitivity due to age-rc-
lated changes in che central nervous syscem. A difference in
acuicy betw een the eyes can cause a loss o f stereoacuity at
any age (Lam et al. 1 996). W h en correlations between
visual acuity, concrasc sensitivity, and stereoacuity were
taken into account, only contrast sensitivity differed signifi­
cantly betw een younger and older subjects (G reene and
M adden 19 8 7 ; Schncck c t al. 2 0 0 0 ).
Increased instability o f gaze could be a factor in the loss
o f stereoacuity with age. Fixation disparity increased
with age in the direction o f exophoria, but this was noc
associated with a decrease in stercoacuity (Yekta et al.
1 9 8 9 ). In people over 6 0 years o f age there is an increasing
incidence o f convenience insufficiency associated with cxo-
phoria for near vision (Pickw ell 1 9 8 5 ). The normally
acccptcd near point o f vcrgcncc is 10 cm , but an increase up
to the norm al reading discance o f 25 cm would have no
practical consequences for stereopsis (Pickwell and
H am pshire 1981).
N orm an et al. (2 0 0 8 ) tested subjects between the ages
o f 18 and 83. They found no significant age-related changes
in stereoacuity, even when the stimuli were presented on a
depth pedestal. However, older subjeccs were less able со
d etect the sign o f depth o t a cyclopean shape in a random -
line stereogram when che disparicy was large (51 arcm in).
N orm an c t al. (2 0 0 0 ) investigated the effects o f aging
on the abilicy to discrim inate betw een 3 -D shapes defined
by disparity. O lder observers (m ean age 7 4 ) performed
qualitatively as well as young observers (mean age 2 2 ),
except that older observers perceived less depth in surfaces
containing large disparities and high spatial frequencies.
Norm an c t al. (2 0 0 6 ) confirm ed that older observers
have reduced sensitivity to disparity-defined shape but arc
affected in a sim ilar way by changes in disparity magnitude,
and by noisy stim uli. Young and old observers could see
depth in dynam ic random -dot stereogram s in which frames
changed every 14.3 ms. For all subjects, added noise affected
dynamic stereograms less than nondynam ic stereograms.
In summary, it seems that basic stereoacuity does not
decline with age after effects o f loss o f contrast-sensitivity is
taken in to account. However, older people show som e loss
in discrim inating 3-D shapes defined by disparity and have
difficulty coping with large disparities in random -line ste­
reograms.
Norm an cc al. (2 0 0 0 ) found that older observers could
n o t reliably d etect a 3 -D surface defined by m otion parallax
when texture elem ents survived for only cwo frames. Tli us,
in briefly exposed images, older observers decected dispar­
ity buc noc patterns o f m otion.
The developm ent o f the eye was reviewed in Mann
(1 9 6 4 ) and Robinson (1 9 9 1 ). The evolution o f the visual
system was reviewed in C ronly-D illon and Gregory (1 9 9 1 ).
The developm ent o f the visual system was reviewed in
Purves and Lichtm an ( 1 9 8 5 ), Salapatek and C ohen (1 9 8 7 ),
Lam and Shatz (1 9 9 1 ), Sim ons (1 9 9 3 ), Daw (1 9 9 5 ), V ital-
Durand et al. (1 9 9 6 ), Slater (1 9 9 8 ), and Atkinson (2 0 0 0 ).
For reviews o f the developm ent o f binocular vision see
Aslin and Dum ais ( 1 9 8 0 ), Yonas and Owsley (1 9 8 7 ),
T im n ey ( 1 9 8 8 ), and Held (1 9 9 1 ).
7 .7 D E V E L O P M E N T O F A U D IT O R Y
L O C A L IZ A T IO N
N ew born infants turn their heads coward a racde presented
to one or other side (M uir and Field 1979). However, head
turning со concinuous speech or to a rattling sound was
found to decline during the second m onth before increas­
ing to ics previous level in the fourth m onth (Field et al.
1979, 1 9 8 0 ). This could represent the replacem ent o f an
innate subcortical response in the newborn by a voluntary
cortically mediated response in 3-m onth old infancs.
W ith two clicks about 5 ms apart, subjects hear and
localize only the leading click. This is known as the prece­
dence cffecr (Section 3 5 .3 .1 b ). It has been reported char
neonates do n o t show the precedence effect (C lifton et al.
1981; M uir et al. 1 9 8 9 ). The onset o f the precedence cffecr
corresponded to the upswing in the incidence of head turn­
ing in the fourth m onth. M uir et al. concludcd that the
onset o f the precedence effect is due to the developm ent o f
cortical m echanism s o f auditory localization.
The abilicy со discrim inace a shift in che lateral direction
o f a sound increases wich age. Thus, M orrongicllo ; 1988)
found that 6-m onch-old infancs could only decect shifts
larger than 12°, while 18-m onth-olds could d etect a
shift o f 4°.
 Seven -m onth-old infants, in the dark, often reached со
the source o f a sound that was in the m idlinc or 30° or 60° to
the side. However, chey were more likely to reach when che
source o f chc sound could be seen (Perris and Clifcon 1988).
C lifton cc al. (1 9 9 1 ) sounded a racde in chc dark in various
azimuch positions and ac discances ot 15 cm or 6 0 cm . Six-
monch-old infancs showed some evidence o f reaching in the
correcc location buc only when che racde was w ithin reach­
ing distance. Their accuracy in reaching was n o t affected by
che relative intensities o f che near and far racdes (Litovsky
and C lifton 1992). In ocher words, die infancs did noc use
overall sound intcnsicy со discriminate between a racde
wichin reach and one beyond reach. Adulcs did use sound
incensicy со judge che relative discances o f sound sources.
The infancs muse have used some ocher cue со distance, such
as interaural differences in incensicy or time.
Conductive hearing loss in one car ac an early age produces
audicory defcccs analogous со visual defcccs produced by early
monocular deprivation. The visual defects are known as
amblyopia and arc described in Section 8.4. Audicory defcccs
due со monaural deprivation are known as am blyaudio.
Losses include wcakcningoi chc representation o f the deprived
ear in the audicory corcex and disrupccd binaural inccgrarion.
As wich amblyopia, che effects o f monaural deprivation occur
only when monaural deprivation occurs in a critical period in
early developmenc (Popescu and Pol ley 2010).
The audicory syscem adapcs со recurrenc sound pacccrns.
For example, birds learn со produce specific songs and children
learn chc speech pacccrns ot their native language (Kuhl 2004).
Som e o f these adaptive changes occur in chc auditory brain­
stem (Tzounopoulosand Kraus 2 0 0 9 ), but mosc o f chcm occur
in chc audicory corcex (KeuroghJian and Knudsen 2 0 0 7 ).
 8
E F F E C T S OF VISUAL DEPRIVATION

8.1 Effects of dark rearing 391 8.3 The critical period •1 H

8.1.1 Physiological cffccts o f dark rearing 3 9 1 8.3.1 Critical period in subprimates 4 1 5
8.1.2 Behavioral effeccs of dark rearing $ 9 $ 8.3.2 Critical period in monkeys 4 1 8
8.1.3 Recovery o f sight in humans 3 9 4 8.3.3 Critical period in humans 4 1 8
8.1.4 Effects of blindness 395 8.4 Amblyopia 4 1 9
8.2 Monocular deprivation 3 9 6 8.4.1 Types of amblyopia 4 1 9
8.2.1 Retinal cffccts of monocular deprivation 3 9 6 8.4.2 Loss of contrast sensitivity and acuity 4 2 1
8.2.2 Subcortical cffccts of monocular deprivation 397 8.4.3 Spatial distortions 4 2 4
8.2.3 Cortical effects of monocular deprivation in 8.4.4 Temporal resolution and motion detection in
subprimates 4 0 0 amblyopia 4 2 7
8.2.4 Cortical effects of monocular deprivation in 8.4.5 Motor symptoms of amblyopia 4 2 9
primates 4 0 5 8.4.6 Development and treatment o f amblyopia 4 3 0
8.2.5 Effects o f binocular dissociation 406 8.5 Amblyopia and stereopsis 4 3 3
8.2.6 Effects of monocular enucleation 407 8 .5 .1 Amblyopia and stereoacuity 1 3 3
8.2.7 Mechanisms of cortical plasticity 408 8 .5 2 Amblyopia and binocular suppression 4 3 3

8 .1 E F F E C T S O F D A R K R E A R IN G C ells in the accessory optic system o f dark-reared cats

8 .1 .1 P H Y S IO L O G IC A L E F F E C T S O F D A R K
R E A R IN G
8 .1 .1 a S u b c o r tic a l E ffe c ts o f D a rk R e a rin g
Earlier studies reported that rats and monkeys reared in
total darkness showed no obvious changes in the number,
size, or staining characteristics o f cells in either the retina or
L G N (C h ow 1 9 7 3 ; H endrickson and B o o th e 1 9 7 6 ). Also,
it was reported that che sensitivity o f L G N cells in the cat to
spatial frequency or orientation was not affected by dark
rearing (M ow er c t al. 1981 a; Z hou ct al. 1995).
M ore recent studies have revealed some retinal effects
o f dark rearing. Dark rearing blocked the segregation o f
O N and O F F ganglion in the developing mouse retina
(T ia n and C openhagen 2 0 0 3 ). G anglion cells o f dark-
reared rats were less responsive and had smaller receptive
fields w ith disturbed O N and O F F regions (D i M arco
et al. 2 0 0 9 ).
In normally reared rats, the level o f brain-derived neu-
rotrophic factor (B D N F ) in ganglion cells increased during
the first postnatal m onth. In dark reared rats, the level o f
B D N F was reduced (Seki c t al. 2 0 0 3 ). Thus, visual experi­
ence increases the level o f B D N F in ganglion cells.
lose their inputs from the ipsilateral eye, which arise from
binocular cells in the ipsilateral visual cortcx (Grasse and
Cynader 1986). Th e accessory o p tic system is discussed in
Section 2 2 .6 .1 .
There is som e evidence that eyelid suturing o r corneal
opacification leads to elongation o fth e eye and axial myopia
(see Section 6.3.1).
M any cclls in the superior colliculus respond to visual,
auditory, and somatosensory stimuli. C ells in the superior
colliculus o f cats reared in the dark from birth remained
multisensory. However, the cells had enlarged reccptive
fields and did n o t show the normal response enhancem ent
when stim ulated simultaneously by stim uli in different
m odalities (W allace c t al. 2 0 0 4 ).
8 .1 .1 b L o ss o t G e n e ra l C o r tic a l R c sp o n siv ity
Dark rearing disrupts the norm al developm ent o fth e visual
cortcx. C ats reared in the dark for the first 6 m onths showed
a 50% reduction in the num ber o f synapses in area 17 that
received inputs from the L G N (Turlcjski and Kossut 1985).
Even though som e cortical cells responded to stim ulation
in either eye, the cars were perm anently stereoblind.
In binocularly deprived kittens, many cells in the
visual cortex arc unresponsive, weakly responsive, or
respond erratically. The cells apparently do not die o r lose
their synaptic connections, since they recover their rcspon-
sivity when an excitatory am ino acid is applied locally
(R am oa et al. 1 9 8 7 ). They also becom e more responsive
when cortical inhibition is reduced by application o f bicuc-
ulline (T sum oto and Freeman 1 9 8 7 ). C o rtical area 17 is
involved in the visual perform ance o f dark-reared cats, since
contrast sensitivity is degraded by ablation o f this area in
such cats (Lehm kuhle c t al. 1984).
In dark-reared rats, pyramidal cortical cclls that receive
inputs from the L G N have a lower density o t dendritic
spines (W allace and Bear 2 0 0 4 ). Also, dark-reared rats
develop fewer G A B A crg ic inhibitory inputs to pyramidal
cells in the visual cortex than do normally4 reared rats
(M orales ct al. 2 0 0 2 ). The role o f inhibition in cortical plas­
ticity is discussed further in Scction 8.2.7d .
The expression o f neurotrophins in the visual cortex
increases just after young rats open their eyes. There are tour
main neurotrophins: nerve growth factor (N G F ), brain-
derived ncurotrophic factor (B D N F ), and neurotrophins
N T -3 and N T -4/ 5 (S ectio n 6 .4 .3 d ). The neurotrophin
N G F is required tor che m aturation o f N M D A synapses
while B D N F is required for the m aturation o f the
G A BA ergic system (C o tru fo cc al. 2 0 0 3 ). These neurotro­
phins increase the num ber o f receptors on the postsynaptic
mem branes o f N M D A and G A B A crgic synapses, which
increases experience-dependent synaptic plasticity.
Dark-rearing or suppression o f ganglion-cell activity by
intraocular injection o f tetrodotoxin decreases the expres­
sion o f B D N F and prevents che m aturation o f cortical neu­
rons. The neurotrophin returns ro norm al levels after vision
is restored. A dm inistration ot B D N F counteracts the effects
o f dark rearing in m ice (G ianfranceschi c t al. 2 0 0 3 ). The
expression ot N G F and N T -3 is n o t affected by lack o f
visual inputs (C astrcn et al. 19 9 2 ; Schoups cc al. 1 9 9 5 ). The
role o f neurotrophins in cortical plasticity is discussed fur­
ther in Section 8.2.7f.
The effects o f visual stim ulation on N M D A receptors
depend on both the strength and temporal frequency o f
light stim ulation. M oderate stim ulation at 1 H z produces
long-term depression (L T D ), while stronger stimulation
produces long-term potentiation (L T P ). Stim ulation ac fre­
quencies below 1 Hz produces no L T D In dark-reared cacs,
L T D is less chan norm al in response Co stim ulation ас 1 Hz
buc is greater than norm al wich lower frequencies o f stim u­
lation. Blocking N M D A receptors reversed these effects
(P h ilp o t cc al. 2 0 0 3 ). These results suggest thac dark rearing
increases the num ber ot N M D A receptors, which produces
a shift in the frequency-response funccion.
In norm al animals, lateral connections develop between
cortical cells with similar orientation preference (Sections
5.5.6a and 6 .4 .6 b ). C ats binocularly deprived for ac least rhe
firsc 4 weeks o f life develop abnormal clusters o f horizontal
con n ection s (Callaway and Katz 1 9 9 1 ). Bilaterally enucle­
ated fetal monkeys show a progressive reduction in the size
o f V I accom panied by an increase in the size o f extrascriace
corcex (D ehay ec al. 1996). Also, monkeys reared with both
eyelids sutured have tar fewer neurons in chc corpus callo­
sum chac term inate in areas 17 and 18, and their distribu­
tion is severely restricced (Innocenci and Frosc 1980).
Dark-reared m onkeys and monkeys reared with the eye­
lids sutured show a reduction o f visually responsive cclls in
the posterior parietal cortex (area 7 ). This is accom panied
by an increase in the num ber o f cells responsive to som a­
tosensory inputs and o f cells showing only sponcaneous
accivicy (Hvviirincn ec al. 1 9 8 1 ; Carlson cc al. 1987).
Subsequenc visual experience failed со rectify these dcficics
fully.
8 .1 .1 c L o ss o f R e sp o n se S p e c ific ity in ch c C o r tc x
D uring the first 3 or 4 weeks after birth, normal and dark-
reared kittens have a sim ilar num ber o f cclls in the visual
cortex that arc tuned to orientation and movement. Also,
both cypes o f kiccen possess binocular cells, o f which some
are cuncd со disparity. After 4 weeks, cclls tuned to orienta­
tion, m otion, and disparity increase in num ber and stim u­
lus specificity in norm al animals. By contrast, in dark-reared
animals, the number o f tuned cells decreases and chc num ber
o f cells with nonspecific tuning increases (Pettigrew et al.
1 9 6 8 ; Pettigrew 1974; Buisserec and Imbcrc 1 9 7 6 ; Fregnac
and Imbcrc 1978; Braascad and Hcggelund 1 9 8 5 ; Czepica
ec al. 1994).
Dark-reared cats have f ir fewer com plex cells in corcical
area 18 chan do normal animals (Blakem orc and Price
1987b ). C ells that rccain cheir sensitivity to orientation
tend to be m onocular and cuncd со vertical or horizontal.
They resemble oriencacion-cuned cells o f che neonate cat
(Buisserec ec al. 1982).
Blockage o f all neuronal activity in the visual co rtcx by
infusion o f cecrodocoxin in intanc ferrets suppressed devel­
opm ent o f orientation seleccivicy (C hapm an and Scryker
1 9 9 3 ). Presumably, rccention o f some selective cells in b in ­
ocularly deprived animals is due to effects o f spontaneous
visual inputs.
C ells in the visual cortcx o f kittens that were dark-reared
until 5 weeks ot age rapidly regained some stimulus speci­
ficity when sighc was rcscored (Im bcrc and Buisserec 1975).
Even alter 12 m onths o f dark rearing, cells recovered some
stim ulus specificity for oriencacion, alchough noc for direc­
tion o f mocion (Cynadcr et al. 1 9 7 6 ) (P o rtrait Figure 8 .1 ).
Lack o f visual experience beginning after the age o f 12
weeks did not reduce the orientation specificity o f cells in
the ca ts visual cortex (Buisscret et al. 1982).
Thus, cortical cells o f cacs develop som e scimulus speci-
ficitvi in the first few weeks o f life in the absence o f visual
experience. Ic seems chac sponcaneous retinal activity before
the eves open is involved in this early developm ent (M iller
and Erw in 2 0 0 1 ). However, visual experience is required
during the postnatal critical period for che m aintenance and

Figure я. i. M ax Cymulcr. B orn in 1 9 4 7 - \ Ic o b tain ed a B .S c . from
M c G ill U n iv ersity in 1 9 6 7 and л P h .D . trom М П * in 1 9 7 2 . A fter
p o std o cto ral tra in in g a t th e M ax Planck Institu te in G erm any he held
acad em ic p osition s in the d epartm en ts o f psychology and physiology
a t D alhou sie U niversity in H alifax. C an ad a. In 1 9 S 8 he becam e head
o f the O p h th a lm o lo g y Research G ro u p in th e U n iv ersity o f B ritish
C o lu m b ia . H e is a fellow o f the Royal S o c ie ty o f C an ad a and recip ien t
o f t h e K illam Prize and th e G o ld M ed a l in H e a lth Scien ces from the
Scien ce C o u n c il o t B ritish C o lu m b ia .
further developm ent o f stimulus specificity, especially to
high spatial frequencies and fine binocular disparity.
C o rtical cells o f dark-reared ferrets had orientation
tuning but it did not reach normal levels. O rientation
tuning was rudim entary in ferrets with both eyes occluded
(W h ite et al. 2 0 0 1 ). In both cases, connections between
cells tuned to the same orientation were less extensive than
norm al. Binocular occlusion in the cat reduced orientation
and direction selectivity in areas 17 and 18. A lso, receptive
fields o f cortical cclls had no sharp inhibitory side bands
and were unusually large (Singer and Tretter 1976).
8 . 1 . Id E ffe c ts o n O c u la r D o m in a n c e
C o lu m n s
Swindale (1 9 8 1 ) found a perm anent loss o f anatom ically
defined ocular dom inance colum ns in area 17 o f 30-w cck-
old dark-reared cats or cats reared with the lids o f both eyes
sutured from birth. C olum ns developed in cats that were
allowed binocular vision after an initial 6 weeks o f darkness.
There was much less recovery after betw een 8 and 25 weeks
•
and no recovery after 25 weeks o f darkness (Swindale 1988).
O cu lar dom inance colum ns did not recover in cats dark-
reared for betw een 9 and 16 weeks (M ow er et al. 1985).
However, restoration o f binocular vision produced some
recovery o f orientation selectivity and binocularity. O cu lar
dom inance colum ns remained normal in cats kept in the
dark after 6 weeks o f norm al vision. Visual experience o f
betw een 4 8 and 128 hours during an 8-week postnatal
period o f darkness was sufficient for normal development
o f colum ns in area 17. D ark rearing did not prevent devel­
opm ent ot ocular dom inance colum ns in area 18 ol cats
(Swindale and Cynader 1986).
O cu lar dom inance colum ns begin to develop before
birth in monkeys but not in cats (Section 6 .7 ). I.cVay c t al.
(1 9 8 0 ) found ocular dom inance colum ns in 7 -week-old
dark-reared monkeys.s
8 .1 .2 B E H A V IO R A L E F F E C T S O F
D A R K R E A R IN G
Dark-reared cats have profound deficits in visually guided
behavior such as obstacle avoidance, paw placement,
directed jum ping, and visually elicited blinking. However, a
large moving display elicited optokinetic nystagmus (V ital-
Durand c t al. 1 9 7 4 ). W hen cats were returned to the light
after 4 m onths ot darkness, these visually m ediated behav­
iors recovered after 7 weeks. After 7 m onths o f darkness,
these functions took 10 weeks to recover fully (Van Hof-
van D uin 1976a). A lso,cats reared in darkness for 4 m onths
were initially unable to respond to a grating o t any spatial
frequency. However, th eir grating acuity returned to normal
(6 .9 cpd) after about 4 m onths in the light. After 6 m onths
o f darkness, acuity did not fully recover (T im n cy ct al.
19 7 8 ; Sm ith D C e ta l. 1980).
C ats reared with both eyelids sutured showed more
severe disruption o f behavior and less evidence o f recovery
after restoration o t sight than did cats raised in darkness
(M ow er et al. 1982). Lid suturing allows diffuse light to
enter the eyes and this must be responsible tor the greater
severity and permanence o f deficits. We will see that dark-
reared cats have a prolonged period o f cortical plasticity
compared w ith norm al cats. Visual stim ulation must accel­
erate term ination ot the critical period in young cats, even
when the stimulus is diffuse light.
M onkeys reared in darkness during the first 3 or 6
m onths showed optokinetic nystagmus and pupil constric­
tion. A prefercntial-looking procedure revealed a grating
acuity ofbetw een 2.5 and 7.5 cpd,com pared with a normal
value o f 15 cpd. However, initially, they did not show avoid­
ance or startle responses to approaching objects and were
not able to reach tor an o b ject. These responses took about
a week to develop ( Regal et al. 1976).
M onkevs raised for 7 weeks with both evelids sutured
had reduced contrast sensitivity in both eyes. However, the
deficit was much less than that produced in the occluded
eye o t a m onkey reared with only one eye sutured.
Furtherm ore, sensitivity to visual flicker and spectral sensi­
tivity were not m uch affected by bilateral eye sutures. N one
o f the binocularly deprived monkeys had binocular vision
as assessed by binocular summation o t grating detection or
by their ability to d etect depth in a random -dot stereogram
(H arw erth et al. 1 991).
 M onkeys that had been dark reared for the first year o f
life showed rapid recovery in the ability to detect and visu­
ally track a moving light sp ot in dark surroundings.
However, their tracking m ovem ents were jerky. Even after
one year in the light, they continued to bump into objects
and their eye-hand coord ination remained poor when
they readied tor objects. They did not learn to respond to
threatening gestures or to a threatening face (C arlson 1990).
Thus, binocular suturing produces more perm anent
damage to higher centers o f visual processing than to early
levels o f processing.
8 .1 .3 R E C O V E R Y O F S I G H T IN H U M A N S
In 169 0 Joh n Locke w rote his Essay Concering Human
Understanding. After reading the essay, the Irish lawyer and
scientist M olvneux w rote to Locke to ask how a man with
congenital blindness who has recovered his sight would sec
the world. W ould he be able to distinguish a cube from a
sphere w ithout touching them ? This has becom e known as
M olyneu x s q u estio n . The question interested him because
his wife was blind. He suggested that a person w ith restored
sight would not be able to do so. M olyneux repeated his
question in 169 3 and Lockc finally responded in the second
edition ol his Essay Concerning Human Understanding
(1 6 9 4 ). As an em piricist philosopher, L ockc agreed with
M olyneux that we learn to perceive visual space through
association with touch and movement.
In 17 2 8 , W illiam Chesselden, surgeon to Q ueen
C aroline and ophthalm ologist at St. Thom as’s hospital in
London, reported thac a young man on whom he had per­
form ed a cataract operation could not name shapes until
after a long period o f learning. Ju st after his sight was
restored, the patient reported that objects seemed to touch
his eyes. I.atta (1 9 0 4 ) described a man who had his sight
restored at the age o f 3 0 after being alm ost blind trom birth.
H e quickly learned ro distinguish colors, simple shapes, and
the letters o f the alphabet. But he remained contused when
confronted with com plex natural scenes or pictures. D istant
objects seemed near and he had difficulty interpreting fig­
ures representing three dim ensions and showed no evidence
o f stereoscopic vision.
Von Senden ( I 9 6 0 ) reviewed 6 6 cases betw een 1920
and 1931 in which bilateral cataracts were removed. Useful
sight was restored in only a few cases. Gregory and Wallace
(1 9 6 3 ) described recovery o f visual function in a man who
had bilateral cataracts removed when he was 52. H is cata­
racts had developed at the age o f 10 m onths, although he
may have had some residual vision. Basic visual functions
were not tested. He soon learned to recognize capital letters
that he had learned to recognize by touch. However, it took
him many m onths to recognize objects, such as small-case
letters that he could not recognize by touch. H e did not
learn to read by sight although he could tell rhe time.
H e had no impressions ot depth when shown perspective
drawings. This patient was periodically depressed but seems
to have been one o f the few who learned to make som e use
o f their restored sight.
Ackroyd et al. (1 9 7 4 ) described a woman who had
bilateral cataracts removed when she was 2 7 vears old.
She had been able to see until she was 3 years old. Six
m onths after the operation her elcctroretinogram and
visual-evoked cortical potentials were w ithin normal lim its
as were her lum inance threshold and dark adaptation. She
could d etect and locate large o bjects, especially if they
moved, but could not recognize simple visual patterns. She
regarded the operation as a failure and reverted to the life o f
a blind person.
Apkarian (1 9 8 3 ) described a 12-ycar-old girl who
had her sight restored after being effectively blind since the
age o f 3 m onths. After several m onths o f training
she showed some developm ent o f visual acuity, could recog­
nize simple objects and point to objects. However, she
reverted to the behavior o f a blind person when at home.
A 34-year-old man had sight restored after 3 0 years o f
blindness. Although he regained some visual functions
he reverted to the behavior o f a blind man (C arlson ct al.
1986).
Fine et al. (2 0 0 2 ) measured basic visual functions in a
man who had cataracts removed at age 4 3 , although the
cataracts had not developed until after he had learned to
read and he had 20/ 80 Snellen acuity before the cataracts
were removed. C o n trast sensitivity showed no evidence o f
im provem ent 2 0 m onths after the operation. Letter acuity
improved slightly but only during the first few postopera­
tive days. M easurements o f the Stiles-C raw ford effect indi­
cated that the photoreceptors becam e aligned w ith the
center o f the pupil over a period o f 10 days.
M ioch c and Perenin (1 9 8 6 ) tested 13 adults who had
had bilateral cataracts removed betw een 4 m onths and 7
years o f age. Their contrast sensitivity, particularly at high
spatial frequencies, was markedly impaired for both station­
ary and drifting gratings in both the central and peripheral
retina. Their temporal m odulation sensitivity was also
impaired over the whole tem poral-frequency range. Patients
with neonatal cataracts were more severely affected than
were those with cataracts that developed later.
C hildren with congenital cataract in one (Pratt-
Joh n son and Tillson 1 9 8 9 ) or both (T vtla 1 9 9 3 ) eyes failed
standard clinical tests o f stereopsis after removal o f the
cataract, even when it was removed after only a few
m onths. However, some o f the children with binocular
cataracts showed evidence o f coarse stereopsis when allow­
ance was made for their amblyopia by testing with large
stim uli, and when allowance was made for strabismus by
optically aligning the images (Tytla et al. 1 9 9 3 ). A 1-day-
old baby had a m onocular cataract removed and was given
occlusion therapy. Right years later the child had good
acuity in borh eyes and stereoacuity o f 5 0 arcsec (G regg and
Parks 1992).
 8 .1 .4 E F F E C T S O F B L IN D N E S S
8 .1 .4 b C ro s s -M o d a l P la s tic ity in th e B lin d

8 . 1 .4 a A c tiv ity in th e V isu a l C o r t e x o f th e There is som e evidence that early-blind people have
E a rly B lin d heightened ability to d etect the directions o f sounds, espe­
cially sounds originating from a peripheral location
Postm ortem exam ination o f the brain o f a person who had
(Rauschecker 1995; I.essard et al. 1 9 9 8 ; Rdder et al. 1999).
had the right occipital lobe removed 4 0 years before death
Blind people certainly have heightened ability to d etect tac­
revealed retrograde degeneration o f axons serving that
tile Braille patterns. The question addressed in this section
occipital lobe in the right optic tract and in both optic
is w hether the response o f the visual cortex to nonvisual
nerves (B eatty et al. 1 9 8 2 ). M agnetic resonance imaging o f
stim uli increases in people who have been blind Irom an
11 early blind subjects revealed atrophy o t the optic chiasm
early age.
and optic radiation and loss o f gray m atter in cortical
M ost cells in the prim ary visual co rtex o f sighted people
area V I . However, there was an increase in the volume o f
respond to only visual stim uli. However, there are inputs to
w hite m atter tracts associated with the somatosensory and
the peripheral visual cortex from the auditory cortex and
m otor cortices (N oppeney e t al. 2 0 0 5 ).
from the polyscnsory area o f the temporal lobe (Falchier
G lucose m etabolism measured by positron emission
e ta l. 2 0 0 2 ).
tomography ( P E T ) was higher in the visual cortex o f early
Asanuma and Stanfield (1 9 9 0 ) found substantial inner­
blind humans than in blindfolded persons with normal
vation o f the L G N by axons o fth e somatosensory system in
sight or with blindness o f recent onset (Veraart et al. 1990).
congenitally blind m ice and in m ice enucleated at birth,
Also, spontaneous activity in the visual cortcx o f monkeys
especially when cortical lesions accom panied enucleation.
and cats deprived ol vision was sim ilar to that in nonde­
Rakic et al. (1 9 9 1 ) surgically reduced the num ber o f
prived anim als (Singer and Tretter 1976). The fM R I
inputs to V I in monkeys at em bryonic day 8 1 . W h en the
revealed heightened activity in V I and the posterior pari­
monkeys were 3 years old, exam ination revealed an area
etal cortex o f early-blind humans as they performed a
adjacent to V I w ith unusual cytoarchitectonic features.
taetile-discrim ination task (Sadato e t al. 2 0 0 2 ).
They/ called this “area X .”
A ctivity in the early-deprived visual cortex could, in
Kahn and Krubitzer (2 0 0 2 ) enucleated opossums on
theory, arise Irom any o l the follow ing causes:
postnatal day 4 , well before ganglion-cell axons had entered
the cortex. In the mature animals, area 17 was reduced in
1. Retarded development o f inhibitory synapses Toward the size and the adjacent area had novel arch itectonic features,
end o fth e critical period for experience-dependent like area X in monkeys. M uch o f the visual cortex that
neural plasticity there is a large increase in inhibitory wouId norm ally have responded to visual stimuli responded
G A B A crgic inputs onto pyramidal cells. The increase only to auditory stimuli or only to tactile stim uli applied
does not occur in dark-re ared rats (M orales et al. 2 0 0 2 ) mainly to the head. Som e cells responded to both types o f
(Section 6 .6 .3 ). stim ulation. Thus, inputs from sense organs serving other
m odalities invade the visual co rtex when visual inputs are
2. Retention o f excess dendrites In the norm al immature
removed in the em bryo.
cortex there is an exuberant grow th o f dendrites
Early blind subjects show some m odification o f evoked
followed by pruning as the co rtcx matures (Section
potentials from the occipital co rtcx when they read Braille
6 .4 .4 ). Ifd en d ritic pru ningd id n o t occur in blind
(U h l et al. 1991). There has been som e dispute about
animals it could account for the high activity in the
whether this occurs in the early blind, in the late blind, or in
visual cortex. However, it seems that enucleated mice
both. Using positron em ission tom ography ( P E T ) , Sadato
develop fewer dendritic spines than normal mice.
et al. (1 9 9 6 ) found heightened bilateral activity in V I and
Heumann and Rabinow icz (1 9 8 2 ) removed both eyes
in the extrastriate cortex o f early blind subjects as they read
o t mice at birth. This did n o t produce any significant
Braille or performed a tactile discrim ination task. Simply
loss o f neurons or glial cells in areas 17 and 18
touching a stimulus had no effect. Sighted subjects showed
com pared with norm al m ice. However, between 10
a reduction o f activity in the visual cortex when perform ing
and 180 days after enucleation there was a progressive
a tactile discrim ination task.
loss o f dendritic spines on pyramid cells in cortical
C o h en et al. (1 9 9 9 ), also, found heightened P E T activ­
layer 5 and then in layer 3. This caused shrinkage
ity in the occipital cortex when early blind subjects read
in the volume o fth e cortex o fb etw een 8 and
Braille. Subjects who becam e blind after the age o f 14 years
13% and an increase in the densitys o f cortical cells.
showed no such activation. Also, transcranial magnetic
3. Invasion o f inputsfrom nonvisual areas The L G N and stim ulation o fth e visual cortex disrupted Braille reading in
visual cortex o f the early blind arc invaded by inputs the early blind but n o t in the late blind.
from other sensory modalities. The evidence for this Biichel et al. (1 9 9 8 ) recorded brain activity with P E T in
will now be reviewed. congenitally blind human subjects and in subjects who had
been blind since puberty as they read Braille or listened to
spoken words. In both groups o f subjects, Braille reading,
but not the auditory task, elevated brain activity in extras-
triate area 19, the occipitotem poral ju n ctio n , and the poste­
rior parietal cortex. O n ly the late-blind group showed
elevated activity in the primary visual cortex. The fact that
the elevation o f brain activity was task-specific suggests that
ir was nor due to general arousal. Burton (2 0 0 3 ) reported
fM R I activity in several visual areas o f both early and late
blind persons reading Braille. Som atosensory innervation
o f the visual cortex in the blind could also involve feedback
from higher centers.
A ctivation ot the visual cortex bv
* nonvisual stimuli does
nor prove that the visual cortex perform s nonvisual func­
tions. C ohen et al. (1 9 9 7 ) approached this question by
applying transcranial m agnetic stim ulation to the visual
cortex o f sighted and blind subjects. This induced errors in
Braille reading in blind subjects but did not affect tactile
tasks in sighted subjects. M agnetic stim ulation o f the visual
cortex o f sighted subjects disrupts visual o b ject recognition
(Epstein et al. 1996).
A neurom agnetom eter (Section 5 .4 .3 d ) applied to early
blind subjects revealed activity in the visual cortex as the
subjects counted changes in the pitch o f a sound (Kujala
ct al. 1 9 9 5 ). Passive listening to the sound had no effect.
Heightened P E T activity was found in cxtrastriate areas o f
the occipital cortex o f congenitally blind subjects as they
performed an auditory discrim ination task (W eeks ct al.
2000).
8 .2 M O N O C U L A R D E P R IV A T IO N
M onocular deprivation may be induced in animals by any
o f the following m ethods:
1. M onocular enucleation, or removal o t one eve.
*
2. O ccluding the cornea or suturing the eyelids o t one eye.
W ith lid suturing the retina is illum inated by diffuse
light.
3. C reation o f an artificial strabismus by surgically
deviating an eye. T en ccto m y involves simple section ot
the tendon o f a muscle at its point o f insertion on the
globe. M yectom y is a m ore severe procedure involving
removal o f the whole o f one or more extraocular
muscles.
4 . O p tical deviation o f the visual input to one or both eyes
by prisms.
5. O p tical induction o f aniseikonia by applying a
m agnifying lens in front o f one eye or by paralyzing
the ciliary musclcs o f one eye w ith atropine.
6. Im m obilization o f an eye by paralysis o f the extraocular
muscles.
These experimental procedures are designed to m im ic
naturally occurring am blyopia in humans. Am blyopia is
caused by disorders such as strabismus, unequal refractive
power in the two eyes (anisom etropia), aphakia, and
cataracts.
W h en cats or primates are subjected to a disruption ot
norm al visual experience in one eye in early life, binocular
cells o f the visual cortex develop abnorm al patterns o f
ocular dom inance, and stereopsis is deficient o r lost.
Profound changes occur only when m onocular deprivation
occurs during a critical period early in life. However, even a
b rief period o f m onocular deprivation in adult monkeys
produces a temporary reduction in excitatory and in h ib i­
tory ncurotransm itters in rhe visual cortex associated with
the deprived eye (see H endry and Jon es 1986).
8 .2 .1 R E T IN A L E F F E C T S OF
M O N O C U L A R D E P R 1VA T I О N
Retinal X and Y ganglion cells have been reported to be ana­
tom ically and functionally normal in cats reared with mon-
ocular occlusion (Sherm an and Stone 1973; Kratz et al.
1 9 7 9 ; C lcland et al. 1 9 8 0 ) or with convergent or divergent
strabismus induced by tencctom y in one eye (Clcland c t al.
1 9 8 2 ; G illard-C rew ther and C rew ther 1988). C ats with 4
years o f postnatal m onocular deprivation had a normal elec-
troretinogram as indicated by flash- or pattern-evoked elec­
trical responses from the retina (Baro c t al. 1990).
M ore recently, it has been reported that rhe level o f
brain-derived ncurotrophic factor (B D N F ) in ganglion
cells is reduced in a light-deprived eye o f infant rats (Seki
et al. 2 0 0 3 ). This neurotrophin is transported trom the
retina to the cortex through ganglion cells and L G N relay
cells. M onocular deprivation therefore introduces an asym­
metrical concentration o f B D N F in cortical ocular d om i­
nance columns. The shift in ocular dom inance that normally
occurs after m onocular deprivation was reduced when the
balance o f B D N F in the retinas ot m onocularly deprived
rats was restored by adding B D N F to the deprived eye or
removing it from the norm al eye (M andolesi et al. 2 0 0 5 )
(Section 8 .2 .7 f).
R etinal effects have been reported in cats reared with
bilateral convergent strabismus induced by m yectom y o f
both lateral recti. The receptive fields o f X -ty p e ganglion
cclls were found to be unusually large (C h in o et al. 1980).
There was also loss o f contrast sensitivity in X ganglion cells
serving the central retina o f cars reared with convergent or
divergent strabismus induced by myectomy o f the lateral
rectus and oblique musclcs o t one eye ( Ike da and W right
1 9 7 6 ; Ikeda and Tremain 1979; C h in o et al. 1980). Thus,
defects at the level ot the retina o r L G N occur when muscle
tissue is removed so that reinsertion o f the muscle is not
possible.
In the monkey, m onocular occlusion for 2 4 m onths
after birth led to some decrease in the size and density o f

G unter K onstantin von N oorden. B orn in Fran kfu rt am M ain in
1 9 2 8 , H e o b ta in ed an M .D . from l.W . G o e th e U niversity. Fran kfu rt
am M ain , in 1 9 5 4 . H e was a resid ent and th en assistant professor o f
o p h th alm o lo g y a t th e State U niversity o f Iowa from 1 9 5 7 to 1963*
From 1 9 6 3 to 1 9 7 2 he was associate to lu ll professor at th e W ilm cr
Institu te o f Jo h n s H o p k in s H osp ital an d the U n iv ersity o f B altim o re,
M aryland . From 1 9 7 3 to 1 9 9 5 he was professor and d ire cto r o f t h e
O cu la r M o tility Service at Baylor C o lleg e o f M ed icin e, H o u sto n . H e is
now clin ica l professor o f o p h th alm o lo g y a t th e U n iv ersity o f South ern
Flo rid a, Tam pa- H e was president o f the A m erican A ssociation
o f P ediatric O p h th a lm o lo g y , the In tern atio n al Strab i sinological
A sso ciatio n , and the A m erican A ssociation o t Research in V isio n and
O p h th a lm o lo g y . H e was a co recip ie n t o f the H e cto cn G o ld M ed al o f
th e A m erican M ed ical A sso ciatio n , the Fran ccsch ctti Prize from the
G erm an O p h th a lm o lo g ica l So ciety , the P ro cto r Award from A R V O ,
the Bow m an M ed al from the O p h th a lm o lo g ica l S o c ie ty o f t h e U K , the
A Icon Research Award, th e Ja ck so n L ectu re Award from th e A m erican
A cadem y o f O p h th a lm o lo g y , and the A . von H u m b o ld t R esearch Prize,
retinal ganglion cells, whereas deprivation tor 12 m onths
had no ctfccc (N oordcn c t al. 1 9 7 7 ) (P o rtrait Figure 8 .2 ).
M onocular occlusion ot three adult human subjects tor
one week produced a flattening o f the Stiles-Craw ford
function, which m anifested itself as an increased sensitivity
to light entering the eye through the periphery o f the pupil
and a decrease in resolution o f low -intensity gratings (Birch
D G c t al. 1980). This was probably due to a changc in the
alignm ent o f cones with respect to the pupil.
S .2 .2 S U B C O R T I C A L E F F E C T S O F
M О N О С U L A R D Е Р R I VA T I О N
8 .2 .2 a E ffects o f M o n o c u la r E nu cleation
on the L G N
The laminae in the L G N in to which inputs from the
tw o eyes segregate are present at birth (Section 6 .3 .5 ).
Their developm ent in the prenatal and early postnatal
periods depends on m olecular markers and com petitive
interactions betw een retinogeniculate projections Irom the
tw o eyes.
Effects o f early postnatal m onocular enucleation are evi­
dent in the lateral geniculate nuclcus, although not in such
a severe form as in the visual cortex. Postnatal m onocular
enucleation, at least in the cat, leads to cell death in the
L G N (Kali! 1980).
Rakic (1 9 8 1 ) removed one eye trom m onkey fetuses in
the second m onth o f gestation. O n e year after birth the
L G N lacked the norm al lam inar structure. Neurons in lam ­
inae 1, 4 , and 6, w hich would have been innervated by rhe
missing contralateral eye, received inputs trom the rem ain­
ing ipsilateral eye. Also, the visual cortex lacked ocular
dom inance columns.
W h ite (1 9 8 9 ) removed one eye from em bryonic cats at
various tim es after em bryonic day 4 4 . The area in the LG N
innervated by the remaining eye was tw ice that innervated
by a norm al eye, and the ventral m agnocellular layer was
absent. Also, there was an increase in the num ber o f X cells
and a decrease in the num ber o f Y cells. The functional
properties o f the cclls were norm al. C atscnuclcatcd between
em bryonic
/ days
4 4 4 and 51 lacked ocular dom inance col-
umns in the visual cortex, although the projections o f t h e
rem aining eye were topographically organized (Shook and
C halupa 1986).
The developm ent o t the L G N in the cat was severely
disturbed when retinal action potentials were abolished for
several weeks after birth by the application o f tetrodotoxin
(Archer et al. 1 9 8 2 ). Total blockage o t retinal activity in
one eye by tetrodotoxin for one week in 7-week-old kittens
produced severe reduction in cell size in all L G N laminae
innervated by rhe deprived eye. The loss was m ost severe in
the binocular laminae, but there was also som e loss in the
m onocular laminae (Kuppermann and Kasamatsu 1983).
8 .2 .2 b E ffe c ts o f M o n o c u la r S u tu rin g on
L G N S tr u c tu r e
In the cat, m onocular suturing w ithin the first 4 postnatal
weeks leads to a reduction in the size o f relay cclls in the
binocular lam inae o t the L G N served by the deprived eye
(W iesel and Hubei 1 9 6 3 b ; H ickcv c ta l. 1977). The reduc­
tion in size of relay cells in the L G N was about 20% tor cells
projecting to area 17 o f the cat and up to 60 % for those
projecting to area 18 (Garey and Blakem ore 1977). Axons
from a visually deprived eye developed abnorm al patterns
o f term ination in the L G N . M any X cells had unusually
broad term inal fields in lamina A and the term inal fields o f
many Y cells were greatly reduced w ith thin dendritic
branching (Friedlander ct al. 1 9 8 2 ; Sur et al. 1 9 8 2 ). These
changes are accom panied by a loss o f neurofilam ents in cell
cvtoskclctons (D u ffy and Slusar 2 0 0 9 ).
Several investigators have reported a decrease in the
ratio o f responsive Y cells to responsive X cells in the LG N
A-laminac serving m onocularly deprived eves o f cacs
(Sherm an et al. 1972; Sireteanu and H offm ann 1979;
Mangel cc al. 1983; Fricdlander and Scanford 1984). Using
histological procedures, LeVay and Ferster (1 9 7 7 ) found
that Y cclls in deprived Л -lam inac shrank more than X cclls.
Also, there were fewer Y cells relative to X cells.
It is n o t clear whether the decrease in the ratio o t Y cells
to X cells was due to the difficulty o f detecting shrunken
Y cells, death o t Y cells, an increase in X cells, or a conver­
sion o f Y cclls into X cells. Lysel et al. (1 9 7 9 ) found a
reduced proportion ot visually responsive Y cells in deprived
lam inae o f the L G N but noc in che opcic radiacion. 'Ibis
evidence suggests that there was no actual loss ot Y cells in
the LG N .
O th er evidence suggests that m onocular lid closure does
not lead со loss o f cclls or atfccc che racio o f X and Y cells in
the cat LG N (K alil 19 8 0 ; Levitt et al. 2 0 0 1; Shapley and So
1980). N or docs it affect chc racio o f parvo- со magnocel-
lular cells in the monkey ^Blakemorc and V ital-D urand
YuzoM . C hino. B orn in T okyo in 1 9 4 3 . H e ob tain ed his B .Sc.
1986a). The reasons for this con flictin g evidence are not in p sych obiology at S t. N o rb crt C o lleg e, W isco n sin , and h i* P h .D .
clear. in visual n eu roscien ce at Syracuse U niversity. H e held an academ ic
In cats reared wich o n e eye sutured, relay cells in chc ap p o in tm en t at the Illin ois C o lleg e o f O p to m e try from 1 9 7 2 to
1 9 8 5 . H e is now professor at th e U n iv ersity o f H ou ston C o lleg e o f
L G N ot che deprived eye showed evidence o t reduced m et-
O ptom etry-
abolic accivicy, as reflccccd in chc decreased level o f chc met-
abolic enzyme cytochrom e oxidase (W ong-R iley 1979a).
These effects were postsynaptic, bccausc there was no eye has been found to be lowered, but only for gratings with
change in the size ot presynaptic terminals. There was also high spatial frequency (Jo n es c t al. 1984a; C h in o et al.
som e loss ot proteins associated with the cytoskeleton o f Y 1994a) (P ortrait Figure 8.3). A similar defect occurred in
cells o f the deprived eye (B ickford ec al. 1998). cacs raised wich m onocular occlusion (M atfei and Fiorencini
Decrease in cell size in che L G N also occurs in monkeys 1976; Lehm kuhle ec al. 1980). Also, X cells in che L G N o f
wich che lens in one eye removed buc wich illuminacion o f scrabismic cacs showed lowered efficiency o f signal trans-
che retina at normal levels. In monkeys reared with one mission and unusually long laccncy, especially in layers
eyelid sutured, che LG N laminae serving che deprived eye innervaced by che deviating eye (C h en g et al. 1995).
were pale and shrunken. This shows that lack ot patterned O th er investigators found that m onocular occlusion
stimulacion racher than lack o f light is an imporcanc factor did not affect the spatial properties o f X and Y cells in the
in the effects ot m onocular deprivation (N oorden and cat LG N (Shapley and So 1980; D errington and Hawkcn
Crawford 1 977). However, che deficics produced by lid 1 9 8 1 ) or o f parvo- and m agnocellular cells in the monkey
suture are not as severe as those produced by enucleation or (Blakem orc and V ital-D urand 1986a). The reasons for this
abolition o f action potentials. This suggests that accivicy con flictin g evidence are not clear.
arising in a sucured eye is better than no input. M onocularly deprived kittens with chc visual cortcx
Young ferrets move abouc before chey open cheir eyes on removed showed che same loss o f response o f Y cells in the
postnacal day 32. Akerman ec al. (200 2 )fo u n d that ferrets L G N to stim ulation o f the deprived eve as did deprived k it­
devoid o f visual stim ulation during this period showed tens wich the visual cortex intacc. Thus, che L G N deficit is
defects in the segregation ot O N - and O F F -cen te r cells in noc due to suppressive corticofugal influences (Z ctlan c t al.
the I.G N . It chus seems chac visual stimulacion chrough chc 1981). Also, m onocular deprivation in cats did not affect
closed eyelids is required tor the normal developm ent ot the response properties o f X or Y ganglion cclls in the optic
these cclls. nerve. Thus, changes in relay cells in the L G N occur post-
synaptically.

8 .2 .2 c E ffcccs o f M o n o c u la r S u tu rin g on
L G N F u n c tio n 8 .2 .2 d In tc ro c u la r C o m p e titio n in th e L G N

Tliere has been som e controversy regarding the eifeccs o f The following evidence dem onstrates that the effects of
m onocular deprivation on the functional propercies o f relay m onocular occlusion in the I.G N arc due, at least in part, to
cells in che L G N . The spacial concrasc scnsicivicy o f X cells a lowered level o f inputs from the deprived eye because o f
in layers ot the cat L G N receiving inputs trom a strabismic com petition with inputs from the normal eye.
 Relay cells in che L G N o f chc cac and dog chac receive
inpucs irom chc m onocular crescent o f chc deprived eye
retain cheir norm al size, m etabolic accivicy, and proporcion
o f Y cells (G uillery and Stelzner 1 9 7 0 ). Furtherm ore, relay
cells o f a m onocularly occluded eye develop normally when
the corresponding retinal region ol the nonoccluded eye
has been lesioned (G uillery 1 9 7 2 ; Sherm an and W ilson
19 7 5 ; W ong-Riley 1979b ). *
C ats and monkeys reared with both eyes in total dark­
ness show no obvious changes in che number, size, or seam­
ing characreriscics o f L G N cells (C h ow 1 9 7 3 ; H endrickson
and Boothe 1 976). This dem onstrates that the reduced size
o f L G N relay cells in m onocularly deprived animals is due
to com petitive interactions with inputs from the normal
eye rather than to a simple absence o f visual inputs.
Delivery o f the neurotrophin T N -4 into the visual
cortex prevents the shrinkage o f L G N cells in che m onocu­
larly deprived ferrec (Riddle ec al. 1995). Also, blockage o f
N M D A recepcors in the kitten visual cortex renders the
L G N immune со che effects o f m onocular deprivacion
(K leinschm idc et al. 1 9 8 7 ; Bear and C olm an 1990). These
findings suggest thac activity-dependent compecicion for a
limiced supply o f growth factor is responsible for selective
shrinkage o f L G N relay cells serving a deprived eye.
There is also evidence o f a loss o f gcniculocortical affer­
ent* from a deprived eye o f cats (Thorpe and Blakemore
1975).
Changes in the size o f cells in the L G N are closely co r­
related with changes in the ocular dom inance colum ns o f
the visual cortex (V ital-D u ran d et al. 1 9 7 8 ). As long as the
eye has nor been occluded for more than about 6 weeks, rhe
cells in the L G N recover to full size soon after the occlusion
is switched to the o ther eye (D iirsteler et al. 1976).
8 .2 .2 e E ffe c ts o f In d u c e d S tra b ism u s o n th e L G N
Strabism us induced in kittens by m yectom y o f the lateral
rectus and superior oblique muscles produced a reduction
in the size o f cells in L G N laminae receiving inputs from
the deviated eye, in proporcion со che degree o f amblyopia
(Trem ain and Ikeda 1982). However, scrabismus induced
by ceneccomy (tendon section) produced no such effect.
Also, loss o f visual acuity was m ore severe for an eye made
strabism ic by myectom y than by tenectom y (M itch ell et al.
1984).
D ifferences betw een tenectom y and myectomy
probably arise because severed cendons reattach to che eye
after a few days, whereas a myeccomized eye remains w ith­
out muscle attachm ent (Crew cher et al. 1985). Another
factor may be loss o f proprioceptive inputs in myectom y
(Section 3 2 .5 ).
K ittens reared with convergent strabismus induced by
m onocular mveccomy showed a specific loss o f tunccional
cells in che L G N laminae served by rhe periphery o f rhe
tem poral retina (Ikeda et al. 1 9 7 7 ). It was suggested that
this is because, for an eye deviated nasally, the peripheral
tem poral retina is hidden by the nose and receives an impov­
erished input.
Convergent strabismus in kittens induced by m onocu ­
lar m yectom y severely reduced the synaptic arbors o f Y cells
in the A laminae serving both eyes (G arraghty et al. 1989).
Boch eyes are atfecccd because scrabismus misaligns che
scimuli in che two eyes but does noc deprive eicher eye o f
paccerned visual inpucs. By concrasc, m onocular occlusion
affecrs mainly the laminae serving the occluded eye because
that eye lacks patterned inputs.
M onocularly deprived monkeys and monkeys reared
with esotropia induced by tenectom y show shrinkage of
LG N cells serving the deprived eye, especially in the parvo­
cellular layers (N oorden and M iddleditch 1 9 7 5 ; Crawford
and N oorden 1 9 7 9 ; Tigges c t al. 1 9 8 4 ). Normal ccll size
recovered in 4-year-old monkeys that had been reared for
3 0 days with induced esotropia (Craw ford and Noorden
1996). Postm ortem analysis o f the L G N o f a human strabis­
mic amblyope revealed reduced ccll size (N oorden and
Crawford 1992).
Signal transmission in parvocellular units o f the L G N
was normal in m onkeys reared with esotropia induced by
myectom y betw een the ages o f 2 0 and 3 0 days (Sasaki et al.
1 9 9 8 ). Brown and Salinger (1 9 7 5 ) claim ed that chronic
im m obilization o f one eye led to substantial loss o f X cells
but n o t o f Y cells in the L G N . The effects o f severing prop­
rioceptive inputs from the extraocular muscles are reviewed
in Section 32.5.
8 .2 .2 f E ffe c ts o f M o n o c u la r D e p riv a tio n o n
th e C o llic u lu s
In mammals, the superior colliculus is a paired structure in
the m idbrain involved in guiding saccadic eye movements.
It is the hom ologue of che optic tectum ot nonmammalian
vertebrates. The superficial layers o f the superior colliculus
receive direct inputs trom the contralateral retina and inpucs
from che ipsilateral retina routed chrough che visual cortex
(Kawam ura et al. 1974). The cells have large receptive fields,
and mosc o f chem are binocular and direccionally seleccive.
After removal o f che visual cortex, cells in the superior
colliculus lose their ipsilateral input and their directional
selectivity and becom e more responsive to flickering
light (Berm an and Cynader 1 9 7 5 ). Thus, the visual cortcx
exerts some control over the stimulus selectivity
в
o f collicu-
lar cclls.
In m onocularly deprived cars m ost collicular cells do
not respond to the deprived eye, not even the cclls that
receive a direct input from the deprived eye. Thus, borh
direct and cortical inputs to che superior colliculus o f cats
are absent from an eye sutured from birth (H offm ann and
Sherm an 1 9 7 4 ). The absence o f response to direct
inputs cannot be due to changes in ganglion cells, because
these cells are n o t affected by m onocular deprivation.
After removal o f rhe visual cortcx m ost cells in the collicu ­
lus contralateral to the deprived eye began to respond only
to the deprived eye (W ickelgren and Sterling 1969). The
intact cortex must have suppressed the direct inputs from
the deprived eye. Removal o f the cortcx removed this sup­
pression.
Before testing, W ickelgren and Sterling waited up to 4
weeks after the visual cortex was removed. Recovery o f 4
direct inputs could have been due to long-term structural or
m etabolic changes or to rapid release from cortical suppres­
sion. Berman and Sterling (1 9 7 6 ) observed recovery o t the
d irect inputs w ithin one hour after cortical ablation. 'Ibis
result rules out long-term changes.
Unlike cells in the visual cortex, many cells in the supe­
rior colliculus retain their binocularity in cats reared with
artificial strabismus or alternating occlusion o f the eyes. The
collicular cells may receive their ipsilateral inputs through
the corpus callosum. However, in strabism ic cats and in cats
with sectioned right m edial and rectus muscles, binocular
cells in the superior colliculus contralateral to the normal
eye are heavily dom inated by the normal eye (C o rd o n and
Gum m ow 1 9 7 5 ). This was not apparent in strabismic cats
that had been forced to use the deviating eye (G ordon and
Presson 1 977).
8 .2 .3 C O K IT С A L E F F E C T S О F M О N О С U L A К
D E P R I V A T I O N IN S U B P R I M A T E S
8 .2 .3 a C o r tic a l E ffects o f Induced
Strabism us in C ats
Hubei and W iesel (1 9 6 5 ) conducted one ot the first experi­
ments on the etfects o f abnorm al visual experience on the
developm ent ot the visual cortex. They reared kittens to the
age o f 3 m onths or more with a surgically induced divergent
deviation o t one eye. This permanently reduced the number
o f binocular cclls in area 17 to about 20 % com pared with
80 % tor a norm al cat. However, there were roughly equal
numbers o f m onocular cclls that responded only to the left
eye or only to the right eye. Thus, the ocular dom inance col­
umns remained roughly sym m etrical. It seems that binocu ­
lar cells with a left-cye dom inance were converted into
left-m onocular cclls and those with a right-cyc dom inance
were converted into right-m onocular cells.
Sim ilar results were observed in cats reared with prisms
that disrupted alignm ent o f the visual axes (B en n ett et al.
1980) and in kittens with extraocular muscles cu t and rein­
serted in another position (recession), rather than severed
(Sireteanu et al. 1993a) (P ortrait Figure 8 .4 ). C ats reared
with anisom etropia produced by a lens before one eye devel­
oped a preponderance o f cortical cells responding to the
normal eye and reduced contrast sensitivity in the defo­
cused eye (Eggcrsand Blakem ore 1 978).
Although m ost cells in areas 17 and 18 o f strabismic
cats lose their binocularity, binocular cells sensitive to
Fi£u*< *.<. R itxandm Sirctcanit* B o m in R o m an ia 1 9 4 $ . Sh e train ed as
a bioph ysicist a t the U n iv ersity o f B u ch arest, R o m an ia ( 1 9 6 8 ) , and
ob tain ed a P h .D . in biophysics from th e S cu o la N orm alc Su pcriorc
in Pisa in 1 9 7 6 . She held p o std o cto ral fellow ships a t the Institu t
d :\ n a to m ic, U n iv crsite de Lausanne, and th e D e p a rtm e n t for
C om parative N eurobiologv, U n iv ersity o i U lm , trom 1 9 7 6 to 1 9 7 8 .
She was a sen ior investigator at the M ax -P lan ck -In stitu te for psychiatry
in M u n ich from 19 7 S to 19 S 2 an d at the M ax-P lan ck -In stitu te for
brain research in F ran k fu rt from 1 9 8 2 to 1 9 9 9 . From 1991 to 1 9 9 9
she was professor o f n cu ro scicn cc in the D e p a rtm e n t o f Z oo logy,
U n iv ersity o f M ain z. She was th en professor o t b iolog ical psychology
at the U n iv ersity o f F ran k fu rt and head o f the Research G ro u p tor
Psychophysics and N europsychology a t the M a X 'P la n c k ln stitu tc for
Brain R esearch in F ran k fu rt. Sh e received the award o t the H cin z-an d
M clcn c-A d am -Stifxu n gfor “E xcellen ce in R esearch in O phthalm ology**
in 1991 and the Prize o f the Biclschow sky S o cie ty fo r R esearch in
Strabism u s in 1 9 9 4 . She died in 2 0 0 8 .
m otion-in-depth have been found to survive in area 18
(Cynadcr et al. 1 9 8 4 ). In spite o f the loss o t binocular cells,
the amblyopic eye o f strabism ic cats drove about as many
cells in area 18 as did the nonam blyopic eye (Schroder et al.
2 0 0 2 ). However, in the suprasylvian area o f the dorsal
stream only about 30% o f cclls were driven by the ambly­
opic eye compared with 60 % for the nonam blyopic eye. In
area 21a o t the ventral stream only 5% o f cells were driven
by the amblyopic eye compared w ith 75 % tor the o ther eye.
Thus, amblyopia has m ore effect in the ventral stream than
in the dorsal stream.
C ells in area 17 driven by the deviating eye o f strabismic
cats show reduced sensitivity to high spatial frequencies,
loss o f contrast sensitivity, broadened orientation tuning,
and loss o f tem poral resolution (C rcw th cr and C rcw thcr
1993). Strabismus has a particularly strong deleterious effect
on the temporal properties o f cclls in area-18 (C h in o c t al.
1988). The weakened response o f neurons serving the devi­
ated eye shows in both the visual-evoked response and in
optical imaging o f responses over the surface o f the cortex.
 S ch m id t c t al. (2 0 0 4 ) induced convergent squ in t in kit­
tens and tested them with large square-wave gratings o f
various orientations and spatial frequencies. In area 17, o ri­
entation preference was impaired and overall activity was
less with stim ulation o f the deviating eye than with stim ula­
tion o t the nondeviating eye. The interocular differences in
V E P am plitude were related to the interocular differences
in the strength o f response indicated by optical imaging.
Both differences increased as the spatial frequency ot the
stimulus increased to 3.5 cpd.
C h in o et al. (1 9 9 1 ) reported that cats reared with a
15-diopter base-in prism before one or both eyes had a
reduced proportion o t cortical cells tuned to vertical. But,
a 15-diopter prism produces strong curvature o f vertical
lines, which may have contributed to the loss ot cells tuned
to vertical. The effect did not occur when the nondeviating
eye was sutured, which indicates that it was due to rivalry ot
inputs rather than to eye deviation alone. C h in o and Kaplan
(1 9 8 8 ) found reduced sensitivity to vertical gratings when i is « t s.s. Ja c k C raw ford. B o rn in n o rth G e o rg ia , U n ited States, in 1 9 3 3 .
H e ob tain ed a P h .D . in physiological psychology at the U niversity o f
recording from X -cells in the I.G N o f strabismic cats. The
G eo rg ia in 1 9 6 2 and con d u cted p o std o cto ral w ork at the U n iv ersity o f
behavioral correlate o f this effect is known as the vertical M ississippi M ed ical S ch o o l. H e is professor and h old er o f th e I'rederic
e ffe c t (Section 8.4.2b ). B. A sch c C h a ir in O p h th a lm o lo g y at th e U n iv ersity o f Texas M ed ical
There has been some conflicting evidence on the effects S ch o o l in H ou ston .

o f strabismus on the width o f ocular dom inance columns.

C ats with a natural strabismus have abnormal ocular dom i­
(Y in o n et al. 197 5; Berman and Murphy 1982; Freeman
nance columns (von Griinau and Rauschcckcr 1983). bowel
and Tsum oto 1983; M itchell ecal. 1984).
(1 9 9 4 ) found that the ocular dominance columns in area 17
In norm al kittens, horizontal axons in the visual cortex
were unusually wide in cats reared with divergent strabismus
co n n ect corcical colum ns wich sim ilar oriencacion sclcctiv-
induced by monocular tencctomy. Tiem an and Tumosa
itv. C ells in these connected colum ns tend to respond in
(1 9 9 7 ) reported that they were 11% wider in cats reared with
synchrony (Section 5.5.6). In kicccns reared wich scrabis-
alternating m onocular occlusion. However, the periodicity
mus, response synchronization was normal becween cell
o f ocular dom inance columns varies widely in normal cats,
groups served by chc same eye buc unusually weak becween
and Rathjen ec al. (2 0 0 2 ) found no significant difference
cell groups served by different eyes (Low el and Singer 1992;
between norm al and strabismic cats. O th er investigators
K o n ig ct al. 1993). The crucial factor seems to be the lack o f
found that, although the ocular dom inance colum ns o f the
correlated inputs from the two eyes, which weakens form a­
deprived eye ot cats and monkeys were reduced in width,
tion o f con nections between cells responding со chc cwo
there was no overall change in the com bined width o f left-
eyes in favor o t connection s between cells responding to
eye and right-eye colum ns (see Crawford 1998) (Portrait
neighboring regions o f the same eye. This could explain
Figure 8.5). The crucial factor is probably the extent to which
why ocular dom inance colum ns in strabism ic cats respond
strabismus is accompanied by amblyopia. It is to be expected
alm ost exclusively cocichcr chc lefio r chc righceyc (G ood hill
that an amblyopic cvc has fewer binocular cells that arc dom ­
and Lowel 1 9 9 6 ).
inant for that eve.
* The ocular dom inance colum ns of that eve *
Alchough inpucs from chc eyes o f scrabismic cats projccc
would then be narrower than those o f the normal eye.
со independent ocular dom inance colum ns, che orientation
A ll form s ot binocular interaction, both excitatory• and
colum ns retain their usual pinwheel organization and co n ti­
inhibitory, arc drastically reduced in cacs wich a natural
nuity across ocular dom inance colum ns (Low el et al. 1998).
strabismus (H offm ann and Schoppm ann 1984). C h in o
In normal cats, pinwheel centers tend to occur in the middle
c t al. (1 9 9 4 b ) induced strabismus in 4-week-old cats by a
o f ocular dom inance colum ns (Section 5.7.1). This tendency
m onocular prism or by surgery. After tw o weeks, m ost cells
is less evident in strabismic cats, (Engclm ann et al. 2 0 0 2 ).
in the visual cortcx showed som e response to binocular
stimuli, but there was a prevalence o f suppressive interac­
tions. After 3 or 8 m onths ot strabismus, both excitatory
8 .2 .3 b E ffe c ts o f S tra b ism u s o n th e
and suppressive interactions were reduced, especially for
C o r p u s C a llo su m
cells tuned to higher spatial frequencies.
C onvergent strabismus (esocropia) has a greacer cffecc In normal cats, callosal connections arc initially widely dis­
on cortical cells than divergent strabismus (exotropia) tributed over the surface o f the cortex. Later, they becom e
c t al. 1 982), although it has been claim ed chac this proce­
dure works onlv when afferents from the extraocular mus-
cles are also paralyzed (C rew ther et al. 1978). Thus,
removing the eye removes its inhibitory influences on co rti­
cal cells and allows dorm ant excitatory inputs from the
deprived eye to recover. However, full recovery for most
cclls is n o t im m ediate, as it would be it it involved only/ а
simple removal o f inhibition from the good eye. Removal
o f inputs trom the good eye must allow some restorative
processes со occur in che weakened, buc sc ill presenc, excit­
atory inputs trom the deprived eye. Som e ot these restor­
ative processes occur alm ost im m ediately; others cake some
cime. W e will see lacer that restoration o t physiological
functions in a deprived eye after removal o fth e good eye is
accom panied by som e restoration o f visual function.
S . 2 . 3 f Loss o f Sen sitivity in the N ondcprived Eye
In strabism ic cats, cells in the visual cortex driven bv the
nondeviating eye show some loss in contrast sensitivity
(C h in o et al. 1983). Also, behavioral tests reveal some loss
o f contrast sensitivity in che nondeviating eye in strabismic
cats (H olopigian and Blake 1983) and strabism ic humans
(Levi and Klein 1 9 8 5 ; D obson and Sebris 1989).
Freeman and Bradley (1 9 8 0 ) claim ed that amblyopic
humans have higher than norm al hyperacuity in the non-
amblyopic eye, but Johnson et al. (1 9 8 2 ) could not confirm
this.
N ine children with strabism ic amblyopia and four o fs ix
children with anisom etropic amblyopia showed some loss
in detection o f mocion-defined forms wich cheir nonam bly-
opic eye. Snellen acuity o f the nonam blvopic eye was normal
(G iaschi ct al. 1 992).
Loss o f sensitivity in a nondeprived eye may be due to
persistent blur o f t h e retinal image arising from instability
o f gaze. Also, it could perhaps be due to loss ot synaptic
density. Tum osa et al. (1 9 8 9 b ) reported thac corcicai syn­
apses form ed by a nondeprived eye do not increase in
number but becom e spread less densely over wider areas.
8 .2 .4 C O R T IC A L E F F E C T S O F M O N O C U L A R
D E P R IV A T IO N IN P R IM A T E S
M onocular deprivation has been produced in intant m on­
keys by surgically or optically induced strabismus, by sutur­
ing or occluding one eye, or by blurring the image in one eye
(induced anisom etropia). In each case, the response o t bin­
ocular cells in V I ro stim ulation o f rhe deprived eye is
reduced or absent (Carder et al. 1991).
8 .2 .4 a C o r tic a l Effects o f Strabism us
and A m blyopia
In strabismic monkeys, only a few cortical cclls show
strong binocular activation, although the eyes activate
approximately che same num ber o f neurons (K iorpes cc al.
1998). O n ly 3 days o f prism -induced strabismus in 4-week-
old monkeys increased the number o f cells in V I that
responded only weakly to binocular stim uli (Z hang et al.
2 0 0 5 ). However, the same cells responded to binocular
phase disparity. These results suggest that strabismus pro­
duces binocular suppression before it affects stereopsis. In
prism-reared monkeys, inhibitory connections between
surviving binocular cells were less affected than excitatory
connections (Sm ith c t al. 1997).
Som e recovery* o f sensitivityi ot binocular cortical cells
occurred when the prisms that induced the strabism us were
removed after they had been worn tor 4 weeks, but n o t after
they had been worn fo r 8 weeks (M ori et al. 2 0 0 2 ). However,
monkeys reared with prism -induced strabismus between
the ages o f 4 and 14 weeks showed som e im provem ent in
stereoacuity after receiving extensive training in the task
(N akatsuka et al. 2 0 0 7 ). Training also produced some
im provem ent o f disparity sensitivity in cells in V 2 but not
in V I .
Surgically induced strabismus in monkeys disrupted
binoculariry more than lens-induced anisom etropia
(K iorpes et al. 1 9 9 8 ). Both deficits reduced the optim al
spatial frequency tuning o f cortical cclls responding to the
affected eye, especially for cells serving the foveal area.
The contrast sensitivity o f cortical cells was n o t affected,
but the behavioral loss o f contrast sensitivity suffered by
amblyopes m ight depend on che relacive num ber o fco rd ca l
cells responding racher chan cheir sensicivicy.
Amblyopia can be induced in monkeys by rearing rhem
wich a defocusing lens before one eye o r by surgically induc­
ing strabismus. B o th procedures applied soon after birth
produced som e shrinkage o f the ocular dom inance colum ns
serving the amblyopic eye (H endrickson et al. 1987). The
shrinkage was greater when the amblyopia was induced at
an earlier age. The shrinkage was correlated with loss ot
concrasc sensitivity in rhe amblyopic eye (Craw ford and
H arw erth 2 0 0 4 ).
H orton e ta l. (1 9 9 7 ) did n o t observe shrinkage o f ocular
dom inance colum ns in a monkey with natural anisom e­
tropic amblyopia, although the tim e o f onset o f t h e an i­
som etropia was not known. H orton and Stryker (1 9 9 3 )
observed no colum n shrinkage in the visual cortex o f a man
in whom anisom etropic amblyopia had been detected at
age 41/2 years. N or was there any colum n shrinkage in the
cortex o f a 79-year-old woman who had had amblyopia due
to esotropia from the age o f 2 years (H o rto n and H ocking
1996d ).
These results suggest th at amblyopia can be induced
after the critical period for induction o f colum n shrinkage.
Esotropia induced in 9-day-old monkeys reduced c y to ­
chrom e oxidase, especially in layer 4 C , and decreased
expression ot o ther chem ical markers lying along the
centers o f ocular dom inance colum ns in lavers
i
3 to 5. It did
n o t affect the mean spacing o f cytochrom e-oxidase blobs
centered in ocular dom inance colum ns. However, the m on­
keys were not amblyopic.
F.arly m onocular deprivation o f various types in the
m onkey leads to a reduction or loss o f visually evoked
potentials (VF.Ps) associated with asynchronous dichoptic
visual flicker (B a itch et al. 1 9 9 1 ). N ine hours o f m onocular
occlusion in adult humans did not reduce the cortical
potentials evoked by a texturcd stimulus presented to rhe
occluded eye but tem porarily increased the response from
che seeing eye (Tyler and K aitz 1 9 7 7 ).
Human brain potentials (V E P s) from V I had longer
latency and smaller amplicude when a reversing checker­
board pattern was presented to the am blyopic eye than
when it was presented to che normal eye. However, the
latency and am plitude ot the V E P to m otion onset ot a
checkerboard were the same for the amblyopic eye and
norm al eye (K ubova et al. 1 9 9 6 ). This suggests that the
m otion pathway, which probably involves mainly the mag­
nocellular system, is relatively spared in amblyopia.
Neural activity at the human V 1-V 2 border, as revealed
by m agnetocnccphalography, had longer than normal
latency and reduced am plitude when a grating was pre­
sented to an amblyopic eye (Anderson et al. 1999). Sim ilar
reduced activity in V I and extrastriate cortex was revealed
by fM R I (Barnes et al. 2 0 0 1 ). Imamura et al. (1 9 9 7 )
found reduced PF.T activity in the extrastriate corcex buc
n o t in V I .
8 .2 .4 b C o r tic a l E ffe c ts o f M o n o c u la r
Su tu rin g in Primates
M onocular deprivation by lid suturing tor more than a year
can lead to com plete loss o f visual functions in che deprived
eye in infant macaque and squirrel monkeys (Sparks et al.
19 8 6 ; W ilson and Nevins 1 991). The loss seems to occur in
the nasal visual Held (tem poral retinas) betore it is com plete
in the cemporal visual field (T iem an cc al. 1 9 8 3 a ; W ilson
et al. 1 989). This may be related to the fact that the tem po­
ral retina has a greater density o f ganglion cells than the
nasal retina (Section 7 .2 .4 ).
M onocular deprivation produced by suturingor occlud­
ing one eye causes a contraction o t ocular dom inance col­
umns tor the deprived eye and an expansion o f those for the
norm al eye (Baker et al. 19 7 4 ; LeVay et al. 1 9 8 0 ; M ovshon
ct al. 1987). These changes can Ik seen in the autoradio­
graph o f the visual cortex o f a m onocularly deprived monkey
(D es Rosicrs c t al. 1 978). Changes in ocular dom inance do
not involve any significant change in the overall density o f
neurons or o f synapses w ithin cortical layers ( O ’Kusky and
C o lon n ier 1 982).
Daily 1-hour periods o f binocular vision reduced the
loss o f contrast sensitivity and binocular suppression that
would otherw ise have occurred in monkeys wearing a dif­
fuser over one eye betw een 3 and 18 weeks o f age (Sakai
et al. 2 0 0 6 ).
In m onkey striate co rtcx, m onocular deprivation also
produces a severe reduction in the size o f cytochrom c-
oxidase blobs centered in ocular dom inance colum ns d om i­
nated by the deprived eye (Trusk et al. 1990; W ong-Riley
1994; H orton et al. 1999). Autopsy specim ens o f human
brains trom cases ot m onocular enucleation showed the
same effect (H o rto n and H edley-W hite 1984).
The CO I and cyt b genes, located on m itochondria,
express R N A transcription factors that are concerned with
synthesis o f cytochrom e oxidase. The concentration o f these
transcription factors is reduced in the visual co rtex ot m on­
ocularly deprived monkeys (H evner and W ong-Riley 1993;
Kam inska e t al. 1 9 9 7 ). There is thus a direct link between
visual activity and gene expression (see Section 6.6).
It was noted in Section 8.2.2a that m onocular depriva­
tion in cats produces some loss o f cvtoskelcton proteins in
Y-cells in the L G N innervated by the deprived eye. Dutfv
and Livingstone (2 0 0 5 ) found a sim ilar loss in cells in the
m onkey visual cortex that receive inputs from L G N m ag­
nocellular layers o f the deprived eye. They also found an
eye-specific loss o f cytoskeletal protein in cortical layer 4 B ,
which docs n o t receive direct inputs from the I.G N .
8 .2 .5 E F F IIC T S O F B IN O C U L A R
D IS S O C IA T IO N
An eye receiving patterned visual inputs gains a com petitive
advantage over a closed eye. This disrupts the development
o f binocularity. T h is section is concerned with what hap­
pens when both eyes are open but receive stimuli that
can n ot be fused because they are spatially or temporally
dissociated.
8 .2 .5 a Spatial D issociation o f Visual Inputs
All forms o f m onocular deprivation have one thing in
com m on — they reduce the frequency with w hich bin o cu ­
lar cells are activated sim ultaneously by similarly patterned
inputs. H ebb (1 9 4 9 ) proposed that the efficiency o f synap­
tic transmission is increased when subsets o t presynaptic
inputs are correlated (Scctio n 6 .5 .1 ). A corollary o f this rule
is that synaptic efficiency is lessened when the inputs are
persistently uncorrclatcd. The cortical effects o f m onocular
deprivation seem to be good examples o f the Hebbian
model (C loth iau x et al. 1991).
C ontinu ed exposure o f kittens to prisms that completely
dissociated the images in the tw o eyes led to loss o f bin o cu ­
lar cells and o f stereopsis, but there was no change in ocular
dom inance (Blakem ore et al. 1975; Sm ith et al. 1979).
M onkeys seeing through 13-diopter base-in prisms that
com pletely dissociated the images in the two eyes trom age
3 0 ro 6 0 days had very few binocular cells in rhe visual
cortex and had no stereopsis (Craw ford and N oorden 1980;
Craw ford c t al. 1 9 8 3 ). These deficits were still present
3 years after the prisms were removed (Craw ford et al. 1984;
Craw ford cc al. 19 9 6 a , 19 9 6 b ). Since chis treatm ent affected
both eyes equally, there was no amblyopia o r strabismus.
Three m onkeys were raised in a cylinder lined wich ver­
tical stripes and with 13.5-diopter base-in prisms on each
eye (N oorden and Craw ford 1 981). D isruption o f cortical
binocularity was as severe in these monkeys as in those
raised with the same prisms buc in a normal visual environ­
m ent. It was expected that the repetitive pattern o f stripes
would have provided sufficient fusible stimuli to allow bin­
ocular cells ro develop. However, a 13.5-diopter prism
introduces a nonlinear prismatic displacem ent and severe
curvature o f vertical lines and o f horizontal lines above and
below the horizon. These second arvd i istortions would have
been opposite in the rwo eyes and would have prevented
fusion.
C ats reared with binocular lid closure bu t with flicker­
ing diffuse light presented through the closed lid o f one eye
did n o t develop greater ocular dom inance for that eye
(Singer et al. 1 9 7 7 ; W ilso n et al. 1 977).
M alach and Van Sluyters (1 9 8 9 ) challenged the simple
view that correlated inputs to the tw o eyes are all-im portant
in the developm ent o f binocularity. They exposed 4-week-
old kittens to a 2-day period o f m onocular deprivation and
then allowed them binocular vision, but with the previously
deprived eye deviated. These anim als showed some recov­
ery o f the num ber o f cells driven by the deprived eye,
although not to the level attained by animals allowed
norm al binocular vision from birth. To reconcile these
results with rhe H ebbian m odel, one must assume rhat the
correlation betw een inputs from misaligned eyes is higher
than that betw een inputs from a closed eye and an open eye.
Nevertheless, the basic fact remains that normal binocular
vision is required to m aintain or restore the full com ple­
m ent o t binocular cells.
8 .2 .5 b T e m p o ra l D is s o c ia tio n o f V isu a l Inpucs
A nother way to dissociate visual inputs is to reverse the
occluder betw een the eyes on alternate days so that the eyes
see the same stimulus but n o t at the same tim e (H ubei and
W iesel 19 6 5 ; Blakem ore 1 9 7 6 ). This procedure affects both
eyes equally and, although it induced stereoblindness, it did
not lead to loss ofvisu al acuity in either eye or to an im bal­
ance in the num ber o t cells responding to each eye (Blake
and H irsch 1 975).
T iem an et al. (1 9 8 3 a , 1983b ) occluded each eye o f kit­
tens for a variable proportion o f each day until they were 4
m onths old. I he eyes were alternately occluded for the same
period each day, or one eye was occluded for twice or eight
times as long as the other. All groups showed a severe loss o f
binocular cortical cells. The greater che im balance o t eye
exposure the higher was the percentage o f cells that
responded only to the m ore experienced eye. C o rtical cells
o f kittens with a balanced input had relatively norm al recep­
tive fields. C ells responding to the less experienced eye
showed a poorer response to visual m otion, were more
broadly tuned to orientation, and had smaller receptive
fields than cells responding to the more experienced eye.
These deficits were m ost pronounced in the hemisphere
ipsilateral to the less experienced eye, w hich received inputs
from the tem poral hem iretina. Also, the nasal visual field o f
the less experienced eye becam e reduced in size, and the cats
ignored novel objects presented in the nasal hetnifield o f
the more deprived eye when both eyes were open or when
only the more deprived eye was open (Tum osa et al. 1982,
1983). There was no recovery after restoration o f normal
binocular vision.
Wensveen et al. (2 0 0 3 ) reared monkeys with a defocus-
ing lens worn on alternate eyes on successive days. Since
both eyes were open, each eye had normal visual experience
on alternate days. Consequently, both eyes developed
normal contrast sensitivity. However, the monkeys required
higher than normal contrast to support stereopsis, even for
large disparities. Also, the spatial frequency that yielded the
highest stereoacuity was lower than normal.
Visual inputs from the two eyes do not have to be pre­
cisely synchronous for normal developm ent. C ats devel­
oped norm ally i f stimuli to the tw o eyes were alternated at a
frequency o f more than 10 Hz (Blasdel and Pettigrew
1979). The animals were restrained during visual exposure.
W h en kittens were allowed to move about while wearing
alternating shutters that exposed each eye for longer than
0.5 s, depth discrim ination was disrupted and there was a
reduction in the num ber o f binocular cells in the visual
cortex (A ltm ann et al. 1987).
8 . 2 . 6 E F F E C T S OF M O N O C U L A R
ENUCLEATION
8 .2 .6 a A n a to m ic a l E ffe c ts o f
M o n o c u la r E n u cle a tio n
Removal o f one eye causes axons from that eye to degener­
ate and increases the num ber o f axons from the remaining
eye. Thus, when hamsters and rats had one eye removed in
utcro, the optic nerve from the remaining eye had about
20% more axons than that o f an eye o t a norm al animal
(Sengelaub and Finlay 1 9 8 1 ; Jeffery and Perry 1 9 8 2 ). In
cats, the rem aining eye had about 1 8 0 ,0 0 0 ganglion cells
com pared with 150,1)00 in an eye o f a normal cat. All co rti­
cal neurons o f early m onocularly enucleated cats responded
to the rem aining eye and had norm al response properties
(Shook et al. 1 9 8 5 ). However, their receptive fields were
smaller than those ot cortical cclls in normal cats (Chalupa
e ta l. 1 9 8 4 ; S ton e and Rapaporr 1986).
Rem oval o f one eye in fetal m ice and ferrets, bctore gan­
glion-cell axons reached rhe chiasm , reduced rhe num ber o f
uncrossed axons trom che surviving eye in the optic tract.
Axons th at would have been uncrossed accumulated at che
chiasm (see Taylor and G uillery 1 9 9 5 ). Enucleation in the
neonate, after ganglion-cell axons had reached the L G N ,
increased the num ber ot uncrossed axons in the optic tract
(L u n d eta l. 1 9 7 3 ;G o d e m e n te ta I. 1987; C han and G uillcry
1993). Thus, w ith early enucleation, uncrossed axons in the
surviving eye are inhibited from entering the chiasm . This
suggests that, in the norm al eye, uncrossed axons depend on
the presence o f crossed axons from the other eye for their
entry inco chc uncrossed pachway. The crossed axons muse
activate a chem ical signal that guides uncrossed axons
through chc chiasm (C h an and G uillcry 1993). This issue
was discussed in m ore detail in Section 6.3.4a.
The sim ilarity betw een the visual pathways after early
m onocular enucleation and che visual pachways o f albinos
prompced G uillcry (1 9 8 9 ) со suggesc chat chis early chiasm -
torm ing mechanism is absent in albinos.
8 .2 ,6 b Visual Effects o f M o n o c u la r E n u cle atio n
In animals reared with only one eye, a larger than normal
proportion o f the visual corcex is devoted to che remaining
eye. This suggests that people who had one eye removed at
an early age would have better than norm al acuity in chc
rem aining eye. In con form ity with this expectation, sub­
jects who had early m onocular enucleation had higher co n ­
trast sensitivity than that o f binocular subjects viewing with
one eye. The earlier the enucleation was perform ed, the
larger was the range o f spatial frequencies over which co n ­
trast sensitivity was enhanced (N icholas et al. 1996).
However, gracing acuity o f enucleated subjects was no
better than that o f norm al subjects viewing with both eyes
(Reed cc al. 1 9 9 6 ). A t low contrascs, normal subjeccs were
superior (R eed c t al. 1 9 9 ?). The improved perform ance ot
normal subjects when viewing with boch eyes was probably
due to binocular sum m ation, as discussed in Section 13-1.
A group o f 15 observers who had been unilaterally enu-
clcated betore the age ot 36 m onths had a higher threshold
for detection o f temporalward m otion o f a random -dot dis­
play than o f nasahvard m otion (Steeves et al. 2 0 0 2 ). The
developm ent o f symmetry o f m otion detection depends on
early binocular vision, as explained in Section 22.6.1.
8 .2 .6 c C ross-M od al Innervation in
M o n o c u la r D eprivation
Toldi et al. (1 9 8 8 ) removed one eye o f rats at birth.
Responses o f cortical cells to stim ulation o f the vibrissae
revealed an encroachm ent o f somatosensory inputs into the
visual cortex. M onocular enucleation after che first week
did n o t produce chis effect. Toldi et al. ^1 9 9 4 ) obtained
anatom ical evidence o f cross-m odal innervation o f che
visual cortex o f the rat after early m onocular enucleation. In
norm al rabbits, abouc 2 % o f cells in che visual corcex
responded со visual and tactile stimuli. After removal o f one
eye o f adult ra b b its, 3 0 % o f cells began со respond to caccile
Stim uli (N ew ton et al. 2 0 0 2 ). This increase could have been
4118 • BASI C ME C HANI S MS
due to sprouting o f initial tactile-responsive cells or to
encroachm ent o f axons from neighboring cortical areas.
Cross-m odal innervation o f the visual cortex was discussed
in Section 8.1.4.
8 .2 .7 M E C H A N IS M S O F C O R T I C A L
P L A S T IC IT Y
8 .2 .7 a H o m o sy n ap tic and H eterosy n ap tic Plasticity
Th e effects o f m onocular deprivation have three co m p o ­
nents.
1. Changed activicy in cclls responding со a deprived eye
ac recipient layer 4 C before visual inpucs impinge on
binocular cclls. O n e faccor could be chc degree ot
correlacion becween presynaptic activicy and
poscsynapcic activity in gcniculocortical afferents from a
given eye. For a deprived eye, the correlation is reduced,
which would weaken the cells rcsponsivity. This would
be a Hebbian homosynaptic mechanism because ic
depends on activicy from only one eye. O therw ise, a
general non-H ebbian homeoscatic m echanism could
directly enhance activity o t deprived neurons by the
process o f synaptic scaling described in Section 6.5.4.
2. Depression o f cortical activity from the deprived eye
and enhanced activity from che nondeprived eye. We
will see chac chis requires som e residual accivicy in the
deprived eye coupled wich accivicy in che nondeprived
eve. These effeccs muse occur in binocular cells. Thev
i 4
depend on che excenc со which presynaptic inpucs from
the eyes correlate with postsynaptic activity. This is a
Hebbian heterosynaptic mechanism because ic
depends on compecicion between inpucs trom che two
eyes.
3. Long-term consolidation o f changes in synaptic
contacts. This involves m aturation and stabilization o f
synapses through developm ent o f processes that inhibit
changes after the critical period.
M ost cells in the rat visual cortex are driven onlv*
by the contralateral eye. For these cells, effects o f m onocular
deprivation are n o t due to com petition betw een inputs
from the two eyes. Therefore, the hom osynaptic m echa­
nism can be Studied in isolation trom the heterosynaptic
m echanism .
M affei et al. (2 0 0 6 ) recorded from slices o f m onocular
regions o f the rat visual cortex after the animals had been
subjected to m onocular lid suture on postnatal days 18 to
2 1 . Pyramid cells serving the deprived eye in layer 4 retained
their normal excitatory responses and interconnections.
However, the amplitude o f connection s betw een pyramid
cclls and inhibitory inrcrneurons (basket cells) increased
substantially. The long-term potentiation (L T P ) o t these
inhibitory synapses boosted inhibition in layer 4. Matfci
et al. produced evidence that I.T P o f inhibitory synapses is
due to the mismatch betw een the absent presynaptic firing
from m onocularly deprived pyramid cells and the sponta­
neous postsynaptic firin g o f the inhibitory cclls. It is known
that inhibitory cells fire spontaneously.
M rsic-Flugel et al. (2 0 0 7 ) produced d irect evidence tor
borh hom osynaptic and heterosynaptic processes. They
used tw o-photon imaging ot calcium transients to sim ulta­
neously plot changes in responsivity o f hundreds o f cells in
the m ouse visual cortex after suturing one or both eyes tor
up to 8 days. The ocular dom inance o f m ost binocular cclls
shifted in tavor ot the nondeprived eye. This represents het-
erosynaptic com petition betw een inputs from the two eyes.
However, cells that normally responded mainly or only to
the deprived eye showed an increase in responsivity, rather
than the depressed activity reported by M atfei et al. Also,
5 days o f binocular deprivation enhanced responsivity o f all
cells. These latter effects represent the effects o f hom osyn­
aptic synaptic scaling (see Section 6 .5 .4 ).
8 .2 .7 b E ffe c ts o f B lo c k a g e o f M o n o c u la r In p u ts
Inputs from an eye may be totally blockcd by injectin g tct-
rodotoxin. The eye is said to be inactivated. Suturing an eye
docs not totally block inputs because some light gets
through the eyelids. In kittens, lid suture produced greater
suppression o t responses o f binocular cortical cells to stim ­
ulation o fth e deprived eye than did m onocular inactivation
(R ittcn h ou se et al. 1 9 9 9 ). Thus, responses to stim ulation o f
a deprived-eye are depressed m ost effectively when there is
som e residual activity in that eye.
In another experim ent from the same laboratory, one
group o f young m ice were subjected to 5 days o f m onocular
inactivation with tetrodotoxin, and a second group were
subjected to 5 days o f m onocular occlusion (Frenkel and
Bear 2 0 0 4 ). After the effects o f the tetrodotoxin had worn
off, it was found that cortical responses to stim ulation o f
the inactivated eye were not depressed but that responses
tor the eye that had not been inactivated were enhanced. By
com parison, responses for the eye that had been sutured
were suppressed and there was also some enhancem ent o f
responses to stim uli applied to the other eye. Reciprocal
m odifications o f cortical responses in m onocularly deprived
rats were accom panied by decreased visual acuity in the
sutured eye and increased acuity in the nondeprived eye
(In y e t al. 2 0 0 6 ).
Sm ith and Trachtenberg (2 0 0 7 ) used optical im aging to
track the developm ent o f neural activity in the visual cortex
o f m ice. O n e eye o f 9-day old m ice was either sutured or
removed before the eyes opened and before the onset ot the
critical period. For the eye-sutured m ice, the retinotopic
maps o f both eyes were disorganized at postnatal day 13.
For the enucleated m ice, developm ent o f rhe retinotopic
map o f the rem aining eye was accelerated.
The fact th at depression o f cortical activity from a
deprived eye requires some activity in that eye can be
explained in terms o f decorrelated presynaptic and postsyn­
aptic activity. There is no decorrelated activity when all
inputs from an eve are absent.
8 .2 .7 c E ffe c ts o f B lo c k a g e o f P o stsy n a p tic A ctiv ity
A shift in ocular dom inance during m onocular deprivation
does not occur for regions o f the cat visual cortex in which
all postsynaptic cortical activity has been blocked by tetro ­
dotoxin (w hich blocks excitatory synapses) or muscimol
(which activates G A B A inhibitory neurons) (Shaw and
Cynader 1984; R eiter et al. 1 9 8 6 ). M ore specifically, the
shift in ocular dom inance was elim inated by blockage ot the
postsynaptic pathway that involves cA M P-dependent pro­
tein kinase (see Shim egi et al. 2 0 0 3 ).
Paradoxically, binocular cortical cclls o f monocularly
deprived kittens became more responsive to inputs trom the
elosed eye than to those from the open eye when postsynaptic
cortical activity was blocked by muscimol (Reiter and Stryker
1988). I l l is effect is known as reverse o cu lar dom inance
shift. It seems that the more active presynaptic afferents trom
the open eye were selectively retracted when postsynaptic
activity was blocked (H ata et al. 1999). Thus, growth or
retraction o f afferent inputs depended on the monosynaptic
correlation between pre- and postsynaptic activity in genicu-
locortical afferents of the open eye. There was no decorrela­
tion in the inputs from the occluded eye because there was
neither presynaptic nor postsynaptic activity tor these inputs.
These synapses therefore remained intact.
Thus the effects o f m onocular deprivation are n o t due
only to im balance o f inputs to binocular cells. They arc also
due to imbalance between presynaptic and postsynaptic
activity at the level o f geniculocortical inputs (H ata and
Stryker 1 9 9 4 ; K hibnik et al. 2 0 1 0 ).
H aruta and H ata (2 0 0 7 ) produced further evidence for
the hom osynaptic m echanism . They suppressed the activity
o f the visual cortex with muscimol in 4-w eek-old kittens.
Som e o f the animals also had both eves sutured. After
в
2 weeks there was retraction o f synaptic arbors o f geniculo­
cortical afferents o f the open eyes but n o t o f the sutured
eyes. In neither case was there any im balance between inputs
to binocular cells. For the seeing eyes there was decorrela­
tion betw een homosynaptic presynaptic and postsynaptic
activity at the level o f geniculocortical afferents. For the
occluded eyes there was n o decorrelation. Thus, the hom os­
ynaptic m echanism can induce cortical plasticity in the
absence o f the heterosynaptic mechanism.
8 .2 .7d R o le s o f In tr a c o r tic a l and
In te rc o r tic a l In h ib itio n
The role o f inhibition in the developm ent o f ocular
dom inance colum ns was discussed in Section 6.7.2c.
C o rtical plascicicy depends on che dcvelopmenc o f corcicai
inhibition. Perhaps a critical level o f cortical inhibition is
required for the detection o f synchrony betw een inputs
from the two eyes.
The neurotransm itter G A B A (gam m a-am inobutyric
acid) m ediates intracortical inhibition. The effects ol
G A B A can be removed by application of its antagonist,
bicucullinc. Seven days o f m onocular deprivation in kittens
produced less than the expected shift in ocular dom inance
when che cortcx was infused wich bicucullinc during the
period ot deprivation (R am oa et al. 1988). W ith in 3 0 s o f
intravenous in jection or corcicai application o f bicucullinc
in m onocularly deprived cats, betw een 4 0 and 60 % o f co rti­
cal cells tested began to respond again to excitatory stim ula­
tion o f the deprived eye, although n o t to the point o f
gaining dom inance over binocular cclls (D u ffy c t al. 1976;
Burchfiel and D uffy 1 9 8 1 ; Sillito et al. 1981; Mower and
C hristen 1 9 8 9 ).
Blakem ore et al. (1 9 8 2 ) argued that part bu t not all o f
this effect was due to che tact thac bicucullinc raises the gen­
eral level o f excitability• o f cortical cells to weak excitatory
inputs. This could cause an increase in the probability o f
correlated activity between weak inputs from the deprived
eye and activity from the norm al eye.
G enetic disruption o f the enzym e responsible for syn­
thesis o f G A B A in m ice leads to a retention o f responsive­
ness o l a deprived eye (H ensch et al. 1 9 9 8 ; Feldman 2 0 0 0 )
and partial restoration o f neural plasticity in response to
m onocular deprivation in adult rats (H arau zovet al. 2 0 1 0 ).
Also, enhancem ent o f activity at G A B A ergic synapses with
diazepan in norm al m ice produced an early onset o f t h e
critical period o f cortical plasticity (Fagiolini and Hensch
2 0 0 0 ). A b rief 2-day infusion o f diazepan triggered rhe
onset and term ination o f the critical period, even in dark-
reared m ice (Iwai cr al. 2 0 0 3 ).
There are about 2 0 G A B A receptor subunits. By study­
ing the effects o f m onocular deprivation in m ice with spe­
cific genetic defects, Fagiolini et al. (2 0 0 4 ) revealed that
G A B A receptor type u\ is specifically required for cortical
plasticity. These receptors occur on synapses proximal to
the soma o f pyramidal cclls. C o rtical plasticity was reduced
when there were either too many or too tew o f these recep­
tors (K atagiri et al. 2 0 0 7 ).
Som a-proxim al synapses are innervated by specific
inhibitory interneurons (P V basket cells) that emerge at the
onset o f the critical period. At the end o f the critical period,
PV cells becom e enclosed by the extracellular matrix.
Removal o f the enclosing network restores plasticity in
adult animals (see S ection 8 .2 .7 f).
The neurotrophin B D N F is required for the develop­
ment o f G A B A ergic inhibition. Overexprcssion o f B D N F
accelerates the m aturation o f P V interneurons and the onset
o f the critical period. Dark rearing reduces this neurotro­
phin and delays rhe term ination o f the critical period.
Adm inistration o f B D N F in dark-reared m ice restores the
developm ent o f G A BA ergic in h ibition (G ianfranceschi
et al. 2 0 0 3 ).
Subplate neurons play a crucial role in the early develop­
m ent o f the visual cortex (see Section 6 .4 .5 c). These neu­
rons are present during the critical period, after which they
die. D uring the critical period, G A B A ergic synapses switch
from being excitatory to being inh ibitory (Section 6.4.4d ).
O cu lar dom inance plasticity does not occur when
G A B A ergic synapses fail to mature into inhibitory syn­
apses. M aturation o f G A B A ergic synapses, specifically those
involving receptor type a 1, is controlled by subplate neu­
rons (Kanold and Shatz 2 0 0 6 ).
Intercallosal inhibition is also involved in ocular d om i­
nance plasticity. B locking intercallosal inputs from the co n ­
tralateral visual cortex with muscimol restored binocularitv
in rats th at had been m onocularly deprived during the criti­
cal period (R estani et al. 2 0 0 9 ). Also, blocking callosal
inputs during the period o f m onocular deprivation reduced
the shift in ocular dom inance to the nondeprived eye. This
suggests that m onocular deprivation strengthens co n n ec­
tions between callosal
» inputs and inhibitory neurons that
suppress activity arising in the deprived eye.
8 .2 .7 e R o le of H e b b ia n ( N M D A ) Synapses
Hebbian synapses are involved in the developm ent o f b in ­
ocular cells and in neural plasticity in general (Sections
6.5.1 and 6 .6 .3 ).
Seven days o f m onocular deprivation in kittens pro­
duced no detectable change in a biochem ical indicator o f
activity at inh ibitory presynapcic sites in cortical layer 4
(Silver and Stryker 2 0 0 0 ). This suggests that m onocular
deprivation acts at the poscsynapcic m em brane.
M onocular deprivation in rats tor 2 4 hours during the
critical period reduced the expression o f postsynaptic
A M PA receptors in cells in the visual cortex innervated by
the deprived eye (H eynen et al. 2 0 0 3 ). This change was the
same as in long-term depression ( I T D ) at N M D A synapses
in normal animals. Thus, the basic effect o f m onocular
deprivation is the induction o t long-term depression in cells
innervated by the deprived eye. Induction o f L T D requires
presynaptic activity. Consequently, m onocular enucleation
has less effect than m onocular suturing. The decrease in
A M PA receptors is n o t due to reduced sensory input, but
to lack o f correlation between presynaptic and postsynaptic
activity.
i
Dark rearing kittens to 6 weeks o f age arrested the loss
o f N M D A synapses that normally occurs after the critical
period, and thereby extended the period during which
visual experience influenced the form ation o f ocular d om i­
nance colum ns (Fox c t al. 1992; C zepita et al. 1994).
Subsequent exposure to light for 10 days allowed N M D A
synapses to decrease со adulc levels.
W hen N M D A synapses were inhibited by cortical infu­
sion o f a specific antagonise, monocularly deprived kittens

Figure 8.*- M ark F ir n an Bear. B orn in A lexand ria, V irg in ia , in 1 9 5 7 .
H e o b ta in ed а В .Sc. in psychology from D uke U n iv ersity in 1979
and л P h .D . in n cu ro h iolo g y from Brow n U n iv ersity in 1 9 8 4 . H is
p o std o cto ral w ork was at chc M ax-P lan ck In stitu t fu r H irn to rsch u n g , m
F ran k fu rt w ith \\”. Singer and at B row n U niversity w ith I. .N . C o o p er.
I Ic jo in ed the facu lty o f Brow n U niversity in 1 9 S 6 , w here he is now
professor o f n eu roscience. Fox P rofessor o l O p h th a lm o lo g y and Visual
S cien ces, and investigator lo r the H ow ard H ughes M edical Institute.
H e received chc A lfred P. S lo a n Award in 1 9 8 7 .
failed со show an ocular dom inance shift (Bear cc al. 1990)
(Porcraic Figure 8 .8 ). A lso,corcical cells becam e less respon­
sive со che norm al eye (C zep ita and Daw 1996). Infusion o f
an N M D A ancagonisc со one hemisphere prevented a
swicch of ocular dom inance o t binocular cells in chat hem i­
sphere after che occluder was moved со che ocher eye. Cells
in the visual corcex ot che untreated hemisphere showed che
usual transfer o f dom inance after reversal o f occlusion (G u
et al. 1 989).
Antagonises o f N M D A applied in early development
affect other types of synapse and lead to a general loss o f
responsivity and loss oforiencacion and direction selectivity
o f cortical cells in cats and ferrets (M iller et al. 1989a; Daw
19 9 5 ; Ram oa et al. 2 0 0 1 ). Therefore, loss o f ocular d om i­
nance plasticity after blockage ot N M D A receptors could
be due to these general deficits rather than a specific effect
o f loss ot N M D A synapses on cortical plasticity.
Kasamatsu c t al. (1 9 9 8 b ) found considerable ocular
dom inance plasticity in monocularly deprived kittens
receiving continuous cortical infusion o fa n N M D A antag­
onist. The m ajor effect was loss o f orientation tuning. They
concluded that inhibition o fN M D A synapses disrupts syn-
apcic transmission rather than experience-dependent co rti­
cal plasticity.
Roberts et al. (1 9 9 8 ) developed an antagonist that
acts specifically on the N R l receptor subunit of N M D A
synapses (Section 6 .5 .1 ). This antagonist decreased ocular
dom inance plasticity in m onocularly deprived ferrets
w ithout affecting other visual functions. Thus, loss o f
NMDA synapses directly affected cortical plasticity.
However, the procedure used by Roberts c t al. did n o t block
all N M D A receptors. Perhaps their com plete removal
would have produced more widespread effects.
M etabotropic receptors are also numerous in the visual
cortcx during the postnatal period. They arc also involved
in long-term depression o f responses in other parts o f the
brain. However, a m etabotropic antagonist had no effect on
the induction o f long-cerm depression by low-frequency
sim u latio n o t slices o t rat visual cortcx. Furtherm ore, rats
lacking m etabotropic receptors showed norm al long-term
depression at N M D A receptors (Saw tell et al. 1999). This
evidence suggests chac mecabocropic recepcors are noc
involved in the long-term depression ot responses to stim u­
lation o f a visually deprived eye. There is con flictin g evi­
dence about the role ot nitric oxide in cortical plasticity (see
Section 6 .5 .3 ).
8 . 2 . 7 f R o le o f N e u ro tro p h in s an d G e n e tic
T ra n sc rip tio n
Evidence reviewed in Section 6.7.2d shows that the forma­
tion o f ocular dom inance colum ns depends on com petition
between cortical afferents tor a neurotrophin secreted by
targ etccllsin the visual cortcx. The neurotrophins, described
in Section 6.4.3d , are N G F . B D N F , N T -3 , or N T-4/5.
Grow ing axons trom the two eyes com pete tor a limited
am ount o f B D N F . O n ly axons receiving sufficient B D N F
maintain access to binocular cells.
The brain-derived neurotrophic factor (B D N F ) is pro­
duced in postsynaptic cclls o f the visual system during the
critical period for developm ent o f ocular dom inance co l­
umns (Bozzi et al. 1995). Its production is enhanced by
neural activity. It binds to ligands on afferent axons and acts
as a retrograde messenger enhancing synaptic efficiency by
increasing release o f a synaptic transm itter in presynaptic
neurons (Thoenen 1 9 9 5 ; Liu et al. 1996).
The neurotrophin also induces the expression o f cell
proteins (G A P -4 3 and S C G 10) in the L G N , which control
che growch o f axons and synapses (H igo cc al. 2 0 0 0 ).
Neurocrophin also accivaces protein kinases. Three
kinases have been identified: cA M P-dependenc procein
kinase (P K A ), extracellular-signal-regulated kinase (E R K ),
and C a/calm odulin-dcpcndent protein kinase (C a M К II).
Activated kinases phosphorylate substrates that control
synaptic transmission (Scctio n 5.5 .2 c) and m orphological
development. They also activate genes responsible for pro­
tein synthesis. O cular dom inance plasticity that occurs after
m onocular deprivation is suppressed when activation o f any
o t these kinases is disrupted genetically or pharm acologi­
cally (G ordon et al. 1996;G lazew ski et al. 2 0 0 0 ; Beaver
et al. 2 0 0 1 ; Taha et al. 2 0 0 2 ; Berardi et al. 2 0 0 3 ).
The synthesis o f B D N F is regulated by neural activity.
Deprivation o t pattern vision during, and even after the
critical period, results in a decrease in B D N F in the visual
cortex o f the cat (Lein and Shatz 2 0 0 0 ). Dark rearing or
blockage o f neural activity during the critical period o f for­
mation o f cortical colum ns reduces the level o f B D N F in
the L G N and visual cortcx o f the rat (Schoups e t al. 1995).
In particular, protein synthesis is required for ocular dom i­
nance plasticity. Pharm acological suppression o t all protein
synthesis in the visual cortex o f m onocularly deprived mice
impaired the rapid shift in ocular dom inance (T aha and
Stryker 2 0 0 2 ).
In the postnatal period, the concentration o f B D N F in
retinal ganglion cells increases and B D N F is transported
trom retina to cortex. M onocular deprivation reduces the
level o f B D N F in the deprived retina, w hich introduces an
asymmetrical concentration of B D N F in ocular dom inance
colum ns. The shift in ocular dom inance after m onocular
deprivation was reduced when the balance ot B D N F o f
monocularly deprived rats was restored by adding B D N F
to the deprived eye or rem oving it trom the norm al eye
(M andolesi et al. 2 0 0 5 ). There is thus a close connection
between the effects o f m onocular deprivation in the retina
and its cffccts in the cortcx.
O cu lar dom inance colum ns did not develop when an
excess o f neurotrophins B D N F or N T -4/ 5 was applied to
the developing visual cortex o f cats or monkeys (C’abclli
ct al. 19 9 5 ; Hata et al. 2 0 0 0 ). Also, the critical period for
ocular dom inance plasticity occurred at an unusually early
age in transgenic m ice that expressed elevated levels o f
B D N F in the visual cortex (H anover e t al. 1999).
Excess o f these neurotrophins during the critical period
in rhe car m aintained or even restored responsiveness o f
binocular cells to stim ulation o f a deprived eye (Gillespie
et al. 2 0 0 0 ). However, B D N F does not simply restore rhe
norm al functions o f the visual cortex. Infusion o f B D N F
into cortical area 18 o f norm al cats during the critical period
produced a reversal ot the norm al ocular dom inance bias
from the contralateral eye to the ipsilateral eye. It also pro­
duced a loss ot orientation selectivity in cortical cells.
Infusion o f B D N F during the period o f m onocular depriva­
tion produced a paradoxical shift o f ocular-dom inance
toward the deprived eye. In adult cats, B D N F had no effect
on ocular dom inance or orientation selectivity (Galuskc
et al. 2 0 0 0 ).
The nerve growth factor (N G F ) is also involved in co r­
tical plasticity. Infusion o f extra N G F in m onocularly
deprived rats prevented shrinkage ot L G N neurons and
shifts in ocular dom inance in the visual cortex (Bcrardi
et al. 1993a, 1 9 9 3 b ; D om enici et al. 1993). Also, in infused
rats, the tuning characteristics o f cortical cclls did not
change and there was no behavioral evidence ol amblyopia
in the deprived eye (D om enici et al. 1 9 9 1 ; M affei et al.
1992). In m onocularly deprived rats, visually evoked
responses in the ipsilateral visual cortex were reduced, but
this reduction did not occur after ventricular infusion o f
N G F (Yan et al. 1 996).
In the cat, injection o f N G F during the critical period
facilitates recovery o f binocularity and visual acuity follow­
ing a period o f m onocular deprivation (C arm ignoto et al.
1 9 9 3 ; Fiorentini ct al. 1995). Oddly, cortical infusion ot
N G F in the visual cortex o f the adult cat restored the capac­
ity o f the cortcx to manifest an ocular dom inance shift
when one eve was occluded (Gu c t al. 1994; Galuskc c t al.
2 0 0 0 ). For a review o f N G F receptors, see Meakin and
Sh ooter (1 9 9 2 ) and G u (1 9 9 5 ).
O th er investigators found that brain-derived neu-
rotrophic factor (B D N F ) and neurotrophin N T -4/ 5 (trkB
ligands) are more im portant than N G F in the developm ent
ot ocular dom inance colum ns in cats, but they used more
local application o f neurotrophins and anatom ical rather
than elcctrophysiological assessments (C'abclli et al. 1995;
Riddle ct al. 1995).
C h on d roitin sulphate proteoglycans (C S P G s) in the
extracellular m atrix in h ib it axonal and dendritic growth,
in the critical period, the expression o f C S P G s is controlled
by visual experience. Toward the end o f the critical period
C S P G s condense round the soma and synapses o f cortical
cclls. They inhibit cortical plasticity and therefore stabilize
neuronal patterns in the adult visual cortcx. D ark rearing
prevented the expression o f C S P G s in rats. This could co n ­
tribute to the prolongation o f the critical period in dark
rearing (Section 8.3 .1 b ). The removal o f C S P G s restored
ocular dom inance plasticity in m onocularly deprived adult
rats (Pizzorusso et al. 2 0 0 2 ).
The transcription factors CREB (calcium /cA M P
response elem ent binding proteins) belong to the class o f
proteins required for neural plasticity. A ctivity o f these p ro ­
teins is regulated by neuronal activity and neurotrophic fac­
tors through the m ediation o fC a M К 11. The С R E B proteins
in turn regulate transcription o f specific genes. There is high
C R E B activity during the critical period. M onocular depri­
vation in infant m ice induces C R E B mediated expression
o f the gene lacT, in the visual cortex. This induction is
reduced after the end o f the critical period (Pham et al.
1 9 9 9 ; M ower et al. 2 0 0 2 ). Liao et al. (2 0 0 2 ) inactivated
C R E B during the critical period. Inactivation before m on­
ocular deprivation prevented loss o f responses to stim ula­
tion o t the deprived eye. But an eye that had been deprived
before inactivation still recovered. Thus, C R F .B is required
for loss o f function but not for recovery. A ctivation o f
C R F .B in adult m ice rendered them susceptible to m onocu ­
lar deprivation (Pham c t al. 2 0 0 4 ). M ice with reduced
C R F .B levels have impaired long-term memory.
Evidence from the rat suggests that the gene Cpg 15 co n ­
trols the term ination o f the critical period. Expression o f
this gene peaks during the critical period and then declines.
D ark rearing delays this decline (Lee and Nedivi 2 0 0 2 ).
The hom coprotcin O tx 2 is involved in the development
o f the head in the em bryos o f all animals. In mammals,
before the onset o f the critical period, it becom es restricted
to the visual pathways from retina to cortex. W ith the onset
of' che critical period ic is caken up by P V G A BA ergic
interneurons— the interneurons involved in cortical plas­
cicicy (Sugiyama ec al. 2 0 0 8 ). Binocular enucleaced and
dark-reared m ice had a reduced level o f O cx2 in PV neu­
rons, which delayed the macuracion o f chese cells and the
onsec o f the critical period. Delivery o f O tx l to the visual
corcex o f dark-reared m ice rescored rhe macuracion o f PV
cells. Also, delivery o f O c x l со norm al infanc m ice acceler-
accd che onsec o f che critical period tor shift in ocular dom i­
nance. It also acceleraced che enclosure o f P V neurons by
che extracellular macrix, which indicaces the end o f the crit­
ical period. R eduction o f cortical O c x l delayed chc ccrmi-
nacion o f che critical period.
8 .2 .7 g C o r tic a l P la s tic ity an d D c n d r itic S p in es
In norm al animals, dendrices ot spiny stellate cells tend to
remain w ithin their own ocular dom inance colum n, because
they are at a com petitive disadvantage it chey encer the
colum n o fth e other eye. The cerminal a rb o rso f inpucs from
a deprived eye on spiny scellace cells are smaller and make
fewer synapses chan chose in a norm al eye. The cerminal
arbors o t che nondeprived eye are larger chan norm al and
make more chan chc normal num ber ofsvnapses(Friedlander
ec al. 1 9 9 1 ).
Because o f cheir reduced inpuc from che deprived eye,
spiny scellace cells serving a deprived eye are invaded by den­
drices trom che nondeprived eye. These dendrices spread со
an unusual degree inco the adjacenc ocular dom inance co l­
umns o f che deprived eye. The scellace cells serving che
deprived eye chus receive their dom inanc inpuc from rhe
nondeprived eye (Kossel ec al. 1995).
Ic was previously choughc rhac the shift in ocular d om i­
nance caused by m onocular deprivacion is iniciatcd by
changes in che relacive strengchs o f thalam ocorcical inputs
from the tw o eyes in layer 4 . M ore recent evidence suggests
chac chese changes are preceded by changes in incracorcical
circuitry outside layer 4.
C hanges in che upper supragranular cortical layers pre­
cede and may direcc che subsequenc reorganization o f thal­
amocorcical conneccions associaced wich m onocular
deprivacion. Trachcenbergec al. (2 0 0 0 ) found thac 2 4 hours
o f m onocular deprivacion produced loss o f responses from
the deprived eye only in cortical layers outside layer 4.
Longer periods o f deprivation were required to produce
effects in layer 4. Shorc-ccrm loss could arise ( l ) because
cells innervaced by che deprived eye lose no longer-inHucncc
cells in che extragranular layers, or (2) from changes in lac-
eral conneccions becween cells in excragranular layers.
Trachtenberg and Stryker (2 0 0 1 ) produced evidence
for the second possibility, alchough ic docs noc rule our a
contribucion from che firsc possibility. They observed large
losses in horizoncal conneccions becween ocular dom inance
colum ns in che upper layers o f che visual corcex o f kiccens
exposed to only 2 days o f strabismus.
These changes outside layer 4 are associated wich changes
in the dynamics and density ol dendritic spines. Thus,
3 days o f m onocular deprivation in mice during the critical
period increased the m otility ol dendritic spines outside
layer 4 (G ray ec al. 2 0 0 4 ). This increased mocilicy presum­
ably represents the reshaping o f synapses during m onocular
deprivation. M onocular deprivation also reduced spine
density in the excragranular layers o f the visual cortex o f
mice (M aragacc al. 2 0 0 4 ).
N either change was evident in che m onocular segmenc
ot che visual corcex, which shows chac chey depend on com -
pecicion becween inpucs from che cwo eyes. The changes
seem со be due со increased accivicy o f che proceolytic
enzyme tPA/plasmin. Changes in spine mocilicy occurred
in norm al m ice after applicacion o t chis enzyme during the
cricical period o f ocular dom inance plascicicy. M onocularly
deprived m ice lacking chis enzyme did noc show the change
in spine density. Processes controlling spine mocilicy were
reviewed in Seccion 6.4.4.
8 .2 .7 h N e u ro m o d u la to rs and C o r tic a l P la stic ity•
The neocorcex receives inputs trom a variety o t subcortical
areas. Each input involves a discincc neurocransmicter, as
described in Section 5.5.2g. Examples are acetylcholine,
dopam ine, noradrenaline, and seroconin. C o rtical cells
contain a variety o f receptors for each o f chese cransmicrers,
which act as neurom odulators rather than convey sensory
inform ation.
C arccholam incs, particularly noradrenaline, have
been im plicated in che concrol o f neural plascicicy in che
developing corcex ot racs. N oradrenergic axons are among
che firsc со innervace che cerebral corcex, and reach peak
levels in che second poscnacal m onth. In the adulc brain,
noradrenergic axons originacing in che locus coeruleus in
the dorsal pons seem to provide a diffuse, nonspecific inner­
vation o f che ccncral nervous syscem (I.cvicc and M oore
1979).
After che corcex was depleced o f cacecholam ines by
incravencricular injection ot 6-hydroxvdopam ine, m onocu­
larly deprived kitcens recained chc normal proporcion o f
binocular cells in area 17, and cells serving che norm al eye
did noc becom e dom inanc (Kasamacsu and Peccigrew 1979;
Shirokawa ec al. 1 9 8 9 ). Perfusion o f noradrenaline into the
visual corcex o f kiccens for one week shifted ocular dom i­
nance со the contralateral eye but only when che kiccens
were allowed visual experience (Kuppermann and
Kasamacsu 1 9 8 4 ). C orcicai cells showed a shift in ocular
dom inance in anesthecizcd kiccens exposed со 2 0 hours o f
m onocular stim ulation, buc only when che corcex was
direcrly infused wich noradrenaline (Im am ura and
Kasamacsu 1991). Also, kiccens chat had been monocularly
deprived tor one week beginning at age 4 weeks showed
accelerated recovery o f chc norm al paccern o f ocular dom i­
nance when che corcex was intused with noradrenaline.

Figure я. 10 . N igel Dau\ B o rn in L o n d o n , E n glan d , in 1 9 3 3 . H e ob tain ed
a BA in m athem atics; Trom C am b rid g e U niversity in 1 9 5 6 and a P h .D .
from Jo h n s H o p k in s U n iv ersity in 1 9 6 7 . B etw een 1 9 6 9 and 1 9 9 2 he
held acad em ic a p p o in tm en ts in th e d ep artm en t o l physiology and
biophysics a t W ash in g ton U n iv ersity in S t. L ou is. Sin ce 1 9 9 2 he has
been professor o f op h th alm o lo g y , visual sciences, and n cu ro b io lo g v at
Yale U niversity. H e received th e A R V O Friedenw ald Award in 1995-
Figure s. 11. R on illd S. H arw erth. B orn in A tw ood , K ansas, in 1 9 3 9 . H e
ob tain ed a B .S c. from the U n iv ersity o f H o u sto n in 1 9 6 2 and a P h.D .
in b iom ed ical scien ces from the U n iv ersity o f Texas, H o u sto n , in
1 9 7 1 . In 1 9 7 0 he jo in ed th e faculty o f th e C o lleg e o f O p to m e try at
th e U n iv ersity o f H o u sto n , w here he is now professor o f physiological
o p tics. H e received the G len n A . Fry Award in 1 9 8 0 and the G arland
\X'. C lay Award in 1 9 8 3 from the A m erican A cadem y o f O p to m etry .
He becam e Jo h n and R eb ecca M o ores Sch olars Professor in 1 9 9 6 .
E F F E C T S O F V IS U A L D E P R IV A T IO N
8 .3 ,1 C R I T I C A L P E R I O D IN S U B P R I M A TP.S
8 .3 .1 a D u ra tio n o f th e C r itic a l Period
The eyes ol cats are closed until about 10 days after birth.
The period during w hich cortical cclls arc susccptiblc to
m onocular occlusion begins in the 4 th week. In earlier stud­
ies, neural plasticity was found to remain high until the 8th
week and end at about the 12th week (D ew s and W iesel
1970; Hubei and W iesel 1970). The critical period for
effects ofstrabism us is sim ilar ro that for the effects o f m on­
ocular occlusion (L ev itt and Van Sluyters 1982). A similar
critical period was reported in rats and ferrets (Fagiolini
et al. 1 9 9 4 ; G uirc et al. 1999; Issa c t al. 1999).
O lson and Freeman (1 9 8 0 ) sutured one eye o f kittens
lor 10 days at various periods during the first 4 months.
They measured the proportion o f cortical cells that failed to
respond to the deprived eye as a function ol the age at which
deprivation was started. The susceptibility to m onocular
deprivation peaked between postnatal days 2 8 and 4 8 and
subsided through the end o f the 4th m onth. At 4 weeks,
binocular cclls o l kittens deprived o l vision in one eye for
only 12 hours spread over 2 days showed a massive shift in
ocular dom inance to the nondcprived eye. However, the
normal pattern o f ocular dom inance was restored after
7 weeks o f binocular vision (M alach et al. 1984). During
che peak period, eye closure for 3 or 4 days induced a per­
m anent loss o l binocular cells and a deficit in stcreoacuity
(T im n cy 1 9 9 0 ) (P ortrait Figure 8 .1 2 ).
i:i*urc«.12. В п ап Ttnmcy. B orn m Su n d erlan d , E n glan d , in 1 9 4 7 .
H e ob tain ed a B .A . in psychology from E d in bu rgh U n iv ersity in 1 9 6 9
and a P h .D . w ith R . M o ra n t at B ran d eis U niversity in 1 9 7 3 . Betw een
1 9 7 3 and 19 7 S he con d u cted p o std o cto ral work a t Q u een s U niversity
and D alh o u sic U niversity. In 1 9 7 S he gained an academ ic ap p o in tm en t
at the U n iv ersity o f W estern O n ta rio , w here he is now professor o t
psychology and neu roscience.
• 415
 Ic is generally agreed chat about 2 hours o f binocular
vision com bined with 5 hours o l m onocular vision during
che cricical period is sufficient for che developmenc o f
norm al gracing acuity cats (M itch ell ec al. 2 0 0 3 , 2 0 0 9 ).
However, only one o f chrcc cacs creaccd in chis wav dcvel-
/ 4
oped stereoscopic vision. Thus, longer periods o f binocular
vision are required tor che developmenc o f scereopsis chan
for che developmenc o f norm al acuity.
Also, allowing binocularly dark-reared kiccens со see
wich only one eye for a few hours during che peak o f rhe
cricical period produced a discincc shift in ocular dom inance
ro rhe open eye, w hich was evidenr 2 days lacer (Peck and
Blakem ore 1 9 7 5 ).
In earlier studies, che cricical period o f cacs was reporced
со end by che 4ch m onch. Lacer scudies found some effects
o f m onocular occlusion on ocular dom inance when applied
betw een rhe 5ch and 7ch monchs (Cynader and M itchell
19 8 0 ; Cynader ec al. 1 9 8 0 ). D a w ec al. (1 9 9 2 ) agreed chac
che critical period for developmenc ot binocular cells in
layer 4 o f che cacs visual corcex excends со che 7ch monch
buc found significant shifts in ocular dom inance in ocher
layers after m onocular deprivacion applied in che llc h
monch. The critical period lascs longer for binocular cells in
area 17 chan for chose in che excrascriace corcex (che lateral
suprasylvian area) (Jo n es cc al. 1984b ). Ic has also been
reporced chac che cricical period for loss o f binocularicy ends
before che critical period for changes in recepcive-field
scruccure (Berm an and M urphy 1 9 8 2 ).
In norm al cats,depth-discrim ination thresholds assessed
on a jum ping stand arc much lower wich binocular chan
wich m onocular viewing. Cacs wich one eyelid sutured for
more chan 31 days from che tim e che eves opened showed
no binocular superiority. Cacs m onocularly deprived ac
4 monchs showed binocular su p erio rly (T im nev 1983).
The cricical period for developm ent o f binocularity in
Fcrrecs excends becween poscnacal days 35 and 7 0 . Liao
ec al. ( 2 0 0 4 ) found chac m onocular deprivacion from birch
produced perm anent loss o t binocularity and oricnracion
cuning in corcical cclls serving the deprived eye. However,
corcical cells fully recovered when binocular vision was
rescored after 3 weeks o f m onocular deprivacion chac scarred
ac day 4 9 . Thus, recovery occurred after che end o f che crici­
cal period ifn o rm al vision had been presentduring che early
part o t the cricical period.
Sawcell ec al. ( 2 0 0 3 ) found chac 3 days o f m onocular
deprivation in m ice shifted ocular dom inance only when
applied ac an early age. There was increased activity from
stim ulation o f rhe nondeprived eye and reduced activity
from che deprived eye. Adulc m ice showed som e shift after
5 days o f deprivation. Buc this shift involved only an increase
in the norm ally weak ipsilateral cortical activity evoked by
stim ulation o f the open eye. There was no reduction o f
activity from the deprived eve. In y e t al. (2 0 0 6 ) found some
recovery o f visual acuity in m onocularly deprived eyes o f
rats even in the adult.
Binocular cells have closcly m atched orientation and
spatial-frequency selectivity in their m onocular receptive
fields. In m ice, che rcccpcivc fields are initially noc macched.
They becam e macched only i f the m ice had binocular expe­
rience during a critical period ending at postnatal day 31
(W an gec al. 2 0 1 0 ).
8 .3 .1 b P o s tp o n e m e n t o f th e C ricica l
P erio d in C a ts
In kittens reared in the dark for up to 10 monchs, subse­
quent m onocular occlusion caused a marked shift in ocular
dom inance to the open eye (T im n cy c t al. 1980; M itchell
and T im n ey 1982; M ow er and C hristen 1 9 8 5 ; Beaver et al.
2001b ).T cn m onths is well beyond the normal critical
period. Cynader (1 9 8 3 ) found some effects o f m onocular
occlusion in cats that had been dark reared for 2 years. After
term ination o f darkness, che period o f susceptibility со
m onocular deprivacion lasced abou t 6 weeks.
Tli us, che cricical period occurs later if the animal is kept
in the dark. But the darkness must be com plete. M onocular
deprivation produced only slight cortical changes in kittens
reared for betw een 4 and 12 m onths with binocular sutures
th at provided diffuse illum ination through che eyelids
(M ow er ec al. 1981b ). Six hours o f exposure со a normal
visual environm ent in 6-week-old kittens that had been
dark reared for the first 5 m onths, elim inated the delaying
effects o f dark rearing (M ow er e t al. 1983). Thus, term ina­
tion o f rhe critical period depends on stim ulation. However,
stim ulation need n o t be prolonged, and diffuse illum ina­
tion seems to be sufficient.
Although m onocular deprivation in adult rats did not
induce shifts in ocular dom inance, m onocular deprivation
preceded by 10 days ot total binocular deprivation resulted
in a shift (H e et al. 2 0 0 6 ). The effect o f tocal deprivacion
lasted for several days. Thus, cocal lighc deprivacion delays
cerminacion o f che cricical period and may rescore corcical
plasticicy in the adult rat.
There is a large increase in inhibitory G A B A ergic inputs
onto pyramidal cells at the end o f the critical period (Section
8 .2 .7 d ). Dark-rearing slows the m aturation o f inhibitory
circuits in rats (M orales e t al. 2 0 0 2 ; D i C risto et al. 2 0 0 7 ).
Light deprivation in the adult rat reversed inhibitory cir­
cuits to an immature state. This reduced functional G A B A
inh ibitory synaptic density and thereby restored ocular
dom inance plasticity ( Huang c t al. 2 0 1 0 ).
M ice subjected to a few days o f m onocular deprivation
during che critical period showed a shift in ocular dom i­
nance to the nondeprived eye. Binocular vision recovered
after the closed eye was allowed to see. However, these m ice
were highly susceptible to m onocular deprivation o f that
same eye when they were adult (H ofer ec al. 2 0 0 6 ). Thus,
early m onocular deprivation produces long-lasting changes
that are specific to the deprived eye, even after binocular
vision has been restored.
previously deprived eye fully recovered. In a normal envi­
ronm ent, the acuity ot the deprived remained lower than
that o f the o ther eye.
Although reverse occlusion leads to som e recovery o f a
previously deprived eye, it is at the expense o f a loss o f visual
capacity in the other eye. Furtherm ore, when sight is
restored to both eyes after a period o f reverse suturing, the
reverse-sutured eye loses ics newly gained capacity, and the
o ther eye recovers. Thus, the gain achieved by reverse sutur­
ing is not perm anent in rhe cat (M itch ell 1988b).
8 .3 .2 C R I T I C A L P E R I O D IN M O N K E Y S
By the sixth postnatal day, V I o f macaque monkeys co n ­
tains an adult-like proportion o f disparity-sensitive cells,
although the cells are poorly tuned to spatial frequency and
are n o t very responsive (C h in o et al. 1997). The cells mature
in rhe first 4 weeks, by w hich tim e monkeys begin to show
evidence o f stereopsis.
M onocular enucleation in rhesus m onkeys at one week
o t age elim inated ocular dom inance colum ns in layer 4 C S
leaving a uniform autoradiograph and uniform cytochrom e
oxidase staining (H o rto n and H ocking 199 8 b ). In colum ns
belonging to the missing eye, layers 4 C a and 4 a were much
reduced. M onocular enucleation at age 12 weeks produced
only mild shrinkage o f ocular dom inance columns.
M onocular enucleation at any age did not affect cytochrom e
oxidase stripes in V 2.
M onocular occlusion in the rhesus m onkey from rhe
first week o f life causes a strong shift in ocular dom inance ot
cells in V I ro rhe open eye and shrinkage o f colum ns
devoted to the deprived eye (H o rto n and H ocking 1997).
M onocular occlusion from an age o f between 7 and 14
m onths had no influence on ocular dom inance colum ns in
cortical layer 4 C , but there was still som e shift o f ocular
dom inance in cells o t the upper cortical layers (Blakem ore
et al. 19 7 8 ; LeVay et al. 1980). M onocular deprivation in
adult m onkeys has no effect on ocular dom inance.
Reverse suturing in a Cebus monkey after monocular
occlusion for the first 2 4 davs
ф
led to a reversal o f dominance
to the other eye (Swindale ct al. 1981). Reversal o f dominance
occurred even after 90 daysot m onocular occlusion (Crawford
c t al. 1989), but no recovery o f visual function was found
after 19 months o f occlusion (H arw erth et al. 1984).
The critical period in the m onkey depends on the type
o f visual function. Thus, loss o f scotopic sensitivity occurred
only when m onocular deprivation was initiated before
2 m onths o f age. Spectral and contrast sensitivities were
affected when deprivation was initiated before 5 m onths ot
age. Two weeks o f prism -induced strabismus reduced the
disparity sensitivity o f cells in V I m ore severely when
applied at the age o f 2 weeks than when applied at the age
o f 6 weeks (Kum agam i et al. 2 0 0 0 ).
Loss o f binocular vision occurred even when deprivation
was initiated as late as 25 m onths (H arw erth et al. 1990).
A nisom etropia induced in the neonate m onkey by placing
a 10-diopter lens in front o f one eye for 3 0 days produced
little effect in the defocused eye. W h en continued for 6 0
days or more it produced persistent amblyopia in the defo-
cuscd eye as revealed by loss o f contrast sensitivity for high
spatial frequencies (Sm ith et al. 1985b ).
Vcrgcncc eye movements recovered fully after che
eyes o f monkeys were realigned following early surgically
induced esotropia, although stereoacuity remained
deficient (H arw erth et al. 1997).
Som e functions mature before others or are less affected
by deprivation than others. It seems to be a general principle
that the critical period for functions processed at lower
levels o fth e nervous system ends earlier than that for func-
tions processed at higher levels. The critical period for learn-
ingcom p lex skills extends over the lifetime.
8 .3 .3 C R I T I C A L P E R I O D IN H U M A N S
M onocular deprivation in humans occurs as a consequence
ot m onocular enucleation, unilateral cataracts, unilateral
diseases o f the retina, strabismus, or anisom etropia.
M onocular vision or strabismus that develops in an older
child or adult docs not produce any permanent loss o f bin­
ocular functioning when the condition is corrected. E. L.
Sm ith et al. (1 9 8 0 ) had six human adults with normal vision
wear a m onocular occluder for 12 days. This produced
a small decrease in stereoacuity tor a period o t up to 2 hours,
which was probably due to a tem porary inability to co n ­
verge the eyes accurately.
'Ih c critical period for developm ent o f amblyopia in
humans seems to end earlier than chat tor developm ent o f
binocularity. Jacobson e ta l. (1 9 8 1 ) found th at infants with
esotropia from shortly after birth developed differences in
acuity betw een the two eyes at a mean age o f 2 0 weeks. O n e
infant with esotropia from 10 m onths o f age developed
signs o f amblyopia 4 weeks later. A ccording to this evidence,
the critical period for the developm ent ot amblyopia extends
from the age o f about 4 m onths to at least 12 months.
8 .3 .3 a C o r r e c tio n fo r S tra b ism u s
Covering a strabism ic eye to avoid diplopia was practiced in
ancient times. The use o f face masks with decentered view­
ing holes to correct strabismus also has an ancient origin.
The face mask procedure was systematized by Em ile Javal
( 1 8 3 9 - 1 9 0 7 ) (see Charnw ood 1951).
Infants with severe strabismus over several years never
recover stereoscopic vision, even when the strabismus is
corrected by surgery.
Banks e t al. (1 9 7 5 ) obtained an estim ate of the critical
period for normal visual developm ent in humans by testing
binocular fun ction ing in 2 4 adults in whom strabismus in
excess o f 1 0 ' had been surgically corrected at various ages.
C ongenital csotropcs who had corrective surgery before the
age o f 3 years tended to develop more normal binocular
functions than those who had the correction at a later age
(see also Enoch and Rabinow icz 1976). For subjects in
whom strabismus developed after the age o f 4 years, surgery
produced com plete restoration o f binocular fun ction ing no
m atter when the surgery was perform ed. Banks et al. con­
cluded that the sensitive period during which normal bin­
ocular inputs are required for binocular functioning in
humans is betw een the ages o f 1 and 3 years.
Birch c t al. (1 9 9 0 ) assessed che effects o f surgery and
eye-occlusion therapy on acuity, eye alignm ent, and stere­
opsis in a group o f 8 4 esotropes under 1 year o f age. Three
patients who responded adequately to optical and occlusion
therapy achieved near normal stereopsis and acuity. Their
esotropia probably arose from anisom etropia. The remain­
ing patients required surgery, w hich, in about 88 % o f cases,
resulted in good eye alignm ent, although some patients
required secondary surgery. N one o f the patients undergo­
ing surgery developed postoperative random -dot stercoacu-
ity b etter than 2 0 0 arcsec, and only 35 % showed this level o f
perform ance (see also A tkinson et al. 1991). However, most
o f the patients showed normal developm ent o f acuity in
both eyes after surgery followed by occlusion therapy.
In an early study o f 8 2 cases o f surgical correction, b in ­
ocular vision, as indicated bv
ф
binocular fusion and coarse
stereopsis, was n o t restored unless surgery was performed in
the first year (D eller 1 988). in another study, five o f seven
patients in whom early-onsetesotropia was corrected during
rhe first 19 weeks achieved scereoacuity o f between 4 0 and
4 0 0 arcsec when tested 2 years later (W rig h t e t al. 1994).
A bout 4 0 % o f a group o f infantile esotropes had some
stereovision when tested at 5 years o f age (Bireh et al.
(1 9 9 5 ). Those who had been surgically corrected before
they were 8 m onths old had foveal stereoacuity o f about 60
arcsec. Those corrected betw een 9 and 12 m onths o f age
had stereoacuity o f between 6 0 and 2 0 0 arcsec, and those
corrected betw een 13 and 16 m onth s had stereoacuiries in
excess o f 2 0 0 arcsec. However, in a later study, restoration o f
som e stereopsis in infantile esotropes under 2 4 m onths o f
age was tound to depend m ore on the duration ot strabis­
mus rather than on the age at which surgical correction was
applied (B irch et al. 2 0 0 0 a ).
Eizenman et al. (1 9 9 9 ) measured visual evoked p oten­
tials (V E P ) in response to dynamic random -dot stereo­
grams in children w ith early-onset esotropia. For eight
children who had their strabismus surgically corrected
before the age o f 12 m onths the V E P showed evidence that
the images in che tw o eyes were fused. Six o f eight children
wich correction after 17 m onths showed evidence o f fusion.
Fusion does not necessarily mean chac che children had
stereoscopic vision.
I hus, early surgery may produce som e restoration o f ste­
reopsis but, in any case, surgery is justified by the am eliora­
tion o f amblyopia and by che cosmecic im provem ent (see
Smich et al. 1 991).
M ohindra cc al. (1 9 8 5 ) measured acuicy and stereopsis
in 19 esotropic infants during the first 3 years o f life. Those
with prismatic correction showed evidence o f coarse stere­
opsis during this time. However, none o f che 19 esotropes
had stereopsis after che age o f 6 years w hether they had
worn a prismatic correction or not. Thus, the full adverse
effects o f infantile esotropia are n o t evident until after the
third year.
8 .3 .3 b C o r r e c tio n for C a ta ra c t
There has been a good deal o f debate about the best age to
correct congenital cataracts by surgery. A com plicating
factor is chac many infancs wich bilaceral or unilaceral cara-
ract have associated visual detects, such as nystagmus, and
strabismus, which persist after the cacaraccs have been
removed.
A survey o f 231 cases ac che W ilm er Inscicuce becween
1925 and 1943 revealed chat good vision (20/70 or better)
was achieved in only 9% o f cases when surgery was performed
before che age o f 2.5 years and in 69 % when it was performed
after that age (Ow ens and Hughes 1948). The advantage o f
later surgery was evident even in patients with no associated
defects (Iiaglcy 1949. According со chese rcsulcs, ic is bcccer
со delay surgery for congenital cataract. The exact ages at
operation were not specified in these studies.
In a later study, eight intants with congenital unilateral
cataracts developed reasonable acuity in the affected eye
when operated on before che age o f 4 0 days (Beller ec al.
1981). In anochcr study, 5 o f 10 children developed good
acuity when cataract surgery was performed before the age
ot 4 m onths. There was less recovery o f acuity in two ch il­
dren operated on between the ages o f 4 and 5 m onths (R o bb
ec al. 1987). Subjects in these tw o studies did not recover
binocular vision, perhaps because the good eye w asoccludcd
tor several hours each day for many m onths.
Pracc-Johnson and Tillson (1 9 8 1 ) removed unilaceral
cacaraccs trom three intants before the age o f 5 monchs, and
bilaceral cacaraccs from chrec infancs becween th e ages o f 7
and 11 monchs. They all developed reasonable acuicy in che
affecced eyes. However, all chese paciencs had ocherwise
norm al eyes, and the bilateral cataracts did not becom e
opaque until they were several m onths old.
W righ t et al. (1 9 9 2 ) tound that 5 o f 13 patients who
had surgery for m onocular congenital cataracts before the
age o f 9 weeks developed vergence eye movements. O n e
patient developed stereoacuity o f 2 0 0 arcsec.
8 .4 A M B L Y O P IA
8.4.1 T V P E S О F A M В LY O PIA
W hen monocular deprivation is applied over a long period,
the deprived eye manifests amblyopia, literally "blunt vision.”
The defect has been known for ac least 2 0 0 vcars.
In 17 6 4 , Thom as Reid, professor o f m oral philosophy in
Glasgow, reported that 2 0 people with strabismus had
defective sight in one eye.
ЛИ form s o f amblyopia involve a loss o f contrast sensi­
tivity for high spatial frequency gratings on the central
retina, and weak or absent stereopsis. Although m isaccom -
modation may be one cause o f amblyopia, spectacles can n ot
cure it. Am blyopia does n o t involve retinal defects—
receptors are oriented normally, foveal pigment density is
norm al (D elin t c t al. 1 9 9 8 ), as is the elcctrorctinogram
(Hess and Baker 1 9 8 4 ). Evidence reviewed in Section 8.2
shows that the physiological effects of m onocular depriva­
tion are m ost severe in the visual cortex. Psychophysical evi­
dence, also, shows that loss of contrast sensitivity in
amblyopia is largely o f cortical origin (sec Kiorpes c t al.
1999) (Portrait Figure 8 .1 4 ).
Four types o f am blyopia are defined by their etiology.
Deprivation amblyopia is due to loss o f form vision
because o f a cataract, ptosis, or retinal disorders.
Anisometropic am blyopia is due to unequal refraction in
the tw o eyes resulting from unequal eye growth (axial
anisom etropia) or corneal defects. The greater the
degree o f anisom etropia, the greater is the depth o f
amblyopia and the greater is the loss o f acuity in the
affcctcd cvc and o f binocularity and stereopsis.
Hyperopic anisom etropes show a grater loss than
Figarc8.i-«. Lynne K iorpes. B o rn in N ew Jersey in 1951 She ob tain ed a BA
at N orth eastern U niversity in 1 9 7 3 and a P h .D . in psychology w ith 1).
T eller from the U n iv ersity o f W ash in g to n in 1 9 S 2 . A fter p o std o cto ral
work a t the U n iv ersity o f W ash in g ton she ob tain ed an acad em ic
p osition a t N ew York U niversity, w here she is now a professor.
4
myopic anisom ccropcs (Rucsrcin and C orliss 1999;
Levi et al 2 0 1 1 ).
Persistent blur o f one retinal image produced by
continuous application o f atropine to one eye o f
monkeys during 10 postnatal m onths resulted in loss
o f contrast sensitivity in that eye (K iorpes et al. 1987).
Refractive error due to pathological dilation o f one
pupil in humans (A die syndrom e) can also produce
amblyopia (F irth 1999).
Strabismic amblyopia is due to early m isalignm ent o f
one eve.
4
M eridionalatnblyopia is due to an uncorrectcd
astigmatism. It affects vision only for images oriented
along the astigmatic axis.
Amblyopia occurs in about 3% o f the population.
Strabism ic and anisom etropic amblyopia occur with about
equal frequency (Flom and Neumaier 1966).
W h en disruption was applied equally to both eyes of
kittens, by alternating occlusion or by prismatic dissocia­
tion o f visual inputs, both eves developed normal or near­
normal acuity. However, there was a reduced num ber o f
binocularlv driven cells and loss o f stereopsis (Blake and
Hirsch 1975). Similarly, in a sample o f 1 14 human infants
with untreated alternating esotropia, grating acuity, as m ea­
sured by preferential looking, remained normal in boch eyes
although stereopsis was lost (B irch and Stager 1985).
However, Day et al. (1 9 8 8 ) found a small equal loss o f grat­
ing acuity in both eyes o f 1-year-old alternating esotropes,
as assessed by co rtical potentials (V E P ) evoked by a grating
with swept spatial frequency that alternated in phase
(Section 7.2 .1 b ). The preferential-looking procedure used
by Birch and Stager may not have been able to detect the
small difference recorded by D a y e t al.Scrabismic am blyo­
pia is more prevalent am ong esotropes (inward deviation)
than am ong cxotropcs (outward deviation). The cffccts on
the visual cortex o f cats are also greater for induced esotro ­
pia than for induced cxotropia (Scctio n 8 .2 .3 a ). Three rea­
sons for this difference have been suggested.
1. Exotropia develops m ore slowly than esotropia.
2. Amblyopia does not occur in alternating strabismics,
and exotropia is more likely to be alternating than
unilateral.
3. In esotropes, foveal stimuli in the deviating eye com pete
with stim uli in the dom inant temporal hemifield of the
other eye. In cxotropcs, foveal stimuli com pete with
stimuli in che nond om inant nasal hemifield o f the other
eye (Bucklcy and Scabcr 1982; Fahic 1987).
For reviews o f am blyopia sec Levi ( 1 9 9 1 ), Ciuffreda
et al. ( 1 9 9 2 ), and M cK ee et al. 2 0 0 3 ). Vie shall now see that
different types o t amblyopia produce different symptoms.
 A uditory defects due со monaural deprivation, known
as amblyaudio, were described in Section 7.7.
8.4.2 L OS S O F C O N T R A S T S E N S I T I V I T Y
AND A C U I T Y
8 .4 .2 a A n iso m e tro p ic and Strab ism ic
A m blyopia C o m p ared
Sym ptom s o f amblyopia include a reduction in contrast
sensitivity, som etim es for all spacial frequencies and som e­
times for only high spatial frequencies (Hess and Howell
19 7 7 ; Bradley and Freeman 1 9 8 1 ). There is also a loss o f
gratingacuity (H arw erth e ta l. 1 9 8 3 a ; K ratzand Lehm kuhle
1983) and impaired perform ance on vernier acuity and
o ther hyperacuicy casks (Levi and K lein 1982a; Bedell et al.
19 8 5 ; Bradley and Freeman 1985a).
These sympcoms differ betw een strabism ic and ani-
som etropic amblyopia in the following ways.
1. Loss ofcontrast sensitivity an d hyperacuity In
anisom etropic am blyopes, deficits on hyperacuicy casks,
such as vernier acuicy, arc proporcional со losses in
resolucion and concrasc sensicivicy (Levi and Klein
1982b, 1 9 8 3 ) (Porcrait Figures 8 .1 5 and 8 .1 6 ).
However, chere is con flictin g evidence on chis poinc
(K iorpes e t al. 1 9 9 3 ). There is evidence that, in
anisom etropic am blyopia, loss o f acuity results from
loss in concrasc sensitivity due to image blur arising
from defects in refraction. The simplest explanation o f
che loss in hyperacuicy is that amblyopic eyes have lost
Figure я. 15. D ennis M . L evi. I Ic ob tain ed a d ip lom a in o p to m e try from
W in v a tersra n d S c h o o l o f o p to m e try in So u th A frica in 1 9 6 7 . From
th e U n iv ersity o f H o u sto n he received an O .D . in 1971 and a P h.D .
in 1 9 7 7 . H e th en jo in ed th e facu lty o f the C o lleg e o f O p to m e try at
th e U n iv ersity o f H o u sto n . H e is now professor o f o p to m e try and
vision science and dean o t the S ch o o l o l O p to m e try at the U niversity
o f C a lifo rn ia a t Berkeley. H e received th e G len n Fry Award and the
G arland C lay Award from th e A m erican A cadem y o f O p to m etry .
Fi*«tcS.i6 Stanley K lein . H e o b tain ed a B .S . in physics from the
C a lifo rn ia In stitu te o f T ech n olog y in 1961 and л P h .D . in physics from
Bran dcis U niversity in 1 9 7 6 . B etw een 1 9 6 7 and 1981 he m oved trom
assistant to full professor in the jo in t science d ep artm en t o f C larem o n t
C olleges* C a lifo rn ia . In 1981 he was ap p oin ted professor in the C ollege
o t O p to m e try in th e U niversity o f H o u sto n . In 1 9 8 7 he m oved to the
sch ool o f o p to m e try in the U n iv ersity o f C a lifo rn ia at Berkeley.
che visual channcl responsible for detection o f fine
detail (high spacial frequency). This could involve a loss
o f high-frequency sensitivicy or increased noise in the
high-frequency channel. See Pelli et al. (2 0 0 4 b ) for
discussion o f this issue.
In strabismic amblyopes, losses in hvperacuities are
more severe than can be accounted for by loss in
contrast sensitivity (B arbeito et al. 1 9 8 8 ; Swindale and
M icchell 1994). This is crue in cacs, monkeys, and
humans (Levi and Klein 1982b, 1990; M urphy and
M icchell 1991; Kiorpes 1 9 9 2 ; Levi ecal. 1994a,
1994b). In many scrabismic children, contrast
sensitivity is alm ost the same in both eyes,
buc che deviacingeye has a severe deficit in
hyperacuity tasks.
W ilson (1 9 9 1 b ) modeled these differences between
strabism ic and anisom etropic amblyopes. H e
concluded that chc fovea o f a scrabismic eve
*
suffers
from spacial undersam pling, as indicated by loss o f
grating resolution, and from position uncertainty, as
indicated by reduced vernier acuity. B u t chere is no
change in receptive field size. O n the other hand, he
concluded that the fovea o f an anisom etropic
amblyopic eye shows loss o f sensitivity but does not
show undersampling or position uncertainty.
2. Interocular summation an d masking In normal vision, a
binocular grating requires less contrast lor detection
than a m onocular grating (Section 13.1.2a). W ith
dichopcic gratings o l equal contrast, binocular
summation is not evident in amblyopes. However,
binocular sum m ation does o ccu r in strabismic
amblyopes if the concrasc o f chc gracing presenced
M s t c r i s l СОГТ
 to chc amblyopic eye is suitably increased relative to
that in the norm al eye (Baker et al. 2 0 0 7 ). Thus absence
o f summ ation in strabism ic amblyopes is due to the
weakened input from the am blyopic eye rather than to
absence o f binocular sum m ation. Sec Baker c t al.
(2 0 0 8 ) and M ansouri et al. (2 0 0 8 ) for more
inform ation on this topic.
Interocular transfer in people with loss o f binocular
vision will be discussed in Section 32.4.
3. Displacement o f the image In strabism ics, the images arc-
out o f register by the same am ount over the whole
visual field. However, this affects central vision more
than peripheral vision because receptive fields are
smaller in the center. The lack o f image registration in
the central field o f strabism ic amblyopes leads to a loss
o f cortical binocular cclls for that region. Thus,
although the central visual field o f strabism ic amblyopes
has the norm al density o f ganglion cclls, it has a rcduced
num ber o f binocular cortical cells devoted to it. The
result is that the central retina is spatially undcrsamplcd
at the cortical level (Levi and Klein 1 9 8 5 ) and probably
also more su bject to intrinsic noise (H ess et al. 1999).
In the norm al eye, the decline o f vernier acuity with
increasing retinal eccentricity is much steeper than the
decline o f resolution acuity. This could account for why
hyperacuity, which is measured with stim uli on the
central retina, is affected m ore than resolution acuity in
strabism ic amblyopes o f both early and late onset (Birch
and Swanson 2 0 0 0 ).
In anisom etropes, one image is larger than the other so
that the displacem ent o f one image relative to the other
increases with eccentricity. Thus, the foveal region is
affected less than the periphery. There is thus a more
balanced loss o f hyperacuity and resolution acuity in
anisometropes.
4. Interocular suppression an d confusion Loss o f acuity in a
strabism ic eye when che other eve is closed is attributed
J j
to a m b ly o p ia . W h e n b o t h eyes are o p e n , th ere are th re e
a d d itio n a l reasons f o r loss o t acu ity. ( 1) The strab ism ic
eye deviates an d disp laces th e visual cargec to а
peripheral lo c a tio n . ( 2 ) The visual targec appears
d ip lo p ic , an d che im age in che d e v ia cin g e y e may be
suppressed. ( 3 ) The im age o t chc visual carg et in o n e eye
m a y be su p erim p o sed o n a discincc im age in che Ocher
eye, resulcing in b in o c u la r rivalry.
Freeman ec al. (1 9 9 6 ) measured che acuicy o f chc
scrabismic eye relacive со chac o f che norm al eye in nine
small-anglc scrabismic subjeccs. Amblyopia accounccd
for 3 4 % o f che loss chac occurred wich boch eves open.
Image decencering accounted tor 44 % and incerocular
suppression fo r 20% o f chc binocular loss. Inscabilicv o f
gaze, which can accom pany amblyopia, did noc
r i * u « * . r . R obn f Hc$t. B orn in A ustralia in 1 9 5 0 . H e studied o p to m e try
at th e Q ueensland Institu te o l T e ch n o lo g y in B risbane from 1968
to 1 9 7 0 . H e ob tain ed л M .S c. .it A ston U niversity in Birm ing ham ,
E n glan d , in 1971 and a P h .D . w ith E. H ow ell at the U n iv ersity o f
M elbo u rn e in 1 9 7 6 . H e held research p o sitio n s a t the U niversity o f
C am b rid g e from 1 9 8 0 to 1 9 9 0 . In 1 9 9 0 was ap p oin ted professor
o l o p h th alm o lo g y a t M c G ill University» M o n treal. H e received the
C h am p n cw M edal from the W orship fu l C o m p an y o f Sp ectacle M akers,
L o n d o n in 1983» th e E d rid g e-G reen M edal from th e Royal C o lleg e o f
Surgeonv, L o n d o n , in 1 9 8 9 , the B o b ie r award from the U n iv ersity o f
W aterloo in 1 9 9 4 , and a D .S c . from A sto n U niversity in 1 9 9 8 .
contribute to the loss o f contrast sensitivity
(H iggins c t al. 1982}.
5. Effects o f luminance As die level o t illum ination
decreases, cones, w hich are concentrated in the central
retina, lose their sensitivity more rapidly than rods,
w hich arc more numerous in the periphery. Loss o f
contrast sensitivitv ac low levels o f lum inance is less
4
evident in scrabismic amblyopes than in anisom etropic
amblyopes. This seems to be because scrabismic
amblyopes use cheir relacively norm al periphery
under scotopic con d ition s (H ess et al. 1980)
(Porcraic Figure 8 .1 7 ).
In an amblyopic eye, acuicy declines in proporcion со
illum ination o f che good eye (N oorden and Leffler
1966). V ision in che am blyopic eye may be cocallv
suppressed when che good eye is open.
6 . Contributionfrom monocular inputs M cKee cc al. (2 0 0 3 )
factor analyzed the scores ot 4 2 7 strabismic and
anisom etropic adults on tests o f vernier acuity, grating
acuity, and contrast sensitivity. The am blyopic eye ot
strabism ic amblyopes (with disrupted binocular vision)
and anisom etropes (with preserved binocular vision)
showed a similar loss o f vernier acuitv. However,
strabismics showed less loss o f contrast sensitivityё than
did anisom etropes. M cK ee cc al. suggested chac, in
strabismic am blyopia, the inputs from both eyes survive
even though their binocular con nections have been
 disrupted by ocular m isalignm ent. M any o f these inputs
may be rearranged to drive the rem aining m onocular
cclls and thereby contribute to contrast sensitivitv.
4 4
The loss o f vernier and grating acuity in a strabism ic eye
could be due to the attentional dom inance o fth e
norm al eye, even when the norm al eye is closed.
The equal loss o f acuity and contrast sensitivity in
anisom etropes could be due to form deprivation arising
trom defocus o f the image in the amblyopic eye.
7. Contrast norm alization In spite ot loss in contrast
sensitivity in strabism ic amblyopia, gratings above
threshold appear to have the same contrast in the
amblyopic eye as in the nonam blyopic eye. This is
contrast norm alization. A nisom etropic amblyopes
require a higher contrast before gratings in the tw o eyes
appear to have the same contrast (H ess and Bradley
1 980). C ontrast discrim ination thresholds for stimuli
applied to one eye are not much affected by amblyopia
(see Levi 1991).
Bccausc o f loss o f contrast sensitivity for high spatial
frequencies one m ight expect that amblyopes would
pcrccivc sharp edges as blurred. However, for a group
o f amblyopes, an edge seen by the am blyopic eye
appeared as sharp as an edge seen by the normal eye
(H ess c t al. 2 0 0 3 ). W ith the good eye, subjects could
see the blur in an edge that was optically dcfocuscd to
simulate the loss o f acuity in the amblyopic eye.
Am blyopes must have learned to judge an edge as
being maximally sharp when ir stimulates the detectors
with the highest spatial-frequency sensitivity in chc
am blyopic eye. A sim ilar m echanism may explain why
an edge appears sharp when moved o ff the fovea o f a
normal eye (Section 9 .6 .5 ).
8. Effects o f stimulus eccentricity In a norm al eve, detection
o f high spatial frequencies is confined to the central
retina. The contrast-scnsitivity function for the
am blyopic eyes o feso tro p ic strabism ics was reduced for
high spatial frequency sine-wave gratings presented
w ithin the central 5" o f the retina. W ith m ore severe
amblyopia, the deficit spread over a larger range o f
spatial frequencies and eccentricities (Thom as 1978).
Hess et al. (1 9 8 0 ) reported that strabism ic amblyopes
show loss o f contrast sensitivitv m ainly in the central
4 4
retina, while anisom etropic amblyopes show loss o f
sensitivity in both the central and peripheral retina.
After allowing for effects o f spatial scale, Bradley e t al.
(1 9 8 5 ) found that the deficit in contrast-scnsitivity was
n o t related to retinal locus in seven o f nine amblyopes.
However, they did not relate the results to the type o f
amblyopia.
O ptim al detection o f contrast requires a stimulus
con tain in g about 10 periods o f a grating. Theretore, as
the spatial frequency o f a grating is decreased, a larger
stimulus is required for optim al detection (H ockstra
et al. 1 9 7 4 ; Howell and Hess 1 9 7 8 ). Thus, in
com paring con trast sensitivities at different spatial
frequencies, one must take the size o fth e stimulus into
account.
C o n trast sensitivity for low spatial frequencies
increased m ore rapidly with increasing width o f the
grating for the amblyopic eye than for the norm al eye
o f strabism ic and anisom crropic amblyopes (Hagem ans
and W ild t 1 9 7 9 ). W ith large stim uli, the amblyopic
eye was som etim es more sensitive to gratings o f low
spatial frequency than the normal eye. Field size had
little effect for gratings o f high spatial frequency (K atz
e t al. 1 9 8 4 ).
9. H onifielddifferences The nasal hemifield (uncrossed
inputs from tem poral hem irctinas) is more susceptible
to early m onocular deprivation or esotropia than is the
temporal hemifield (crossed inputs from the nasal
hem irctinas) in cats (Sherm an 1 9 7 3 ; Ikcda and
Jacobson 1977; Singer 1 9 7 8 ; Bisti and C arm ignoto
1986) and humans (Sirctcanu and Fronius 1 9 9 0 ). Thus,
cells in area 17 o feso tro p ic cats showed a marked loss o f
response to stimuli presented in the nasal visual field
(tem poral retina) o fth e deviated eye (K alil et al. 1984).
This could be a consequence o fth e fact that nasal
hem irctinas develop more rapidly than temporal
hem irctinas and to the fact that the stimulus fixated bv 4
the norm al eye o f an csotrope falls on the nasal
hcm irctina o f the amblyopic eye. This issue is discussed
in more detail in Section 8.5.2.
In anisom etropic amblyopes, acuity loss dim inished
symmetrically with increasing eccentricity in the nasal
and temporal retina (Sireteanu and Fronius 1981).
Hemifield differences are discussed in Sections 12.3.4
and 7.2.4.
8 .4 .2 b O r ie n ta tio n D is c rim in a tio n in A m b ly o p ia
Strabism ic am blyopes show high thresholds for discrim i­
nating the orientations o f sinusoidal gratings with high spa­
tial frequency (Skottu n et al. 1986b).
A deficit in orientation discrim ination could be due to:
(1 ) loss o f orientation detectors, (2 ) broadening o f the
bandwidth o f orientation detectors, or (3 ) defective
integration o f orientation signals over large areas. There
seems to be no evidence bearing on the first possibility.
Evidence bearing on the third possibility is reviewed in
Scction 8.4.3c.
D em anins c t al. (1 9 9 9 a ) conducted experim ents to
determ ine w hether the bandwidth o f orientation detectors
in strabism ic amblyopes is unusually broad. They measured
oriencacion discrim ination using a random array o f G abor 8.4.3 SPATIAL D I S TO R T I O N S
patches o f various sizes. Reducing the size o f л G abor patch
O th er sym ptom s o f amblyopia include confusion betw een
increases its Fourier oriencacion bandwidth and its Fourier
neighboring stimuli (Pugh 1 9 5 8 ); distortions o f length,
spatial-frequency bandwidth. In a second condition, they
position, and direction (m etam orphopsia) (H ess et al.
varied orientation bandwidth independently o f spatial-
1 9 7 8 ; Bedell and Flom 1981; Froniusand Sireteanu 1989;
frequency bandwidth by using elongated Gabors. Stimulus
Lagreze and Sireteanu 1 9 9 1 ); and defective m otion and
contrast was at a constant level above the contrast-detection
shape discrim ination (W att and Hess 1987). Spatial phase
threshold. If loss in orientation discrim ination in strabismic
discrim ination is also defective (Pass and Levi 1982; Bennett
amblyopia is due to an abnorm al bandwidth o f orientation
and Banks 1 9 8 7 ; Kiper 1994). For instance, strabismic
detectors, varying the orientation bandwidth o f the stim u­
amblyopes need higher than normal contrasts to discrim i­
lus should have an effect. The results indicated that the
nate the relative phases o f a grating com posed o f a funda­
am blyopic loss occurred only for stim uli wich narrow
m ental and its third harm onic (I.awden et al. 1982).
Fourier orientation bandwidth. The thresholds tor the
It has been argued that spatial distortions in m ost ani­
amblyopic and nonam blyopic eyes for stimuli with broad
som etropic amblyopes can be explained in terms o f loss o f
orientation con ten t were similar. For stimuli with broad
co n trast sensitivity. But spatial defects in strabism ic am bly­
orientation contenc, subjects probably judged che orienta­
opes cannot be explained in this way (Rcnrschler and 1 lilz
tion o f the envelope o t the G abor patches (second-order
1 9 8 5 ; Fronius and Sireteanu 1 9 8 9 ; Hess and Holliday
orientation ) rather than that o f their con ten ts (first-order
1 9 9 2 ; Hess and Field 1 9 9 4 ). Som e strabismic amblyopes
stim uli). Subjects would be particularly prone to use the
show л loss o f hyperacuity bu t no spatial distortions, while
envelope o f elongated G abors with broad orientation
others show only spatial distortions. Furtherm ore, in scra­
tuning. For such stim uli, the orientation o f the envelope is
bism ic amblyopes, hyperacuicy defects are greatest in the
much m ore evident than that o f the contents.
central retina, while distortions are greatest in the periph­
Л supplementary experim ent revealed that amblyopes
ery (D em anins and Hess 1996b).
showed little deficit when only the orientation o fth e enve­
Spatial distortions are n o t due to loss o f retinal recep­
lope was varied. D em anins et al. concluded that deficits ot
tors or ganglion cells, because there is no evidence that
orientation discrim ination in strabismic amblyopes for
amblyopes show such losses. M asking and adaptation stud­
first-order stimuli are particularly severe at high spatial fre­
ies on a mixed group o f amblyopes revealed that spatial-
quencies and low contrascs. O rientation deficits are reduced
frequency channels o f am blyopic eyes have normal
o r absent for low spatial-frequency or second-order stimuli
bandwidths and tuning functions, except that they require
(G abo r envelopes).
higher contrasts for their activation (H ess 1980). The visual
In a norm al eye, the loss in orientation discrim ination
distortions in strabismic amblyopia must have som ething
with increasing retinal eccentricity can be com pensated tor
to do with how spatial inform ation is coded in the visual
by a proportional increase in the length o f the test line.
cortcx. Four factors that have been suggested arc reviewed
Similarly, poor orientation discrim ination tor a single cen-
in the following sections.
cral line by an amblyopic eye can be com pensated for by
increasing the length o f the line ( Vandenbussche et al.
1986).
8 .4 .3 a S p atial U n d crsa m p lin g
People with norm al vision show greater acuity tor verti­
cal gratings than for gratings in other orientations (see It has already been m entioned that diplopia in the central
Howard 1 9 8 2 ). In Section 8.2.3a it was m entioned that field o f strabismic amblyopes leads to a reduction in the
early strabismus leads to a selective loss o f cortical cells num ber o f cortical cells responding to the deviated eye for
tuned to vertically orientated stimuli. Thus, strabismic that region o fth e visual field. Thus, the central visual field o f
amblyopes show a selective loss o f contrast sensitivity for the deviated eye o f strabismic amblyopes has fewer cortical
vertical gratings. This is known as the v e r t ic a l e f f e c t processing units devoted to it, so it is spatially undcrsamplcd
(Sireteanu and Singer 1 9 8 0 ). The vertical effect seems to be (Levi and Klein 1985). Loss o f spatial sampling at the co rti­
a consequence o t strabismus rather than o t amblyopia, since cal level should affect pattern acuity more than contrast sen­
it did not occur in monkeys in w hich amblyopia was sitivity or grating acuity. For example, Levi e t al. (1 9 8 7 )
induced w ithout m isalignm ent ot the visual axes (H arw erth found that, in strabismic but not anisom etropic amblyopes,
et al. 1 9 8 3 c). The vertical effect occurs only for high spatial 3-line bisection acuity was reduced to a greater extent than
frequency stim uli in unilateral strabismics (Kelly et al. could be accounted for in terms o f loss o f grating acuity.
19 9 7 ; Sharm a et al. 1 9 9 9 ). It occurs in both eyes, although This was also true o fth e periphery o f a normal eye and, as in
it is n o t as strong in rhe nondeviatingeye. The vertical effect the normal eye, the pattern acuity o f the strabism ic eye
is probably due to the fact that strabismus induces horizon­ improved as the num ber o f samples in the stimulus was
tal binocular disparity betw een vertical contours bur not increased. Thus, the center ot the deviated eye o f a strabis­
between horizontal contours. mic amblyope resembles the periphery o f a normal eye.
 W an g et al. (1 9 9 8 ) used a 3-line bisection test with lines
com posed o f a variable num ber o f dots scrambled about the
mean position with a variable standard deviation. An ideal-
observer analysis provided separate estim ates o f spatial
uncertainty and sam pling efficiency (num ber o f dots used
to total num ber o f dots). Spatial uncertainty was elevated
about 10-told in both anisom etropic and strabism ic ambly­
opes relative ro that in norm al subjects. However, loss o f
spatial integration efficiency was found only in strabism ic
amblyopes. They suggested that this is due m ainly to loss o f
fine-scale detectors at the cortical level.
A regular lattice o f independent detectors can resolve а
grating only it the spatial period ot the grating is at least
tw ice that o f the detectors. A grati ng finer chan this Nyquist
lim it is said to be undersampled and forms a moire pattern
with the detectors, which may be visible even though the
grating is n o t (see Figure 9 .9 ). This is known as aliasing.
Foveal cones are arranged in a regular m osaic, and there are
least as many ganglion cells as cones. Thus, cone density
determ ines the Nyquist lim it in the fovea. Aliasing is noc
norm ally evident in the central retina because the eye is not
capable o f form ing images as fine as the spacing o f the cones.
It can be made visible by form ing a laser interference image
on the retina that bypasses the optics (Section 9 .1 .3 ).
In the peripheral retina there are fewer ganglion cells
than receptors, so that ganglion-cell density becom es the
lim iting factor in the periphery. Also, the cones are not so
regularly arranged outside the fovea because they are inter­
spersed with rods. C oletca and W illiam s (1 9 8 7 ) predicted
thac, because o f che irregular arrangem ent o f cones in the
excrafoveal region, a gracing wich chc same periodicity as
the mean spacing o t receptors (tw ice the Nyquist limic)
should appear tilted 9 0 ". They confirm ed this effect in the
excrafoveal region o t norm al subjects. Thus, orientation
reversal provides a psychophysical m ethod for estim ating
che spacing ot less regular detectors.
I f the visual cortcx o f amblyopes has reduced spatial
sam pling, the misperception ot grating orientation should
be evident at unusually low spacial frequencies. Sharma
ec al. (1 9 9 9 ) projected a laser interference grating on the
retinas o f three strabism ic amblyopes. b o th the amblyopic
and nonam blyopic eyes showed reduced contrast sensitiv­
ity at low spatial frequencies, w hich, for tw o o f the subjects,
was m ost pronounced tor vertical gratings (see Section
8.4 .2 b ). The am blyopic eyes showed loss o f co n trast sensi­
tivity at higher spatial frequencies, and there was severe
misperception o f the orientation o f gratings w ith spacial
frequencies ot betw een 2 0 and 6 5 cpd, which is well below
the 120-cpd limic sec by che recinal recepcors.
These resides suggest chac inpucs from an am blyopic eye
are severely undcrsampled ac the cortical level. Spatial
scram bling o f d etectors alone would noc produce misper-
cepcion of oriencacion for gracings wich che spacial frequen­
cies used by Sharm a ec al. However, chc mispercepcion o f
orientation that they found was n o t quite the 9 0 ° value
predicted by pure undersampling. Tlius, the visual cortex o f
strabism ic amblyopes may suffer from both undersampling
and disarray. It may not be possible to dissociate the two
effects in practice because random loss o l cortical units
responding to stim ulation o f an am blyopic eye would result
in an irregular detector array, which would produce both
undersampling and scrambling.
8 .4 .3 b C ro w d in g
In a norm al eye, Snellen acuity, vernier acuity, and grating
acuity arc adversely affected when the test stimulus is
flanked by other stim uli in the same eye. This is know n as-
crow d in g (Section 4 .8 .3 ). In a norm al eye, the spatial range
ot crowding is proportional to visual resolution. This sug­
gests thac che range o f crow ding is proportional со che
size of stim ulated receptive fields. This is the scale shift
hypothesis. Thus, the range of’ crow ding increases with
retinal eccentricity and with stim ulus size.
The magnitude and spacial excenc o f crow ding are larger
in che deviating eye o f strabismic amblyopes than in people
with normal vision, or in anisom etropic amblyopes (H ow ell
et al. 1983; Hess et al. 2 0 0 1 ; Levi D M et al. 2 0 0 2 ; Bonneh
c t al. 2 0 0 4 ). In strabism ics, chc effects o f crow ding on che
contrast threshold for detection o f a local grating were par­
ticularly severe ac high spatial frequencies (P o la ce ca l.2 0 0 5 ).
Strabism ic amblyopes have difliculcy isolating spatial rela­
tionships tor pattern identification, although they can dis­
tinguish a simple form from its background. This pactern o f
deficits occurs in children wich early or lace onsec o t strabis­
mus (B irch and Swanson 2 0 0 0 ).
The larger extent ot crow ding in an am blyopic eye could
be due to an absence o f small receptive fields. If so, crow d­
ing would be predictable from the scale shift hypothesis.
Levi cc al. (2 0 0 2 ) gained only partial support for chis idea.
They concluded chat suppressive interactions in the cortex
serving an am blyopic eye extend over larger than normal
distances. In a norm al eye, inhibition is replaced by facilita­
tion when o b jects are separated by more chan a eercain dis­
tance. Amblyopes did not show this facilitation (Polat et al.
2 0 0 4 ).
8 .4 .3 c S p a tia l S c ra m b lin g
Perhaps the cortical local sign m echanism is spatially scram ­
bled in strabism ic am blyopia. Thus, there may be disarray,
or misregistration ot the posicions o f the receptive fields o f
cortical cells relative to their neighbors. Strabism ic ambly­
opes show distortions when they attem pt to draw letters or
grarings(Pugh 1958; H e sse tal. 1978). Drawings o f m em o­
rized circles ot dots made by strabismic amblyopes using che
defective eye were distorted in size and shape (Sireceanu
ec al. 1993b, 2 0 0 8 ). However, drawings o f com plex scenes
chac remained visible did noc show equivalent distortions
and mosc amblyopes did not report seeing distortions in
natural scenes. M osc uncreated anisom etropic amblyopes
(aged 4 со 13 years) showed defective contour inccgration
o f G abor patches sec in a random array when viewing wich
the am blyopic eye (C hand na ec al. 2 0 0 1 ).
The m eth o d o f equ ivalen t n oise has been used со mea­
sure che degree o f spatial disorder in an am blyopic eye rela-
cive со a norm al eye. For a given visual cask, excernal noise is
introduced inco che stimulus presented to a norm al eye
until perform ance with that eye m atches that with an
amblyopic eye. W ith this m ethod, Hess et al. (1 9 9 7 b ) found
that 10 o f 11 strabism ic amblyopes had reduced ability to
d etect aligned m icropatterns (G abo r patches) in a random
field ot m icropatterns when using their deviating eye. For
m ost strabism ic amblyopes, perform ance with the ambly­
opic eve was similar to that with the norm al eye when spa­
tial jitte r (noise) was introduced into the stimuli presented
to the norm al eve.i Hess et al. concluded that the fundamen-
tal dcfect in strabism ic am blyopia is topographic disarray o f
orientation detectors in the visual cortex rather than poor
contour integration. However, the distinction between
these detects is n o t well defined. M ost anisom etropic
amblyopes performed norm ally on this task (H ess and
D em anins 1 998).
Hess c t al. (1 9 9 9 ) measured the am plitude threshold for
detection and discrim ination ot radial spatial modulations
o f an annul us. For strabism ic amblyopes, the threshold was
higher than norm al and was largely indcpendcnc ot che spa­
cial frequency o f che m odulations. They concluded chac the
defect is due ro spatial disarray o f high-level detectors. They
argued that the defect would be limited to high spatial fre­
quencies if were it due to undersampling.
Levi et al. (2 0 0 0 ) questioned this conclusion. They
measured rhe am plitude threshold for d etection o f spatial
m odulations in a row or annulus o f G abor patches. They
also used the equivalent noise procedure for these tasks.
Strabism ic amblyopes showed a m odest deficit on both
tasks but not when the G abor patches were well separated,
either by reducing their num ber at a fixed eccentricity or by
increasing the size o f the stimulus. They also found that the
am blyopic defect could n o t be m odeled by the addition o f
external noise. They concluded that the amblyopic deficit
in these tasks is due to an abnorm ality in the high-level
com parison process that detects stimulus alignment.
However, in a subsequent paper, Levi et al. (2 0 0 8 ) found
that a m ajor factor responsible for a deficit o f an amblyopic
eye in detecting a local grating in w hite noise was the
increased internal noise.
Kovacs et al. (2 0 0 0 ) used similar stim uli and found that
the poor perform ance o f strabism ic amblyopes was not due
ro loss o f acuity or contrast sensitivity.
Dem anins et al. (1 9 9 9 b ) argued that, with a stimulus
near the Nyquist lim it, a spatially scrambled array o f d etec­
tors should have near normal orientation discrim ination
because a subset o f detectors would fall below the Nyquist
lim it. However, the discrim ination o f the direction o f
m otion o f a grating should be defective, becausc m otion
directions are averaged over a region. For an undersampled
array, orientation and m otion discrim ination should be
equally defective. In eight strabism ic amblyopes D em anins
et al. found three who showed evidence o f spatial scram ­
bling with high spatial-frequency gratings and one who
showed evidence o f undersampling.
Ellem berg et al. (2 0 0 2 a ) found that strabism ic ambly­
opes failed to show any effect o f crow ding on the perceived
co n trast o f a G abor patch in a horizontal array o f parallel
patches. A nisom etropic amblyopes showed the normal
crow ding effect. The strabism ic amblyopes misperccived
alignm ent and orientation ot the patches. Normal subjects
did nor show the crow ding effect when the patches were
disordered. F.llemberg et al. concluded that strabismic
amblyopia is, at least in part, due to spatial scram bling aris­
ing from abnormal lateral interactions in the visual cortex,
while anisom etropic amblyopia is due to loss o f contrast
sensitivity and resolution.
8 .4 .3 d D e fe c tiv e S tim u lu s In te g ra tio n
C ollin ear line elements are easily detected in an otherw ise
random array (Section 4.2 .6 c). This is thought to depend
on lateral con nections in the visual cortex (Polat 1999).
Also, the visibility (determ ined by the contrast threshold)
o f a small G abor patch is enhanced when it is flanked by
two collinear G abor patches and reduced when it flanked
by orthogonal patches. In a mixed group o f amblyopes, co l­
linear facilitation, measured psychophysically and by evoked
potentials was reduced or replaced by inhibition (Polat
e ta l. 1997).
M onocularly deprived cats have difficulty with form-
discrim ination tasks, such as distinguishing between an
upright and inverted triangle, with the deprived eye. There
was some loss ot transfer o f learning ot simple discrim ina­
tions from the deprived eye to the normal eye (G an z et al.
1 9 7 2 ). A m blyopic monkeys o f both the strabism ic and an i­
som etropic type showed reduccd ability to d etect a ring o f
aligned G abor patches set in a random array ot patches
(K ozm a and Kiorpes 2 0 0 3 ). Som e animals showed reduced
ability even in the nonam blyopic eye. The deficit was not
clearly related to losses in contrast sensitivity or acuity. This
evidence suggests that long-range cortical con nections arc-
disrupted in amblyopia.
O th er investigators have reported that amblyopes have
normal abilities in some orientation detection tasks.
Strabism ic amblyopes showed normal visibility enhance­
m ent for aligned texture elem ents (Levi and Sharm a 1998).
Three strabism ic am blyopes had a norm al ability to detect
orientation-defined texturcd regions in regular arrays o f
G abor-patches (Mussap and Levi 1 9 9 9 ). However, ambly­
opes showed som e deficit in detection o f a dotted line
masked by random -dot noise (Mussap and Levi 2 0 0 0 ).
They concluded that texture segmentation based on
M icchell 1 9 9 4 ). M onkeys reared wich one eye sutured
showed reduced contrast sensitivity to a uniform flickering
field in the deprived eye, especially at higher temporal fre­
quencies. M onkeys reared with prism -induced binocular
dissociation had normal temporal m odulation sensitivity in
each eye but did not show the binocular summation evident
in norm al eyes (H arw erth ct al. 1983b ). Som e human
amblyopes showed norm al flicker sensitivity, some reduced
sensitivity, and others enhanced sensitivity in the affected
eye relative со che norm al eye (M anny and Levi 1982).
Bradley and Freeman (1 9 8 5 b ) concluded that flicker
sensitivity can be severely deficient in che amblyopic eye ac
one spatial Irequency but can appear norm al it the stimulus
includes chose spatial frequencies that are detected nor­
mally. They found contrast sensitivity in amblyopia to be
highly dependent on spatial frequency, with high spatial
frequencies being m ost atfected, but to be largely indcpen-
denc o f tem poral frequency. They concluded chat losses in
temporal sensitivity are a consequence o t losses in spatial
contrast sensitivity.
Sokol and Nadler (1 9 7 9 ) reported a reduction in the
amplicude o f che electrorednogram (F.R G ) elicited in an
am blyopic eye by a patterned stimulus, although n o t by a
hom ogeneous flashing light. N onlinear com ponents o fth e
V E P in response to dichoptic flicker are less evident in the
stereoblind (see Section 13.1.8b).
8 .4 .4 c L o ss o f M o c io n S e n sitiv ity
There has been some debate about w hether amblyopia
selectively affects mocion dececcion (see Hess and Anderson
1993). D isplacem ent thresholds arc elevated in human
amblyopes, mosc markedly in che fovea. D isplacem ent sen­
sitivity in che fovea ot strabism ic amblyopes, like that in the
norm al fovea, is improved by che addicion o f a scacionary
reference scimulus. However, mocion sensicivicy in the fovea
o f anisom etropic am blyopes is degraded by che addicion o f
a reference scimulus, as is thac in the normal periphery.
Thus, in this respect, che m otion sensicivicy o f scrabismic
amblyopes, buc noc o f anisom ecropic amblyopes, resembles
chat o f the norm al peripheral retina (Levi et al. 1984).
The threshold for detection o f m otion o f a vertical grat­
ing was elevated in the deviating eye o f paciencs with early-
onset esotropia, even in che absence o f dcfeccivc nystagmus
(Shallo-H offm ann et al. 1 9 9 7 ). Scrabismic amblyopes had a
weaker than norm al m otion aftereffect (H ess et al. 1997c).
F.llcmberg et al. (2 0 0 2 b ) reported that discrim ination
o f the direction o f coherent m otion in a random -dot kine-
matogram was impaired in subjects who had early torm
deprivation because o f cataracts. The im pairm ent was
greater after binocular deprivation than after m onocular
deprivation. A deficit also occurred in the cask o f dececcing
global torm in Glass patterns (Lewis et al. 2 0 0 2 ). These
resulcs con flict with the finding chac m onocular deprivacion
produces more severe defects chan binocular deprivation.
F.llcmberg cc al. suggesced chat tasks involving the detection
o f global moving or static forms in com plex displays involve
activity in higher centers, where inputs from chc two eyes
com pete rather than com bine.
D iscrim ination o f the direction o f coherent m otion in a
random -dot kinematogram was impaired in a mixed group
o f strabism ic and anisom etropic amblyopes (Sim m ers et al.
2 0 0 3 ). The deficit was m ore pronounced for second-order
m otion o f contrast-defined regions than tor first-order
m otion o f lum inance-defined regions. Similarly, amblyopes
showed a greater loss for detection o f stationary second-
order stimuli than for detection o f firsc-order scimuli (W ong
et al. 2 0 0 1 ). The extra loss tor second-order stimuli presum­
ably arises in extrastriate areas, where second-order stimuli
are processed.
Human brain potentials (V E P s) had longer latency and
smaller amplitude when a reversing checkerboard pattern
was presented to the amblyopic eye than when it was pre­
sented to the normal eye. However, the latency and am pli­
tude o f the VF.P to m otion onset o f a checkerboard were
the same for the am blyopic eye and norm al eye (Kubova
et al. 1996). Tli is suggests that the m otion pathway, proba­
bly involving mainly the m agnocellular system, is relatively
spared in amblyopia.
Patients lacking static stereopsis due to infantile or late
onset esotropia may perceive m otion-in-depth created by
opposite m otion o f dichoptic stim uli (M aeda et al. 1999).
They presumably use difference-of-m otion signals rather
than change-of-disparity signals (see Section 3 1 .3 ).
8 .4 .4 d A sv m m ecrv o f M o tio n D e te c tio n
In normal subjeccs, sensicivicy to m otion o f small displays
presented to one eye is higher tor centripetal m otion
(toward che fovea) than for centrifugal m otion (away from
the fovea) (M a tecff et al. 1991). The gain o f optokinetic
nystagmus (O K N ) is also higher fo r stim uli moving cen-
tripetally (Section 2 2 .6 .1 c). Thus, the gain o f m onocular
horizontal O K N for a normal eye in response to a textured
display filling one-halt o f the visual field is higher when che
scimulus moves coward che fovea chan when ic moves away
from rhe fovea (O h m i ec al. 1986). In paciencs wich early-
onsec esocropia, sensicivicy со cencripetal mocion was
norm al, buc a cencrif ugal bias was evident in the nasal hem i-
field (Faw cett cc al. 1998).W e will see in che next section
that, in early-onset esotropes, m onocular O K N has higher
gain when the display moves nasally rather than temporally.
This asymmetry could be due to asymmetry in mocion
d etection at the cortical level or to defective transmission o f
morion signals to subcorcical cencers controlling O K N (see
Section 2 2 .6 .1 ).
Tychsen and Lisberger (1 9 8 6 ) reported that, for cwo
esotropes o t early onsec, m onocularly viewed small line
scimuli appeared to move more rapidly when moving nasally
chan when m oving cemporalIv. However, Brosnahan ec al.
(1 9 9 8 ) found that, in early onset esotropes, a gracing
appeared to move m ore slowly when m oving nasally, with
fixation on a stationary point. Ac least part o f the asymme­
try in perceived velocity could be due to the inability o f
subjects to in h ibit pursuit eye m ovem ents when the grating
moved nasally. Roberts and W estall (1 9 9 0 ) found no direc­
tional asymmetry in perceived velocity in esotropes.
S ch or and l.evi (1 9 8 0 ) found chac, in scrabismic and ani-
sometropie amblyopes, the contrast-sensitivity tunction tor
detection o f m otion o f a grating moving nasally was the same
as that tor a grating moving temporally. Shallo-H otfm ann
c t al. (1 9 9 7 ) reported that, in rhe deviating eye o f early-onset
esotropes, the m otion-detection threshold was elevated
more for a gracing moving nasally, and in the nondeviating
eye it was elevated more tor a grating moving temporally.
Th e relation between asymmetry o f perceived velocity and
O K N asymmetry is clearly not yet understood.
Nasotcm poral asymmetry in response to moving grat­
ings can be detected in evoked potentials from the visual
cortex. К о asym m etry is evident in human neonates, per­
haps because early co rtical m otion detectors are not direc-
tionally selective (Section 7 .3 .4 c). A strong asymmetry,
evident at 2 m onths,changes to symmetry by 6 to 8 months.
The VF.P o f infantile esotropes remains asymmetrical
(N orcia et al. 19 9 1 ; N orcia 19 9 6 ; Birch et al. 2 0 0 0 b ).
Asymm etric evoked potentials associated with asym­
m etrical O K N in patients with infantile esotropia are co r­
related with loss o f stereoacuity and o f bifoveal fusion
(Faw cett and Birch 2 0 0 0 ). The asymmetry o f the V E P is
reduced if surgery for strabismus is done before 2 years o f
age (N orcia et al. 1995).
8 . 4 . 5 M О Т О R S V M P T O M S O F AM В I.VO PI A
8 .4 .5 a Pupillary R esponses and A cco m m o d a tio n
Am blyopic eyes have a smaller pupillary response than do
norm al eyes (Brenner ct al. 1 9 6 9 ). They also show abnormal
accom m odative responses. Low contrast sensitivity increases
the threshold for detection o f image blur, which results in
an abnorm ally large depth o f focus and a high steady-state
error o f accom m odation. Also, the range o f accom m oda­
tion is reduced, and vergence accom m odation is defective
(see C iuffrcda and I lokoda 1983).
8 .4 .5 b E cc e n tric Fixation
Strabism ic and anisom etropic amblyopes show e c c e n t r i c
f i x a t i o n and instability o t gaze when they try to fixate an
o b je c t with rhe affected eye. Gaze is stable for fixation with
the norm al eve or both eyes (Sch o r and H allm ark 1978;
Ciuffreda er al. 1980). According ro a theory proposed by
W orth (1 9 0 3 ), amblyopia produces a loss o t acuity in the fovea
o f the affected eye. Consequently, the amblyopic eye uses
an eccentric retinal location tor fixation. However, several
investigators failed to show that acuicy in an am blyopic eye
is higher in the region used lor fixation than in the fovea
(see Flom 1978).
A m blyopic eyes also show s a c c a d i c d y s m e t r ia . This can
be hypometria (undershooting) or saccadic disconjugacy.
The disconjugacy som etim es occurs for vergence eye move­
m ents in only one direction and sometimes tor those in
both directions (M axw ell c t al. 1 9 9 5 ). These abnorm al eye
movements may also be present in the norm al eye ot strabis­
mic amblyopes (see Bedell and Flom 1985).
8 .4 .5 c D irec tio n a l P reponderance o f O K N
In Section 22.6.1 ir is explained how, in the absence o f
inputs from the visual cortex, O K N in each eve occurs only
in response to stim uli moving nasally. This is known as
d ire c tio n a l p re p o n d e ra n ce . In tovcate animals, inputs
from the visual cortex convert O K N into a bidirectional
response.
Adulc amblyopes show disturbances o f m onocular
O K N evoked by stimuli moving in the temporal direction
(Sch o r and Levi 1980; S ch or 1 9 8 3 b ; Sparks et al. 1986;
H artm ann e t al. 1 9 9 3 ). The disturbances are m ost evident
for stimuli confined to the tem poral hem iretina o f one eye
(W estall and Sch or 1 9 8 5 ). D irectional preponderance ot
O K N is m ost evident in people with early-onset esotropia
(D em eran d N oorden 1 9 8 8 ; W estall e ta l. 1 9 9 8 ). Also, with
early-onset strabismus, directional preponderance o f O K N
is less likely to be confined ro rhe deviating eye (Steeves
et al. 1999).
W ith m onocular viewing, voluntary pursuit eye move­
m ents ot esotropes, also, are defective in the temporal direc­
tion (Sch o r 1 9 7 5 ; Tychsen et al. 1985; Bedell et al. 1990;
Kiorpes e t al. 1996).
N ot all srcrcoblind amblyopes showed a strong direc­
tional preponderance ot O K N , but all amblyopes lacking
interocular transfer o f threshold elevation showed direc­
tional preponderance (W estall et al. 1989). In another
study, directional preponderance was found only in strabis­
mics with no measurable binocularity (Valmaggia et al.
2 0 0 3 ). D efects o f eye movements may persist even when
corrective surgery is conducted 2 0 weeks after birth and
after some stereopsis has been restored (A iello ec al. 1994;
W right 1 9 9 6 ). The relationship between defective stereop­
sis and pursuit eye movements is reviewed in Kommerell
(1 9 9 6 ) and in Section 2 2 .6 .1 .
Disparity-induced changes in vergence arc absent in
amblyopia, even though vergence in response to changes in
accom m odation is normal (Kenyon et al. 1981).
8 .4 .5 Л A b n o rm a l V isu a lly G u id e d R esp o n se s
Strabism ic amblyopes showed systematic errors in poincing
ro visual targets when using their am blyopic eye (Fronius
and Sireteanu 1 9 9 4 ). C ats reared with strabismus showed a
deviation in jum ping со a platform when tested with the deprivation than by binocular deprivation. In the cat,
deviating eye. K ittens younger than 4 m onths overcame this both forms of early deprivation have more severe effects
deficit with practicc (O lson 1 980). An extended period o f on tem poral and spatial resolution than does ablation o f
m onocular deprivation in the kitten also produced deficits area 17 in a normally reared adult cat (Lehm kuhle et al.
in visually guided paw placem ent, which were more severe 1 9 8 2 ). A t least part o f the effect o f deprivation in the
the longer the deprivation lasted (D ew s and W iesel 1970). cat must therefore involve the extrastriate area and
possibly other higher areas. The cat extrastriate area
receives direct visual inputs (LeVay and G ilb ert 1976).
8 .4 .5 e S u m m ary
Cars raised with o n e eye sutured failed to respond to
Am blyopia is not due to defects in the retina or in the
objects presented in the binocular field o f the deprived
LG N . Several lines ot evidence suggest that it results trom
eye. However, after removal o f the whole visual cortex,
inputs from the eye with more normal visual experience
the cats responded to stimuli in any part ot the visual
gaining greater access to cortical cells than inputs trom the
field o f cith er eye (Sherm an 1974) (P ortrait
deprived eye.
Figure 8 .1 8 ). The subcortical and extrastriate centers
The spatial distribution ot detects in contrast sensitivity
m ediating the responses o f these cats must be at least
and acuity over the visual field o f an am blyopic eye depends
partly immune to the effects ot m onocular deprivation.
on the spatial frequency ot the stimulus, the severity o t the
visual deprivation, and w hether the amblyopia is due to 2. Immunity ofth e monocular visualfield Inputs to cells
strabismus or to anisom etropia (H ess and Pointer 1985). serving the m onocular fields do n o t have to com pete
The nasal hemifield (uncrossed cortical inputs) is more sus­ with inputs from the o ther eye. Therefore, in
ceptible to the effects o t deprivation than the temporal m onocularly deprived animals, a high proportion o f
hemifield (crossed cortical inputs) in both cats and humans. cells in the m onocular region o f the visual cortex have
This could be a consequence of the tact that nasal hem ircti­ normal receptive fields (W ilson and Sherm an 1977).
nas develop m ore rapidly than tem poral hemirctinas. A lso ,co n trast sensitivity in human anisom etropic
In anisom etropic amblyopia, deficits on hyperacuity amblyopes is normal outside the binocular field (Hess
tasks arc proportional to those in resolution and contrast and Pointer 1985).
sensitivity. In strabismic amblyopia, hyperacuities are more
3. Immunity o f Siamese cats In Siamese cats, alm ost all
severely affected than resolution acuity or contrast sensitiv­
cortical cells arc driven onlv/ bv/ the contralateral eve,
/ '
ity. The central visual field o f strabismic amblyopes is
and m onocular deprivation has little i f any effect on the
affected more than the peripheral field, because the periph­
rcccptivc field properties o f cortical cells in these
ery has larger receptive fields. This m ight explain why hyper­
anim als (Berm an and Payne 1982; Berm an et al. 1989).
acuity, which is a function ot the central retina, is affected
more than resolution acuity in strabism ic amblyopes.
In anisom etropes with aniseikonia, the peripheral field
is affected m ore than rhe central field. Spatial distortions
that occur in some strabism ic amblyopes are uncorrelated
with loss o f contrast sensitivity or loss o f hyperacuity. They
probably reflect both undersampling and topographic
scram bling in the visual cortex. Flicker detection can be
defective in some amblyopes but it may not show at all spa­
tial frequencies. O th er am blyopic symptoms include insta­
bility o f gaze and visual pursuit and errors in pointing.

8 .4 .6 D EV ELO PM EN T AND T R EA TM E N T OF
A M B L Y O P IA

8 .4 .6 a A m b ly o p ia and N eu ra l C o m p e titio n

Loss of binocularity in m onocularly deprived animals

M tsrruy S. Shcm iu n. B orn in P ittsbu rgh in 1 9 4 4 . H e obtain ed
results from com petition betw een inputs from the two eyes a B .S c . in b iology from the C a lifo rn ia In stitu te o f T ech n o lo g y in 1965
tor access to cortical cells. The following lines of evidence and a P h .D . in anatom v4 from the U niversity
J
o f Pennsylvania
Ф
in 1 9 6 9 .

suggest that amblyopia can be understood in the same way.
1. M onocular deprivation is most disruptive Visual
perform ance is degraded m ore by m onocular
In 1 9 7 2 he o b tain ed an academ ic a p p o in tm e n t in the d ep artm en t o f
physiology a t th e U n iv ersity o f V irg in ia. In 1 9 7 9 he was appointed
professor o l neu robiologv. S U N Y a t Stony B ro o k , where he is now-
leading professor o f n eu robiology. H e is the D r. Lee V isitin g Research
Fellow o f C h rist C h u rch C o lleg e, O x fo rd U niversity.
4. Effects o f deprivation take tim e to develop In monkeys
with esotropia induced surgically on the 6 th postnatal
day, acuicy in both eyes remained normal for four
weeks, after which acuity o ft h e deviated eye began to
deteriorate relative to that o fth e nondeviatcd eye
(K iorpes and B o o th e 1980).
5. E qual eye deviation does not induce amblyopia E. L.
Sm ith et al. (1 9 9 2 ) reared m onkeys lor betw een 3 0 and
9 0 days with base-in prisms (P o rtrait Figure 8 .1 9 ). This
caused a severe loss o f binocular cells but no shilt in
ocular dom inance, since cells responsive to cither left or
right eye were retained. This procedure did not induce
amblyopia. Also, amblyopia in the same monkeys was
not produced in a subsequent period, in which one eye
was sutured, even though amblyopia was produced by
m onocular suturing applied at the same time in
monkeys reared with normal vision. Thus, amblyopia is
a result o f a shift in ocular dom inance, w hich excludes
one eye from access to cortical cclls. An eye that retains
access to a substantial num ber o f cortical cells is not
am blyopic, even though all binocular cclls arc absent.
6. Enucleation o f the good eye induces recovery A cuity in a
previously occluded eye shows some recovery after
enucleation o f the good eye in the cat (H offm ann and
Lippert 1 9 8 2 ; Sm ith and H oldefer 1985). M onkeys
raised for 4 vears with induced strabismus showed some
Figure я. 19. E a ri Sm ith. F.irl S m ith received b is O .D . and P h .D . from
the U n iv ersity o f H o u sto n and join ed the facu lty o t the C o lleg e o f
O p to m e try a t the sam e university in 1 9 7 8 . H e holds the G reem an -
P ctty P rofessorship in vision d evelopm en t and has been the dean o f
the C o lleg e o f O p to m e try since 2 0 0 3 . H e received th e G len n Fry
Award from th e A m erican A cadem y o f O p to m e try in 1 9 9 6 and the
In tern atio n al G lau co m a Review Award in 1 9 9 9 and 2 0 0 2 . H e was
selected by th e Texas O p to m c tric A ssociation as its E d u cato r o f the
Year in 2 0 0 3 .
recovery o fth e deviated eye after the normal eye had
• J a
been removed. In the deviated eye of one monkey,
grating acuity improved from 0 .2 8 to 6.3 cpd and
sensitivity to flicker increased by 25 H z over an
11-m onth period after removal o fth e nondeviating eye
(H arw erth et al. 1986a). The same type o f recovery has
been noticed in am blyopic humans after loss o fth e
nonam blyopic eye (Vereecken and Brabant 1984).
7 . Reduced evoked potentials Visually evoked cortical
potentials recorded in human strabismic amblyopes are
reduced in am plitude and show longer latency with
stim ulation o l the am blyopic eye than with stim ulation
o f the norm al eye. Patients with alternating strabismus
showed norm al V E Ps for whichever eye was used for
fixation at a particular tim e, and a reduced response for
whichever eye was not used (see Franceschetti and
Burian 1971). There is also reduced interocular
summation o fth e V E P in m onocularly deprived kittens
(Sclar ct al. 1986) and in human amblyopes (Srcbro
1978; Sokol and Nadler 1979).
Patients with small-angle strabismus and anomalous
correspondence showed some evidence o f interocular
summation o fth e V E P , but patients with large-angle
strabismus and binocular suppression showed no
summation o fth e V E P (C am pos 1980; C am pos and
C h icsi 1983). In these studies, there was no control for
effects o f changing accom m odation. However Harris
c t al. (1 9 8 1 ) obtained reduced amplitude, increased
latency, and reduced interocular summation o f the
V E P o f amblyopes in response to a sinusoidally drifting
laser speckle produced as an interference pattern. Such
a stimulus bypasses the optics o f chc eye and renders
results immune to changing accom m odation.
8. Effects o f section ofth e chiasm If strabismic amblyopia were
due to suppression o f inputs from the deviated eye by
those from the nondeviatcd eye, one would expect visual
performance o f the deviated eye to improve after section
o f the chiasm. D i Stcfano and Gargini (1 9 9 5 ) induced
esotropia in 20-day-old kittens. W hen the kittens were
6 8 m onths old, chc chiasm was sectioned. This caused a
large increase in responsiveness to stimuli presented in the
nasal hemificld o f the deviated eye. This supports the idea
that loss o f response to inputs from an esotropic eye is due
to suppression from the nondeviatcd eye.
It can be concluded that amblyopia arises when inputs
from a deprived or deviated eye have reduccd capacity to
com pete lor access to binocular cells in the visual cortex.
Normally, binocular cclls rcceivc stimuli from the two eyes
chat m atch in orientation and m otion. The correlated inputs
allow binocular cclls to acquire m atching tuning for
oriencacion and mocion during che cricical period chrough
long-ccrm pocenciation. W ith m onocular deprivation,
inputs from the cwo eyes arc not correlated. Therefore,
inputs from the norm al eye suppress chose from che deprived
eye by the process o f long-term depression. Consequently,
inputs from che deprived eye fail to guide the tuning prop­
erties o f cortical cells.
8 .4 .6 b T r e a tm e n t fo r A m b ly o p ia
Surgical correction tor strabismus usually produces align­
m ent o f the eyes but does n o t cure amblyopia. In fact, there
is a risk that surgery induces amblyopia (Pratt-Johnson and
Tillson 1 983). In one study, four o u t o f 2 0 patients were
amblyopic before strabism ic surgery but 16 o f the 2 0 were
amblyopic after surgery. Postsurgical exercises over a mean
period of 4 years reduced the severity of amblyopia in most
o f these patients. By com parison, in a group o f 2 0 adults
with early-onset esotropia thac had noc been surgically co r­
rected, only three were amblyopic (G o od e t al. 1993). It
seems that many people with early-onset large-angle esotro­
pia develop norm al vision in each eye, even though they lack
stereoscopic vision (Murray and C alcu tt 1990). C orrection
for strabismus is discussed further in Section 10.2.2e.
A traditional treatm ent for am blyopia is to patch the
good eye. This is known as rev erse p a tc h in g . The idea is
thac che weak eye has m ore chance to recover when the
good eye does noc suppress it. Evidence from animal studies
cited earlier shows that a previously deprived eye recovers
to a greater extent when the good eye is covered. However,
evidence from reverse parching in cars suggests that rhe
deprived eye recovers only at the expense o f the good eye
(M urphy and M itchell 1987).
A sim ilar reciprocal effect has been observed in children
with one eve patched and there is som e risk o f children
developing a double amblyopia if the good eye is occluded
continuously for too long (O d om c ta l. 1 9 8 1 ). Furtherm ore,
recovery o f an am blyopic eye when the good eye is patched
is unstable. For example, when both e y e so fa cat were finally
opened after a period o f reverse occlusion, the relative per­
form ance o f the eyes tended to revert to the prepatching
state (M itch ell 1988b).
Birnbaum et al. (1 9 7 7 ) reviewed 2 3 studies on improve­
m ent o f visual acuity by amblyopia therapy. Although the
methods were not described and there were wide variations
in success rate, there was no evidence thac chcrapy was more
successful in chose under 7 years o f age chan in chose above
this age.
In a m ore recent study, 9 0 % o f a group o f 6 4 strabismic
and anisom etropic amblyopes under 7 years of age showed
some im provem ent o f acuity after various regimens o f
patching over a period o f about 4 m onths. A bout 70 % o f
them showed a doubling o f acuity in the amblyopic eye.
C h ild ren older than 7 years showed less im provem ent after
therapy. However, 6 7 % o f all those that improved showed
some subsequent loss o f acuity in the year following cessa­
tion o f therapy (R u tstcin and Fuhr 1992).
Lee and Iscnberg (2 0 0 3 ) conducted a study on 61 ch il­
dren (ages 3.5 to 8 years) with anisom ecropic amblyopia or
small-angle scrabismus. They were rested during a regimen
o f eye patching that extended over a 36-w eek period. Alm ost
all the children showed a progressive im provem ent in
Snellen acuity with a final im provem ent o f at least 2 lines.
Stereoacuity as measured by the T itm u s Fly test also
improved, especially in the children with anisom etropic
amblyopia who had significant stereoscopic vision before
treatm ent.
It has been proposed that optim al perform ance of both
eyes is achieved by pacching che good eye fo r abouc h alf che
cime, with binocular vision allowed for the o ther halt
(M itch ell e t al. 1986). However, a retrospective study o f
3 1 7 patients over a period ot 15 years revealed no difference
betw een the effects o f part-tim e and full-tim e occlusion
therapy applied before or after 1 year o f age (Ross-D im m est
and M orris 1990; Simmers et al. 1 9 9 9 ). In another regimen,
known as penalization, the image in the good eye is o p ti­
cally blurred so as to reduce suppression o f the image in the
am blyopic eye (see Fahic 1983).
Strabism ic amblyopia has been reviewed by M itchell
( 1988c), and the effects o f different regimens o f occlusion
on recovery from early m onocular deprivation in kittens
and their relevance to humans has been reviewed by M itchell
(1 9 9 1 ). Tlicrapies for amblyopia have been reviewed by
G arzia (1 9 8 7 ).
8 .4 .6 c E ffects o f Visual T rainin g on A m blyopia
Ir has been assumed in clinical practice that treatm ent for
amblyopia is ineffective after die age o f about 8 years.
However, evidence is accum ulating thac adulcs rcrain suffi­
cien t cortical plasticity to allow them to improve vision in
an am blyopic eye.
It has been claim ed that vision in an am blyopic eye is
improved byexposingtheeye to a rotatinggraring(Cam pbell
et al. 1 9 7 8 ). However, ochers failed to replicate chis effect
(M itch ell c t al. 1983).
Adult amblyopes showed some improvement o f vernier
acuity with 5 to 10 hours o f practice. However, as with
people with normal eyes, the im provem ent was specific to
the task and to the orientation o f the stimulus (Fahle 1997;
Levi c ta l. 1997).
Polat et al. (2 0 0 4 ) obtained a tw o-fold improvement in
contrast sensitivity and letter-recognition in a mixed group
o f adult amblyopes after an unspecified period o f training.
Training consisted o f the detection o f a patch o f grating in
various orientations presented alone o r Hanked by high-
conrrast gracing pacches, wich various separations between
target patch and Banking patches (see Polat 2 0 0 4 ). Zhou
et al. (2 0 0 6 ) obtained a 6 4 .4 % im provem ent o f contrast
sensitivity and a 4 5 % im provem ent in grating acuity in a
group o f 2 3 anisom etropic amblyopes aged 14 to 2 7 years.
The patients were trained with 1-liour sessions tor 12 days
to dccccc gracings over a wide range o f spacial frequencies.
The im provements were substantially retained when the
patients were tested 12 m onths later.
Six o f a group o f 11 am blyopes betw een the ages o f 14
and 2 8 showed a 2 0 % mean reduction o f the contrast
threshold for letter identification after 1-hour training ses­
sions extended over 8 days. Im provement transferred trom
training with lum inance-defined letters ro testing with co n ­
trast-defined letters but n o t to an acuity task using letters
(C h u n g e t al. 2 0 0 8 ).
Li e t al. (2 0 0 8 ) asked w hether training over a longer
period than those used in previous experim ents would gen­
erate greater im provement. They trained seven amblyopes
aged betw een 18 and 4 0 to d etect m isalignm ent o f two
horizontal rows o f G abor patches. Training sessions o f 1.5
hours were given for 5 0 days. Positional acuity o f the ambly­
opic eye improved gradually over the 50-day period, until it
reached the level o f the norm al eye. Im provem ent was more
rapid with those with milder am blyopia. The improvement
was retained when tests were repeated 2 m onths later.
All these results indicate that the adult visual system
retains some neural plasticity. Levi and Li (2 0 0 9 ) have
reviewed the question o f whether perceptual training can
be a treatm ent for amblyopia.
8 .5 AM BLYOPIA AND STEREO PSIS
8. 5. 1 AMBLYOPIA AND S T E R E O A C U I T Y
People with early strabismus, anisom etropia, o r uniocular
cataract surfer partial or com plete loss ot binocularity (Levi
c t al. 1 9 7 9 ; Hess et al. 1 9 8 1 ). Those with severe strabismus
fail tests o f stereopsis w hether or n o t their strabismus is
accom panicd by am blyopia (C o o p er and Feldman 1978b ).
Thus, the crucial factor in loss ot stereopsis is strabismus
rather than amblyopia. However, amblyopes with stereo­
scopic vision show raised contrast thresholds tor detection
o f depth in random -dot stereograms (W ood et al. 1978).
There is usually only a partial loss o f binocular cells with
anisom etropic am blyopia and with strabismus o f less than
3 ° . In these conditions, loss ot stereopsis and binocular
sum m ation o f threshold stimuli is confined to high spatial-
frequency stim uli and is thus m ost evident in the foveal
region. Therefore, for small-angle strabism ic amblyopes,
stereopsis and binocular sum mation can be norm al for low
spatial frequency stim uli, and the loss is not evident in the
visual periphery (H olopigian et al. 1986). The same is true
o f people with alternating strabismus (Siretcanu 1982).
People with Jarge-angle strabismus or severe anisom etropic
amblyopia surfer com plete loss o t stereoacuity.
A patient with astigm atic anisom etropia that reduced
acuity only tor horizontals in the arfcctcd eye had normal
stereopsis (Pelli 1 983). Stereopsis depends on good acuity
tor verticals, and this was n o t affected in this patient.
It is shown in Section 3 1 .5 .2 that stereopsis is n o t a uni­
tary ability. A person can be blind for m otion-in-depth
while possessing normal stereoscopic acuity for stationary
objects. A lso, selective loss o l one type ot stereopsis can be
confined to one area o f the visual field. Static stereopsis and
m otion-in-dcpth stereopsis are also differentially affected
by early strabismus (Sch o r et al. 1983). Many subjects in
whom the angle o f strabismus was between 2 and 5 ' lacked
both static and m otion-in-depth stereopsis in the central
visual field bur n o t in the peripheral field. Subjects with
strabismus angles betw een 6 and 10° had lost static stereo­
scopic vision in the whole field, although many o f them had
m otion-in-depth stereopsis in the peripheral field (K itaoji
and Toyama 1987).
Som e stereodeficient subjects could discrim inate depth
produced by disparity betw een the envelopes o f G abor
patches (second-order) even though they could n o t detect
that produced by the disparity o f the carrier grating within
the envelope. These subjects also failed standard tests ot ste­
reopsis (M cC o ll e t al. 2 0 0 0 ). The experim enters concluded
that som e stereodeficient subjects are able to process sec­
ond-order disparities. However, the disparity o f the enve­
lope is necessarily on a coarser spatial scale than the disparity
contained in the carrier grating. This may be why stercodc-
ficient subjects can detect only envelope disparities.
Thom pson and Nawrot (1 9 9 9 ) found 10 strabismic
amblyopes to be defective in both stereoacuity and depth
discrim ination based on m onocular m otion parallax, even
when the m otion parallax stimulus was presented ro the eye
with normal acuitv and contrast sensitivity. They concluded
Ф 4 4
that strabismics have a general d efect o f depth perception.
However, in a later paper, Nawrot et al. (2 0 0 8 ) produced
evidence that loss o f sensitivity to m otion parallax in eso­
tropes is due to their abnorm al pursuit eye movements.
These abnorm alities were described in Section 8.4.5.
Sue Barry, a professor ot neurobiology. had early strabis­
mus that had been surgically corrected. She did n o t have
amblyopia but had no stereoscopic vision. W h en she was
4 8 years old she began a series o f training exercises in which
she learned to converge her eyes on the same o bject. She
gradually acquired stereoscopic vision. She recorded her
experiences in a book in which she also reports other sim i­
lar cases (B arry 2 0 0 9 ).
8.5.2 A M B L Y O P I A AND B I N O C U L A R
SUPPRESSION
In strabismus, corresponding regions in the two retinas
receive images from distinct regions o t space. For well-sepa­
rated o b jects this produces diplopia. For closely spaced
objects that differ in shape, corresponding retinal regions
receive distinct images that undergo rivalry. This gives rise
to the symptom called co n fu sio n . M any people w ith stra­
bismus o f early onset overcome these symptoms by sup­
pressing vision in the deviating eye, although they can see
wich chat eye when ic alone is open. This is known as sc ra ­
b ism ic su p p re ssio n . It seems to have been firsc reported by
von G raefe (1 8 5 4 ).
Travers (1 9 3 4 ) conducted early experim ents
readied chc following conclusions. W h en boch eves are
open, strabism ics have beccer access со inform ation pre­
sented со cheir normal eye than со chac presented со the
deviating eye. Also, stimuli seen by che norm al eye are noc
affected by com peting scimuli presented to che deviating
eye. In alternating strabismus, che eye used at a given time
for fixation suppresses the nonfixating eye. Strabism ic sup­
pression cakes a second or cwo ro develop after the nondevi­
ating eye has been opened.
It has been claim ed that scrabismic suppression is more
pronounced in the nasal hem iretina chan in che temporal
hem iretina, especially in esotropes (Section 8.4.2a).
Jam polsky ( 1 9 5 5 ) found that suppression in exotropia
occurs only w hen the image in thcdeviacingeye falls on the
cemporal hem iretina. Patients experienced diplopia when a
prism took the image into the nasal hem iretina. He co n ­
cluded that suppression in exocropia is confined со che tem ­
poral hem iretina and that suppression in esotropia is
confined to the nasal hem iretina.
Pratt-Johnson and T illson (1 9 8 4 ) agreed with these
findings but questioned the conclusion. The image in the
deviating eye o f an o b je ct fixated by the nondeviating eye
normal vision during binocular rivalry (D ale 1982).
However, the tw o types o f suppression differ in the follow ­
ing ways.
and
1. Strength o f suppression Suppression is stronger in
normal rivalry than in strabismic suppression
(H olopigian et al. 1988).
2. Suppression o f sim ilar images In normal vision, similar
images show binocular facilitation, and suppression
occurs only between very dissimilar images. For
instance, when observers with normal vision view
dichoptic vertical gratings rocatcd o u t o f alignm ent by a
few degrees they see a fused image o f a slanting surface.
G ratings rival only when chey are misaligned by many
degrees. In strabism ics, suppression occurs betw een
both similar and dissimilar images (Sch o r 1977).
Strabism ics suppress the image in the deviating eye even
when the gratings have a very sim ilar orientacion. Thus,
people wich normal vision have a suppression
m echanism for strongly dissimilar images and a fusion
mechanism for sim ilar images, whereas strabismics have
only a suppression m echanism lor both sim ilar and
dissimilar images.
C clls in the visual cortices o f strabism ic cats and
monkevs did not exhibit binocular facilitation to
4

falls on the nasal hem iretina in esotropia and on the tem po­
ral hem iretina in exocropia. Pracc-Johnson and Tillson
found chac, under these circum stances, suppression involves
che whole binocular field o f che deviating eye, except for the
m onocular crescent. However, suppression is noc triggered
when a prism brings the image in the deviacing eye into the
opposite hem iretina. The pacienc has nor acquired rhe abil­
ity to suppress the deviating eye under these unusual cir­
cum stances and therefore experiences diplopia.
It is generally agreed that, in the m onofixation syn­
drom e, suppression is lim ited to a scotom a in one retina
(see Section 1 0 .2 .4 f). Suppression o f one eyes image also
occurs in anisom etropic amblyopia, but the depth o f sup­
pression is less than that in strabism ic amblyopia (H olopigian
e ta l. 1 988).
For subjects with normal vision, vernier acuicy for a cargec
presented to one eye is degraded by chc presence o f a similar
cargec wich a fixed horizoncal olfsec presented со che ocher eye.
This is known as crowding (Seccion 8.4.3b). For amblyopes,
vernier acuicy was noc affected when the cargec was presenced
со the good cvc and chc compccing cargec was presenced со chc
amblyopiceye( M cKeeand Harrad 1993). Eleccrophysiological
evidence o f scrabismic suppression has been reported in V I
and M T o fth e monkey (Thiele et al. 1997).
It is com m only assumed that strabismic suppression is
an exrreme form o f suppression observed in people wirh
similarly orientated drifting gratings. But stim ulation
o f che deviated eye suppressed the responses o f cells to
stim uli in the nondeviated eve, whatever the relative
orientation o f the stimuli (see Sengpiel and Blakemore
1996).
In animals with normal vision, binocular facilitation
develops because scimuli wich macching features tend
to fall on or near corresponding points. This produces
synchronized neural accivicy, w hich strengthens
short-range facilitator у neural connection s through the
Hcbbian-synapsc m echanism . Lack o f synchrony
betw een nonm atching stimuli leads to the form ation o f
long-range inhibitory lateral connections. In strabismic
animals, stimuli with m atching features do not fall on
corresponding points and therefore do noc produce
synchronous activity. Thus, the short-range binocular
facilitation m echanism fails to develop in strabismics,
leaving only che long-range inhibicory m echanism .
3. Chromatic vs. achrom atic suppression Suppression
during normal binocular rivalry causes a greater
reduction in sensitivity o f the chrom atic mechanism
than o f che achrom atic mechanism (Section 1 2 .3 .2 f).
By com parison, strabism ic suppression involves an
equal loss o f sensitivity in the two mechanisms
( Smi t h e t al. 1985a).
 9
IMAGE F O R M A T I O N AND A C C O M M O D A T I O N

9 .1 lin a g e r e s o lu t io n 435 9 .6 .1 T h e b lu r s tim u lu s 453

9 .1 .1 M o n o c h r o m a t i c a b e r r a t io n s 435 9 .6 .2 B lu r d e t e c t io n 454
9 .1 .2 C h r o m a t i c a b e r r a t io n s 4.<7 9 .6 .3 B lu r d is c r im in a t io n 455
9 .1 .3 M e a s u re s o f im a g e q u a lit y 43$ 9 .6 .4 D e p t h o f fie ld a n d a c c o m m o d a t io n a c c u r a c y 457
9 .1 . 4 C o m p e n s a t io n o f a b e r r a t io n s 441 9 .6 .5 N e u r a l c o m p e n s a t io n f o r im a g e b lu r 459
9 .1 . 5 T h e N y q u is t lim it a n d a lia s in g 44! 9 .7 A c c o m m o d a t i o n t o d e f o c u s b lu r 161
9 .2 M a c h i n c r v0 o f a c c o m m o d a t i o n 441 9 .7 .1 S te a d y -s ta te a c c o m m o d a t io n 4(>l
9 .2 .1 O p t i c s o f a c c o m m o d a t io n 443 9 .7 .2 D y n a m ic s o f a c c o m m o d a t io n 462
9 .2 . 2 T h e m e c h a n ic s o f a c c o m m o d a t io n 444 9 .7 .3 R e s p o n s e t o u n e q u a l a c c o m m o d a t iv e d e m a n d 464

9 .2 .3 P h y s io lo g y o f a c c o m m o d a t io n 447 9 .8 C u e i n g t h e s ig n o f a c c o m m o d a t i o n 465
9 .2 .4 M e a s u r in g a c c o m m o d a t io n 44$ 9 .8 .1 H u n t in g a n d d y n a m ic e r r o r f e e d b a c k 465
9 .3 T o n ic a c c o m m o d a tio n 450 9 .8 .2 B lu r s ig n a n d le n s a b e r r a t io n s 466
9 .3 .1 *1 h e t o n i c s t a t e o f a c c o m m o d a t io n 450 9 .8 .3 B lu r sig n a m i t h e S t ile s - C r a w f o r d e f f e c t 468
9 .3 . 2 A c c o m m o d a t iv e a d a p t a t io n 45/ 9 .9 A n is o m e tr o p ia a n d a n is e ik o n ia 469
9 .4 V o l u n t a r y4 a c c o m m o d a t i o n 452 9 .9 .1 R e la t io n o l a n is o m e t r o p ia t o a n is e ik o n ia 469
9 .5 P r o x im a l a c c o m m o d a tio n 452 9 .9 .2 M e a s u r e m e n t o f a n is e ik o n ia 471
9 .6 D e t e c t i o n o f d e f o c u s b lu r /5 3 9 .9 .3 A d a p ta tio n t o a n is e ik o n ia 473

9 .1 IM AGE R E SO L U T IO N C onsider a beam o f rays approaching the eye and

9. 1 . 1 M ON O CH RO M A TIC ABERRATIONS
Ideally, the wavefront o f the converging beam o f light rays
em erging from the lens is a spherical surface orthogonal со
the rays. The curvature o f the wavefront closely m atches
the curvature o f the retina. The eye form s a wide-angle
optical system (see Navarro 2 0 0 9 ).
M onochrom atic aberrations are distortions o f the wave-
front o f m onochrom atic light. They can be measured by
objective or subjective ray-tracing o r by Harcm ann-Shack
wavefront sensors. The wavefronts produced in human
eyes have com plex shapes chac vary from person со person
and wich the accom m odative state o f the eye. The main
com ponents o f m onochrom atic aberration are as follows.
Spherical aberration Spherical aberration arises
primarily from differences in the refractive power o f
chc lens ac ditfcrcnc distances from che opcic axis.
parallel to the visual axis, as in Figure 9.1a. The rays
thac strike the margins o f che lens (marginal rays) arc
refracted to the marginal p oint. A t this point, the
density o f rays (lig h t intensity) is greatest around the
perim eter o f the blur circle. Rays near the visual axis
(paraxial rays) are refracted to chc paraxial poinc.
At this p oint, ray density is greatest at the center o f the
blur circle. The b lu rcirclc has the smallest diam eter at
the waist. Positive spherical aberration is the distance
in diopters betw een chc marginal poinc and the
paraxial point. Ic is usually measured by observing che
images formed by annular apertures o f ditfcrcnc radii.
Typically, che marginal image form ed by che edge o f
a 4-m m -diam etcr pupil o f an unaccom m odated eye
has a spherical aberration o f about 1 D . This defines
the radially sym m etrical com ponent o f spherical
aberration. M ost eyes have a positive aberration when
unaccom m odated. The aberracion is reduced when che
eves accommodace со a near discancc and becom es
m

For a posicive aberration, che wavefront is more curved negative for som e eyes (A tchison et al. 1 9 9 5 ; H e ec al.
chan the ideal wavefronc, as shown in Figure 9.1a. 2 0 0 0 ). Spherical aberracion is rcduccd when chc pupil
For a negative aberration, the wavefront is less curved constricts so that it covers the more curved parts o f the
chan the ideal wavefronc, as shown in Figure 9.1b. lens, as shown in Figure 9.1c.
 Ideal w a ve fron t M arginal Paraxial
A ctual w avefront
(a) Positive spherical aberration.
F«p»c*,2 . A trigm atisnu T h is lens has greater refractive pow er a lo n g the
vertical m erid ian ( Y ) than along the h o rizo n tal m eridian ( X ) . Assume
th at a parallel beam o flig h t arrives ac the lens. R ay bundles parallel to
the Y m erid ian arc focuscd a lo n g th e near fo ca l lin e. R ay bundles
parallel to th e X m eridian arc focused alo n g the f i r fo ca l line.
(b> N egative spherical aberration.
(c) Less aberration w hen the iris covers cu rved parts o f the lens.
l’<A«r« 9. i. S p h ericalaberration .
Astigmatism This is a cylindrical com ponent ol
spherical aberration. The image is n o t simultaneously
in focus along different meridians, as shown in
Figure 9.2. In m ost eyes, the cylindrical com ponent
o f spherical aberration is the dom inant com ponent
(H ow land and Howland 1977).
Coma This is due to cither asymmetrical spherical
aberration (astigm atism ) or m isalignm ent o f the eyes
optical com ponents.
Light scatter l i g h t scatter occurs at the surfaces o t the
cornea and lens and by internal reflection. The tear
layer on the outer cornea reduces scatter by sm oothing
out roughness in the epithelium.
Distortion M ore com plex optical distortions due ro
irregularities in the curvature ot the lens show as
deform ations o f che image o f a rectangular grid
o f lines. Given that the distortions are constant,
neural mechanisms arc able to compensate
tor them.
Diffraction In an optical syscem wich no aberrations or
light scatter, the image o f a point o flig h t is blurred by
diffraction at the edge o f che aperture. The image o f a
point o f m onochrom atic light is a central luminous
disk, know n as A iry ’s disk, surrounded by bright and
dark rings o f dim inishing luminance. The rings occur
because light waves alternately sum and cancel round
the edge o f the pupil. The angular diam eter o f the disk,
0 , is:
в (l)
where A is the wavelength o f the light and a is the
diam eter o fth e eyes entrance pupil, in the same units.
Thus, Ai rvs disk increases in size as the wavelength o f
light increases and as pupil diam eter decreases. For a
pupil diam eter o f 3 mm and a wavelength o f 5 5 0 nm,
about 7 5 % o f the light from a point is contained in
A irys disk, which spreads over about three cones in che
ccntral retina, as shown in Figure 9 .3 ( O ’Brien 1951).
In m onochrom atic light, blur o f a central image is due
mostly to diffraction for pupil diameters up to about
2 mm. The eye is said to be diffraction lim ited.
At larger diameters, spherical aberration becom es
the dom inant factor in m onochrom atic light.
Defocus blur 'I he image o f an o b ject becom es
more blurred as the o b ject’s radial distance from
the p o in t where the eyes are accom m odated increases.
A dcfocuscd image has less contrast than an in-tocus
image (W alsh and Charm an 1989). D efocus blur is
under feedback con trol, since it changes when the eyes
accom m odate.
Object blur M osc sol ill objects have sharp edges.
Textures, such as wood grain and patterns on the skins

6 yjm o r 75 arcsec
Figure 9.3- R etin al im ages o ftw o p oin t sources. Til с upper c) i agram show s that
A iry's disk spreads over up to seven retinal c o n c s. The low er diagram
showv the lu m in an ce di$tribu tion$ o f tw o n eig h b o rin g p o in t * o f light.
(Rnjr.iwn |VomEimlc? 1952)
o f animals, are typically blurred, as are clouds, shadows,
and poorly focused photographs. Such o b jccts have
o b ject blur, which is not under feedback control and
therefore rem ains as the eyes accom m odate on the
blurred o b jcct.
9.1.2 CHROMATIC ABERRATIONS
C hrom atic aberration is due to differences in the refraction
o f different wavelengths. For white light, chrom atic aberra­
tion is the largest factor determ ining image quality (van
M eeteren 1 974). C hrom atic aberrations may be effectively
canceled by an achrom atizing lens w ith a com bination ot
glasses o f ditferent refractive indexes. This is n o t possible
with the lens o l an eye with a high water content. C hrom atic
aberration o f the eyes is therefore not optically corrected.
However, we will see that its effects are corrected by a neural
mechanism .
9 .1 .2 a L ongitu din al C h r o m a tic A berration
Longitudinal chrom atic aberration is due ro shorter wave­
lengths being m ore strongly refracted than longer wave­
lengths (Wald and G riffin 19 4 7 ; Bedford and Wyszecki
1 9 5 7 ). Thus, the wavelength com ponents o f a point o f
w hite light produce a scries o f images at dirfcrent distances
Irom the retina. A t any instant, the person can accom m o­
date on only o n e o f the images, leaving the others blurred.
For example, when the image form ed by long wavelengths
(red light) is in focus, the image form ed by short wave­
lengths (blue light) falls short o f the retina and creates a
blurred image, as illustrated in Figure 9.4. W h en the blue
image is in focus, the red image falls beyond the retina.
There seem to be wide individual differences in the wave­
length that is habitually brought into clear focus (C ooper
and Pease 1988).
Longitudinal chrom atic aberration may be measured
by having the su bject binocularly fixate a distant target
while accom m odation o f one eye is measured for a target
viewed only by that eye. D ifferences with m onochrom atic
light o f different wavelengths indicate the longitudinal
com ponent o f chrom atic aberration. M ethods of measuring
accom m odation are described in Section 9.2.4.
O bjective m ethods of measuring longitudinal aberra­
tion, in which the investigator observes the retinal image,
agree closely with subjective m ethods, in which the subject
makes settings. The small difference is probably due to the
fact that objective m ethods use light reflected from a retinal
layer that differs from the layer where the image is registered
(C harm an and Jen nin gs 1976) (P ortrait Figure 9.5).
Longitudinal aberration is expressed as the difference
in accom m odation in diopters for an o b ject illuminated
in m onochrom atic light o f two specified wavelengths.
Howarth and Bradley (1 9 8 6 ) reported an average value
o f chrom atic aberration of 1.82 D betw een wavelengths
o f 4 2 0 and 6 6 0 nm. Longitudinal chrom atic aberration
increases only slightly with increasing retinal eccentricity
(R y n d erseta l. 1998).
Focus point
for red light
L on g itu d in ala n d transverse (brotn atic aberration s, Ih c sch em atic
eye has a single refractive surface w ith a n od al p o in t a t its cen ter of
curvature. D ifferen t w avelengths o f lig h t passing throu gh the nodal
p o in t arc refracted equally. Гог o th e r rays, blue light is refracted m ore
than red light. T h is eve is acco m m o d ated o n the im age produced by red
lig h t, leaving the im age produced by blue lig h t o u t o f focus.
(AdifttJ from !li»bo* ct j I . 1990)

Fijpr*9.5. W. N eilC barm an . B<»rn in B rig h to n , E n glan d , in 1 9 3 7 . A fter
d o cto ra l and p o std o cto ral work on visual m icroscopy at Im perial
C o lleg e, he worked at th e N ation al Research C o u n c il in O ttaw a and
th en as S e n io r S cien tific O fficer a t the A to m ic E n ergy Research
E stab lish m en t in H arw ell. In 1 9 7 0 he m oved to an academ ic
ap p o in tm en t in the D e p a rtm e n t o f O p h th a lm ic O p tic s at the
U niversity o f M an ch ester. In 1 9 9 7 he becam e head o t the D ep artm en t
o f O p to m e tr y and N eu roscience. H e retired in 2 0 0 2 . H e is a fellow о f
th e In stitu te o f Physics an d o f the O p tic a l S o c ic ty o f A m erica. 1 Ic won
th e O w en Aves M ed al in 1 9 9 6 and the Prentice M edal o f the A m erican
A cadem y o t O p to m e try in 2 0 0 5 .
9 . 1 . 2 b T ran sv erse C h r o m a tic A b e rra tio n
Transverse chrom atic aberration arises because different
wavelengths refract со different retinal locations, as shown
in Figure 9.4. It is expressed as the visual angle betw een the
images formed by an o b ject illum inated by two specified
wavelengths. There is one visual axis tor which red and blue-
light fall on the same retinal location. This is rhe a c h r o ­
m a t ic a x is . It the pupil and fovea were centered on the eye s
optic axis, the achrom atic axis would pass through the fovea
and there would be no transverse chrom atic aberration tor
an o b je ct imaged on the fovea. H ie aberration would
increase with increasing retinal eccentricity. However, the
visual axis through the fovea is displaced trom the optic axis
by the angle a . In addition, the pupil may not be centered
on the optic axis. These factors usually cause blue light from
a fixated o b ject to fall m ore to the nasal side o f the retina
than red light from the same object.
O ver a sample o f subjects, transverse chrom atic aberra­
tion at the fovea varied betw een 7 3 and 109 arcsec (Sim o n et
and Cam pbell 1990). Differences could be due to differences
in angle O. and/or to different offsets o t the entrance pupil
from rhe optic axis. An aberration caused by one o f these
factors could be partially canceled by the other factor.
For pupil sizes o f 3 to 5 m m , longitudinal chrom atic aberra­
tion produces more image blur than transverse chrom atic
aberration (C am pbell c t al. 1990).
Transverse chrom atic aberration causes the image ot
an o b jcct produced by red light to be larger than the
im age produced by blue light. Therefore, the aberration
increases with increasing distance from the achrom atic axis
(T hibos 1987). However, the increase does not have much
effect on visual acuity because o t the low spatial resolution
o f the peripheral retina. Transverse chrom atic aberration
may help to reduce the effects ot aliasing o t high-frequency
gratings in the peripheral retina (Section 9 .1 .5 ). Both types
ot chrom atic aberration increase slightly as the distance ot
a viewed o b ject decreases (C harm an and Tucker 1978b).
Transverse aberration in the retinal periphery is difficult
to measure because o f the poor resolving power outside
the fovea. But the principal factor tor transverse chrom atic
aberration is not retinal eccentricity but rather the in ci­
dence of the principal ray on the cornea. This can be varied
by holding the stimulus in a central position and moving
a pinhole aperture near the eye to different locations
with respect to the pupil. This keeps the image on the fovea.
Isaac New ton used this procedure in 1670 to demonstrate
chrom atic aberration.
Thibos et al. ( 1 9 9 0 ) used the following procedure to
measure transverse chrom atic aberration. The ciliarvj rnus-
cles were paralyzed and the pupil dilated. Two vertical black
rods were presented, one above the other, one on a red back­
ground and the other on a blue background. A pinhole
aperture was moved ro different locations in front o f the
pupil. Transverse chrom atic aberration caused the images o f
the tw o rods to tall out o t alignm ent. For example, when
the pinhole was on the tem poral side o f the pupil, the line
on the blue field appeared more temporal than the line on
the red field, 'flic m ovem ent required to bring the tw o lines
into vernier alignm ent provided a measure ot transverse
chrom atic aberration for that angle o f incident light. The
aberration increased almost linearlvi to about 0.33° as the
aperture was moved to a position 4 mm from the center o f
the pupil.
C hrom atic aberrations affect depth perception in two
ways. First, they produce chromostereopsis, as described in
Section 17.8. Second, they indicate whether the eye is undcr-
or overaccom m odated, as described in Sections 9.6.2 and
25.1.4. The visual system adapts to chrom atic aberrations,
and this process is probably responsible for color-contingent
aftereffects that were described in Section 4.2.9c.
9.1.3 M E A S U R E S OF IM AGE Q U A L I T V
9 . 1 . 3 a P o in t- an d L in e -S p re a d F u n c tio n s
The distribution ot light over the image o t a p o in t is the
p o i n t - s p r e a d f u n c t i o n , described in Section 3.2.4. The dis­
tribution o t light across the image o f a thin line is the
lin c-sp rcad fu n ctio n . For an aberration'free eye and a
given wavelength o t light, blur o t the in-focus image ol a
fine point or line is due only to diffraction o f l i g ht at the
edges o fth e pupil. Since the degree o fd itfractio n is inversely
proportional to pupil diameter, blur due to diffraction can
be calculated, as indicated in Section 9.1.1.
It is difficult to calculate image blur due to the co m ­
bined effects o f all the optical aberrations o f the eye.
Therefore, the actual point-spread function must be m ea­
sured by scanning a photom eter over rhe image. Postm ortem
changes affect measurements made on an excised eye ot a
cadaver. M easurements must therefore be perform ed on a
living eye. An image ot a bright line is form ed on the retina
and a photom eter is scanned over a secondary image o f the
line created in space by reflection o f the retinal image.
Flam ent ( 1 9 5 5 ) was the first person to use this d ou ble-p ass
p ro ced u re (see van M eeteren 1 9 7 4 ). C am pbell and Gubisch
( 1 9 6 6 ) used it to produce the line-spread functions shown
in Figure 9.6.
The wider the line-spread function, the lower the ability
o f the eye to resolve a grating. The line-spread function
resulting from diffraction imposes an upper limit on the
spatial frequency o f a sine-wave grating that can be imaged
on the retina. This c u to ff frequ en cy in cycles per degree is
given by:
'<«•" 9.6. L in e-spread fu n ction s o fth e hum an eye. E ach curve is the
n orm alized d istrib u tio n o f illu m in an ce in the foveal im age o f a th in
(2) lin e, m easured as d escribed in the tex t. T h e narrow er curve in each case
C u t-off frtxiuencv = ^ in radians or —^ -—
1 ' Я Я 57.3 in d icates the calcu lated d iffractio n im age o l the line a t the given pupil
d iam eter. (л&рмс! (тшСш-рМ! ямЮяЫкЬ iмне-)

where d is the diam eter o f the pupil and Я is the wavelength

o f the light. Aberrations other than diffraction reduce the
c u to ff frequency below this theoretical lim it. However, a
wider point-spread function may improve the detectability
o f the position o f an image because more receptors are stim ­
ulated, which can provide an improved estimate o f the
mean position o f the stimulus.
The line-spread function depends on pupil diam eter in
a com plex way, as shown in Figure 9.6. As the pupil enlarges,
diffraction decreases and spherical aberration increases.
A t m oderate light levels, a diam eter o f about 2 mm achieves
the best com prom ise between these effects. In dim light,
che pupil dilates to allow m ore light in to the eye at the cost
o f lowering image quality. A t pupil diam eters less than
about 2 mm, m ost light dispersion is due to diffraction, and
the optical system can be treated as linear.
9 .1 .3 b T h e M o d u la tio n T ra n sfe r F u n c tio n
W h en a sinusoidal grating o f a given spatial frequency is
transm itted through an optical system, its am plitude o f
luminance m odulation is attenuated by the summed effects
o f aberrations, diffraction, light loss, and light scatter. The
function relating the attenuation o f luminance modulation
to spatial frequency is the m od u lation tran sfer fu n ctio n ,
or M T F , o f the system (see Figure 9.7).
The contrast o f a grating is usually indicated by
M ich clso n c o n tra st, which is the lum inance modulation
divided by the sum o f the maximum and m inim um lum i­
nances, as shown in Figure 3.8.
Th e M T F o f the eyes optical system relates the propor­
tional loss o f contrast in the image to the spatial frequency
o f a sinusoidal grating. The M T F is obtained by measuring
the contrast o f t h e retinal image o f a sinusoidal grating o f
fixed contrast at each spatial frequency over the visible range
o f spatial frequencies. M easurements arc made by the dou­
ble-pass procedure in w hich a ph otod etector is scanned
over the aerial image o f a grating reflected back o u t o f the
eve. The measurements are corrected for the effects o f che
double traverse o f the light through rhe eye. If there is no
loss o f contrast, contrast transmission is 1. If all concrasc is
lost, contra.sc transmission is 0, and the image a hom oge­
neous grey patch.
Figure 9 .7 A shows the theoretical m odulation transfer
functions o f an aberracion-freeeye for m onochrom atic light
o f 5 4 0 nm and various pupil diameters. Ic can be seen that
as pupil diam eter is reduced, the effects o f diffraction
increase, and the M T F declines m ore steeply with increas­
ing spatial frequency.
 Figure 9 .7 B shows chac alm ost all che concrasc in the
stimulus is preserved at spatial frequencies below about
5 cpd. W ith a small pupil, contrast for a grating o f about
4 0 cpd is reduced about 10-fold. Above about 6 0 cpd, all
contrast in the image is lost. This means that the system
does resolve gratings above this spatial frequency. As pupil
diam eter increases, optical aberrations increase, and the
high-frequency lim it is reduced, as shown in Figure 9 .7 B .
M odulation transfer functions can be normalized to the
highest spatial frequency transm itted by an ideal diffrac­
tion-lim ited system, as shown in Figure 9 .7 C . Any depar­
ture from the ideal is due to factors other than diffraction,
such as spherical and chrom atic aberrations and light scat­
ter in the optical media (C am pbell and G ubisch 1966).
The M T F o f any linear optical system can be calculated
from its line-spread function, as explained in S ection 3.2.4.
The line-spread function is the Fourier integral of the M T F.
The M T F for an image form ed by rays near the optical
axis o f the eye shows higher contrast sensitivity than the
M T F for an image form ed by light entering the eye o ff
axis. This effect was investigated by measuring the M T F
for different positions o f an artificial pupil w ith respect
to the optical axis (van M eeteren and Dunnew old 1983).
The effect was present with a 2-m m artificial pupil, which
produced off-axis com a. It was absent with a 0.8-m m pupil,
which indicates that image quality is diffraction-lim ited at
all eccentricities lor this size ol pupil.
If the eye is astigm atic, the M T F will vary with the
orientation o f the rest grating.

9 .1 .3 c M easurin g W av efron t A berration s

For a point o b je ct the wavefront o f converging light rays

em erging from an ideal optical system is spherical, and the
rays intersect at a point. A n optical aberration distorts
the wavefront, and the rays no longer intersect at a point.
The extent to w hich different portions o f the wavefronc
depart from spherical is the w avefront a b erra tio n . Each
type o f aberration produces a characteristic wavefront
N orm alized spatial fre qu e ncy o f grating
aberration.
An a b erro m eter is an instrum ent for measuring wave- 1'igun 9 ". M odulation transferfunctions o f th e eye. (Л ) I h co rctica l
front aberrations. In early versions, the retinal image o f a m od u lation transfer fu n ctio n s for an im age using light o f 5 4 0 n m in an
square grid seen in m onochrom atic light was photographed ab erratio n -free cvc for various pupil d iam eters. ( A d j p t t J &•>» W tod a n d c h « m a n
IW5). ( B ) Transfer fu n ctio n s for four pu pil sizes from m easu rin g light
and the distortions in the image o f the grid were analyzed.
reflected from the foveal im age o f a gratin g. T h e fu n ctio n s result Irom
W avefront aberrations can now be recorded and loss o f co n tra st due to d iffractio n and op tical aberrations. (A J a p u s l from

analyzed in real time. A narrow beam o f infrared light is с*юрМ‘ м<1СпЫиЬ 1966) ( C ) Transfer fu n ctio n s n orm alized to th e highest

projected onto the retina. l ight reflected from the retina
is passed through an array o f small lenses o n to a charge-
coupled d etecto r known as a H a rtm an n -S h ack sensor.
spatial freq u en cy tran sm itted by a d iffractio n -lim ited system w ith light
o f 5 7 0 n m . E m p irical fu n ctio n s d ep art fu rth er from ideal fu n ctio n as
pupil size increases spherical and ch ro m atic ab erration s. {Ad»|.t<d6o«
С *л р Ь « и « v J G p Iu k Ii 1 9 6 $ )

Each lens creates a spot image. T h e locations o f the spots

relative to those produced by a perfect wavefront indicate
rhe slopes o f the local wavefronts. The distortions are
com puted into a set of orthogonal functions, known as
Xernikc polynom ial basis functions. These functions also
indicate the rate at which aberrations increase as pupil
diam eter is increased. 'Ih e functions correspond to the
classical m onochrom atic aberrations ot the eye (W alsh et al.
1 9 8 4 ; Artal c t al. 2 0 0 1 ). However, the m ethod does not
measure effects o f chrom atic aberration, and the results do

Figure9 .4 . D av id W illiam s.. I Ic o b ta in ed a B .S. from D en iso n U niversity
in 19 7 5 and a P h .D . from the U niversity o f C a lifo rn ia a t San D ieg o in
1 9 7 9 . In 1 9 7 9 he jo in ted th e sta ff at the B ell L ab oratory in New Jersey.
In 1981 he jo in ted the C e n te r for V isio n Research a t the U n iv ersity o f
R och ester, where he is now professor and d irector.
n o t necessarily agree w ith conventional measures o t image
qualify ('Iliibo s ec al. 2 0 0 4 ; Prieto et al. 2 0 0 5 ).
The point-spread function and the M T F o t the eyes
optical system may be derived from wavefront aberrations.
For a review o t these procedures see Liang and W illiam s
(1 9 9 7 ) (P ortrait Figure 9 .8 ). W atson and Ahum ada (2 0 0 8 )
developed a model tor predicting visual acuity trom wave-
front aberrations.
The optical quality o t the image in the human eye is
substantially constant out to an eccentricity o f about 12".
Beyond this eccentricity, image quality declines with
increasing distance from the optic axis (Jen n in g s and
Charm an 1 981). In the foveal region, resolution is lim ited
by the optical properties o f the eye rather than by the den­
sity ot receptive fields. W ith increasing eccentricity, the
lim iting factor becom es the density o f receptive fields
(W illiam s e t al. 19 9 6 ; W ang et al. 1997).
9 .1 .4 C O M P E N S A T I O N O F A B E R R A T IO N S
It has been known for som e tim e that corneal astigmatism
is to som e extent com pensated by astigmatism o f the lens
(Southall 1 937). 'Ih e decrease in astigmatism in infancy
(Section 7 .3 .1 ) could be due to the progressive develop­
m ent o f a cornea-Iens com pensatory mechanism.
M ore recently, m easurem ents o t wavefront aberrations
have revealed that, in m ost people, the sum o f the separate
aberrations o f cornea and lens is larger than the aberrations
o f the whole eye. Thus, the lens partially com pensates for
several aberrations in the cornea (A rtal e t al. 2 0 0 1 ).
M cLellan c t al. (2 0 0 6 ) measured the various co m p o ­
nents o f optical aberration in human eyes. They then co n ­
structed synthetic model eyes with the same total refractive
error but with the sign or orientation of the aberrations
random ized. For a 6-m m pupil the resolving power (m od u ­
lation transfer function) o f natural eyes was higher than
that o f the synthetic eyes for spatial frequencies up to
6 0 cpd. This is further evidence that the aberrations o f
the human eye are com bined in an advantageous manner.
The advantageous layout o f the optical com ponents
ot the eye could be due to any o t the following factors.
(1 ) Fixed genetic factors. (2 ) Feedback from mechanical
interactions between cornea and lens during develop­
ment. (3 ) Feedback from visual experience during early
development.
Artal et al. (2 0 0 6 ) found that the com pensatory pro­
cess was present in people w ith different eye shapes and
different refractive errors. They concludcd that this adapt­
able com pensation is due to m echanical interactions
betw een cornea and lens, but they did not rule out a con tri­
bution from visual feedback. Kelly et al. (2 0 0 4 ) measured
the wavefront aberrations o f the corneas and lenses o f
3 0 young adults. They found a mean com pensation for
corneal astigmatism o f 41 % , for a spherical aberration o f
36% , and for com a ot 51% . C om pensation for spherical
aberration was not adjusted to individual variations in co r­
neal aberration, w hich suggests that it depends on a fixed
genetically determ ined process. Com pensations tor astig­
matism and com a were individually adjusted, which sug­
gests that they depend on an active feedback mechanism
o f some sort. The nature o f these com pensation processes
is as yet unknown.
'Ih e lens does not com pensate for corneal aberrations
in older people, probably because o t changes in the size
and shape o fth e lens (A rtal et al. 2 0 0 2 ).
9 .1 .5 T H E N Y Q U I S T L I M I T A N D A L IA S IN G
The human retina has betw een 4 and 6 m illion cones. The
peak density at the fovea is highly variable trom person to
person (1 0 0 ,0 0 0 to 320,000/ m m 2). G rating acuities pre­
dicted trom these cone densities are 4 7 cpd and 8 6 cpd
respectively. Thus, the average retinal mosaic is able to deal
with the highest spatial frequency (6 0 cpd) transm itted by
the eyes optics (C am pbell and Gubisch 1966). C o n e den­
sity falls steeply with increasing eccentricity. It is 10 times
lower at an eccentricityt o f 4° than at the fovea. Th e human
retina has at least 100 m illion rods and a central rod-free
area about 1.25° in diameter. Bevond an eccentricity ot 20°,
4 4
the density o f rods and cones declines more rapidly in the
temporal retina than in the nasal retina. The tw o eyes have
sim ilar num bers o f cones and rods and sim ilar photorecep­
tor topography (C urcio et al. 1990).
 Any detector array is subject со chc limicacion chac
cwo scimuli can be resolved only if chey excice cwo dececcors
ac a discrim inably higher level chan chey excice a dcceccor
in an incermediace locacion. Thus, a sec o f independenc
dececcors arranged in a square laccicc can resolve a periodic
scimulus, such as a gracing, only i f che spacial period o f chc
gracing is ac lease tw ice che spacing o f che dececcors. This is
che Nyquisc limic. A stimulus with a smaller spacial period
is undersampled. For a hexagonal laccicc, like che cone
m osaic, ic is easy со prove that the Nyquisc limic is V3 cimes
che spacing o t chc dececcors.
The smallest period in radians, v, o fa n extended grating
that can be resolved by the optics o f che eye is lim ited by the
wavelength o f che lighc, A, and by diffraction, w hich is
inversely proportional to pupil diameter, a (W estheim er
1 9 7 2 ). Thus,
Я period ind icated by the arrow s. The p attern is m ost evid en t when
V - — (3)
Л the spatial freq u en cy o f the gratin g is slightly h igh er than th at
Image quality is best when the pupil diam eter is 2.4 mm
and the wavelength o t light is 5 5 5 nm. Putting these
values in equation (3 ) gives a cone separation o f 2 7 .4 arcsec,
which is close to the value reported by O ’Brien (1 9 5 1 ). It is
an advantage to have recepcors as large as possible so thac
they capture the maxim um num ber ot photons. But if they
arc too large they fail to match che resolving power со the
eyes optics. Having the cones touch avoids loss o f photons
in the intercone spaces. This advancage must outweigh the
disadvantage o f leakage o f generator potentials between
closely adjacent cones (Snyder and M iller 1977).
Lord Rayleigh defined a criterion for che lim it o f resolu­
tion o t two points. For a diffraction-lim ited system, the
minim um separation o f two point sources, A9, thac can
jusc be resolved is chac separation for which che distance
becween che images is che radius o f A iry’s disk. Thus, from
equacion (1 ):
1.22 A
Ав = (4)
a o f receptors sufficient to prevent aliasing would degrade
Ac lease chree aligned dececcors are required со resolve
cwo points. Therefore, in the ideal system, the diam eter o f
the deteccors should be h a lf che diamecer ot A iry’s disk.
The image o f a grating finer than the Nyquist lim it forms
an interference pattern, or m oire patcern, wich che receptor
m osaic, as illustrated in Figure 9.9. Tli is process is known
as aliasing. Although the grating may noc be visible, the
inccrfcrence pattern could be visible because che bars ot
che grating com e into and out o f phase with the receptors
at a spatial frequency lower than chac o t che gracing. It the
spatial frequency o f che receptor mosaic is/ and chat o f the
stimulus grating is f + « , then the interference pattern has
a spatial frequency o f n.
The effects o f aliasing are n o t normally visible because
che opcics o f the eye are not capable o f form ing images
as fine as the Nyquist lim it. Thus, the opcics o t che eye
Fiju<«?,9. A liasing. A fine gratin g p ro jected o n to a hexagonal retinal
m osaic produces an in terference (m o ire) p attern w ith a spatial
o f th e m osaic.
conscicuce an anti-aliasing filter. Tli is lim itation does not
apply in the peripheral retina, where gratings beyond the
cu to ff frequency o f the classical contrast sensitivity fu n c­
tion may produce detectable moire patterns (Snyder et al.
1986; Thibos et al. 1 9 9 6 ). Because o fth e hexagonal packing
of receptors, the moire pattern formed betw een a grating
and the receptor mosaic changes as the interference pattern
is rotated 60°.
It has been argued that a random distribution o f cones
in the foveal region provides an anri-aliasing mechanism
(Yellocc 1 9 8 2 ). The measurements on which che argument
was based were from a photograph o f the co n e outer seg­
ments o f the human fovea. But the image plane ot che eye s
opcical system is at che level o f che inner segments. Hirsch
and Hylton (1 9 8 4 ) found chac che inner segmencs form
a highly regular hexagonal lattice in the central fovea o f the
macaque monkey. They argued that a random distribution
resolution. A regular lattice provides a basic m etric ot the
positions o f photoreceptors. All subsequent visual process­
ing depends on the fineness, calibration, and preservation
o f che basic mecric.
The resolving power o f che recina has been invescigaced
by converging cwo laser beam s on the recina со form a
fine inccrference patcern (Cam pbell and G ubisch 1966).
Since the patcern bypasses chc opcics o f che eye, ic may be
finer chan che paccern chac che eye’s opcical syscem can
resolve. The period o f che fincsc visible inccrference paccern
revealed chac che mean spacing o f foveal recepcors is abouc
0.5 arcm in. This corresponds со a resolucion limic o f abouc
6 0 cpd, a value chac tallies with anatom ical determinacions
o f che spacing o f foveal concs. Above chc 6 0 — cpd lim it,
a coarser paccern chan che incerference pattern may be
visible because o f aliasing.

F a r o b je c t
Fixorc9.il. U>egeom etry o f accom m odation. T o focu s the im age o f a poin c o n th e retin a, th e d ivergent in cid e n t w avefront m u st b e con v erted in to a
convergent w avefront w ith a curvature fixed by the d iam eter o f the eye. T h e curvature o f t h e in cid en t w avefront is inversely p ro p o rtio n a l to the
d istan ce o f th e o b je c t, o r I /d. B u t 1 /d is th e d istan ce o f th e o b je c t in d iop ters. T h erefo re, th e discancc o f an o b je c t in diopters provides a con v en ien t
m easure o f th e acco m m o d atio n needed to focus its im age.
An unaccom m odated lens has maximum diam eter and
minim um thickness and curvature. The accom m odation o f
a human eye is clinically assessed when in its unaccom m o­
dated state. An unaccom m odated em m etro p ic eye can co r­
rectly focus on an o b jcct at infinity. Its far point is therefore
at infinity (zero diopters). An a m etro p ic eye cannot focus
an o b ject at infinity and is either myopic or hypermetropic.
For an unaccom m odated m yopic eye, a point at infinity
form s an image in front o fth e retina, as in Figure 9.12a. The
person is said to be nearsighted. To be in focus, a point at
infinity must be brought forward to the far point shown in
Figure 9 .1 2 b . A negative lens is needed to focus a point at
infinity.
For an unaccom m odated h y p erm etro p ic eye, a point at
infinity forms an image beyond the retina, as in Figure
9 .1 2c. C o rrection for hyperm etropia requires a positive lens
to bring a p o in t at infinity in to focus. The person is said to
be farsighted. For example, an eye with the far point 0.5 m
in front o f the eye (negative d irection) has myopia o f - 2 D.
An eye with the far point 0.5 m behind the eye (positive
direction) has hyperopia o f + 2 1).
The crucial structural factor that determ ines the refrac­
tive state o f an eye is the ratio o f the axial length o fth e eye
to the radius o f the cornea, the A L / C R ratio. A shorter eye
requires a m ore highly curved cornea to bring the image
into focus in the retina, while a longer eye requires a less
highly curved cornea. G rosvenor and S co tt (1 9 9 4 ) found
that the mean A L / C R ratio o f several hundred cm m ctropes
was very close to 3.0. The mean ratio o f myopes was 4.1 and
that o f hypermctropes was 2.6. Em m etropic eyes with a
ratio significantly larger than 3 .0 are at risk o f becom ing
myopic (G rosvenor 1 9 8 8 ). Thus, it is not the axial length o f
the eye, alone, that determ ines the refractive state o f the
eyes. Nevertheless, m agnetic resonance imaging has revealed
that m yopic eyes tend to be larger in all dim ensions than the
eyes o f em m etropic and hyperm etropic eyes (C h en g c t al.
1992).
E m ergent w a ve fron t
W av efron t o f far o b je c t o f far object
W avefront o f near o bject —
\ i
,
N ear object
d --------
As eyes grow, their optical properties change to preserve
a favorable A L / C R ratio by the process o f em m etropization
(S ectio n 6.3 .1 c). Factors involved in am etropia are dis­
cussed in Section 9.6.2a.
The distance, in diopters, betw een the near p o in t and
the far point is the range o f a cco m m o d atio n .
H eath (1 9 5 6 a ) described the first four types o f accom ­
m odation listed below.
Tonic accommodation refers to the resting state in the
dark or in an em pty field (Section 9 .3 ).
Proximal accommodation is evoked by the apparent
distance o fa n o b je ct (Scctio n 9.5 )
Blur accommodation is evoked by blur o f the retinal
image o fa n attended o b ject (Scctio n 9.6).
Convergence accommodation is triggered by a change in
horizontal vergence (Section 10.4.2).
Voluntary accommodation is evoked by deliberate effort
in the absence o f visual stim uli (Section 9 .4 ).
Developm ental aspects o f accom m odation were dis­
cussed in Sections 6 .3 .1 b and 7.2.1.
9 .2 .2 T H E M E C H A N I C S O F
A C C O M M O D A T IO N
9 .2 .2 a C om p arativ e A spects o f A cc o m m o d a tio n
In land animals, the cornca perform s m ost o f the refraction.
Aquatic animals live in a medium with a refractive index
sim ilar to that o f the cornea. They must therefore rely on
the lens to refract light o n to the retina. For this reason fish
have spherical lenses with a short focal length.
The m echanism o f accom m odation in fish was first
described bv Beer in 1894. The lenses are stiff'w ith a fixed
 about 0 .2 5 I). In the clin ic, the range o f
accom m odation can be measured by che push-up
m ethod. This involves measuring the range o f distances
w ithin which a letter chart appears in clear focus.
In the m inus-lens m cchod, lenses o f varying power
are introduced until the su bject detects blur. In this
m ethod, the image does noc change in size as much
as it does in the push-up m ethod.
Laser speckle optometer A divergent low-energy laser
beam is shone o n to a diffusely reflecting surface.
The randomly reflected lighc beam s form a series
o l interference speckle patterns at different distances
from the surface (Ingelstam and Ragnarsson 1972).
The subject is asked to focus on a visual target on the
surface. An overaccom m odated (m yopic) eye focuses
on a speckle pattern nearer than the target.
A m ovem ent o f the eye to one side causes the speckle
pattern to appear to move over the surface in the
opposite direction. An underaccommodated
(hyperopic) eye focuses on a speckle pattern beyond
the surface so that the pattern appears to move over the
surface in the same direction as the eye. The refractive
power o f the lens required to null the apparent m otion
o f the speckle pattern provides a measure o f the
accom m odative state o f the eye. An allowance must be
made for the wavelength o f the laser light.
In a variant o f the m ethod, the laser beam is shone
o n to the surfacc o f a revolving drum. Instead o f
m oving the head, the observer reports che dircccion o f
m otion o f the speckle pattern relative to chat o f chc
drum (C harm an 1979). The clarity o f the pattern is
independent o f the refractive state o f the eye and
therefore does not provide an accom m odative stimulus.
However, to prevent any effect o f the speckle pattern,
the duration o f the stimulus may be kept less than the
reaction time o f accom m odation (К о the et al. 1987).
See Ben nett and R abbetts (1 9 8 9 ) for a fuller discussion
o f subjective optom etry.
9 .2 .4 c O b je ctiv e O p to m e tr y
In objective optom etry the optom etrist, rather than the
subject, perform s a nulling procedure (see Howland 1991).
O bjective m ethods include the follow ing:
Purkinje-image m ethod In this procedure, changes
in the shape o f the fron t surface o f the lens are
indicated by changes in the size o f che third Purkinjc
image o f a point o f light reflected from the lens
surfacc. This procedure is n o t affcctcd by small
changes in the direction o f gaze. It is thus suitable
for measuring changes in accom m odation that
accom pany changes in vergence (K rishnan ct al. 1977).
Sin ce the lens reflects only a fraction o f the light, the
m ethod requires a bright point o f light, which results
in glare.
I'incham coincidence optometer A narrow collim ated
beam o f light from a slit is projected into the eve. The
beam is slightly o ff axis, so that the image o f the slit
falls on the fovea for an em m etropic eye but to o n e or
other side o f the fovea for an am etropic eye. 1-ight
reflected from the retina is passed through the same
collim ating lens and split into two halves. O n e h alf is
viewed directly and the other through a Dove prism,
which reflects it to the opposite side o f the optic axis.
The displacem ent required to bring the tw o h a lf images
into vernier alignm ent is a measure o f refractive error.
The instrum ent can d etect a change o f accom m odation
o f 0 .2 D but the light source introduces glare.
Retinoscopy The retinoscope is derived from
H elm holtzs ophthalm oscope. A sm all m irror reflects a
point source o n to the p atien ts eye. The optom etrist
observes the retinal image formed by the point through
a hole in the center o f the mirror. As the m irror is
rotated about a vertical axis the image appears to sweep
across the patien ts pupil. The fir point o f a strongly
myopic eye lies between the eye and the sight hole.
This causes the image to move over the pupil in a
direction opposite to the direction o f m irror rotation.
The far point o f a hyperm etropic eye lies on the side o f
the pupil opposite the sight hole. This causes the image
to move over the pupil in chc same direction as the
mirror. The m otion o f the image is nulled when the
sight hole is brought into coincidence with the anterior
focal point o f the patients eye by the addition o f an
appropriate lens. The power and sign o f the added lens
indicates chc refractive correction that the patient
requires. In static retinoscopy, the patient fixates a
distant target, and the lens is assumed to be relaxed to
its far p o in t o f accom m odation. In dynamic
retinoscopy, the patient fixates a near target. Dynamic
retinoscopy is rather unreliable and is n o t often used
(W h itc fo o t and Charm an 1992).
Partial coherence interferometry (PC I) Fcrcher and
Roth (1 9 8 6 ) developed this procedure. The eye is
illuminated by a split beam o f coherent light. The two
beams reflect o f f the various surfaces in the eye. The
distance between a given pair o f surfaces is measured by
introducing a delay between the beam s and observing
che interference pattern produced in their com bined
reflected images. D istances betw een specified surfaces
can be measured with a precision o f betw een 0 .3 and
10 |im (D rexler et al. 1998). Longitudinal movements
o f the eye do not disturb the procedure.
 9 .2 .4 d A uto refractors indicates the sign and m agnitude o f m isaccom m odacion o f
the eye relative to chc apcrcure (K ruger 1979).
In che objeccive m ethods described so far, che optom etrist
In ecce n tric p h o to refra ctio n light from an eccentric
makes the settings. In an auto re tractor, the optom etrist is
infrared L E D is reflected irom the recina со form a gradienc
replaced by photodetectors. Ic chus becom es possible со
o f light over chc pupil. In early inscrumencs accom m odation
measure concinuous and rapid changes in accom m odation.
was indicated by the size o f the patch o f light in the pupil
There are several types o f autorefractor. O n ly che infrared
(B obicr and Braddick 1985). Schaetfel ct al. (1 9 9 3 ) used an
optom eter is described here, since chis is the instrum ent
array o feccen cric L E D s and measured the gradienc o f light
m ost com m only used in research laboratories. O th er cypcs
intensity in che pupil. The change in gradient was found to
o f inscrument arc described in B en nett and R abbetts
be reasonably linear over ± 5 diopcers. Roorda ec al. (1 9 9 7 )
(1 9 8 9 ).
analyzed the effects o t aberrations and different light
An in frared o p to m e te r uses infrared light so that
sources. Asymmetrical aberrations disrupt che lighc gradi­
there are no visible stim uli. O n e type o f instrum ent is
enc, buc cheir effects may be canceled by averaging the
derived from Fincham ’s coincidence optom eter. The images
gradients obtained with light sources on opposite sides o f
o f tw o slits illum inated by infrared light coincid c on the
the pupil. Changes in pupil size must also be allowed tor.
retina when accom m odation is at infinity. Reflections
This m ethod is inexpensive, quick, and useful tor measuring
o f chc images arc formed on a pair o f phococleccric cclls.
refraction in children. Suryakumar c t al. (2 0 0 7 a ) com bined
The relacive oucpuc o f che cwo photocells varies as a
a phocorcfractor wich a video eye cracker so chat changes
funccion o f accom m odacion (C am pbell 1959) (Porcraic
in accom m odation and vergence may be measured ac chc
Figure 9 .1 7 ).
same cime.
A sccond type o f infrared optom ecer is based on the
retinoscope. The su bject accom m odates on a cargec viewed
through a Badal lens. A patch o f infrared light is formed
on che recina. The image o f a vertically moving occluder 9 .3 T O N IC A C C O M M O D A T IO N
sweeps over the patch o f lighc ac a frequency o f 2 4 0 Hz.
An achrom atic lens focuses the retinal image in an aperture. 9 .3 .1 T H E T O N IC ST A T E O F
For an cm m ctropic eye, the reflected image o t the target A C C O M M O D A T IO N
is superimposed on che aperture. For an amecropic eye, che
U nder open-loop conditions, accom m odation reverts to a
reflecced image falls nearer chan or beyond che aperture.
state known as to n ic a cco m m o d a tio n , or rcscing focus.
Photodcccccors record chc phase lag bccwccn chc leading
There are tour ways со open che visual-feedback loop:
and lagging edges o f che image o f chc occluder, which
( i ) viewing through a pinhole, (2 ) dark viewing, (3 ) view­
ing a hom ogeneous stimulus or one with low con trast, and
( 4 ) coupling m otion o f the stimulus to chc oucpuc o t an
opcomecer.
O n average, chc eyes becom e about 1.5 D myopic in
dim light, a con d ition known as dark focu s, dark accom ­
m odation, or n ig h t m yopia. Ncvil M askclync, the
A stronom er Royal, was che first со notice the effect in 1789
(see Roscnficld et al. 1993). H e needed an extra diopter lens
when observing stars at night.
After the eyes were suddenly placed in the dark, accom ­
m odation drifted exponentially into the state o f dark focus
wich a time conscant o t I to 3 seconds (Baker ec al. 1983).
W h en light was restored, accom m odation returned to
its previous state with a tim e constant o f betw een 0.2 and
0.4 seconds.
Dark focus is influenced by the triadic relationship
betw een pupil diameter, vcrgcncc, and accom m odation.
The pupil enlarges in che dark, and vergence reverts со che
rcscing scatc o f vcrgcncc.
f igure 9 . 1". ha'gus Campbell. B o r n in G la s g o w in 1 9 2 4 . A f t e r g r a d u a t in g in The mean value o f dark focus varies from person to
m e d ic in e in G la s g o w h e b c c a m c a le c t u r e r in p h y s io lo g y a t C a m b r id g e
person (W csthcim er 1 9 6 3 ; Lcibow itzand O w ens 1975). In
U n iv e r s ity in 1 9 5 3 . In 1 9 8 Я h e w a s a p p o in t e d p r o fe s s o r o t n e u r o s e n s o r y
p h y s io lo g y a t C a m b r i d g e . H e r c c c iv c d t h e T i l l y c r M e d a l o f th e O p t i c a l a given person, dark focus varies with a peak-to-peak am pli­
S o c i c t v o t A m e r ic a in 1 9 7 8 . H e d ie d in 1 9 9 3 . tude o f up to 1 D and becom es more variable after a period
in toc.il darkness (W cscheim er 1957; K rum holtz ct al.
1986). W e will see in the next section that the state o f dark
Focus is influenced by rhe prior state o f accom m odation.
However, the mean value is reasonably consistent when a
given person is retested under the same conditions (M iller
19 7 8 ; M ershon and Am erson 19 8 0; O w ens and Higgins
1983).
Dark focus shows som e relationship to a persons refrac­
tive error. C orrected hyperopes were found to have a high­
est dioptric value o f dark accom m odation, and late-onsec
myopes the lowest (M cB rien and M illod ot 1987; G oss and
Z hai 1 9 9 4 ). The mean magnitude o f dark focus was found
to decrease trom 1.85 D in young adults to 1 D in 60-year
olds (W h ite fo o t and Charm an 1 992).
At high lum inance, accom m odation is m ost accurate
when the distance o f t h e target corresponds to the resting
state ot accom m odation. O veraccom m odation occurs tor
more distant targets and underaccom m odation for nearer
targets (Lcibow icz and O w ens 1 975). As luminance is
reduced, accom m odation is pulled toward the position o f
dark focus. A t scotopic levels, it remains close to the posi­ b'igvrc 9.is M arkR oscn/ictd. B o rn in L iv erp ool, England. H e graduated in
tion o f dark focus at all viewing distances. C orrective lenses op co m ctrv from A sto n U niversity. U .K .. in 1 9 8 4 and o b tain ed a P h .D .
in 1 9 8 8 from A sto n U n iv ersity w ith B. G ilm artin . H e is now associate
can com pensate tor the adverse effects ot m isaccom m oda-
professor in the D e p a rtm e n t o f V isio n Scien ces a t the (S U N Y ) State
tion at low lum inancc (Jo h n so n 1976). C o lleg e o t O p to m etry . H e was elected fellow o f the A m erican A cadem y
The resting position o t accom m odation tends to co in ­ o t O p to m e try in 1 9 9 0 . In 1 9 9 6 he was awarded the first research
cide with the position for which the optical quality o f the d ip lom atc in b in o cu lar vision from the A m erican A cadem y o l
O p to m e try and in 2 0 0 5 th e M ich ael G . H arris Fam ily Award for
image is optim al, especially with that position tor which
E x ccllcn cc in O p to m c tric E d u catio n from th e A m erican O p to m ctric
astigmatism is least (D en icu l 1 9 8 2 ). Also, m icrofluctua­ Fou n d ation .
tions o f accom m odation decrease as the optical quality o f
the image increases (A rnult and Dupuv I9 6 0 ; D enicul
1982).
9.^.2 A C C O M M O D A T IV E ADAPTATION
The lum inance at which the eyes adopt a state of dark
focus is higher than that at which they adopt the state o f The state o t dark focus is su bject to adaptation. A fter a
dark vergence (Section 10.2.1). Lum inance that is too low stimulus at the near point o f accom m odation had been
to evoke accom m odative responses wich m onocular view­ fixated for 8 m inutes the posicion o f dark focus increased
ing may do so with binocular viewing. This is because, with by a mean value o f - 0 .3 4 D. This effect took about 10 hours
both eyes open, the stim ulus evokes a change in vergence, to dissipate. Sim ilar fixation at the fir point decreased
which then evokes a change in accom m odation ( Jiang et al. dark focus by 0.21 D. This effect dissipated in abouc
1991). one hour (E b cn h o ltz 1983, 1991). Baker et al. (1 9 8 3 )
The subject of dark focus has been reviewed by obtained similar adaptation effects. The aftereffect
Rosenfield c ta l. (1 9 9 3 , 1994) (P o rtrait Figure 9 .1 8 ). lasted 5 minutes after 5 m inutes o t adaptation and
The eyes also becom e myopic when viewing low- several hours after 1 hour o f adaptation (Tan and O ’Leary
conrrasr or blurred stim uli, a condition known as em p ty 1986).
field myopia. Pilots becom e myopic when viewing an M onocular and binocular viewing produced similar
em pty sky. These form s o f myopia arc due to several factors, aftereffects in both eyes (Fisher ec al. 1987a, 1987b, 1988b).
including the resting accom m odative state, the absence ol Ihe aftereffect decayed more rapidly in the dark chan in
chrom atic aberration .vs an accom m odative stimulus an evenly illum inated field (S ch o r et al. 1 9 8 6 b ; W olfe and
(C am pbell and Primrose 1 953), and increase in the depth O ’C o n n ell 1987). The aftereffect is weaker and decays
o f field with dimly illum inated or blurred stim uli (H eath more rapidly chan adaptive changes in the resting state o f
1956b). vergence (Section 10.2.1) (Fisher c t al. 1990).
The stimulus contrast at which the eyes first show em pty Dark focus shifted by different amounts according
field myopia— the accom m odation contrast threshold— to the apparent distance o f targets that had been viewed for
is higher tor a grating o t high spatial frequency than for one 5 m inutes. The targets were ac che same optical distance
o f low spatial frequency (W ard 19 87a). (Rosenfield cc al. 1990).
 9 .4 V O L U N T A R Y A C C O M M O D A T IO N
A truly voluntary accom m odation response is one that is
deliberately executed when there is no stimulus to initiate
it. This occurs in the following circum stances:
1. Accommodation to an imagined object It has been
claim ed that, in the dark, accom m odation may be
partly under voluntary con trol, since it varies with
instructions to think o f a far o b ject or a near o bject.
It also varies with knowledge ot the nearness o t unseen
surrounding surfaces (Provine and Enoch 1975;
M alm strom and Randle 19 7 6 ; Rosenficld and
C iuffreda 1991 b). However, these changes may be
evoked by changes in vergence through the mediation
o f vergence accom m odation (M iller 1 9 8 0 ; Rosenficld
e ta l. 1 994).
2. Deliberate misaccommodation Normally,
accom m odation brings the o b ject that fills on the fovea
o f one or both eyes in to focus. However, som e people
can deliberately m isaccom m odate a stimulus on which
the eves arc fixated.
3. Accommodation to unusual stimuli W ith practice,
observers are able to change their accom m odation in
response to a stimulus that is n o t normally associated
with accom m odation. C o rn sw cctan d Crane (1 9 7 3 )
presented a dim point o f light to one eye through a
small artificial pupil. Because o f the large depth o f field,
the image remained essentially unchanged as
accom m odation changed. A tone o f variable pitch was
delivered to one ear. The pitch o f a tone to the other ear
was controlled by the output o f an optom eter that
recorded changes in accom m odation o f the su b jects
eye. Subjects were asked to keep the tw o pitches the
same. A t first thcv could noc do the cask. But, after 3
hours o f distributed practice, they becam e quite
proficient. H ie skill transferred to a task in w hich two
horizontal lines were kept superimposed when the
vertical mocion o f one line was under manual concrol
and th at o f the second line was controlled by che output
o f the optom eter. Thus, people can learn to concrol
accom m odation in response to a new sensory cue, when
the feedback signal is also novel.
9 .5 P R O X IM A L A C C O M M O D A T IO N
Proximal accom m odation is induced bv differences in the
apparent distances o f o b jects in the absence o f real differ­
ences in distance. A n accom m odative response occurs auto­
matically when an observer sw itches attention from an
o b je c t ac one apparenc distance со one ac anocher apparenc
distance. Proximal accom m odation is therefore noc volun­
tary alchough ic is evoked when a person voluncarily changes
gaze from an o b ject ac one apparent distance to an object
at anocher apparenc distance.
W h en an o b jcct moves closer to an eye its image becom es
larger. The changing size cue can be isolated trom changing
image blur by viewing che targee chrough a pinhole, which
increases che depth ol field and therefore renders che
response essentially open-loop (M organ 1968). Hennessy
et al. (1 9 7 6 ) found no effect o f objecc distance on
accom m odation with pinhole viewing. O cher investigators
observed proxim al accom m odation under these circu m ­
stances (M e l .in ec al. 1 9 8 8 ). Proximal accom m odation is
also evoked when blur is under open-loop control by link­
ing che oucpuc o f an optom ecer со che stimulus (Kruger and
Pola 1987).
C am pbell and W estheim er ( i 9 6 0 ) observed that, with
normal pupils, accommodative responses were less variable
when a step change in blur was accom panied by a change in
image size. Kruger and Pola (1 9 8 6 ) found thac changing
image size enhanced accom m odative responses со sinusoi­
dal changes in accom m odative blur. Thus, step or sm ooth
changes in image size induce accom m odation. The primary
effect o f a change in image size may be a change in vergence,
produced by an apparent change in che distance o f che
scimulus. The accom m odative change may be mediated
by the linkage between vergence and accom m odation.
It has noc been proved chat changing image size controls
accom m odation directly.
Kruger and Pola (1 9 8 5 ) measured accommodative
responses to a M altese cross sinusoidally modulated in
depch buc noc in size, in size buc noc in depch, and in boch
depch and size. Image blur was rendered open-loop by illu ­
m inating the scimulus wich m onochrom acic lighc and by
using the output o f an optom eter to move the carget in
depch so as со keep che blur o f che image conscanc. Changes
in size alone elicited changes in accom m odation, as can
be seen in Figure 9 .1 9 . The M altese cross appeared to
advance and recede as its size was m odulated. Adding
changes in size to changes in accom m odative blur had no
effect on the gain o f accom m odation but did reducc the
phase lag o f the response considerably.
Kruger and Pola argued thac M organ (1 9 6 8 ) and
Hennessy et al. (1 9 7 6 ) did not find an influence o f target
size because they used only scacic scimuli.
Kruger and Pola (1 9 8 9 ) asked what happens when
changes in blur and changes in target size are in councer-
phase. For a depth m odulation o f a M altese cross ac
0 .0 5 H z, che accom m odative response was in phase with
changing blur rather than with changing target size. This
result indicates chac blur was che dom inant stimulus. At
a frequency o f 0 .8 Hz the response shifted into phase
with the scimulus o f changing size. These results suggest
char the visual system needs more tim e to respond ro chang­
ing blur than ic needs со respond со changing size. Kruger
and Pola claim ed thac the response to both cues was approx­
imately che sum o f che responses со each cue tested alone.
 V) v (C o llin s cc al. 1995). The question is complicaced by chc
fi R ange o f
a. 5 accom m odation facc that image blur in an eye with constant lens aberrations
0 D
тэ S teady-state varies with the axial length o f che eye. For example, a given
a> 4 erro r spherical aberracion ot che lens produces a greater degree o f
с
Ideal response line , image discorcion as the lens-to-recina discance is increased.
а(/> Q
0) з U nder-accom m odation Sin ce aberromecers measure lens aberracions indirectly by
a>
•js 2 recording image distortions, allowance must be made for
as ^
3
Tonic accom m odation effects o f eye length. See C h en g ec al. (2 0 0 3 ) for a discus­
(dark focus)
sion ot chis point.
1 1
о O ver-accom m odation The eyes reach their full size ac abouc chc age o f 15 years.
8 .
< -L
People who develop myopia after chis age are said со have
+1 0 -1 -2 -3 -4 -5 -6
Far S tim ulus verg en ce (dioptres) Near la te -o n se t m yopia. Ic is generally agreed that chis type
of myopia is associated with prolonged use ot the eyes in
Kij-urc 9.20. Л t y fii.il accom m odation response curve. J (тот U W am) С Ьм тдп
near work (O w ens 1991; Blackie and Howland 1999).
I9 8 S )
People with late-onset myopia accom m odate less well to
near stimuli chan do emmecropcs or hypermecropcs
(M cB rien and M illodoc 1986). In particular, chey show a
weak increase in accom m odacion со blur produced by che
W hen chere are cwo overlapping stim uli at differenc
introduction o f a negative lens. They show a normal decrease
but neigh boring distances, as when an o b ject is seen through
in accommodacion in response to blur produced by a posi­
a mesh, accom m odation usually settles at an interm ediate
tive lens (Gwiazda et al. 1993; Jiang 1997; A bbo tt et al.
depth (M andelbaum I9 6 0 ; Rosenfield and Ciuffreda
1998). Although myopes are relatively insensitive to blur
1991a). This suggests that accom m odative stim uli arc
produced by negacive lenses, chey showed normal acuity
averaged over a local area. W hat that area is has not been
and concrasc scnsicivicy for images blurred in chis way
determined. Analogous effects occur in vertical vergence
(Radhakrishnan ec al. 2 0 0 4 a , 2 0 0 4 b ). Ic would seem chac
(S ectio n 10.6.3b).
sonic myopes do noc increase cheir accom m odation to
It seems that accom m odation responses arc evoked by
near stim uli because chey can adequacely perceive che
blur o f a luminance-defined edge, but not by blur ot an
ouc-of-focus images. Ic has generally been found chac
edge defined only by color. An equilum inant red-green or
myopes wearing spectacle corrections have lower contrast
red-blue grating did not elicit appropriate accom m odation
sensitivicy chan cmmecropes (Fiorenrini and M atfei 1976;
even though the gratings were visibly o u t o f focus (W olfe
Scrangec al. 1998).
and O w ens 1 981). But this could be because the eye is
Late-onset myopia could be due to reduced sensitivity
more sensitive to a lum inance border chan to a chrom atic
со defocus blur or со a weakness in che mocor syscem.
border, especially for a grating o f high spatial-frequency.
Rosenfield and A braham -C ohen (1 9 9 9 ) approached this
Switkes ec al. (1У 90) com pared che accommodative
question by com paring che blur-dececcion thresholds o f a
responses со lum inance and chromacic gratings chac were
mixed group o f early-onset and lace-onset myopes with
equated for apparcnc concrasc. This was done by setting
those o f a group o f cmmecropes. A ccom m odacion was
each grating an equal num ber o f increm ent thresholds
paralyzed with a cycloplegic drug while subjects viewed
( JN D s ) above the contrast threshold. O n ce again, only the
a bipartite letter display chrough a Badal lens. O n e h a lf o f
lum inance grating elicited accom m odation responses.
che display was moved in depch uncil subjects could dececc
Totally color-blind subjects showed little or no accom ­
blur. The mean chreshold for chc 12 cmmecropes was
modative responses to change in target distance (Hearh
0 .1 0 9 + 0 .0 0 5 D and that for 12 myopes was 0 .1 8 7 + 0 .0 2 3 D.
1956c). They tended to adopt che position ot dark accom -
N o distinction was made between early-onscc and lacc-
m odacion. However, the insensitivity o f color-blind people
onset myopes. There are two ways to interpret these results.
to changing image blur may be due со cheir poor visual
They could signify thac myopes accom m odate less well
acuicy racher chan ro their lack o f cone receptors.
because they do n o t detect image blur. O n the other hand,
they could signify chac myopes arc adapced со image blur
9.6.2 BLUR D E T E C T IO N arising trom their m isacconunodation. This question is dis­
cussed further in Seccion 9.6.5b .
9 .6 .2 a B lu r D e te c tio n in M yo p es
In any case, chese results do noc prove chac inadequace
It is widely believed thac myopia is due primarily to the detection o f image blur is the only cause o f myopia. O cher
axial length o f che eye being to o long in relacion ro rhe possible factors include abnorm al axial length o f che eye,
curvacure o f che cornea, as described in Seccion 9.2.1. opcical aberrations, or an oculom ocor defect. The role
O n rhe ocher hand, there arc reports that myopia is associ­ o f image blur in the growch o f che eye was discussed in
ated with unusually large optical aberrations in the eye Seccion 6.3.1c.
 9.6.21) Blur, M o n o cu la r D ip lop ia,
and C o n tra st-S e n sitiv itv
4

D efects in chc optics o t chc cvc can produce m onocular

diplopia (Fincham 1 9 6 3 ). For example, hypermetropia
coupled wich positive spherical aberration, or myopia
coupled w ith negative spherical aberration produces
m onocular diplopia (C offeen and G uyton 1988; Woods
e t al. 1996a). Also, m onocular diplopia can be produced by
astigmatism.
In m onocular diplopia, chc image o f a line viewed wich
one eye is flanked by a faint ghost image with an angular
separation o f 0. W hen the spatial period o f a grating equals
20, the bars o f che firsc image arc 180" o u t o f phase with
those o f chc ghost image. C onscqucndy, chc concrasc o f chc S patial frequency (cpd)

image will be reduced. In fact, contrast will be reduced for

rtgwt9.2i. I f f i i t o f b lu r on th e con trast sensitivity fu n ction . The co n tra st
gratings with frequencies 1/20, 3/ 2 0, 5/2 0, etc. Tin is p ro ­ sensitivity In n ctio n o t on e su b ject w ith an in -focu s vertical grating and
duces periodic notches in the contrast sensitivity function. w ith a grating -2 1 ) o u t o f focus. Pupil d iam eter 6 m m . The predicted

The locations o f these notches may be calculated for a given
eye from the eye’s aberrations.
Apkarian e t al. (1 9 8 7 ) detected dips in the contrast
sensitivity function when the orientation o f the grating
corresponded to chac ac w hich diplopia due со astigmatism
was evident. W oods et al. (1 9 9 6 b ) detected modulations
in the contrast scnsicivicy funccion wich simulated myopia
or hyperopia, especially with m onochrom atic gratings.
Atchison c t al. (1 9 9 8 ) revealed notches in che contrast-
co n tra st sen sitiv ity fu n ctio n was derived Irom m easurem ents ot
transverse ab erration s alo n g chc h o riz o n ta l m eridian o t chc eye. (л.Цч«ч!
from S i r J . I W )
in blur arising from a sinusoidal change in stimulus distance
was lowest when blur was initially abouc 1 diopccr away
from minim um . The results are shown in Figure 9 .2 2 . The
stimulus was described as a small high-concrasc object.

sensicivity functions o f hyperm etropic subjects that were
predicted by the aberrations o t cheir eyes. Predictions were
less successful wich a myopic subjccc.
Strang et al. (1 9 9 9 ) measured concrast-sensitivity
functions for an in-focus image, and for images dcfocuscd
- 2 D and + 2 D . Pupil diam eters were 2 ,4 , and 6 mm. W hile
chc funccion wich an in-focus image showed chc usual
m o n o to n ic decline with increasing spatial frequency, func­
tions with dcfocuscd images showed the predicted notches
for both directions o f defocus. An example is shown in
Figure 9 .21.
Walsh and Charm an (1 9 8 8 ) used similar m ethods to
measure che chrcshold tor dccccting sinusoidal changcs in
image blur o f a sinusoidal grating as a function o f temporal
frequency, pupil size, and mean position o f tocus. Sensitivity
to changes in blur was abouc 0.1 1) higher when the image
was defocused about 2 D compared wich when ic was in
focus. Note that defocusing a sine-wave grating reduces its
contrast buc does noc change ics spatial-frequency content.
S en sitiv ity to a d ifferen ce in sta tic blu r is measured
by asking subjects to discrim inate betw een a fixed com pari­
son stimulus and a test stimulus set at various levels o f
blur. Blur may be optically incroduccd inco chc stim uli pre­
sented at the same distance. In this case it is n o t necessary to 4

9 .6 .3 B L U R D IS C R IM IN A T IO N paralyze the lens. Blur may also be produced by defocusing

Ну W ebers law, one would expect a given blur added со a

sharp edge would be m ore noticeable chan che same blur
added со a less sharp edge. However, a smaller change in
blur can be detecced when the stimulus is initially slightly
blurred than when ic is initially in sharp focus. I.cc us firsc
look at the evidence for this seemingly counterintuitive
fact.
In measuring a persons sen sitivity to a ch an ge in
d cfo cu s b lu r the lens is firsc paralyzed w ith hom atropinc M ean d efocus (diop(res)
and the visual target is viewed through an artificial pupil.
The cargcc is also viewed chrough a Badal lens so chac ics n*»r<9.22- D iscrim in ation o fd e fa u s btun Threshold fo r d etectio n o f
л change in blur o f a visual o b je ct m ovin g back am i fo rth alo n g the
image does n o t change in size when the target is moved in
visual axi* At 2 H z av a fu n ctio n o f th e m ean d cfo cu s blur o f th e im age.
depth. W ith these procedures, C am pbell and W estheim er T h e eye was h om atrop in ized an d a 3-m m artificial pupil wav placed
(1 9 5 8 ) showed that the threshold for detection o f a change b efore the eye. (AbfiuA »V*mC—pbdJ uxl WotWinwr 195*)
a change in chc relative responses o f different spatial- 9 .6 .4 b D e p th o f F ield and P u p il D ia m e te r
frequency channels.
A pupil controlled by the iris muscles acts as an aperture
Л similar dipper function occurs in any system that
stop to control the am ount o f light entering the eye.
contains detectors with overlapping tuning functions,
Changes in pupil size also affect the optical quality o f che
as explained in S ection 3.1.3b.
image. Thus, as the pupil enlarges, diffraction decreases,
spherical aberration increases, and the Sciles-Crawford
effect increases. Also, depth o f field decreases with
9 .6 .4 D E P T H O F F I E L D A N D
increasing pupil size. For a given viewing distance and
А С С О M M O D АТ I О N А С С U К Л С Y
level o f illum ination, the pupil adjusts autom atically to
9 .6 .4 а C h aracteristics o f the D e p th o f Field achieve the best com prom ise betw een these various optical
factors'.
For a given sratc o f accom m odation, the range o f distance
D epth o f field decreases with near viewing. Photogra­
over which an o b ject can move w ithout image blur being
phers counteract this effect by reducing che aperture o f the
detectable is the dep th o f field. The range o f distance over
cam era for near shots. For tar shots, the aperture can be
which an image can move w ithout blur being detectable is
increased to allow more light in to the camera. For the same
the dep th o f focus. In linear terms, depth o f field and depth
reasons, the pupil con tracts for near viewing and enlarges
o f focus differ, but in terms o f visual angle or diopters, they
for far viewing.
are the same.
C am pbell (1 9 5 7 ) measured the depth o f field for a
It optical aberrations are ignored, and the resolving
black disk as pupil diam eter was increased, with illum ina­
power o f the system is know n, one can calculate the depth
tion and viewing distance constant. D epth o f field with a
o t field tor an o b ject at a given distance and a pupil o f a
2-m m pupil was ± 0 .4 3 D and that with a 6-m m pupil was
given size (see Sm ith and Atchison 1997, p. 2 3 3 ).
± 0 .2 1 D. O gle and Schw artz (1 9 5 9 ) found thac depth o f
In practice, optical aberrations have a considerable
field increased about 0 .1 2 D for each m illim eter decrease
effect on depth o f field, so that accurate calculations arc
in pupil diameter. As depth o f field increases, the steady-
impossible (C am pbell 1 9 5 7 ). D epth o l field can be deter­
state error o f accom m odation increases, because accom m o­
mined psychophysically by asking observers to m onocularly
dation tends to be pulled inco che scacc o t dark focus. W ich
fixate one o b ject and report when the image ot another
a very small pupil, o b jects at all distances are in focus, and
o b je c t becom es blurred. A more refined psychophysical
accom m odation falls into the state o f dark focus o f about
procedure involves measuring resolution acuity w ith a
1 D (H cn n essy ct al. 1 9 7 6 ). The accommodacion/scimulus-
checkerboard at different out-of-focus distances (O gle and
distance curve then becom es flat (C am p bell 1 9 5 7 ; Ward
Schwartz 1 9 5 9 ). Pupil size should be controlled by an
and Charm an 1985).
artificial pupil and accom m odation can be paralyzed.
For a sinusoidal grating, image blur reduces the
A m ore objective m ethod tor measuring depth o f field is
contrast o f the image w ithout affecting its spatial frequency
to determ ine the m inim um out-of-focus blur ot an image
or phase. As the pupil contracts, blur due to diffraction
that evokes a change in accom m odation. A ccording to this
increases. The theoretical loss o f contrast in the image o f a
m ethod, depth o t field is defined as the range o f distance
grating in an aberration-free eye for various pupil diameters
in o b ject space within which a stimulus can move w ithout
is shown in Figure 9.7a. I lowcver, blur due to spherical
generating a change in accom m odation.
aberration decreases as the pupil gets smaller. Figure 9.7b
U nder optim al conditions, and with a pupil diam eter
shows the measured overall loss o f contrast in the image
o f 2.5 m m , depth o f field is about 0.3 D (C am pbell 1957).
o f a sinusoidal grating as a function o f the spatial frequency
This m eans that errors o f focus w ithin about 0 .3 D do not
o f the grating. Figure 9.7 c shows the loss in concrasc relative
cause detectable blurring o f the image and would n o t be
to a diffraction-lim ited system.
expected to evoke an accom m odative response.
For a given size o t pupil, there is a distance beyond
which all objects are in focus at the same tim e— the depth
9 .6 .4 c D e p th o f Field and S p a tia l F re q u e n c y
o t field extends to infinity. As an o b ject approaches an
observer, with pupil size held constant, stimulus vergence Blur reduces the contrast in the image o f a sinusoidal grat­
increases and depth ot field decreases. ing and therefore pulls down the eye’s m odulation transfer
The b o u n d aricso f the depth o f field, however measured, function. This lowers the upper lim it o f spatial-frequency
are nor sharp. A lso, they are not stable because o fth e m icro­ resolution, as shown in Figure 9.7. For dilated pupils, depth
fluctuations o f accom m odation described in S ection 9.7.2. o f field increased from 2.5 D with a grating o f 3.5 cpd to
Any factor thac decreases rhe depth o f field should about 17 D at 0.25 cpd (Legge et al. 1987).
improve the accuracy and stability o t accom m odation. The contrast o f a grating becom es more and more atten­
D epth o f field and accuracy o f accom m odation are affected uated as the grating moves from the plane o f focus. This
by the factors described in the following sections. causes a progressive decline o f the highest resolvable spacial
frequency. Figure 9 .2 5 shows che theoretical modulation
transfer functions for .in aberration-free eye with a 4-m m
pupil and m onochrom atic light o f wavelength 5 3 5 nm.
As image defocus increases, the contrast ot the images of
high spatial frequency gratings becom es progressively
attenuated. Negative values o f the transfer function repre­
sent regions o f spurious resolution. In a real eye, effects
o f defocus arc modified by spherical and chrom atic
aberrations.
The m ain point is th at only detectors sensitive to
low spatial frequency can register an image that is well
out o f focus. Therefore, whatever th e stimulus, the initial
accomm odative response to an out-of-focus o b ject is
evoked only by detectors o f low spatial frequencies.
Charm an and Heron (1 9 7 9 ) dem onstrated chis p o in t by
measuring changes in accom m odative from a prefocused
stimulus at a distance o t 0 .2 5 or 0 .1 6 m to a gracing ac
0.5 m. As che spacial frequency o f che gracing increased
from 1.0 cpd со 16 cpd, the response weakened until no
response occurred. The spatial frequency ac which the
response ceased varied betw een subjects.
As an image com es in to focus, higher spatial-frequency
com ponents o f the stimulus becom e resolved, and accom ­
modacion com es under che control o f detectors sensitive
to high spatial frequency. Accordingly, the final accuracy
o f accom m odation is determ ined by the highest d etect­
able spacial frequency in the stimulus (C harm an and Tucker
1977).
Charm an and Tucker (1 9 7 8 a ) measured the accuracy
o f steady-state accom m odation as a function o t the spatial
frequency o f a sinusoidal grating with 8 0 % contrast. A t a
spatial frequency o f 0 .4 cpd, the steady-state error was sim i­
lar to that observed with an em pty field. As spacial fre­
quency increased to 3 0 cpd, accom m odation accuracy
improved. W ith a grating o f 2 5 % contrast, subjects showed
1 .0
0 .8
£
to
с 0 .6
2 nance and as a linear funccion o f increasing concrasc
с
.9 0 .4
я
TJ 0 .2
I
0 0 .5 3 D
- 0 .2
10 20 30 40
S patial frequency (cpd)
к*ш с 9.25. M odulation tran sferfu n ctio m fo r le t eh o f defocus.. T h e eye is
assumed to be a b e rra tio n free w ith a p u p il d ia m e te r o f 4 m m .
T h e s tim u li arc sine-wave g ra tin g s in m o n o c h ro m a tic lig h t o f
5 >5 n m . A m o d u la tio n tra n s fe r o f l in dicate s fu ll tran sm issio n o f
c o n tra s t. (Av4j|iud f»«4» Ch.»rmiu JvcUr 1977)
accurate accom m odation to a grating with a spatial fre­
quency o f 5 cpd, but could n o t m aintain accurate accom ­
m odation to a grating o f 15 cpd (W ard 1987b).
However, one must allow for the facc chac che contrasc-
sensicivicy funccion (Seccion 3 .2 .5 ) peaks between 3 and 5
cpd. The visual system becom es progressively less sensitive
as spatial frequency is increased above 5 cpd and loses all
sensitivity to contrast m odulations at a spatial frequency
o f about 6 0 cpd. O w ens (1 9 8 0 ) found thac che accuracy o f
steady-state accom m odation for a high contrast sinusoidal
grating was also optim al at these same spatial frequencies.
Thus, with a sinusoidal grating stimulus, accom m oda­
tion and detection rely on the same contrast-detection
m echanism .
A ccom m odation is more accurate tor people with
high acuity than for those with low acuity (Legge c t al.
1 9 8 7 ). Amblyopes show reduced contrast sensitivity and
reduced accommodative response over m ost o f t h e spatial-
frequency range (W ood and Tom linson 1 9 7 5 ; Ciutfreda
and H okoda 1983).
The above results apply to sinusoidal gratings in
which anything that increases image blur reduces only the
concrasc o f che gracing. However, che resulcs do n o t apply
to more complex stim uli in which increases in image blur
may affect the shape or phase o f the image. K otulak and
S ch or (1 9 8 7 ) found chac changing the spatial frequency,
lum inance, and contrasc o f a difference o f Gaussian (D O G )
scimulus affected visual detection and accom m odation
responses in differenc ways. They concluded chac changing
concrasc affects visual dececcion and accom m odation in a
similar way for a simple sine wave, bur not for a broadband
stimulus.
C iutfreda and Hokoda (1 9 8 5 a ) found that accom m o­
dation was affected more by stimulus spatial frequency
when subjects accom m odated in a relaxed fashion rather
than strived со obcain che besc focus. O n e cannoc ignore
che possible effect o f instructions in any experim ent on
accom m odation.
9 .6 .4 d D ep th o t Field, C o n tra s t, and L u m in a n ce
D epth ot field decreases as a linear funccion o t log lum i­
(C am pbell 1 9 5 7 ). The decrease in depch o f field is accom ­
panied by im provem ent in visual acuicy due со increasing
lum inance and concrasc. At verv
# low levels o f luminance
or contrast, accom m odation reverts to the state ot dark
focus whatever the distance o f the o b ject (Cam pbell 1954;
Nadell and Knoll 1 9 5 6 ; Joh n so n 1 9 7 6 ). This suggests that
accom m odation is mediated primarily by the cones.
R eduction o f lum inance contrast reduces the accuracy
o f accom m odation to step changes in rhe distance o f a
grating, although accom m odation is m ost stable when
contrast is slightly less than 1 (B ou r 1981). 'Ih c accuracy
o f steady-state accom m odation is affected only slightly by
pattern so chat images chat do noc conform со che usual
pacccrn appear blurred.
Areal ec al. (2 0 0 4 ) measured che wavefront aberration
o f subjeccs' eyes in real tim e by che procedure described
in Seccion 9 .1 .3c. The recorded signals were used со concrol
an adaptive optic*» device chac could change che aberration
parccrn. This device consists o f a flexible m irror like those
used by ascronomers со eorrecr deform ations in celescope
images produced by che atmosphere (H u bin and N oethc
1993). Subjeccs viewed a random -doc display in m onochro-
macic lighc chrough che adaptive opcics syscem. The syscem
presenced eicher che norm al pacccrn o f aberracion or rhe
same aberration pacccrn rocaced со one o t seven angles
becween 45° and 315°. Displays wich unusual aberracion
appeared blurred relacive со che display wich normal aberra­
cion. The effect was measured by having subjeccs adjusc che
blur o f each abnorm al display со m atch chac o f a subse­
quently seen norm al display. M ore reccndy, in same labora-
cory ic was found chac a random-cexcure display appeared
lease blurred when abouc 12% o f aberrations were left
uncorrccced com pared wich when che aberrations were
fully correcccd by adapcive opcics (C h en ec al. 2 0 0 7 ).
O n e problem wich che idea chac people gee used со
cheir own optical aberrations is chac che aberrations change
wich changes in accom m odation and pupil diameccr.
However, som e feacures o f che pome-spread funccion, such
as ics oriencacion, remain scable, and people may learn со
adapt eo che dynamic changes.
A m ore radical nocion is chac che nervous syscem has
some m echanism for com pensating tor aberrations o f che
eyes. This would mean chac acuity would improve as we
adapc со a given image blur.
M on-W illiam s ec al. (1 9 9 8 ) approached chis question
by measuring leccer acuicy and concrasc sensicivicy betore
and after subjeccs viewed che world chrough + 1 1 ) lenses for
3 0 minuces. Boch eescs revealed an improvemenr in acuicy
wich no change in ocular refraction. The improvemenc
cransferred abouc 3 5 % from an eye chac had viewed chrough
chc lens со che ocher eye, w hich had been occluded.
An increase in che gain o f dececcors sensitive со high
spacial frequencies should improve acuicy. Buc chcrc would
also be an increase in high-frequency noise, which would
cancel che improvemenc in acuicy. There could be some
improvemenc it subthrcshold spatial frequencies became
visible. The ocher possibilicy is chac che gain o f lower
spacial-frequency dececcors is reduced, which would reduce
cheir masking etfecc on high spacial-frequency dececcors.
M on-W illiam s ec al. found chac adapcacion со che 4 1 L")
lenses did indeed reduce concrasc sensicivicy for gracings
becween abouc 5 and 25 cpd.
9 .6 .5 b Adapcacion to O b je c c Blur
In addition со defocus blur, image blur arises because objcccs
vary in sharpness. A given nacural objecc has a characteristic
power speccrum, defined as che amplicude o f concrasc as a
funccion o f spatial frequency. Typically, concrasc falls in
inverse proporcion со spacial frequency (DeValois and
DeValois 1 9 8 8 ). This scaciscical propcrcy o f visual scenes is
macched by che differencial sensicivicy o f ditferenc spacial-
frequency channels in che human visual system. This keeps
signal strength roughly conscanc across spacial scales. In
a model o f chis process, Field and Brady (1 9 9 7 ) assumed
chac chc spatial-frequency bandwideh o f cortical cells,
racher chan cheir concrasc sensicivicy, increases wich spacial
frequency.
O cher chings being equal, che perceived blur o f a
well-focused image o f a fam iliar nacural objecc will depend
on how closely ics power speccrum resembles che normal
power speccrum o t chac objecc. An objecc appears blurred
when high spacial frequencies are filtered off, and ic appears
unusually sharp when low spacial frequencies are filcered
off*. Tli is suggests chac we learn to appreciace che degree
o f blur in che images o f fam iliar objects. I f so, exposure to
a fam iliar objecc wich an unusual degree o f blur should
affect a persons judgm enc o f image blur.
W ebster ec al. (2 0 0 2 ) confirm ed chis prediction. They
found chac a few minuces’ exposure со a physically blurred
piccure o f a face, oucdoor scene, or checkerboard caused
a norm al piccure Co appear unusually sharp. Exposure со an
unusually sharp image, produced by filccringoffslow spacial
frequencies caused a normal image со appear blurred. Also,
a normal piccure em bedded in a blurred surround appeared
unusually sharp, and one embedded in an unusually sharp
surround appeared less sharp. This suggescs chac che relacive
sensicivicies o f spacial-frequency channels in the visual
system are continuously adjusccd со com pcnsacc for
variations in che spacial-frequency concenc o f che recinal
image.
In Seccion 9.6.2a ic was mencioned chac myopes are
less sensitive со image blur chan arc emmccropcs. This
suggests thac myopes adapt to the blur resulting from
their inadequate accom m odation. Vera-Diaz et al. (2 0 0 4 )
exposed myopes to a distinctly blurred image produced
by diffusing lenses for 3 m inutes. During and immediately
after the adaptation period the myopes showed a signifi­
cant increase in their accom m odation со a near eargcc.
Emmecropes showed no effect o f adaptation. It thus seems
that myopes show enhanced accom m odation when the
blur signal in increased.
9 .6 .5 c A dap tation to C h r o m a tic A berration
Although the eye has considerable chrom atic aberration,
we are nor aware o f color fringes. G ibson (1 9 3 3 ) reported
that color fringes ot opposite sign were seen for several
hours after removal o f prisms th at had been worn for 3 days.
These so-called p h an tom fringes must be neural rather
than optical in origin, since they showed in m onochrom atic
light (Hay e t al. 1 9 6 3 ). Hay found that, after wearing
chrom atically aberrant lenses continuously for two days,
the color fringes that the lens introduced were no longer
visible. Adaptation to chrom atic aberration may
related to the color-contingent aftereffect described in
Section 4 .2.9c.
9.7 A C C O M M O D A T I O N
TO D EFO C U S BLUR
9 .7 .1 S T E A D Y - S T A T E A C C O M M O D A T IO N
9 .7 .1 a M icro flu ctu a tio n s o f A cco m m o d a tio n
For any system that uses error feedback to m aintain a steady-
state response there is a range o f error signals that are too
small to be detected. This is the systems dead zone. For
accom m odation, the dead zone is the range o f defocus
w ithin which an accom m odative response is n o t evoked.
The ou tp u t o f a system should therefore fluctuate within
the dead zone and a correction should be applied when the
crror-dctcction threshold is exceeded. Fluctuations o f this
kind are seen in the movements o f the eyes as a person
attem pts to steadily fixate a small o bject. Sim ilar fluctua­
tions o f accom m odation should occur when a person
attem pts to focus steadily on an o b je ct at a given distance.
W h en the gaze is fixed on a small target, che accom m o­
dative state o f the eye fluctuates w ith an am plitude o f up
to about + 0 .2 5 D. A low-frequency com pon ent o f up to 0.6
H z can be distinguished from a high-frequency com ponent
o f betw een 1 and 3 Hz (C am pbell et al. 1959; Charm an
and Heron 1 988). Fluctuations o f accom m odation in the
tw o eyes are correlated in phase and am plitude, which
shows that they do not arise only from instabilities in
the ciliary muscles (C am pbell 1 9 6 0 ). The high-frequency
com pon ent is correlated with the frequency o f the arterial
pulse and is therefore not under neural control or scimulus
con trol. The power o f the low-frequency com ponent is
related to the quality o f the image, and its frequency is
related to the frequency o f stimulus oscillation in depth
(W in n 2 0 0 0 ). This shows that low-frequency fluctuations
are under feedback control from the retina. Blur o f the
retinal image must be the crucial stimulus. H ie amplitude
o f fluctuations in accom m odation is maximal at the resting
state o f accom m odation. This is probably because tension
in the accom m odation system is least at this p oint, leaving
the lens freer to oscillate (D cn icu l 1982; Kotulak and Schor
1986b).
D epth o f Held defined by detection o f blur is typically
about + 0 .2 5 D . But an accom modative response can be
evoked by a step change o f stimulus vergence o f only 0.1 D
(Ludlam ct al. 1 968). K otulak and Sch or (1 9 8 6 c ), also,
found that accom m odation is evoked by a degree o f blur
that can n ot be detected psychophysically. However,
CiufFreda et al. (2 0 0 7 ) found no difference betw een subjec­
tive and objective measures o f depth o f field. The difference
may be due to the way depth o f field is measured. The blur-
detection threshold is a time-averaged value lying within
be the zone o f subject uncertainty and by m icrofluctuations o f
accom m odation. But an accom m odative response could be
triggered by a peak value o f blur that m om entarily exceeds
the time-averaged blur threshold. The follow ing evidence
supports this idea.
C am pbell and W estheim er (1 9 5 8 ) paralyzed accom m o­
dation, applied a 3-m m artificial pupil, and moved a test
o b ject back and forth along the visual axis at 2 Hz. Subjects
adjusted the am plitude of m otion until they could just
d etect a change in blur. Target excursions were centered on
various pedestal values o f blur between plus and minus 3 D.
Sensitivity to changes in blur was within the range o f
changes produced by m icrofluctuations o f accom m odation,
which supports the idea that these fluctuations contribute
to the control o f steady-state accom m odation.
W in n et al. (1 9 8 9 ) used an infrared optom eter to
record signals arising from m icrofluctuations o f accom m o­
dation. The lens was then immobilized with a cvcloplegic
drug, and the recorded signals were used to m odulate the
blur o f a Snellen letter. The threshold for detection o f blur
m odulations was approximately the root-m ean-square of
the fluctuations. The peaks o f the fluctuations, although
n o t detected psychophysically, would be capable o f evoking
accommodative responses.
Pupil con striction increases the depth o f field and
thereby reduces the change in image blur as the lens changes
its focal length. I f m icrofluctuations o f accom m odation are
to provide an effective error signal they should increase in
am plitude as the pupil constricts. Gray et al. ( 1 9 9 3 a ) found
that the am plitude o f m icrofluctuations o f under 1 Hz
increased as pupil diam eter was reduced below 2 mm by
artificial pupils. The amplitude of m icrofluctuations above
1 Hz was not affected. Also, increasing pupil diam eter above
2 mm did n o t affect the amplitude ot m icrofluctuations.
They concluded that steady-state accom m odation is co n ­
trolled by low-frequency fluctuations ot accom m odation.
Yao et al. (2 0 1 0 ) found that the magnitude o f m icrof­
luctuations o f accom m odation was correlated with the
objectively determ ined depth o f field, as one would expect
if peak values o f fluctuations evoke accommodative
responses.
A t low levels ot luminance, high spatial frequencies
becom e undetectable, and larger fluctuations o f accom m o­
dation are therefore required to produce a discriminable
change in image contrast. Gray e t al. (1 993b ) tound that low-
frequency m icrofluctuations o f accom m odation increased
near the luminance threshold (below 0 .0 0 4 cd/nr).
W e can conclude that m icrofluctuations o f accom m o­
dation provide error signals required to keep the eyes
reasonably well focused on an o b ject. The system m oni­
tors the changing blur produced by neurally controlled
fluctuations o f accom m odation, and applies an appropriate
correction.
 9 .7 .1 b Steady-State Bias wich a lacency o f 3 6 0 ms со a seep change in depth (Stark
e ta l. 1965).
Th e steady-state bias o f accom m odation manifests itself in
The accom m odative response to a 2 D ramp change in
a tendency to return to che tonic scace o f dark focus ac
discance from an inicial discance o f 2.5 D becam e less stable
abouc 1.5 D , as shown in Figure 9.20. For exam ple, with
as ramp velocicy increased from 0.5 со 5 D/s. Ac higher
a 1-nim pupil, objects closer than che scace o t dark focus
velocities, che accominodacive response m ore trequencly
were severely underaccom m odaced, while o b jects beyond
lagged behind che scimulus and required rapid cacch-up
the resting scace were slightly overaccom m odated (W ard
movements со bring it back on target (H ung and Ciuffreda
and C harm an 1 985). A nything thac increases chc depth
1988).
o f field allows accom m odation more latitude to change
w ithout generating an effective error signal. The tendency
to move coward che resting state is therefore increased, 9 .7 .2 b Gain
which flattens the stim ulus-rcsponsc curve. Thus, pupil
The gain o f acco m m o d a tio n is response am plitude as a
constriction and low stimulus concrasc increase depth o f
function o f chc change in depth o f che stimulus, boch
Held and thus increase the tendency o f che eyes со return со
expressed in diopcers. G ain declines with increasing fre­
the scace o f dark focus.
quency (Scark 19 68; O ’ Neill W D and Brodkey 1970).
Alchough a sccady-stacc bias degrades che accuracy
Subjects may learn to anticipate the m ovem ent o f stimuli
o f any control system, it improves ics stability. The bias
that change sinusoidally, and thereby improve gain and
dam pens any ccndcncy o f the sysccm со drift against the
phase lag (Van der W ild t ec al. 1 9 7 4 ). This problem may
direccion o f che bias, hi ocher words, a bias applies an elastic
be avoided by using unprediccable scimulus changes. See
conscrainc. Also, a biased syscem
/ is noc likelv
t со drift far Charm an and Heron (2 0 0 0 ) for a discussion o f chis issue.
in the direction o f che bias. An unbiased accommodacion
A nocher problem is chac people are able со in h ibit che
syscem fluccuaccs around che cencer o f rhe depth o f field
accom m odative response to a stimulus m oving sinusoidally
(che posicion o f m inim um blu r), while a biased syscem is
in depth (Van der W ild t et al. 1974).
pulled coward one boundary o t che blur-dececcion chresh­
W e saw in Section 9 .6 .4 c thac che gain o f sceady-scace
old region. We saw in Seccion 9.6.1 chac che discrim ination
accom m odacion is optim al for sinusoidal gratings with
chreshold for changes in blur is lower tor scimuli slighdy
spatial frequencies o f 3 ro 5 cpd. O n e can ask how che gain
away from the position o f minim um blur. An unbiased
o f accom m odacion is affected by che tem poral frequ en cy
system requires a large change in focus in one or the other
o f scimulus modulacion in depch.
direccion со gcncrace a dececcable error signal. A biased
C am pbell and W escheimer ( I 9 6 0 ) tound chat che
system requires only a small change o f focus in the direc­
maximum cemporal frequency o f sinusoidal oscillacion
cion o f che bias со gcncrace a detectable signal. In chis way
ot a square-wave gracing thac evoked a detectable change
a sceady-scace error o f accom m odacion improves che etfec-
in accom m odation was about 4 Hz.
civcncss o f chc error signal arising from microfluccuacions
M adiew s and Kruger (1 9 9 4 ) suggesced chac che gain
o f accom m odacion.
o f accommodacion to a grating would be improved by an
increase in either the amplitude or temporal frequency
o f depth m odulation. They proposed that im provem ent
9 .7 .2 D Y N A M I C S О F A C С О M M О D A T IО N would be greater tor gratings o f low spatial frequency
than for those o f high spatial frequency. They measured
9 .7 .2 а Lacency and Phase Lag
accom m odative responses to sine-wave gratings with spacial
Accom m odacion со a 2 D seep change in dcpch occurred frequencies becween 0 .9 8 and 10.5 cpd, modulaced in
with a mean laten cy o f about 3 5 0 ms. Response velocity depch ac frequencies betw een 0 .0 5 H z and 0.8 H z chrough
increased exponentially with a tim e constant o f abouc amplicudes o f 0 .5 or 2 D . The resulcs for one subjecc are
2 5 0 ms со a peak velocity o f about 10 D/s, which was shown in Figure 9 .2 6 . Gain was maximal ac spacial frequen­
reached in abouc 7 50 ms (C am pbell and W cstheim er I9 6 0 ; cies between 3 and 5 cpd, as reported by ocher investigators.
Tucker and C harm an 1 979). Latencies and response times For boch amplicudes o f depth modulacion, gain declined
were sim ilar for m onocular and binocular viewing. Latencies for all spacial frequencies as cemporal frequency increased
o f accom m odative responses were similar for seep changes from 0 .0 5 со 0.8 H z. However, higher tem poral frequencies
in stimulus distance at near distances and ac far distances or higher amplitudes had no more effect tor low spatial
(Shirachi cc al. 1978). frequencies than for high spatial frequencies.
The phase lag o f a cco m m o d atio n со a sinusoidal
scimulus change is che phase delay in degrees becween rhe
9 .7 .2 c Velocity o f A cco m m o d a tio n
peak response and che peak scimulus displaccmenc. The
phase la g o f accom m odative responses to a predictable sinu­ The peak v elo city o f saccades increases linearly with increas­
soidal m orion-in-depch was tound to be 100 ms compared ing amplitude, a relationship known as the m ain sequ en ce

(а) 2 D modulation
(b) 0.5 D modulation
Figure 9 .24*. Spatiotem poralproperties o f accom m odation, G a in o f
accom m odative; responses to a gratin g o f various spatial frequ encies
m odulated in depth at various tem p oral frequ en cies. The am plitude ot
m od u lation was 2 D in (a) and 0 .5 Г) in (b ). R esults for on e su b ject.
(A tfo plcd fitini M m Ii c m and Kro£Cf 1994)
(Seccion 10.5.8). Invescigacors agree chac peak velocicy
o f accom m odation increases with stimulus magnicudc.
However, estim ates o f the slope o f the function relating
velocity to am plitude have varied betw een 0.8 and 2.5.
These differences could be due to individual differences
and to investigators using different ranges and starting
points o f accom m odation and different optom eters.
D uring electrical stim ulation ot the Edingcr-W estphal
nucleus o f aneschecized m onkeys che peak velocity o f
accomm odative responses increased linearly as response
amplitude increased from 0 .5 8 to 17.41 D (V ilupuru and
Glasser 2 0 0 2 ). In five human subjects w ith an accom m oda­
tive range o f at least 6 D , peak velocity o f accom m odation
was a linear function o f am plitude for amplitudes between
0.1 and 3 D (C iutfrcda and Kruger 1988). There was great
intersubject variability betw een the ages o f 2 0 and 3 0 years
(Kaschurirangan c t al. 2 0 0 3 ). Л linear relationship between
velocity and am plitude was evident only for near-to-far
accom m odation.
A ccom m odation tends to relax to the resting state o f
about 1.5 D iopters (Scctio n 9 .3 .1 ). O n e m ight therefore
expect that accom m odation responses would be faster
when the stim ulus moves toward the location o f the resting
state than when it moves away from the resting state. This
would mean that, trom an initial tar position, far-to-near
accom m odation should be faster than near-to-far accom ­
m odation. From an initial near position, near-to-far should
be faster. Shirachi et al. (1 9 7 8 ) found that the velocities
o t accom m odation to step changes in stimulus distance
conform ed to this pattern.
Schaertel et al. (1 9 9 3 ) found far-to-near accom m oda­
tion in the range 1 D to - 7 .1 D to be slower than near-
to -far accom m odation. However, Heron and W in n (1 9 8 9 )
reported that near-to-far accom m odation w ithin the range
- 0 .5 to - 5 D had a longer latency and took longer to reach
its final state than far-to-near accom m odation. But these
investigators did not distinguish between responses toward
the resting state and those away from the resting state.
Yamada and Ukai (1 9 9 7 ) produced evidence that the
presence o f image blur bu t not its m agnitude is registered
before an accom m odative response is initiated. They m ea­
sured dynam ic accommodative responses as a small visual
target m oving stepwise through various depth intervals,
either trom tar to near or from near to tar. Figure 9 .2 7 shows
a set o f near-to-far responses from one subject. Initially,
all responses changed at the same rate. In other words,
the responses did not obey the main-sequence rule typical
ot saccades and vergence. The initial com m on velocity ot
accom m odative responses could reflecc the tim e constant
o t return ot the ciliary muscles to their conic state ot
accom m odation at about 1.5 D. It can be seen in that the
responses leveled oft in order o f their m agnitude. Yamada
and U kai argued chac, during a near-co-far response, blur
is noc preregiscered buc is concinually m onicorcd and
chac chc response hales when blur is minimal. Hut Yamada
and U k a is data do n o t prove chat blur magnitude is noc
preregiscered.
Time (s)
i 9.27. steeom m etfatiee n ear-to-far step responses. Sam ple responses from
o n e su b ject. Iron. Y j n W i Jfid U l u ! I W )
 M arran and Sch or (1 9 9 8 ) argued that the states o f focus
o f the stim uli in these studies were not sufficientlyi different
in the tw o eyes and th at the stim uli may have been rival-
rous. They also pointed out that responses were measured
successively rather than simultaneously. After allowing for
these factors they measured the response o f the two eyes to
lens-induced an iso-accom m odative stimuli. The targets
were dichoptic letters, cach in a binocular fram e. The d if­
ferential blur of the letters provided visual feedback about
rhe relative accom m odation o f the two eyes. Positive lenses,
increasing in steps o f 0.5 D up to 3 D , were introduced
alternately before the left and right eyes. Subjects attempted
to keep both letters in focus while their accom m odation
was measured over a period o f 3 m inutes. The mean an iso-
accom m odative response was 0.75 D for the largest stim u­
lus value. For four o f seven subjects the response became
more consensual as distance was increased. This effect was
a function o f the apparent distance o f the targets rather
than o f the level o f accom m odation (M arran and Sch or
1999).
The aniso-accom m odation responses had a mean latency
o f 11 s and took 4.5 s to com plete, compared w ith a latency
o f 0 .4 s and a com pletion tim e o f 1.25 s for consensual
responses. These differences in dynamics suggest th at aniso-
accom m odation is designed to deal w ith steady-state errors
rather than rapidly changing stimuli.
Koh and C harm an (1 9 9 8 b ) presented subjects with
objects that differed in accom m odative distance by up to
3 L). They found no systematic aniso-accom m odation.
Rather, both eyes tended to accom m odate to the more
distant object.
Flitcroft et al. 1,1992) measured accom m odative
responses to stimuli rapidly changing in accommodative
demand. They m odulated accom m odation demand by sinu­
soidally changing the power o f lenses placed in fron t o f the
eyes. The phase o f stimulus m odulation differed between
the two eyes by either 90" or 180°, or else the modulation
was applied to only one eye. In both humans and monkeys
the accom m odative response represented the vector average
o f the stimuli in the tw o eyes. Thus, when the modulation
was 180" out o f phase in the two eyes there was no response.
W hen the stimulus was modulated in only one eye, the
response was much reduced com pared w ith that in binocu ­
lar viewing. W h en the two eyes were presented with
modulated orthogonal gratings, stimulus averaging did noc
occur. Instead, the response at any tim e was determ ined by
whichever grating was perceptually dom inant (Flitcroft and
M orley 1997).
9 .7 .3 b M o n o v is io n
In rhe therapeutic process known as monovision, one
eye, usually the dom inant eye, is corrected for far vision
and the other eye is corrected for near vision. This is done
with refractive surgery, co n tact lenses, or intraocular lenses.
The proccss involves the deliberate introduction o f ani­
som etropia. Patients learn, with variable success, to see
whichever image is m ost clearly in focus and suppress the
more blurred image. Thus, they learn to use one eye for
far vision and the other eye for near vision.
9 .8 C U E IN G T H E S IG N O F
A C C O M M O D A T IO N
Static blur indicates the magnitude o f m isaccom m odation
but not its direction. This is because an out-of-focus image
is blurred by an equal am ount on either side of the plane
o f focus. Hlur is said to provide an even-error signal.
U nder natural conditions, depth cues such as perspec­
tive, overlap, parallax, and disparity indicate w hether the
eyes are under- or overaccom m odated. In the absence of
such cues, the correct direction o f accom m odation could be
determ ined by trial and error. However, accommodative
responses usually occur immediately in che correct direc­
tion. This means that underaccom m odated images must
differ in some way from overaccom m odated images.
Any such difference could provide an odd-error signal.
W hatever m echanism s are used to sign the direction o f
accom m odation, it has been found that they fail for images
more than 2 diopters out o f focus (Fincham 1 9 5 1 ). Types
o f inform ation that could indicate the direction o f accom ­
modation are described in che follow ing seccions.
9. 8. 1 H U N T I N G AND DYNAMIC
ERROR FEEDBACK
The initial accom m odation со an ouc-of-focus image could
be made ac random and chen correcced if in che wrong
direction. C am pbell and W estheim er (1 9 5 9 ) found chac
subjects made many initial errors in responses to an out-
of-focus image when cues со the direction o f m isaccom m o­
dation were elim inated.
Troelstra et al. (1 9 6 4 ) cried со elim inate all cues to che
direction o f accom m odation, including chrom atic aberra­
cion. They measured che inicial responses со a horizontal
line as it scepped randomly in depth through + 2 D every
4 0 0 ms. Two o f chrec subjeccs always responded in che co r­
rect direction. They presumably used a cue that had not
been com pletely elim inated. H alf the inicial responses o f
the third subject were in the wrong direction but were
quickly corrected. This indicates th at the su bject was hunt­
ing. H unting is therefore a possible mode o fop eration when
o ther cues are not available.
M icrofluctuations o f accom m odation thac occur in che
2-H z range may provide directional inform ation w ithin the
0.3-s reaction tim e o f a response. This would not work for
large changes in accom m odacion, because m icrofluctua-
cions o f blur would noc be deceeced when the image is well
ouc o f focus. Responses со seep changes o f less chan 1 D have
been found со be in chc correcc dircccion (Fincham 1951). In general, subjeccs maincaincd accurace and sccady
Koculak and Sch or (1 9 8 6 d ) developed a model o f accom ­ accom m odacion in whice lighc buc becam e unscable in
modacion concrolled by error signals arising from m icrof- m onochrom acic lighc, especially ac chc viewing discance
luccuacions ot accom m odacion. o f 5 D (2 0 cm ). W h en chrom acic aberracion was reversed,
accom m odation ac all discances bccam c severely unscable
and drifted from the correcc scace toward che scace o f dark
9. 8.2 B L U R S I G N A N D LENS
accom m odation. In another experiment trom the same
ABERRATIONS
laboratory accommodacive responses were evoked by
The visual svsccm
i could relv* on some feacure ot an ouc- sinc-wave gracings concaining chromacic fringes chac
of-focus image chac varies according со whecher che scimu­ simulaced longicudinal chromacic aberracions produced by
lus is nearer chan or beyond che plane ot tocus. O ff-axis ouc-of-focus images (Lee ec al. 1999).
spherical aberracion, chrom acic aberracion, and ascigmacism W ilson ec al. (2 0 0 2 ) used a drug to reduce accom m oda­
vary in chis way. tive responses. O u t-of-focu s images o t a point of light with
narrow spectral bandwidth were presented m onocularly in
a Badal optom eter. The spherical aberrations tor cach sub­
9 .8 .2 a S p h e ric a l and C h r o m a tic A b crra cio n s
ject were measured with a H artm ann-Shack sensor. Subjects
Spherical aberracion atfeccs che shape ot chc poinc-spread were then asked to discrim inate betw een under- and over-
funccion produced by a poinc o f m onochrom acic lighc. focused images. D iscrim ination improved with increasing
Also, che poinc-spread funccion ot an undertocused image pupil size and with increasing defocus blur. W ith a 5-mm
differs from chac o f an overfocused image (W ilso n cc al. pupil, subjects could discrim inate the sign o f defocus o f
2002). an image defocuscd by 0 .3 4 D . This was the smallest
The color fringes produced by chrom acic abcrracions value used. W ilson c t al. did not measure accommodative
vary according со whecher che eve is under- or overaccom - responses but argued that it subjects can detect the sign ot
modaccd on chc cargec. Thus, chc image o f a poinc o f whice spherical aberration ic is likely chac ic can cue chc dircccion
lighc cends со be surrounded by a red fringe when che eyes ot accom m odacion.
arc undcraccommodaced (hypcropic) and by a blue fringe
when chey are overaccommodaced (m yopic). The visual
cffeccs o f chrom acic aberracion were firsc described bv
Polack ( 1 9 2 3 ). Ivanoff (1 9 4 9 ) suggesced chac color fringes
produced by longicudinal chrom acic aberracion could sig­
nify che sign o f misaccom m odacion.
The rcfraccivc scace o t an eye
/ could be derived bv
* com -
paring image qualicy in che chree cvpes o f cone. Fliccroft
(1 9 9 0 ) showed cheorecically chac color opponenc cells in
che visual corcex could perform chis cask. W hac is che evi­
dence chac we make use o t chrom acic aberracion or spherical
aberracion?

9 .8 .2 b A b e rra cio n s an d Scacic A c c o m m o d a c io n

C onsider first chc cffeccs o f eliminacing chromacic abcrra-

cion on che accuracy and scabilicy ot sceady-scace accom ­
modacion. B o b icrec al. (1 9 9 2 ) claim cd chac changes in chc
magnicude or direccion o t eicher form of chromacic aberra­
cion did noc atfccc chc mean error o f scacic accom m odacion.
However, che subjeccive mechod chac chey used со measure
accomm odacion was insensicivc со rapid changes in accom ­
modacion. Koculak ec al. (1 9 9 5 ) found no effecc o f reduc­
ing che spcccral bandwidch of chc scimulus on chc mean
n*urc9.2s. P hilip li. Kruger.: B o rn in S o u th A frica in 1 9 4 7 . H e graduated
sceady-scace error o f accom m odacion. However, chey in o p to m e try from th e U n iv ersity o f 1 Houston and ob tain ed a P h.D .
used only one viewing discance o f 1 m, which is close со chc from th e N ew York State C o lleg e o t O p to m e try in 1 9 8 4 . H e was
posicion o f che rescing scace o f accom m odacion. appointed associate professor a t the C o lleg e o t O p to m e try in 1985
an d professor in 1 9 8 9 . H e was awarded the D istin guish ed
Kruger ec al. (1 9 9 7 a ) recorded accom m odacion for
A ch ievem en t Award o f th e N ew York State O p to m ctric A ssociation
4 0 s, while subjeccs viewed, chrough a Badal lens, a 3.5-cpd in 1 9 9 4 and th e C h a n c e llo rs Award for E xcellen ce in R esearch in
gracing ac diseances o t 0 ,2 .5 , and 5 D (Porcraic Figure 9 .2 8 ). 2003.
 9 .8 .2 c A b e r r a tio n s an d S te p C h a n g e s
in A c c o m m o d a tio n
Fincham (1 9 5 1 ) found that, with a target illum inated with
w hite light, all their subjects eould change accom m odation
appropriately when a l.O -D lens was placed before the eye.
However, 6 0 % o f subjects were unable to change their
accom m odation in m onochrom atic yellow light, for which
there is no chrom atic aberration, or when che chrom atic
aberration was removed by an achrom atizing lens. Subjects
who could accom m odate in m onochrom atic light must
have used som e other sign cue, such as spherical aberration.
C am pbell and W estheim er (1 9 5 9 ) had subjects view a
high-contrast test o b ject through a Badal lens. This elim i­
nated changes in illum ination and image size as the distance
o f the test o b ject was varied. The ciliary muscles were
paralyzed by hom atropine. Tine target was suddenly dis­
placed by 0.5 or 1.0 diopter, and subjects moved a manual
control to bring the image back into focus. W ith practice,
chey were able со move che cargec in che correcc direccion on
every crial. Som e subjects failed in m onochrom atic light,
showing chat they must have been using chrom atic aberra­
tion. But som e subjects continued to perform correctly in
m onochrom atic light and, eventually, all subjects learned to
perforin correctly. C am pbell and W estheim er claim ed that
subjects were using spherical aberracion, since they failed со
respond in m onochrom acic light when spherical aberration
was removed by the incroduccion o f an annular pupil. Buc,
wich boch chrom acic and spherical aberracions removed,
perform ance was rescored when subjects viewed che cargec
through a l - l ) cylindrical lens. Thus, astigmatism can also be
a cue со chc sign ot blur (see also Kruger and Pola 1986).
The aberrations o f a given eye may be measured wich a
Shack-H arcm ann wavefronc sensor (Section 9 .1 .3 c). The
9 .8 .2 d A b e rr a tio n s an d D y n a m ic A c c o m m o d a tio n
The gain and phase lag o f accom m odation evoked by a stim ­
ulus moving sinusoidally in depth have been measured as
a f unction ot che chromacic concent o f che scimulus in che
follow ing ways.
1. Effect o f wavelength Aggarwala ec al. ( 1 9 9 5 a ) used an
infrared optom eter со record accommodacivc responses
со л radial-wedge paccern moving sinusoidally in depth
at 0 .2 H z through an am plitude o f 1.0 D . The pattern
was illuminated with m onochrom atic light with
wavelength ranging between 4 3 0 nm and 6 7 0 nm or
by white light. Th e lights were m atched for luminance.
W ich che m onochrom atic lighcs, che response was very
irregular, compared wich the response with white light,
especially at low and high wavelengths, as shown in
Figure 9 .2 9 . The response was also irregular with w hite
light viewed through achrom atizing lenses that
neutralized che longicudinal chromacic aberracion o f
che eyes.
2. Effect o f chromatic bandwidth O n e would expect
accom m odation to becom e more adequate as the
spectral bandwidth o f the stimulus is increased.
Aggarwala et al. (1 9 9 5 b ) recorded accommodative
responses to a 3.5-cp d grating moving sinusoidally in
depth at 0 .2 Hz through an amplicude o f 1.0 D. G ain
increased and phase lag declined as che spectral
S T IM U L U S S T IM U L U S
•

corrcccions may chen be used concrol an adaptive optics 5 7 0 nm

syscem, which nulls the aberrations. The adaptive optics

system consists o f a flexible mirror, like those used by 5 9 0 ^ m n ^ ^

astronom ers to correct images in telescopes. C h en e t al. С

О

(2 0 0 6 ) measured accom m odative responses o f six subjects

“О
to a 0 .5 D step change in focus o f a m onochrom atic Maltese *6 3 C H ^

cross. H igher-order aberrations ocher chan defocus and E

astigmatism were either present or absent. O n e subject 8
<
could noc accomm odace in eicher con d ition , and one sub­ ■

5 3 0 nm W h it e - lig h t n o r r r a l a b e r r a tio n
je c t could accom m odate only when the aberrations were
present. The o ther tour subjects could accommodace in che *

correct direction w ith or w ithout aberrations. Also, tor A c h r o m n l z n d w h i t e lic j^ .l

these subjects, the gain and latency o f accom m odation were

" г г г г г г г г г р 1 ■ г-гч ■
similar in the two conditions. There may have been some
10 20 30 40 0 10 20 30 40
residual aberrations, or perhaps these tour subjects used
T im e (s)
m icrofluctuations o f accom m odation to d etect the sign o f
defocus. Fi^r< 9.2*. Л к ом т с d a tion as a fu n ction o f w avelength. A su b jects

Removal o f aberrations reduces the depch o f field. O ne
would expect thac chis would improve accom m odation, buc
C hen ec al. found chac none o f cheir six subjects showed
im provem ent when aberrations were removed.
accom m odacivc track in g to sinusoidal target m o tio n in depth.
N o te th at responses to achrom atized w h ite light and to m ost o f the
10 m o n o ch ro m atic ligh ts w ere im paired relative to responses to
w h ite light w ith n orm al ch ro m atic ab erratio n . (A.U?tcifr«ниAguwjb ct
lWi)

IM A G E F O R M A T IO N A N D A C C O M M O D A T IO N • 467
image size is canceled by an opposice neural aniseikonia.
Furtherm ore, neural aniseikonia may persisc after a differ­
ence in image size has been corrected. These stacemencs are
explained lacer in this scction.
A n iseik o n ia o f e cc e n tric gaze occurs for objects dis­
placed to one side o f che median plane o f che head. This is
because such an objecc is nearer со one eye than со che ocher
and therefore projeccs a larger image in chac eye. Lancaster
preferred noc со use che cerm “aniseikonia” for chis etfecc
because ir is present in all eyes. H e applied che term only со
abnorm al sicuacions. Ind u ced a n iseik o n ia is produced by
wearing a fixed m agnifying lens in fronc o f one eye. In this
case, che eye wich che larger image muse move furcher chan
the eye wich chc smaller image when the gaze is direcced со
an ecccncric visual objecc. This is because che eye moves
wich respect to the head-fixed m agnifying lens. Thus, wich
induced aniseikonia, che eyes muse adopc an unusual ver­
gence angle when fixacing an ecccncric objecc. In ocher
words, che locus o f isovcrgencc isdiscurbed by induced ani­
seikonia. This produces a differencial etfecc on phoria
(Seccion 1 0 .2 .3 )— known as opcical an iso p h o ria (Rem ole
1989). F.ye movements are noc affected by aniseikonia due
to intrinsic causes, nor by aniseikonia induced by contact
lenses, because co n tact lenses move wich che eyes.
Sorsby ec al. (1 9 6 2 ) measured anisom etropias o f
betw een 2 and 15 diopters in 6 8 patients. In 4 9 cases, more
chan 5 0 pcrcenc o f che anisom etropia was due to differ­
ences in axial length. Л difference in axial length was the
exclusive or predom inant cause o f anisom etropias o f over
2 diopcers. Л difference in corneal curvacurc accounccd for
very little o f che condicion, and often reduced, racher chan
increased, the anisom etropia due to ocher causes.
There has been considerable dispute about the clinical
significance o f aniseikonia.
9 .9 . l b A n is e ik o n ia in A x ia l A m e tro p ia
The refractive power o t a lens in diopters is the reciprocal
o f its focal length, ^ in meters. The posterior focal length
o t an eye is che distance from the second principal poinc
to the focused image o f a distant o b ject, as illustrated in
Figure 9 .3 2 . In an em m etropic eye, che focused image is on
che recina. It follows th at the linear size o f the image o f a
distant o b je ct subtending angle в at che second principal
poinc o f an eye, wich refraccive power I), is f can 0, o r can
6/D. In other words, che size o f che retinal image is inversely
proportional to che refraccive power o f the eyes opcical
syscem. W hen an axially amccropic eye o f refraccive power
D f is correcced by a lens o f refraccive power D., the
com bined refractive power o f eye and lens is given by
D .^ D .f lV d D A
where d is che discancc from che 2nd principal poinc o f
che correccing lens со che lsc principal poinc ot che eye.
E y e diameter = 24.2 mm
A n te r io r v e r t e x
1 st a n d 2 n d
f o c a l le n g t h = 1 5 .3 m m
p r in c ip a l p la n e s
C e n te r of
r o ta tio n
^ ^ l s t a n d 2 n d
A n te rw r f o c a l le n g th n o d a l p o in ts
= - 1 6 .8 m m
P o s te r io r v e r te x
f o c a l le n g th = 17 m m
1 .8 m m P o s t e r io r f o c a l le n g th = 2 2 .- 1 m m
Figure I b e G uU itrandschernatiс unuccw nm oiLited eye.
The anterior focal point o f the eye is about 15 mm in front
o f che eye, which is abouc where a speccacle lens is worn.
Thus, when an axial amecropia is correcced by a chin spec­
cacle len s,/ = d and, since /->, = 1f f ,D u l - D r This means
chac che size o f che opcical image is che same as chac in
an emmecropic eye. This is known as K napp's law (Knapp
1869).
N ote that the law applies only to axial ametropia
corrected by a chin lens placed at che ancerior focal plane
o f che eye. C onsider rhe case o f an axial myopia. The eyeball
is elongated so thac che in-focus image is formed in fronc o f
chc recina. The ouc-of-focus image on the retina is larger
than rhe in-focus image. A chin speccacle lens worn abouc
15 mm in fronc o f che eye moves che in-focus image
onco che recina bu t does nor affecc ics size. This m eans chac
che in-focus image, which is now on che recina, is che same
size as char in an em m etropic eye, but smaller than che
uncorrected ouc-of-focus image.
W hen an axial hypermecropia is correcced, che image
is magnified wich respecc со che image before corrccrion.
The ancerior vercex discancc is che discancc from che fronc
focal poinc o f che eye со che cornea. For an axial ametropia
corrccced by a chin lens ac a vercex distance o f 18 m m , the
image is changed in size by about 2% for each diopter
o f correction. This decreases to 1.25% tor a vertex distance
o f 12 mm. Thus the change in image size becom es smaller
as che correccivc lens is moved closer со che eye. There is
no change in image size wich concacc lenses because che
vercex distance is zero. For a refraccive amecropia o f lencicu-
lar origin, che image size is changed abouc 1% per diopcer
o f corrccrion (von Bahr 1993). These values apply со
chin lenses. The effeccs are larger tor prescription lenses,
and depend on cheir chick ness and power.
(6) In uncorrecced axial anisom etropia, the image in one
eye is larger than that in the ocher. W e have jusc seen chac a
spectacle lens worn before an eye with axial amecropia causes
rhe image со be che same size as chac in an emmecropic eye.
In spite o f chis, many patients com plain chac chings appear
larger or smaller with a correcced eye chan with the normal
eye. O n e possible reason for this is as follows. An eye with
axial myopia is elongated. As a consequence, the retina is
stretched and receptor density is reduced. Thus, although
the out-of-focus retinal image o f an o b ject is enlarged in
an eye with uncorrcctcd axial myopia, it covers the same
number o f receptors as thac o f che image o f a norm al eye
(R ose and Levinson 19 7 2 ; Bradley ec al. 1 9 8 3 ). W hen chc
retinal image in an eye with axial myopia is brought into
focus and made optically the same size as that in the other
eye, che “neural” image becom es smaller chan that in rhe
o ther eye because it is spread over fewer receptors. In other
words, the images in the two eyes are made equal but a
neural aniseikonia remains. The differential magnification
o fth e images produced by axial anisom etropia need not be
corrected optically, because it is at least partially corrected
by the differential stretching o f the retinas. It is best to
correct anisom etropia with concacc lenses because they do
not change the size o f the images (W in n et al. 1988).
A nother problem with optical correction is chac die recina
may be screcched by differenc am ounts in differenc loca­
tions. This issue does noc seem со have been invescigated.
Relationships betw een anisom etropia and aniseikonia arc
summarized in Table 9.1.
9 .9 .1 c A n ise ik o n ia in Aphakia
Adults with unilateral loss o f a lens (aphakia) can have
vision restored by a spectacle lens, a concacc lens, or a lens
im plant. C o rrection with spectacles leads to aniseikonia o f
20% or more, which severely disrupts binocular vision.
C o rrection with a co n tact lens also produces aniseikonia
because the replacem ent lens is some distance in front of
the original lens. The aniseikonia is betw een 4 and 10%,
depending on w hether the aphakic eye was originally hyper-
mecropic or myopic (O gle ec al. 1958). Scereopsis is possible
T a b le • ).!. SU M M A R Y O F T H E E F F E C T S O F
A N IS O M E T R O P IA O N A N IS E IK O N IA . T H E
S T A T E M E N T S A R E G E N E R A L IZ A T IO N S
A N D M A Y N O T B E T R U E IN E V E R Y C A S E .
C O N D IT IO N A N IS E IK O N IA A N ISE IK O N IA
N EU RA L
U n c o r r c c tc d axial P revent P resen t
a n iso m e tro p ia
C o r r c c tc d axial N o t p resen t P resen t
a n iso m e tro p ia
U n c o r r c c tc d rcfra c tiv c N o t p resen t N o t prevent
a n iso m e tro p ia
C o rrc c te d ref гас ti vc P resen t N o t p resen t
a n iso m e tro p ia
wich chis magnicudc of' aniseikonia in mosc adults, but
n o t in children (H ighm an 1977). C o rrection with a lens
implant produces only about 2% o f aniseikonia because
the replacement lens is in essentially the same position
as che original lens. The am ount o f aniseikonia varies with
che scace o f accom m odation o f chc norm al eye relacive
со the fixed accom m odation o f t h e aphakic eye (Ivashina
1981). Ic also increases if a supplemencary corrective spec-
taclc lens has to be worn (M iyake ct al. 1981). C orrection
wich a lens im plant restores binocular stereopsis in m ost
patients (G irard et al. 1962; Miyake ec al. 1981). W h en
incraocular lenses are implanced inco boch eyes, aniseikonia
will occur it the lenses are noc in equivalent locations or
arc nor parallel (Lakshm inarayanan ec al. 1993). Ic has
been estim ated thac over three m illion lens im plant opera­
tions are performed every year (Lakshm inarayanan et al.
1993).
9 .9 .2 M E A S U R E M E N T O F A N IS E IK O N IA
An c ik o n o m cte r is an instrum ent tor measuring che
m agnitude and meridional direction o f aniseikonia. There
arc tw o basic types, the direcc com parison cikonom cter and
che space eikonomecer.
9 .9 .2 a D ir e c t C o m p a r is o n E ik o n o m c tc r
In the direct com parison cikonom cter dichoptic stimuli
are presented in a stereoscope. In one version che stim uli are
tour pairs o f nonius lines arranged round a central fixation
disc, as shown in Figure 9 .3 3 . Th e subjecc adjuscs che size
ot one image until all chc nonius lines appear aligned. The
difference in size o f che cwo images after che adjuscmenc
indicaccs the magnicudc o f aniseikonia (Barker 1 9 3 6 ; Allen
1937). O bservers may have difficulty com paring che sizes o f
images in chc visual periphery when fixacinga central point.
I f subjeccs are allowed со move cheir gaze со che m onocular
2 - -1
7 5
1 r 1 1
1 ь .2 1
8 6
4 - -3
9.УУ D isplay f o r d irect com parison eikonw ncter. W ith fixatio n o n the
b in o cu lar ccn rral square, od d -n u m b crcd lines a rc presented to o n e eye
and even-num bered lines to chc ocher. M agn ification o f an afocal lens
b efore o n e eye is adjusted until the pairs o f lines appear align ed . {R««lca*t>
6omOfcIc 196*0
images in succession, che images may becom e misaligned It can be used only for people wich stereoscopic vision.
due со fixacion disparicy or phoria, and chis interferes wich People wich severe aniseikonia are unable со fuse che images,
chc measurement o f aniseikonia. and arc chus unable со judge the stereoscopic discorcions
In a related m echod, cwo parallel lines are presenced со chac che inscrumenc produces. A vercical meridional lens
one eve in a sccrcoscope, and a scale is presenced со chc ocher magnifies che image horizoncally. Such a lens worn before
eye. The su bject indicates che perceived discance becween one eye incroduces horizoncal disparicy becween che
che lines by the numbers on che scale. The mean ot several images in che cwo eyes, w hich causes a froncal-planc surface
readings indicaces che magnicude o f aniseikonia for che со appear slanced abouc a vercical axis, as illuscraced in
meridian extending between the parallel lines. A niseikonia Figure 9 .3 4 . The geomecry o t this type o t disparicy is
along ocher meridians is measured by seccing che parallel discussed in Seccion 19.3.3.
lines in other directions. O n e mighc cxpecc chac, wichout a correccive lens,
In a cesc designed by Brecher (1 9 5 1 ) one eye views cwo people wich meridional aniseikonia would experience
poincs o t lighc directly, and che ocher eye views chem corresponding discorcions ot visual space. However, chese
chrough M addox rods, w hich spread che poincs o u t со form discorcions may noc be nociced in a norm al visual environ­
cwo vertical streaks. The m agnitude ot aniseikonia is indi- menc because o f che many veridical m onocular cues со
caccd by che apparenc separacion o f che cwo poincs relacive depch. W hen m onocular cues are eliminaced or reduced,
со che apparenc separation o t che cwo screaks. discorcions due со aniseikonia are apparenc. The degree and
Presencing a poinc со one eye and a screak со che ocher meridional axis o f aniseikonia is indicaced by che m agni­
provides only a weak fusional scimulus. It che subjecc has cude and direccion o t apparenc slanc o f a froncal surface.
a phoria, che poinc will be displaced relacive со che screak, Becween 1932 and 1947, Ames and his associates ac
making che judgm enc o t relacive separacion d ifficu lt This che Darcm ouch Eye Inscicuce in Hanover, New Ham pshire,
problem may be overcom e by nulling che phoria wich a devised cescs o f aniseikonia based on chis principle. See
prism. Anocher way со reduce che tendency со fuse che Burian (1 9 4 8 ) for a history o f the D artm outh Institute.
dichopcic scimuli in che direcc com parison eikonom cccr Figure 9.35 shows chc essential features o f che space
is со alternate chem со che cwo eyes (B recher ec al. 1958). eikonom eter (Am es 1945). The subject views a frame co n ­
A ulhorns phase-ditfcrcnce haploscopc can measure taining a pair o f oblique threads from a distance o f abouc
aniseikonia (A ulhorn 1 9 6 6 ). H alf-circles are presenced 3 m. A pair o f vercical chrcads is suspended abouc 6 0 cm
alccrnacely со cach eye in rapid succession. H orizoncal ani­ in fronc ot che frame and a second pair o t vercical threads
seikonia is measured by projeccing one half-circle above is suspended 6 0 cm beyond che fram e. ’I he subjecc views
che other and adjuscing ic uncil chey appear as a circle.
Vercical aniseikonia is measured by projeccing che half­
circles side-by-side.
P erceived surface
In all chese mechods, che m agnification o f an afocal
lens placed before one eye is changed until the image in that
eye appears che same size as che image in che ocher eye.
Aniseikonia is indicated by che seccing o f che lens.
An ordinary ophchalm ic lens changes cheetfeccive focal
discance o f che image relacive со che objccc, in addicion
со changing che magnificacion o f che image. For purposes
o f measuring aniseikonia, only a change in image size is
required. An afocal lens changes che size o f che image buc
has no power со change che focal discance o t discan с objeccs.
Lenses can be designed chac m agnify images o f objeccs ac
differenc discances by che same anwiinc. A lens unic avail­
able from che American O pcical C om pany can be adjusted
to produce a range ot m agnifications with little change in
the optical distance o f chc image relacive со chc objccc (see
O gle 1 964). A m erid io n al afocal lens is cylindrical, and
magnifies chc image along only one m eridian— che merid­
ian ac righc angles со che axis o f che lens.

Figure 9..14. E ffect o f a m erid io n a l len s on p erceiv ed slan t. A me rid ional

9 .9 .2 b S p a ce E ik o n o m e te r lens h orizon tally m agnifies o n e eye s im age o f л fro n tal surface
(d otted lines). T h e vertical edges o f th e surface appear where
A space eik o n o m eter is an inscrumenc for measuring p ro jectio n s o f the edges o f chc u nm agnificd and m agnified im ages
discorcions in stereoscopic vision induced by aniseikonia. in tersect. (Rednun {fcmC.iUxm 1967)
where a is chc interocular distance (O gle 1964, p. 162).
Vercieal m agnification ot chc same image causes a frontal
surface со appear slanted in the opposice direction. This
is the induced effect discussed in Seccion 2 0 .2 .3 . Overall
m agnification o f one image has no effect on depth judg­
ments (Epstein 1 9 7 2 ). M agnification o f one image contains
boch horizontal and vertical disparicy, so chat their effects
cancel.
O n e can ask whether people adapt со prolonged exp o­
sure to meridional aniseikonia. Burian (1 9 4 3 ) had three
observers with norm al vision wear a horizontal meridional
lens in fronc o f one eye for betw een 8 and 14 days. The lens
magnified che image only in che horizontal direccion.
Ac firsc, chc subjects reported spatial distortions— che tops
o f tables appeared inclined and walls appeared to slant ac
unusual angles. After 2 or 3 days, distorcions were no longer
noticed in normal visual surroundings, but they reappeared
in surroundings where m onocular cues со depch were
impoverished, such as a wide meadow. The space distortions
remained undim inished when measured wich a space
eikonom ecer or horopcer apparatus under condicions where
m onocular cues со depch were reduced со a m inim um .
M iles (1 9 4 8 ) reporced similar resulcs in five subjeccs
exposed со long-term adapcacion со chc induced cffecc pro­
duced by vercieal m agnification o f che image in one eye.
M orrison (1 9 7 2 ) produced sim ilar resulcs in eighc subjects
exposed for an average of 12 days to horizontal aniseikonia
and in cwo subjects exposed to vertical aniseikonia. Remole
(1 9 9 1 ), also, found adaptation o f the perceptual etfects
o f aniseikonia in a real-world setcing buc licde reduction
in eikonom eter settings, even after 4 years.
These results suggest thac long-cerm adapcacion со ani­
seikonia is due to an increased reliance on cues со distance
other chan binocular disparicy racher chan со adapcacion
o f chc stereoscopic system.
O th er evidence suggescs chac exposure со aniseikonia
induces an adaptive recalibracion o f thedisparicy-decection
system. Epstein and M organ (1 9 7 0 ) found that equidis­
tance settings o f two lum inous vertical lines in dark sur­
roundings changed after subjects walked about a building
for one hour wearing a m eridional lens that horizontally
magnified the image in one eye 5% . The aftereffect repre­
sented abouc 3 7 % o f full adapcacion со chc m eridional lens.
Epscein and Daviess (1 9 7 2 ) asked subjeccs со sec a hori-
zoncal luminous line to appear in che froncal plane after
exploring a building for 10 minutes while wearing a lens
thac horizontally magnified one image 4.5% . An isolated
line contains virtually no m onocular cues to depth. O n
average, the apparent frontal plane shifted by 5.7°. They
concludcd chac chc aftereffecc is noc due со recalibracion o f
absoluce depch buc racher со chc recalibracion o f disparity.
F.pstcin and M organ-Paap (1 9 7 4 ) obtained a similar
change in frontal-plane sectings alter inspection o f a surface
slanted 6 0 ° by disparity but only 20" by perspective.
Adams et al. (2 0 0 1 ) had six subjects wear, for 6 days,
a lens that horizontally magnified the image in the right
eye by 3.8% . This had no effect on the perceived slant o f
texturcd surfaces viewed monocularly. Nor did it affect the
relative weighting o f disparity and texture perspective in
a cue conflict situation. In a third test, subjects adjusted the
disparity in a random -dots display until it appeared frontal.
W h en the lens was first introduced che required disparicy
was equivalenc со a slanc o f 7 .5 ”, close со that introduced by
the magnifier. A fter six days the equivalent slant was only
1.4”. An aftereffect o f 3.2° was observed after the magnifier
was removed. In a separate test they established that these
changes were not due to changes in local sign in each retina.
They concludcd that adapcacion со differencial horizoncal
m agnification is due to the recalibration o f the disparity
system, rather than to a change in the relative weighting
o f disparity and other cues to distance or to changes in the
m onocular images.
It is n o t clear why Burian and M iles found that adapta­
tion to aniseikonia did n o t affect slant settings in the
eikonom eter, although Adams et al. found that adaptation
produced a substantial recalibration o f disparity.
All the above investigators used the task o f setting
stimuli to equidistance. G ogel and Szoc (1 9 7 4 ) measured
the effects o f exposure to a conflict betw een disparity and
perspective by a test involving equidistance settings and
by a test involving the alignm ent o f nonius lines. O n ly the
form er test was affected by the adaptation procedure. Since
the nonius test is a m ore reliable indicator o f binocular
correspondence, these results suggest that the basic pattern
ot binocular correspondence is not affected by exposure
to discordant visual cues. Buc chis leaves open chc possibil-
icy chac adapcacion со aniseikonia affects che calibracion o f
disparicy in che perccpcion o f slanc.
O cher aspeccs o f adapcacion со con flictin g depth cues
arc discussed in C hapter 30.
 10

V E R G E N C E EYE M O V E M E N T S

10.1 Eye movements in general 475 1 0 .5 .9 V e r g e n c e g a in a n d p h a s e la g 515

10 . 1 . 1 T yp es o f eye m ov em en t 475 1 0 .5 .1 0 T r ig g e r a n d fu s io n - lo c k c o m p o n e n t s 516
1 0 .1 .2 A x is s y s te m s f o r e y e m o v e m e n t s 476 1 0 .5 .1 1 M o d e lin g t h e v e r g e n c e sy s te m 5 19
1 0 .1 .3 S p e d f ic a t io n o f v e r g e n c e e y e m o v e m e n ts 480 1 0 .6 V e r t ic a l v e r g e n c e 5 21
10.2 Tonic vergence 483 1 0 .6 .1 R a n g e o f v e r tic a l v e r g e n c e 521
1 0 .2 .1 D a rk v erg en ce 483 1 0 .6 .2 V e r t ic a l p h o r ia 522
1 0 .2 .2 S t r a b is m u s 483 1 0 .6 .3 T h e s tim u lu s f o r v e r tic a l v e r g e n c e 52 2
1 0 .2 .3 P h o r ia 486 1 0 .6 .4 D y n a m ic s o f v e r t ic a l v e r g e n c e 524
1 0 .2 .4 F ix a t io n d is p a r it y 488 1 0 .7 C y c lo v e r g e n c e 525
1 0 .2 .5 T o n i c v e r g e n c e a d a p t a t io n t o p r is m s 492 1 0 .7 .1 T y p e s o f t o r s io n a l r e s p o n s e 525
1 0 .2 .6 N o n c o n c o m i t a n t v e r g e n c e a d a p t a t io n 49$ 1 0 .7 .2 M e a s u r e m e n t o f c y c lo v e r g e n c e 52 7
1 0 .3 V o lu n ta r y a n d p ro x im a l v c r g e n c e 496 1 0 .7 .3 D y n a m ic s o f c y c lo v e r g e n c e 528
1 0 .3 .1 V o lu n t a r y v e r g e n c e 496 1 0 .7 .4 C y c lo v e r g e n c e a n d a n g le o f g a z e 530
1 0 .3 .2 P r o x im a l v e r g e n c e 447 1 0 .7 .5 V is u a l s tim u lu s f o r c y c lo v e r g e n c e 530
10.4 Accommodation and vergence 500 1 0 .8 V e r g e n c c 'v e r s i o n i n t e r a c t i o n s 555
1 0 .4 .1 A c c o m m o d a t iv e c o n v e r g e n c e 500 1 0 .8 .1 H e r in g ’s law o f e q u a l in n e r v a t io n $33
1 0 .4 .2 C o n v e r g e n c e a c c o m m o d a t io n 50 2 1 0 .8 .2 V e r g e n c e -v e r s io n a d d it iv it y 53 5
1 0 .4 .3 R e la t io n b e tw e e n A C a n d C A 5 02 1 0 .8 .3 A d a p t a t io n t o a n is e ik o n ia a n d p a r e s is S38
10.5 Vergence evoked by disparity 505 1 0 .9 V e r g e n c e - v e s t i b u la r i n t e r a c t i o n s 5 41
1 0 .5 .1 M o n o c u l a r m o t io n a s s tim u lu s f o r v e r g e n c e 505 1 0 .9 .1 R o t a r y V O R a n d v ie w in g d is ta n c e 541
1 0 .5 .2 P r o c e s s in g d is p a r it y t o r c o n t r o l o f v e r g e n c e W 1 0 .9 .2 L in e a r V O R a n d v ie w in g d is ta n c e 542
1 0 .5 .3 R a n g e o f v erg en ce 506 1 0 .9 .3 V e r g e n c e i n d u c e d b y fo r w a r d m o t io n 544
1 0 .5 .4 S t a b i lity o f v e r g e n c e SO S 10 . 1 0 P h y s io lo g y o f v e r g e n c e 544
1 0 .5 .5 S t im u lu s s u m m a tio n f o r h o r iz o n ta l v e r g e n c e 510 1 0 .1 0 .1 O c u l o m o t o r n e r v e s a n d n u c le i 544
1 0 .5 .6 E f f e c t s o f s tim u lu s p o s it io n 54 1 0 .1 0 .2 S u b c o r t ic a l c o n t r o l o f v e r g e n c e 544
1 0 .5 .7 V e r g e n c e la t e n c y 5 II 1 0 .1 0 .3 C o r t i c a l c o n t r o l o f v e r g e n c e 547
1 0 .5 .8 V e r g e n c e d y n a m ic s 5 13 1 0 .1 0 .4 P h y s io lo g y o f c y c lo v e r g e n c e 548

1 0 .1 E V E M O V E M E N T S IN G E N E R A L (sem icircularcanals, ucriclcs, and saccules). The stimuli

cause chc eyes со rocacc in cheir orbics in che opposicc
direccion со che m ocion o f the head and chereby
1 0 .1 .1 T Y P E S O F EYE M O V E M E N T
scabilizc chc image o f che scacionarv sccnc. These eve
Tlie neurom uscular syscem that controls eye-movemencs is movements are known .is v estib u lo o cu la r responses
perhaps the best understood sensorim otor system. Ic c o n ­ (V O R ) (see Howard 1986).
sists o f six voluncary excraocular muscles around each eye, .vs
shown in Figure 10.1. The musclcs behave in a consisrcnc W hen chc eyes arc open, chc V O R is supplemented by
way со well-defined scimuli. They are concrolled by a nec- o p to k in e tic nystagm us (O K N ), w hich is evoked by
work o f subcortical and corcical neural cencers. Derails chc m ocion o f chc rccinal image o f chc visual sccnc (sec
abouc che muscles and cencers are given in Section 10.10.1. Howard 1 9 9 3 ). The response consists o f alcernacing
F.yc movcmencs serve chc following basic funccions. slow and fasc phases. Slow phases occur in a direccion
chac cancels che m otion o f the image. Q u ick phases
1. Compensation for head?notion C ircular or linear rapidly return chc eyes со cheir scarring position.
m otion o f the head stim ulates che vescibular organs Vescibuloocular responses and O K N are involuncary

Figarc 10.1. E x ln u t c u /a r m u ic l a o f t h e 1 ф e y e .
м/untt\ Cfxinexy o l O h j r U i C - T h o m a s P u b M w r , S fm * x 6 fld . Ilh n o u )
and occur in mosc vcrccbraces. They were che firsc cypes
o f eve movemenc со evolve.
ф
2. Fixation o f the image on thefov ea A nim als wich foveace
eyes are able со hold che image o f a selccced objccc on
che foveas. W h ile fixating a scacionary objecc, che eyes
cxhibic p h ysiological nystagm us. This consiscs o f a
m ixture o f slow drifts and microsaccades wich a mean
standard deviation o f abouc 0.1° (Sccinm an cc al. 1973;
O ct et al. 1 992). The am plitude o f these m ovem ents can
be reduced by voluntary efforc (Sccinm an cc al. 1967). If
image mocion is scopped, che images o f all objeccs fade
from view after a shore cime. Thus, eye m ovem ents are
needed for continued vision.
Marshall and Talboc (1 9 4 2 ) suggested chac che
constant mocion o f che recinal image produced by
fixation trem or improves visual acuicy. However, che
follow ing evidence does noc supporc chis hypochesis.
Acuicy and concrasc sensicivicy were noc adversely
affecced by image scabilizacion before che image faded
(K ecscy 1 9 6 0 ; G ilberc and Fender 1969). Imposed
image mocions ac velocities up to 2.5°/s had no effecc
on acuicy (W cschcim cr and M cK ee 1975, 1977). A
person makes fewer m icrosaccades when dececcing fine
detail, which would be countcrproduccivc if
microsaccades improved acuicy (W m cerson and
C ollcw ijn 19 7 6 ; Bridgcm an and Palca 1980). This
evidence suggescs chac physiological nystagmus has noc
evolved со improve acuicy. However, Rucci cc al.
(2 0 0 7 ) found chac stabilizing che retinal image only
becween voluncary saccadcs improved chc
discrim inacion o fo rch og o n al high spacial-frequency
gracings. This indicaccs chac jiccering fixacion facilitates
che processing o f fine detail. T h e stabi licy o f binocular
fixation is discussed in Section 10.5.4.
3. Change o f gaze Foveace animals can change their
direction o f gaze rapidly from one o b jcct со anochcr.
Trochlea These saccad ic eye m ovem ents are voluntary and occur
S uperior oblique at a velocity o f up со 6 0 0 7 s .
S uperior rectus
4 . Voluntary pursuit o f moving objects Foveace anim als are
able со move chcir eyes so as со maincain chc image o f a
moving o b ject on the foveas.
5. Maintenance o f binocular fixation A nim als with
binocular vision have evolved vergen ce eye m ovem ents
so as со converge che visual axes o n to a selected object
and maincain boch images o f an objccc on chc foveas as
rectus
the o b ject moves in depth.
Lateral rectus
Inferior rectus
A movcmcnc o f an eye considered singly is a d u ctio n —
Inferior oblique
abduction when the eye moves temporally, adduction
(From Cogin W y A N c K r v li/y t ft b r i.u lir when ic moves nasally, and corsion when ic rotates about chc
visual axis.
A com bined movcmcnc o f chc cwo eyes in chc same
direccion is a conjugate m ovem ent, or version. A version
can be in a horizoncal, a vertical, or an oblique direccion.
A conjugate rotation o f the eyes may also occur around che
visual axes— a response known as corsion or cy clo v crsion .
A m otion o f che eyes in opposite directions is a discon-
jugacc mocion, or vergence. Vcrgcnec movcmcncs, also,
o ccu r in a horizontal, vertical, or oblique direction. A dis-
conjugacc rocacion o f chc eyes around chc visual axes is
known as cyclovergcnce.
For reviews o f chc liccracurc on cvc movcmcncs see
C arpenter (1 9 8 8 ). Procedures for measuring eye m ove­
m ents were reviewed by C ollcw ijn cc al. (1 9 7 5 ), Young and
Sheena ( 1 9 7 5 ), and Eizenman ec al. (1 9 8 4 ). For a discus­
sion of chc anacomy and mode o f accion o f che cxcraocular
muscles see Buccner-Ennever (1 9 8 8 ).
10 . 1 . 2 AXIS SYSTEMS F OR EYE M O V E M E N T S
The ccnccr ot rocacion o f an eye is noc ac chc ccnccr o f chc
eye and is noc fixed with reference to the o rb it (Park and
Park 1933). In o ther words, an eye cranslaccs a licclc as ic
rotates. For m ost purposes, however, ic can be assumed chat
human eves rotacc abouc a fixed ccnccr 13.5 mm behind che
fron t surface o f che cornea. The direction o f gaze is specified
wich rcspccc со che median and cransvcrsc planes ot che
head. The straight-ahead, or p rim ary p o sitio n , o f an eye is
noc easy со define precisely, because che head and eye lack
clear landmarks. For mosc purposes, the primary posicion o f
an eye may be defined as che direccion o f gaze when the
visual axis is ac righc angles со chc plane o f chc facc. An cvc
moves from the prim ary posicion into a secon d ary p o si­
tio n when chc poinc o f fixation moves in cichcr a sagittal or
a transverse plane o f the head. A n eye moves in to a tertiary
p o sitio n when chc poinc o f fixacion moves inco an oblique
position.
The posicion or rocacion o fa n eye may be specified using
any o f four axis syscems. Th e choice is arbitrary, although

F ig u re 10 . 1 . A n ophthalm otropc m ad e by R uctc in IS S 7 ,
for a given purpose one syscem may have practical advan­
tages. For analysis o f 3 -D eye rocations in cerms o t quacer-
nions and other geom etries see Tweed ec al. (1 9 9 0 ) and
Judge (2 0 0 6 ).
Sin ce che mid 19ch cencury, mechanical gimballed
m odels, known as o p h ch alm otro p es, have been used to
visualize eye movements. Ruecces ophchalm ocrope o f 1857
is shown in Figure 10.2. For a review o t these devices see
Sim onsz and Tonkelaar (1 9 9 0 ) and Tonkelaar (1 9 9 6 ).
Schreiber and S ch or (2 0 0 7 ) recencly designed a virtual
ophchalm ocrope, which illuscraces
Liscings law.
1 0 .1 .2 a H c lm h o lcz Svstem
In che H clm holcz system, the horizontal axis o t vertical eye
movements is fixed со che skull. The vercical axis abouc
which horizoncal movemencs occur rotaces gim bal tashion
abouc che horizontal axis and does n o t retain a fixed angle
to the skull. The direction o f che visual axis is expressed in
cerms o f elevacion (/) and azimuth (m) (Figure 10.3a).
Torsion is a rocacion o f che eye abouc che visual axis with
respect to the vertical axis o t eye rotation.
1 0 .1 .2 b F ic k Svstem
4 movemencs occur abouc incermediace axes. M ore precisely,
In the Fick system, the vertical axis is assumed to be fixed to
che skull, and che direccion o f che visual axis is expressed in
cerms o f lacicude (<y) and longitude i f ) (Fick 1 8 5 4 ). Torsion
is rocacion o f an eye abouc che visual axis wich respecc со
the horizontal axis ot eye rotation. The Fick system is
the H elm holtz system turned to the side chrough 90"
(Figure 10.3b).
Elevation Latitude
Skull
(a) H elm holtz system (b) Fick system
i i4«fc io. v ,4.xis system sfor specifying eyv m ovem ents, (л) In the H elm h oltz
system the h o rizo n tal axis is fixed to the skull, and the vertical axis
rotates gim bal fash io n , (b ) In the I'ick system the vertical axis is fixed
to the skull.
1 0 .1 .2 c P e rim e te r S y stem .
{ Г с о т Т о л Ы м г с ! Л . 1996) The perim crcr syscem uses polar coordinaCes based on the
prim ary axis o f gaze— the axis straight o u t from che eye
socket and fixed to the head. Eye positions arc expressed in
terms o f che angle o f eccencricicy o fth e visual axis (/>) with
respecc со che prim ary axis, and o t che meridional dircccion
(X’) o f che plane concaining che visual and prim ary axes wich
respecc со che horizoncal meridian ot head-fixed polar axes.
These chree syscems are che same axis syscem, simply
anchored Co the head in ditierent ways (Fry et al. 1945). A
specification o f eye position can be transformed between
che three systems by the follow ing equations:
. tanfl
axis syscems and tan/l = ------- = sin K"tan a-
COS0
sin U = sin 6 cos в = sin .vcos К
1 0 .1 .2 d L is tin g 's S y stem .
Listing proposed chac any rocacion o f an eye occurs abouc
an axis in a plane known as L istin g ’s plane. H elm holtz
called chis L is tin g ’s law. Liscing’s plane is fixed wich respecc
со chc head and coincides wich chc m idfroncal.or equacorial
plane o t che eye when che eye is in ics primary posicion
(plane H D D in Figure 10.4). Elevacions and depressions o f
che eye occur abouc a horizoncal axis in Liscings plane, lat-
eral movemencs occur abouc a vercical axis, and oblique
any unidireccional movcm cnc o f an eye can be described as
occurring abouc an axis in Liscings plane chac is orchogonal
со chc plane wichin which chc visual axis moves (plane
OPB). The excenc o f an eye movemenc is che angle becween
chc inicial and final dircccions o f gaze (chc change o f chc
angle ot eccencricicy p). The direction ot an eye movemenc
is che angle bccwccn chc meridian along which chc visual

Figarc Ю.4. 'Ibe geom etry o fry e m ovem ents. 'Ih c d ire ctio n o f gaze is assum ed
to have m oved from the p rim ary p osition O B to an ob liq u e position
O P throu gh an angle o f eccen tricity along the m eridian B H . w hich is
at an angle к to the h orizon tal m eridian D B D '. T h is is equ ivalent to it
having occu rred ab ou t axis.v y in th e eq u atorial fro n ta l plane (L istin g ’s
plane). The h orizon tal m arker b etw een the sm all vertical bars in itially
m akes an angle о I w ith th e m erid ian along w hich the eye m oves.
A cco rd in g to L istin g s law, th is angle rem ains co n stan t ( o l = $ 2 ). The
eye can also be regarded as having m oved on H elm h o ltz axes, through
an angle o t elevation Я and an angle o f azim uth it. In the H elm h oltz
system , tor angle о to rem ain co n sta n t, the eye and m arker m ust
undergo torsion throu g h a n g le/ relative to the final plane o f
regard D C D '.
axis moves and a horizontal line in L istings plane ( d or ics
supplem ent k).
Torsion in the H elm holtz system is the angle (r) betw een
a horizontal marker on the eye and the plane w ithin which
the visual axis moves (.D'PD ). In Fick s system, torsion is the
com plem ent o f angle r. These tw o torsion angles are a func­
tion o f angle d and the angle o f eccentricity,/'. Any torsion
occurring when the eye is in a primary or secondary posi­
tion o f gaze has the same angular value in all axis systems.
W h en an eye moves into a tertiary position, it shows no cor-
sion in L istings axis system (assuming L istings plane
remains fixed), bu t it has a considerable degree o f torsion in
the Fick or H elm holtz systems. The H elm holtz and Fick
systems, being three-axis systems, can be used to specify tor­
sion, whereas Listing’s system was not designed lor this pur­
pose, because it is only a tw o-axis system.
Listing's law may be tested by impressing an afterimage
o f a short reference line on the eyeball in its primary posi­
tion and seeing w hether the angle betw een the afterimage
and the meridian along w hich the eve moves (angle d ,)
remains constant (see Figure 10.5). According to Listings
law, the afterimage o f a vertical line formed with the eye in
the primary position o f gaze should remain tangential to
one o f a set o f hyperbolic arcs in a frontal plane. This was
10.*. D em onstration o f Listing's law . The eye is placed at the cen ter ol
a concave hem isphere. A n afterim age o f a cross is im pressed o n th e eye
in its prim ary p o sitio n . \Xrhcn chc gaze m oves in d ifferen t d ir e c tio n s
the afterim age retain s the sam e orien tatio n wich respect to the m eridian
a lo n g w h ich th e gaze m oves. T h is ind icates th e validity o f Listing's
law . <From N o cJc* 1**0>
id.<ч A test o f L istin g s lair. (a) The afterim age o f a vertical line
im pressed on the eye in its prim ary p osition rem ains approxim ately
tangential to o n e o f a fam ily o f h yp erbolic arcs in the fro n tal plane
as the eye ch anges its angle o f gaze, ( b ) I f th e eye is n o t in its prim ary
p osition when th e afterim age is form ed , the afterim age d ocs n o t rem ain
tan g en tial to the h yp erbolic arcs cen tered o n the origin al p osition of
gaze. The angular deviations from th e h yp erbolic arcs provides a way
o l d eterm in in g how lar the eye was from th e prim ary p osition o f gaze
w hen the afterim age was im pressed on it. (R edraw n from N akayam a
1978)
found со be approximately true, as shown in Figure 10.6
(Nakayama 1978). The primary position ot gaze may be
specified as rhe cencer o f rhe ser o f hyperbolic arcs. However,
since L istin gs law is formulated with respect to the head,
the law does n o t ensure that the images o f visual lines remain
self-congruent over com bined rotations o t the eyes and
head. The law appears to be correct for conjugate eye move­
ments (Q uereau 1 9 5 4 ; Fry 1 9 6 8 ; Ferman et al. 1987a).
However, when the angle o f horizontal or vertical vergence
changes, the law does not hold, and torsion, as defined by a
change in the angle d does occur (Allen and C arter
1967).
 L istings planes for the tw o eyes were traditionally
defined as coplanar and fixed to the head. However, it is
now known rhat convergence o f rhe eyes produces an o u t­
ward rotation ot L istings plane in each eye. The two planes
swing out about the ccntcrs o f the eyes like saloon doors.
For each eye, one degree o l convergence rotates Listing’s
plane by between 0.5 and 0.9° (M ikhael et al. 1 9 9 5 ; Som ani
et al. 1 998). For a given convergence, L istings law holds for
changes in version with respect to rotated L istin gs planes.
This is the m odified L istin g ’s law. The same rotation o f
L istings plane occurs in cach eye when the eyes converge
symmetrically or asymmetrically through a given angle
(S tciicn et al. 2 0 0 0 ).
M athem atically, rotations o f a sphere about three
orthogonal axes are not com m utative. Thus, the final posi­
tion o f an eye should depend on the order in which 3 -D
movements are executed (H aslw anter 1 9 9 5 ). However, eye
movements arc alm ost com m utative when Listing’s planes
rotate outward by half the angle o l change ot gaze with
respect to the primary position (Q u aia and O ptican
1998). i io.7 Z o i K apou ta. B o m in G re ece in 1 9 5 5 . She o b tain ed a dip lom a
Bruno and Van den Berg (1 9 9 7 ) determ ined that in p h ilolo g y and psychology ас A risto tle U n iv ersity o f ’Ihessalon ika,
G rcccc* in 1 9 7 7 and a P h .D . in exp erim en tal psychology a t the
Listing’s plane in each eye is rotated outward by 2.15° when
U n iv ersity Rene D escartes in 1 9 8 2 . She con d u cted p o std o cto ral work
the eyes are fixated on a point on the horizon at optical a t D u rh am U n iv ersity ,Jo h n s H op kins H ospital» and the N ation al
infinity. Vertical gaze shifts at infinity are accom panied by a Institu tes o f H ealth . She is rcscarch d ire cto r at th e N ation al C en te r

change in cyclovcrgencc o f about 10% o f the gaze shift. The
increasing outward rotation o f Listing’s planes with increas­
ing convergence predicts the fact that the eyes becom e pro­
gressively m ore extorted during downward gaze shifts and
intorted during upward gaze shifts (Section 10.7.4).
The relationships betw een vergence, torsion, and gaze
elevation hold tor both static positions ot gaze and during
changes in gaze (M inken and van Gisbergen 1996). Also,
cyclovcrgencc induced by changing cyclodisparity ot the
images in the tw o eyes and that induced by changes in ver­
gence add linearly, w hich suggests that the two responses
are controlled by distinct systems ( H ooge and van den Berg
2 0 0 0 ). Theoretical models ot these relationships have been
developed by M ok et al. (1 9 9 2 ) and by M inken and Van
Gisbergen (1 9 9 6 ).
Kapoula cc al. (1 9 9 9 ) reported th at the tcmporalward
slant ot L istings plane during convergence is more
consistent am ong subjects for vergence evoked by disparity
than tor accom modative vergence, and is m ost pronounced
when both vergence scimuli are presenc (P ortrait
Figure 10.7).
There is also evidence chac during conjugacc saccades
che eyes undergo cransienc changes in corsion followed by a
slow torsional drill in the opposite dircccion (F.nrighc
19 8 6 a ; Ferman ec al. 1 9 8 7 a ; Scraumann ec al. 1995). For a
discussion o t eye corsion during com bined rotations ot eyes
and head see Tweed ec al. (1 9 9 8 ). Effects o f eye corsion on
the vertical horopter are discussed in Section 14.7. Listing’s
law, even in this modified form , does not hold in ocher cir­
cum stances (sec Section 10.7.4).
for Scien tific Research (C N R S . Fran ce) and d ire cto r o f the IR IS
group B in o cu lar V isio n and O cu lo m o to r A daptation a t the C N R S
L ab oratory o f Physiology o f Perception and A ctio n a t the C o lleg e de
France» Paris.
10.1.2 e The M ech an ism o f L is tin g s Law
The eyes do not obey Liscings law during sleep, showing chac
chey are not mechanically constrained со move chis way
(Cabungcal ec al. 2 0 0 2 ). However, chey obey che law when
chey move in the dark, so visual feedback is not required. This
suggests, butdocs noc prove, chat movemencs obeying Listings
law are neurally programmed (Nakayama 1975). Since
Listing’s plane is fixed to the head tor a given value o f ver­
gence, eye-movement, commands would have to be referred
со the head rather than to axes fixed to the eye. The superior
colliculus controls saccadic eye movemencs in headcencric
coord inaccs, which simplifies che coordination ot eye move­
mencs wich auditory cargecs and wich movemencs o f che arm
(van Opscal et al. 1991). However, stimulation o f cclls in the
superior colliculus o f the monkey did noc induce eye corsion.
Furchermorc, eye movemencs scill obeyed Listings law after
inaccivacion o f che superior colliculus (Hepp ec al. 1993).
Tliis evidence suggescs that L istin g s law is im plemented
downstream from che superior colliculus. Van Opscal ec al.
(1 9 9 6 ) found cclls in che nucleus recicularis tcgm cnti pontis
chac responded со 3 -D movements o f the eyes. W hen stim -
ulaced, chey produced eye movemencs wich a fixed torsional
com ponenc. This suggescs chac chis cencer is involved in
implemencing Liscings' law.
 O cher evidence suggests chat the eyes move according
to m odified L istin g s law because o f the way the extraocular
muscles are inserted on the eye. Each lateral rectus muscle
attaches to the eye at a point forward o f the equator. I f this
were the only point o f attachm ent, the point o f tangency o f
the muscle on the globe would slide upward as the eye ele­
vates. Also, contraction o f one lateral rectus would cause a
torsional m orion o f the eye.
M iller and Robins (1 9 8 7 ) showed that, near the point
o f tangency, each lateral rectus passes through a sleeve o f
connective tissue attached to the eye s orbit. This sleeve acts
as a pulley, which causes the p o in t o f tangency to remain
approximately constant as the eye elevates or depresses. The
direction o f action o f the muscle thus remains fixed with
respect to Listing’s plane. The other extraocular muscles are
probably inserted in a sim ilar way (Simons/ et al. 1985;
Raphan 1 998). The shift in the direction o f action o f the
extraocular muscles during convergence has been observed
by m agnetic resonance imaging ot human extraocular mus­
cles (D cm er et al. 2 0 0 3 ). Sim onsz (2 0 0 1 ) pointed o u t that
the pulley system had been described by Philibert Sappey,
professor o f anatomy in Paris, in 1888.
C lark et al. (2 0 0 0 ) suggested that the pulley system
may allow the noncom m utative effects o f 3 -D eye rotations
to be allowed for by com m utative neural com m ands that
are independent o f eye position However, Tweed e t al.
(1 9 9 9 ) produced evidence from vestibuloocular responses
to sequential rotations o f the body that a pulley system
can n ot replace the need for noncom m utative neural
comm ands.
The attachm ent o f rhe pulley to the o rb it contains
sm ooth muscle, which adjusts the direction o f action of the
muscle (D em er et al. 1 997). Thus, the m echanical system
could be under neural control and account for the m odifi­
cation o f L istings law when che eyes converge. The extent o f
the m odification is to som e extent under neural control
(Section 1 0 .7 .4 ). K lie rcta l. ( 2 0 0 6 ) stimulated rheabducens
nerve and nucleus downstream o f neural centers that could
control how extraocular muscles im plem ent L istin gs law.
Nevertheless, the eyes still moved according to Listing’s law,
which shows that the pulley system iscapable o f im plem ent­
ing the law.
M cC lu n g et al. (2 0 0 6 ) objected to the idea that the
pulley system has any role in the control o f eye movements.
M iller (2 0 0 7 ) provided a review o f the pulley system and a
refutation o f criticism s.
1 0 .1 .2 f C o n se q u e n c e s o f L istin g ’s law
M ovem ent o f the eyes according to L istin g s law has the fol­
lowing consequences.
1. It reduces the degrees o f freedom o f eye movements and
simplifies m otor control. However, there arc o ther ways
in which this could have been done. For example,
torsion as defined in the H elm holtz axis system could
be held constant.
2. It renders eye m ovem ents com m utative and thus
prevents a buildup o f eye torsion as the gaze moves over
a circular path.
3. It econom izes o n the am ount o f eye movement in a
change o f gaze. 1 lowever, Listing’s law in its modified
form does not fully achieve this purpose, because when
the eyes are converged they move with respect to
distinct planes. Tweed (1 9 9 7 ) con clu d cd ,on the basis
o f a com puter sim ulation, that Listing's law in its
modified form achieves the best econom y o f eye
movements com patible with m aintaining retinal
meridians in torsional alignment.
4. I Iclm holcz noted that L istin gs law has the im portant
consequence that, as the gaze travels along any line in
the visual field, the retinal image o f the line remains
self-congruent. This means that the line continues to
stimulate cortical orientation detectors tuned to the
same orientacion.
5. Van R ijn and van den Berg (1 9 9 3 ) suggested that the
modified version o f L istin gs law ensures that lines
orthogonal to the plane o f regard fall on corresponding
vertical meridians. However, Tweed (1 9 9 7 ) pointed out
that this account overlooks the fact that corresponding
vertical meridians are excyclo rota ted about 2°
(see Section 14.7).
6. L istin gs law in both its form s ensures that
corresponding horizontal meridians fall w ithin the
binocular plane o f regard. However, it does n o t ensure
that corresponding epipolar lines are aligned between
the two eyes.
The eyes o f cham eleons obey L istin gs law (Sandor c t al.
2 0 0 1 ). Their eye muscles differ from those o f primates and
they do not use disparity for judging distance. O n e must
therefore assume that the eyes o f cham eleons obey Listing’s
law so as to econom ize on the m agnitude, and hence che
speed, o f eye movements. It is not known how widespread
Listing's law is in different species o f animals.
1 0 .1 .3 S P E C IF IC A T IO N O F V E R G E N C E
EYE M O V E M E N T S
1 0 .1 .3 a T y p es o f V c r g c n c c
In h o rizo n tal vergence, each visual axis moves in a plane
containing the interocular axis. In vertical vcrgcn cc, the
visual axes move in a plane that is orthogonal to the interoc­
ular axis. In cyclovergence, the eyes move in opposite direc­
tions around the two visual axes. C om bined rotations o f the
eyes about two or three axes also occur. Table 10.1 presents
convergcncc is the convcrgencc required for binocular fixa­
tion oi an o b ject at a distance ol 1 m eter in the median
plane. The vergence angle in m eter angles is the reciprocal
o f the distance ot the fixation point in meters. The vergence
angle in degrees corresponding to a m eter angle o f M, for an
interpupillary distance a in meters, is 2 arctan a M /2. Thus,
the convergence in degrees corresponding to 1 m eter angle
varies with interpupillary distance.
In clinical practice, convergence is specified by a third
measure known as prism diopters. A 1-diopter prism dis­
places the visual axis by 1 cm at a distance o t 1 m. It follows
that the angle o f convergence in diopters is the interocular
distance in centim eters divided by the viewing distance in
meters. Thus, a person with an interocular distance o f 6.5
cm must exert 6.5 D ot convergence when fixating an o b ject
in che m idlinc at a distance o f 1 m. M easurements o f ver-
gence in either m eter angles or prism diopters are not appli­
cable at very near discances.
4

An isovergence lo cu s is che pach traced by the point ol

binocular fixation when version changes with vergence con-
scanc. For horizoncal gaze, che isovergence locus is a circle-
passing chrough chc fixacion poinc and che center o f rota­
tion o f each eye. N ote that the V ieth-M iiller circle, or theo­
retical horopcer, described in Seccion 14.5, intersects the
nodal poincs o f che eyes racher chan cheir centers o f roca­
cion. If che eyes change chcir elevation, chc isovergence locus
depends on che axis syscem used со specify eye movements.
In the H elm holtz axis syscem, che isovergence locus is a cor-
oidal surface form ed by rotation o f the isovergence circle
round the line join in g the centers ot rotation ot the two
ri*ur< io.9. C lifton Schor. B o m in 1 9 4 3 . H e o b tain ed a P h .D . in
physiological op tics w ith M erto n Flom and Law rence Stark from
the U n iv ersity o f C a lifo rn ia ac Berkeley in 1 9 7 2 . H e is professor o f
o p to m etry , vision scien ce, and b io en g in eerin g a t th e U niversity o f
C a lifo rn ia at Berkeley. R ecip ie n t o f th e G arlan d C lay Award and G len n
Fry Award from the A m erican Academ y o f O p to m etry .
Isovergence locus
Isoversion locus
H yperbola of
Hillebrand

eyes. In the Fick system, the isovergence locus is che isover­

gence circle and a vercieal line in che median plane (Schor
ec al. 1994) (Porcraic Figure 10.9). In this system, a change
in vergence is required when the gaze moves into an oblique
(tertiary) location.
The loci ot constant version tor changing vergence are
known as hyperbolas o f Hillebrand, as shown in Figure
10.10 and specified by:

—x~ + + 2 хусо$2ф= 1

where x is the distance o f the point o f convergence trom the

median plane ,у ics discancc from chc incerocular axis, and f
the angle o f version with respect to the point midway
betw een the eyes (Fry 1950) (P ortrait Figure 10.11). W ith
increasing viewing distance, che hyperbolas becom e asymp­
i o. io. L o ci ofiso v trg em c a n d h overs ion. L oci o f co n st an t v crgcncc for
ch an g in g version arc circles throu gh th e ccn tcrs o i ro tatio n o f the tw o
eyes. L o ci o f co n sta n t version for ch an g in g vcrgcncc arc hyperbolas o f
H illeb ran d . A s the gaze m oves from A to B , b oth v crgcncc and version
changc.

to tic со scraighc lines chrough che m idpoint o f the interocu­

lar axis.
M addox (1 8 9 3 ) identified che following four types o f
Reviews ot vergence have been provided by Alpern
horizontal vcrgcncc.
(1 9 6 9 ), Toaces ( 1 9 7 4 ), S ch or and C iuffreda (1 9 8 3 ),
C arpenter ( 1 9 8 8 ), C ollew ijn and F.rkelens ( 1 9 9 0 ), and
1. Tonic vcrgcncc
Judge (1 9 9 1 ). The developm ent o f vergence in che child was
discussed in Seccion 7.3.6. 2. Proximal vergence

Fi|«ri 10. 11. GUnn Fry. H e graduated in physics and psychology from
D avidson C o lleg e in 1 9 2 9 and ob tain ed his P h .D . in psychology from
D u k e U n iv ersity in 1 9 3 3 . In 1 9 3 3 he becam e assistant professor o t
applied o p tics a t O h io State U niversity, where he becam e d ire cto r o f the
o p to m e try sch ool and R egents Professor. G len n Fry died in 1 9 9 6 .
3- Accom m odative vcrgcncc
4. Fusional, or disparity-induced vergence
These types o f vergence will now be described.
1 0 .2 T O N IC VERGEN CE
10.2.1 D A R K VERGEN CE
In the dark, the eyes adopt a characteristic state o t vergence
known as dark vergence. Dark vergence is measured by
placing a person in the dark and repeatedly exposing a pair
o f nonius lines for periods o f 100 ms, which is less chan the
latency ot vergence. Betw een exposures, the nonius line in
o n e eye is adjusted until the observer reports thac ic appears
aligned with the nonius line seen just below it in the other
eye. Repeated exposure o f che lines ac one discancc may
induce a change in vergence through the m ediation o l
accom m odation cucs, and chis can atfccc chc results
(Jaschinski-K ruza 1 990). O cher m ethods tor measuring
dark vcrgcncc are described by Rosenficld (1 9 9 7 ). D ark vcr-
gence assessed by the nonius m ethod has been found to
agree closely with objective measurements obtained with a
video-based eye tracker (Jaschinski et al. 2 0 0 7 ).
It is believed that dark vcrgcncc depends on tonic
signals arising irom the vestibular system and
ocu lom otor nuclei, and proprioccptivc fccdback from the
cxtraocular musclcs. The distance o f the point o f dark ver­
gence varies between 0 .6 2 and 5 m for different observers,
with an average value o f about 1.2 m. It is consistent over
time for the same individual i f the co n d ition s o f testing are
conscanc (O w ens and Lcibow itz 1980; Fisher cc al. 1988a).
However, we will see in S ection 10.2.5 that dark vergence
can be altered temporarily by loo kin gfo r som e tim e through
base-in or base-ouc prisms.
H elm holtz (1 9 0 9 ) observed that the eyes tend to diverge
when elevated. In the dark, che eves diverge from che posi­
tion ot dark vergence when gaze is elevated and converge
from chac posicion when gaze is depressed (H euer and
O w ens 1989). A fter the eyes have been held in an elevated
or depressed posture for a few m inutes, the position o f dark
vergence with horizontal gaze is temporarily biased toward
chc previously m aintained scace (H euer cc al. 1988).
In the dark, the eyes also take up a characteristic state of
accom m odation known as conic accom m odacion, or dark
focus (Section 9 .3 ). Dark focus and dark vergence do not
correspond со chc same discancc (O w ens and Lcibow itz
1980).
In deep sleep, anesthesia, or death chc eyes assume a pos­
ture known as the anatomic position o f rest. This repre­
sents the scacc o f chc musclcs when chev lack con ic innervation
(Alpern 1 9 6 9 ). The anatom ic position o f rest is more diver­
gent than dark vcrgcncc, although there is no agreed value
for this position (see Ow ens and Lcibow itz 1983).
10.2.2 S T R A B IS M U S
10 .2 .2 a Types o f Strabism us
A person who cannot converge the visual axes on a selected
o b ject is said to have a squint. The technical term is strabis­
mus or tropia. Properly aligned eyes arc said to be o r th o ­
tropic (P rieto-D iaz 2 0 0 0 ).
The angle o f deviation from the orthotrop ic scace is
measured by observing the direction o f gaze ot the deviat­
ing eye as the patient fixates on a point with the nondeviat­
ing eye. The direction o f gaze is measured by m oving a point
o f light round a perim eter until its reflected image is cen ­
tered on the cornea. The angle ot deviation can be measured
with the fixation target near or far.
There are many types ot strabismus. In divergent strabis­
mus, or exotropia, the visual axes arc directed outward
from the intended point. W h en the angle of deviation is the
same for near as for far viewing, ic is a basic cxocropia. W hen
che exotropia is com bined wich convergence insufficiency
the angle o f exotropia is larger w ith near than with tar view­
ing. W hen com bined wich divergence excess ic is larger
with tar than with near viewing. In convergent strabismus,
or esotropia, the visual axes are directed inward. Esocropia
is about three times m ore frequent than exotropia. In verti­
the cal strabismus che visual axes do noc lie in che same horizon*
cal plane.
 In u n ilateral strab ism u s one eye is consistently used
for fixation when both eyes are open. This type o f strabis­
mus is often accom panied by some loss o f visual function
in the deviating eye, a con d ition known as amblyopia
(Section 8 .4 ).
In a ltern a tin g strab ism u s the person sometimes fixates
objects with one eye and som etim es with the other. In the
deviating eye o f an alternating exotrope rhe temporal h a lfo f
the retinal image is suppressed. Thus, when viewing stereo­
grams, an exotrope sees only the h a lf image in the nondevi­
ating eye (Jam polsky 19 5 5 ; Pratt-Johnson and W ee 1969).
W h en looking at an o b ject to the left, alternating exotropes
use the left eye for fixation. W h en looking at an o b ject to
the right, they use rhe right eye. Steinbach (1 9 8 1 ) found
that the switch in suppression from one eye to the other
occurs during the course o f a large saccade. Van Leeuwen
et al. (2 0 0 1 ) measured the dynam ics o f horizontal saccadic
eye movements o f various am plitudes in alternating
strabismics.
A lternating strabismus occurs in only about one-third
o f esotropes but in about 8 0 % o f exotropes. Am blyopia is
associated with unilateral strabismus rather than with alter­
nating strabismus. This explains why amblyopia develops
more frequently in esotropes than in exotropes (Friedman
e ta l. 1 980).
Patients with in te rm itte n t ex o tro p ia arc able to co n ­
trol the deviation o f the eye when making an effort to fuse
the images o f an object.
In co n c o m ita n t strab ism u s the deviation is the
same for all directions o f gaze, although it may vary accord­
ing to the angle o f convergence and from day ro day.
C o n co m ita n t strabismus is due to a defect ot the vergence
m echanism rather than ro a defect o fextraocu lar muscles. It
is som etim es reduced when retractive errors are corrected
optically.
In n o n co n co m ita n t strabism u s the deviation varies
with the angle o f gaze. It is due to a paresis in one or more o f
the cxtraocular muscles arising trom damage to muscle or to
o cu lo m oto r nerves. N o n con co m itan t strabismus is also
known as paralytic strabismus. N onconcom itant strabis­
mus is particularly evident when patients attem pt to move
the eyes in the direction o f action o f the paretic muscles.
In larg c-an g le strab ism u s the angle o f deviation is
larger than 15 D ; otherw ise it is sm all-an g le strabism us.
Deviation o fo n e e y e o fu p t o 8 I) has been called m icro stra ­
bism us, or m icrotropia. This condition is discussed in
Section 10.2.4f.
In small-angle strabismus, the visual system may m ani­
fest an om alo u s retin al co rre sp o n d en ce (A R C ),d efin e d as
a shift in corresponding regions in the two retinas. The
angular extent ot anom alous correspondence is the angle o f
anom aly, or angle A. In harm onious anom alous correspon­
dence, angle A equals the angle o f strabismus, and there is
no m ovem ent o f the deviating eye when the nondeviating
eye is covered (the cover test). In inharm onious anomalous
correspondence, angle A is less than the angle o f strabismus.
Anom alous correspondence is discussed in Section 14.4.1.
A bout 5% o f people have some strabism ic anomaly o f 5
D or more. In over 3 0 0 0 strabism ic patients, 74 % had co n ­
com itan t strabismus, 10% were paretic, 8% had decom pen­
sated heterophoria, and 6% had convergence insufficiency
(Stidw ill 1 9 9 7 ). A bout 65 % o f cases o f strabismus develop
before the age o f three years, with a mean age o f onset o f
about 3 0 m onths (G raham 1974; Stidwill 1997).
1 0 .2 .2 b V isu a l D e fe c ts in S tra b ism u s
Strabism us that develops before the age o f 1 year is known
as early -o n set strabism u s. W ith this type o f strabismus
the deviating eye sutfcrs from am bly o p ia, which involves a
loss in acuity and other visual functions, as described in
Section 8.4.2.
In strabismus, images falling on corresponding retinal
points are usually dissimilar and therefore engage in rivalry.
A lso, images from a given o b ject fall on noncorresponding
points and create diplopia. Strabism ics o f long standing
avoid both these disturbing effects by totally suppressing
the image in the strabismic eye when both eyes are open.
C linical su pp ression can be studied in strabismic monkeys
(W ensveen e t al. 2 0 0 1 ).
Stereoscopic vision is degraded o r totally absent in
large-angle strabismus o f early onset. It is rare to find any
evidence o f stereopsis in subjects with an angle o f deviation
larger than 4 prism diopters (Parks 1 9 6 9 ; Leske and Holm es
2 0 0 4 ). Binocular vision may be restored when strabismus o f
late onset is corrected. Som e patients with early-onset
esotropia cannot fuse similar images even when the strabis­
mus iscorrected with prisms. They report that, as rhe images
approach each other, they jump over each o ther to produce
the opposite sign o f diplopia. This condition is known as
h o rro r fusionis.
Small-angle strabismus (m icrotropia) docs not present a
cosm etic problem , and there is often some residual stereop­
sis with tests such as the H ow ard-D olm an test and T itm u s
test. The less the deviation the greater the probability o f
som e stereopsis (C oo p er and Feldman 1979; R utstein and
Eskridge 1 9 8 4 ). There has been some dispute about whether
small-angle strabism ics show evidence o f stereopsis when
tested with random -dot stereograms (H enson and W illiam s
1 9 8 0 ; C o op er and Feldman 1981).
1 0 .2 .2 c D ir e c tio n a l P re p o n d e ra n c e and
L a te n t N y stag m u s
Early-onset strabismus is usually associated with reduced
gain ot pursuit eye movements in the tem poral direction
and directional preponderance o f optokinetic nystagmus
(O K N ) for stimuli m oving in the nasal direction with m on­
ocular viewing. Sensitivity ro visual m otion is symmetrical
in strabismic amblyopes so that their asymmetrical O K N
can n ot be due to a defect in m otion sensitivity (S ch o r and
Levi 1 9 8 0 ). A lso, eye rotations in the dark are norm al, so
the defect is not due to muscle im balance. The defect is
m ost likely due to the incom plete developm ent o f binocu­
lar vision in strabismics, which releases the temporonasal
preponderance o f subcortical centers from the counter­
balancing influence o f cortical inputs, as described in
Section 2 2 .6 .1 .
Strabism us of early onset is also accom panied by laten t
nystagm us, w hich occurs when one eye is closed, and som e­
times when both eyes are open (D elFO sso et al. 1 9 8 3 ). In its
simplest form , latent nystagmus is a spontaneous conjugate
jerk nystagmus, which occurs only when one eye is closed.
In strabism ic amblyopia, latent nystagmus is larger when
the affected eye is open than when the normal eye is open.
Th e slow phase o f the latent nystagmus is in the tem porona­
sal direction, so that the direction o f the nystagmus changes
as a cover is moved from one eve to the other. In mosc cases
4
latent nystagmus is also evoked wich the quick phase in the
direction o f gaze when both eyes are open, or in the direc­
tion o f che fixating eye when che ocher eye is open buc in a
deviated position due to strabismus.
Patients wich alternating strabismus can control the
direction o f latent nystagmus by changing the eye used for
fixacion. Som e pacicncs who cannoc control the direction o f
the nystagmus when both eyes are open may do so in the
dark by im agining that they are looking with one eye or the
o ther (D eirO sso et al. 19 7 9 ; Kom m erell and M chdorn
1982). Laten t nystagmus can be regarded as a spontaneous
manifestation o f the tem poronasal preponderance charac­
teristic o f congenital strabismus. D irectional preponder­
ance and latent nystagmus also occur in strabism ic monkeys
(Tychsen and B o o th e 1996).
Poor vergence control and fixation instability have been
implicated in dyslexia (sec Buzzelli 1 9 9 1 ). However, rhe
evidence is equivocal (Evans et al. 1 9 9 4 ). M oores et al.
(1 9 9 8 ) could find no relationship betw een dyslexia and the
ability to control vergence.
10.2.2d E tiology of Strabism us
The etiology o f scrabismus is unclear. A bouc I % o f che p op­
ulation has congenital infantile esotropia, which may noc
be evident at birch buc becom es decectable during che firsc
six m onths (N ixon et al. 1 9 8 5 ). There is evidence o f a
genetic factor (Schlossm an and Priestley 1 9 5 2 ; Graham
1 9 7 4 ). The degree and frequency o f strabismic deviation
tends to increase wich age (Y ildirim ec al. 1999).
Strabism us o f early onset may be associated with an
uncorrected refractive error o f over + 3 I) thar requires the
patient to accom m odate excessively for near vision. This
evokes excessive convergence through che m ediation o f
accom m odative convergence. The esotropia usually begins
as an incermicccnc crossing o f che eyes and progresses со a
conscanc deviation. Ic has been proposed chac a basic cause
o f scrabismus is a defecc in che disparicy feedback m echa­
nism controlling vergence (see Kerr 1 9 9 8 ). Early m onocu ­
lar occlusion in cats leads со misalignmenc o f che occluded
eye, which becom es a perm anent strabismus when boch
eyes are allowed со see (Q u ick ec al. 1 9 8 9 ). Strabismus often
accompanies congenital cataracts. M ore inform ation on
strabismus is provided in Lennerstrand cc al. (1 9 8 8 ) and
N oordcn and C am pos (2 0 0 0 ).
1 0 .2 .2 e T re a tm e n t o f Strabism us
Early correction for hypermecropia may rescore binocular
fixation and stereopsis in accom m odative esotropia (W ilson
ec al. 1993). Patients wich incermicccnc exocropia, unlike
chose wich ocher forms o f large-angle scrabismus, cend со
retain scereopsis.
Ic has been claim ed chac paciencs wich microcropia can
achieve normal recinal correspondence and improved acuicy
and scereoacuicy chrough periodic occlusion o f che good
eye and refraccive correction (C leary ec al. 1998; Houscon
ec al. 1998).
Ic has also been claim ed chac scrabismus may be cured by
wearing prisms for a period ot up со 6 monchs. This mechod
was used widely in che nineceench cencury, especially in
Europe. However, Alpern and Hofsceccer (1 9 4 8 ) reporced
thacconscanc wearing o f prisms increases chc angle o f squ inc.
A lthough some clinicians still advocate che use o f prisms,
debace abouc cheir effectiveness continues (see Noorden
and C am pos 2 0 0 0 ).
Estim ates o f che success o f cherapy for scrabismus in
restoring some binocular vision have varied from 5% or less
(Flom 1963; D obson and Sebris 1 9 8 9 ) to over 50 % (W ic k
and C o o k 1987).
Large-angle con com itan t strabismus and noncon-
com irant scrabismus o f muscular origin may be partially
or complecely correcced by surgically adjuscing che excraoc-
ular muscles or by injection o f a neurocoxin inco selecced
muscles (Scocc 1 9 8 1 ). However, only a small proportion
o f patients wich early-onsec large-angle scrabismus develop
scereopsis, even when che surgery is performed before 2
years o f age (Pracc-Johnson and T il Ison 1983) (Seccion
8.3.3a).
C orrective surgery can lead со the onscc o f amblyopia in
paciencs who were noc am blyopic before surgery (Pracc-
Johnson and Tillson 1983). In mosc cases, poscsurgical
exercises reduce che severicy o f am blyopia (Murray and
Calcucc 1 9 9 0 ). Success races, as reflecced in rescoracion o f
binocular vision, are higher when surgery is performed
before che age o f 2 4 monchs (Keenan and W illshaw 1992).
For such paciencs, rescoracion o f som e scereopsis depends
more on che duration ot rhe scrabismus chan on che age ac
which correccive surgery was performed (B irch ec al. 2 0 0 0 a ).
Surgical corrcction applied even in older children reduces
che poscsaccadic drift evidenc before surgery (Inchingolo
ec al. 1996).
 Strabism us o f late onset is not associated with am blyo­
pia. In m ost cases, corrective surgery can be expected to
restore binocular vision and at least som e stereopsis. The
degree to which stereopsis is restored in late-onset strabis­
mus depends on the visual capacity o f the patient before
surgery and on the extent to which surgery has brought the
eyes into correct alignm ent (Faw cett c t al. 2 0 0 4 ).
There has been some debate about whether restoration o f
stereopsis in strabismus o f late onset becomes less probable as
surgical treatment is delayed. A recent study o f 25 patients
with acute-onset esotropia with mean onset age o f 12 years
indicated that the restoration o f stereopsis did not depend on
the period o f delay before surgery {O htsuki et al. 1994). A
patient may nor be sure when a strabismus developed. Certain
visual defects associated with earlv-onset but not late-onset
esotropia, such as asymmetry o f visual pursuit and dissociated
vertical deviation (D V D ), may indicate whether a strabismus
is o f early or late onset (D em er and Noorden 1988, Schor
et al. 1997). Corrective treatments have a cosmetic value even
if amblyopia is noc cured or binocular vision restored.
10.2.3 PH OKI A
10 .2 .3 a Types o f P h oria
P h oria is a latent strabismus revealed only when che eyes
are d isassociated , chat is, when no fusible scimuli are in
view. I с may be regarded as rhe open-loop vergence error.
O rth o p h o ria is che con d ition o f zero phoria. The eyes can
be disassociated by closing o r covering one eye, by displac­
ing one image wich a vercical prism so thac che images in the
cwo eyes no longer coincide, or by presenting overlapping
buc rivalrous dichopcic scimuli. A horizoncal phoria may be
an inward deviation o f an eye (eso p h o ria) or an outward
deviation o f an eye (cxo p h o ria).
H orizontal phoria is conventionally measured while
one eye is accom m odated on a distant o b ject, because it is
believed that effects o f accom m odation on vergence are
lease wich far accom m odation.
In vertical p h o ria one eye deviates vertically when one
eye is closed. A deviation o f the left eye upward or down­
ward is a left hyp erp h oria or left h y p o p h oria, respectively.
Sim ilar deviations o f the right eye are eicher a righc hyper­
phoria o r a right hypophoria respectively.
A torsional deviation o f an eye is a cy clo p h o ria:
top-inward is an incyclophoria and top-outw ard, an
excyclophoria.
It takes about 2 0 seconds for an eye to com e to rest in its
posicion o f phoria after che eye has been covered (Sch or
1979a). W hen the m agnitude o f phoria varies with che
eccentricity ot gaze, it is known a san iso p h o ria ( Friedenwald
1936). An essential anisophoria is due to paresis o f one or
ocher extraocular muscle in one eye, and optical anisopho­
ria is due to optical m agnification o f che image in one eye by
a spectacle lens.
A horizontal phoria o f up to 4 prism diopters (abouc 2°)
is considered norm al. A small degree o f cxophoria is nor­
mally presenc and is referred to as p h ysiological cxop h o ria.
It increases with age, especially with near vision (Freier and
Pickwcll 1 9 8 3 ). A phoria is called com pensated when not
accom panied by other symptoms. It is uncompensated
when accom panied by symptoms such as headache, eve
strain, blurred vision, or problems with stereopsis. These
secondary symptoms bear no simple relationship to the size
o f chc phoria (Evans 1997).
The sign o f phoria can vary with fixation distance.
Phoria measured w ith discanc cargets is know n as d istan ce
p h o ria. An esophoria that is greater tor far than tor near
viewing is a d ivergence w eakness, and an esophoria chat is
greater for near viewing is a co n v erg en ce excess. An cx o ­
phoria thac is greater for near viewing is a convergence
w eakness, and an exophoria that is greater tor tar viewing is
a divergence excess (see Section 10.4 .3 b ).
The tonic state o t vergence, and hence the direction and
magnitude o f a phoria, can be changed tem porarily by hold­
ing the eyes in an extreme position o f divergence or conver­
gence (Section 10.2.5).
Subjects with norm al vision exposed to 2 4 hours o f
m onocular occlusion showed increased esophoria, espe­
cially for near vision. N orm al phoria returned after one day
o f binocular vision (Bross 1984). An eye occluded for sonic
tim e also developed vertical phoria (Charnw ood 1 9 5 1 ) and
excyclophoria (G r a f et al. 2 0 0 2 ). M onkeys, after one week
of m onocular occlusion, showed decreased saccadic am pli­
tude in che occluded eye (V iirre ec al. 1987).
1 0 .2 .3 b M easu res o f P h o ria
Phoria may be measured objectively by the co ver test. In a
simple qualitative version o f chis ccsc che pacienc fixaces a
spoc, and the clinician observes the change in position ot
each eye as a cover is placed in fron t o f ic. To quantify a
phoria, the clinician increases the power o f a prism placed
before the deviating eye until a change in posicion o f chat
eye is no longer observed when the eye is alternately cov­
ered and uncovered. The power o f the prism indicates che
degree ot phoria in prism diopters, and the orientation o f
the prism indicates the direction o f phoria. This m ethod is
limited by the smallest deviation o f an eye that a clinician
can d etect w hich, on average, is abouc 2 prism diopcers
(R om an o and N oorden 1971).
W h en greaccr precision is required, eye posicion is m ea­
sured objectively. In che clin ic, the rotation o f an eye is m ea­
sured by che displacem ent, with respect to the center o f the
pupil, o f a light spot reflecced o ff rhe cornea. A prism can be
used to bring the light spot in the deviating eye into che
same position relative ro the pupil as the light spot in the
undeviating eye. The setting o f che prism indicates the m ag­
nitude o f deviation (Krim sky 1972). W h en measurements
are made from photographs, the estim ated ocular rotation
per m illim eter o f light displacem ent is known as the
• 18
H irsch b e rg ratio. This m ethod has been used with chil­
♦16
dren (H asebe ec al. 1 9 9 8 ) and m onkeys (Q u jck and B oothe
♦44
1989).
♦ 12
In so-called subjective tests for tropia and phoria, the *1 0
patient aligns visual targets. Given that the patient is able to 2шш2шшАл л а • '• • и J . 0 , ! , 6 4 2 0 1 3 5 7 9 11 13 15

make the judgm ents, subjective m ethods are at least as pre­

cise as objective m ethods. h
*4
The first subjective procedure is known as the altern ate
*2
cover test. The exam iner alternately covers each eye o fth e *0
1
patient, who reports the direction o f apparent movement o f
3
a test o b ject. In exophoria the o b ject appears to move with
5
the occluder, and in esophoria it appears to move against
7
che occluder. The prism power required со null che m otion
9
indicates the m agnitude o f phoria.
In a second type o f subjective procedure a single target Fifwc 10. 12. A tan gen t scale used in th e M addox K ing test. T h e display is placed
is introduced to both eyes in such a way chac che images are in a stcrco sco p e, o n e cvc view ing th e arrow s and the o th e r eye chc scales.
d isassociated and the fusional response is disengaged. For T h e su b ject in d icates w h ich num bered d o ts are aligned w ith the arrow s.

instance, in the M ad d ox-rod test the patient views a point

o f lighc directly with one eye while the other eye views the
same point through a set o f high-power cylindrical prisms
arranged as a gracing. D epending on cheir oriencacion, che
prisms spread che point o f light into eicher a horizoncal or a
vercical line. The power o f a wedge prism required со bring
the poinc and line back inco superimposicion for che pacienc
indicaces che degree o f phoria— horizontal phoria when the
line is vertical and vertical phoria when it is horizontal.
In the H ess-L a n ca ster test che patient moves a red spot
seen by one eye on a screen until it appears superimposed
on a green spot seen by the other eye. The color separation
is achieved with red and green filters. This is repeated for
several angles o f gaze to determ ine whether the tropia or
phoria is co n com itan t or nonconcom icant.
In the third type o f subjective measure o f tropia or
phoria, disassociated dichoptic stim uli are presenced in a
scereoscope so chac che fusional response is disengaged. The in to alignm ent. There is also a co n tro l for varying the verti­
M addox w ing test is essentially a Brewster stereoscope in cal posicion o f cach target. In chc clinic, haploscopcs arc-
which one eye sees calibrated horizoncal and vertical scales known as amblyoscopes, synopcophorcs, or croposcopes,
in the form o f a cross and the ocher eve sees a vertical and a
4
depending on the manufacturer.
horizontal arrow. The pacienc reads oft che posicion ot each Schroeder ec al. (1 9 9 6 ) found som e cescs o f phoria cor-
arrow on chc appropriace scale со indicace horizoncal and rclaccd highly, ochcrs less so. D ifferences becween cescs arc
vercical phoria (Figure 10 .1 2 ). C yclophoria requires an probably due to differences in che degree o f control o f
annular scale. There muse be nochingelse in view that could accom m odativc convergence and vergence adaptation.
lock vergence. Such a device is known as a p h o ro m eter. For a review o f o rth o p tic procedures used in the diag­
O th er stereoscopic devices used in o rth o p tic practice to nosis and treatm ent o f anom alies o f binocular eye move­
measure and treat tropia and phoria are derived trom m ents see Evans (1 9 9 7 ), Goss ( 1 9 9 5 ), and Griffin and
H erings haploscope. The essential features are shown in Grisham (1 9 9 5 ).
Figure 10.13. The subject s head is fixed so that the center ol
rotation o f each eve is above the center o f rotation o f one o f
4
10 .2 .3 c R elation betw een D a rk Vergence
the horizoncal arms o f the inscrumenc. The visual cargecs are
and Phoria
m ounted on the ends o f the arms and reflected into the eyes
by m irrors set a t 4 5 ° to rhe median plane. The accom m oda­ If phoria represents che conic scace o f an eye when relieved
tive distance ot each target is adjusted by moving it along from fusional demand it should be che same as dark ver­
the arm. H orizontal phoria is indicated by the angular gence. W c will see in rhe ncxc seccion chac, wich dissociaccd
position ot the arm required to bring disassociated targets cargecs, che accommodacive scace o f the eyes can evoke a

f .* hm id it. Jo h n Sr»»>:l/>u\ B orn in C h ic a g o , in 1 9 4 2 . H e ob tain ed a
B S E E degree from tlic U n iv ersity o l Illinois in C h am p aign in 1 9 6 4 and
a P h .D . in b ioen g in eerin g at the U niversity o f Illin ois M ed ical C en te r
in C h ica g o in 1 9 7 0 . H e has held faculty p osition s at th e U niversity
o f C a lifo rn ia , Berkeley and the U n iv ersity o f Illin o is, C h ica g o . He
cu rren tly h old s a jo in t p osition as professor o f surgery at the R ob ert
W ood Jo h n so n M cd ical S ch o o l and professor o f biom ed ical
en gin eerin g a t R utgers U niversity.
3. W e will see in chc nexc seccion chac associated phoria
may be reduced under che condicions o f forced
vergence used со measure ic (sec Schor and
Narayan 1982).
Since phoria is related to the position o fd a rk vergence
(to n ic balance), one would also expect fixation disparity to
be related со dark vergence. In con form ity wich chis expec-
cacion ic has been reporced chac, as vergence deviates from
chc posicion o f conic balance, fixacion disparity increases in
the direction o l tonic balance (O w ens and Leibow itz 1983;
Jaschinski-K ruza 1 994). In general, when a person co n ­
verges or diverges outside the position o f tonic balance, the
eyes are pulled back toward it w ithin the limits o f Panums
fusional area, although fixation disparity is not necessarily
zero at the position o f dark vergence. Also, fixation dispar­
ity is more stable for a target at the position of dark ver­
gence (Jaschinski 1 997). Linear modeling suggests that the
rate ot increase of fixation disparity with increasing distance
from the position o f dark vergence is proportional to the
open-loop gain o f vergence (H ung G K 1992a). At near
viewing distances, the position o f dark focus has a small
effect on fixation disparity (Jaschinski 2 0 0 1 b ). There is evi­
dence that subjects select a viewing distance for a near-
vision task that m inim izes fixation disparity (Jaschinski
1998).
1 0 .2 .4 f T h e M o n o fix a tio n S y n d ro m e
Som e people have a perm anent fixation disparity o f up to 8
prism diopters, which is well beyond the normal range o f 8
arcm in, but not evident to casual inspection. Jampolsky
(1 9 5 6 ) used the term “sm all-an g le e so tro p ia ” and later
“fusion d isp arity ” (Jam polsky 1962). Helveston and
N oorden (1 9 6 7 ) used the term "m icro tro p ia ” and sug­
gested that the condition arises because fixation is estab­
lished at the border o f a foveal scotom a in one eye. Parks
(1 9 6 9 ), also, claim ed that a foveal scotom a is the com m on
factor in this type o f fixation disparity. H e used the term
“m o n o fixatio n sy n d rom e” for the inability to bifixatc
because o f a central scotom a in the deviating eye, associated
with normal fusional vergence, retention o f peripheral
fusion, and gross stereopsis. Patients show norm al periph­
eral fusion, as evidenced by visual testing and by binocular
visually evoked potentials (Struck et al. 1 9 9 6 ). Variable fea­
tures o f the m onofixation syndrome include a history o f
large-angle strabismus, anisom etropia, amblyopia, and
phoria. The eves arc cosm etically straight and the condition
does not respond to treatm ent.
1 0 .2 .4 g F ix atio n D isparity and P an u m s
Fusional Area
Under normal viewing conditions, fixation disparity does
n o t extend as tar as the radius ot Panum s fusional area
(Duw aer and van den Brink 1981a). W hen the magnitude
o f fixation disparity is increased by forced convergence or
divergence, the maximum fixation disparicy before diplopia
is seen corresponds со che radius of Panum s fusional area.
Panum s fusional area is enlarged when high spacial fre­
quencies are removed from che scimulus by opcical blurring
(Seccion 12.1.2). Normally, fixacion disparicy also increases
(H ebbard 1964). However, people wich а Пас forced-
vergence curve, signifying a very adaptable scacc o f conic
vergence, do noc show chis dependency o t fixation disparity
on Panum s fusional area (Sch o r et al. 1986a).
Panum s fusional area also increases with eccentricity.
O gle et al. (1 9 6 7 ) found that fixation disparity did not
increase while a square, serving as the fused stimulus,
becam e larger so that its edges becam e more eccentric in the
visual field. O th er investigators have reported that fixation
disparity does increase with increasing eccentricity o f the
fusional stimulus (C arter 1 9 6 4 ; Francis and Ow ens 1983).
The answer to this apparent con flict seems to be that some
people show a dependence on eccentricity and som e do not.
Thus, tor people with an adaptable state o t to n ic vergence,
fixacion disparicy and che forced-vergence funccion are
independenc o f che ecccncricicy o t che fusional scimulus
(Saladin and Carr 1 9 8 3 ; Sch or ec al. 1986a).
The cocal range ot crossed and uncrossed disparicics over
w hich depch is seen in a random -doc stereogram has been
found to decrease trom about 2 3 arcm in tor subjects with
no associated phoria (fixation disparity measured by prism
cancellation) to about 11.5 arcm in for subjects with 4 D o f
phoria (Jim en ez et al. 2 0 0 0 ).
1 0 .2 .4 h Sum m ary
Fixation disparity is a deviation ot one ot the visual axes
from the intended point o f convergence, w hich is too small
to cause diplopia. Fixation disparity is measured by the
offset o f spatially separated dichoptic targets in the pres­
ence o f fusible stim uli. The effect has been attributed to
m onocular fixation error, tonic im balance, leaky integra­
tion o f the velocity signal, asymmetry o f signals for conver­
gence and divergence, and foveal scotom ata. The correlation
between fixation disparity and phoria varies with viewing
distance and with the position o f dark vergence. Fixation
disparity, like Panum s tusional area, increases as the spatial-
frequency co n ten t o f the stimulus is reduced. Also, in some
subjects, fixation disparity, like Panum s tusional area,
increases with increasing stimulus eccentricity.
For detailed reviews o f fixation disparity, see O gle et al.
(1 9 6 7 ), Sch or (1 9 8 3 a ), and Sethi (1 9 8 6 a ).
1 0 .2 .5 T O N I C V IIR G EN С E A D A P T A T I О N
T O P R IS M S
It has been known since the rime o f M addox (1 8 9 3 ) that
viewing the world through base-in or base-out prisms, even
for a few m inutes, leads to a shift o f tonic vergence in rhe
direction o f the induced vergence (Rosenfield 1997). The
shift is revealed by rhe position o f dark vergence, by phoria,
or by fixation disparity while viewing through prisms or
after the prisms have been removed (AJpern 19-16). The
effect decays exponentially after the prisms have been
removed. The effect can last hours but it decays more rap­
idly when norm al binocular vision is allowed (Ludvigh
et al. 196‘i) . Vergence adaptation has also been dem on­
strated in the monkey (M orley et al. 1 9 8 8 ). Dynam ic ver-
gence adaptation to disturbed visual feedback is discussed
in Section 10.8.3.
10 .2 .5 a F o rc cd V c rg cn cc C u rv es
W hen base-out prisms are placed before the eyes, as in
Figure 10.15, more convergence is required to fixate a given
object. Base-in prisms decrease vergence demand. The tunc­
tion relating fixation disparity on th e у-axis to vergence demand
(prism power) on the л-axis is rhe forced-vergence curve
(Ogle 1964, pp 6 9 - 9 3 ; O gle et al. 1967). The ^in tercep t indi­
cates fixation disparity in the absence o f prisms and the
л-intercept indicates the prism power required to reduce
fixation disparity to zero.
People vary widely in the torm o f the forced-vergence
curve. O gle described the four basic types o f curve shown in
Figure 10.16. Type I is sigmoid, showing an accelerating
A
Figure io. i>. 1b e effect o f base-ou t prism s on vergence. B ase-o u t prism s cau sc an
o b jc c t ac p o sitio n A to appear nearer a t position В and increase required
con vergen ce. Base-in prism s have an o p p o site effect.
fixation disparity as prism power is increased from zero, one­
way or the other. Type II shows an accelerating change o f
fixation disparity to decreased vergence demand induced by
base-in prisms, but no change to increased vergence demand
induced by base-out prisms. Туре III shows changes in
response to increased vergence dem and,but not to decreased
demand. Type IV shows little change to cither increased or
decreased vergence demand. People showing this type o f
curve have a flat forced-vergence curve and arc said to “cat
the prism” (O gle and Prangen 1953; Sch or 1979b ). For
such people it is pointless to use prisms o f fixed power tor
the correction o f fixation disparity or phoria. This may
explain why prismatic correction o f fixation disparity has
little or no effect on stereoacuity (R u tstcin 1 9 7 7 ). The state
o f tonic vergence is said to adapt to the vergence demand in
those parts o f a forced-vcrgcncc curve that do n o t change
with changed demand. For all types o f forced vergence
curve the images no longer fuse beyond a certain prism
power.
The forced vcrgcncc curve may vary with ccccn tricity o f
the fusion targets. O gle (1 9 5 0 ) used an array o f letters sur­
rounding a central 1.5° black area containing nonius lines.
There were no fusion targets w ithin 45 arcm in o f the fovea.
H e found that 8 5 % o f subjects showed type I forced-
vergence curves, 10% showed type II curves, and even fewer
subjects showed types II and IV curves. Rutstcin (1 9 7 7 )
used a sim ilar display but w ith a central black area o f only
0.5°. M ost subjects showed type II curvcs, in w hich fixation
disparity adapts to base-in prisms. O thers have also found
that vergence adapts more com pletely when the fusion
stimulus is near the center o f the visual field rather than in
the periphery (C arter 1 9 6 5 ; M cC orm ack c t al. 1991;
M cC orm ack and Fisher 1996).
Forced-vergence curves may also be obtained by expos­
ing subjects to vertical prisms (Eskridge and Rutstcin 1986;
 T yp e I. Increasing fixation disparity as prism
pow er increases either w ay from zero.
Type III. C hanges to increased verg en ce dem and
b u t n ot to decreased dem and.
h.Rurc io. 16. B asic type! offorced-vergen cetu rvet. (.\d»ptcJ from o*lc о J. W )
I.uu cc al. 2 0 0 0 ). For example, Paccl and Firth (2 0 0 3 ) used
M addox rods to measure vertical phoria induced by prior
1 -minuce exposure to a vertical prism o f 2 D before one eye.
This induced a phoria o f 0 .5 5 L) after the prism was removed,
which decayed exponentially. W ith repeated exposures to
rhe prism at 5-m inute intervals the magnitude o f induced
phoria declined.
Haase (1 9 8 0 ) proposed that the reem ergence o f phoria
during prism correction is due to the fact that the full extent
o f phoria is n o t revealed in the initial test. 'I here is a degree
o f latent phoria that is revealed only after the initial phoria
ha.s been relieved. Prism power must be increased several
times at intervals o f several m onths before the full phoria is
revealed. It has been claimed thac hctcrophoria and hcc-
erotropia treated in this way show perm anent correction
after a 5-year follow-up, alchough che prisms muse be co n tin ­
ued со be worn to prevent relapse (Lie and O pheim 1990).
A daptation o f the vergence system to increased vergence
demand has been reported up со 3 prism diopcers vertically
Type II. Increasing fixation d ispanty to decreased
verg en ce dem and. No change to increased dem and.
Type IV. Little change to eithe r increased o r
d ecreased verg en ce dem and.
and 10 diopcers horizoncally (Career 1963, 1 9 6 5 ; Henson
and Norch 1980). 'Ih e form o f che forced-vergence curve
remained reasonably conscanc over monchs and years
(M itch ell and Ellerbrock 1 9 5 5 ; C o o p er ec al. 1981)
although, for som e subjeccs, che funccion showed some dis-
placemenc (D aum 1983).
Fixacion disparicy and phoria can begin со change
wichin che firsc minuce o f exposure со base-ouc or base-in
prisms (Sch or 19 7 9 a , 19 7 9 b ). As exposure cime is increased,
vergence adapcacion becom es more com plece and cakes
longer to recurn со ics prcadapccd scace after che prisms are
removed (M itch ell and Ellerbrock 1955; Brautasct and
Jennings 2 0 0 5 ). Even after phoria has returned со ics pre-
adapccd scace, che effecc o f a prolonged period o f forced ver­
gence is scill evidenc in che rate o f readapcacion to prisms
(Norch ec al. 1986). O n e muse allow adcquacc ineervals
becween cescs o f phoria со avoid aftereffect.
Seth i (1 9 8 6 b ) reported chac nacurally occurring phorias
decay during 4 hours o f m onocular viewing, and thac che
rate o f this decay is correlated wich the rate o f adapcacion со
increased vergence dem and. She concluded chac phoria rep-
resencs che nacural adapted state o f che vergence syscem.
The magnicude o f vergence adapcacion declines wich
increasing age (W in n ec al. 1994).
People adapt to large vergence demands more easily
when the prismatic displacem ent is introduced gradually
(Sechi and Norch 1 987). Vergence adapcacion, as revealed
in che change o f dark vergence, occurs after a period ot
m aintained convergence in che dark buc is smaller and dis­
sipates more rapidly than vergence adapcacion produced by
maintained vergence on a stimulus (Ebenholcz and C icek
1995).
W hen prism power is increased beyond a certain lim it
in eicher direction, diplopia becom es apparent. The d ip lo­
pia lim it varies wich the state o f tonic adapcacion o f che
cxcraocular muscles. For instance, diplopia occurred when a
visual target was viewed chrough 3-diopcer prisms, which
forced vertical divergence. However, after viewing a visual
target for betw een 3 and 10 m inutes through 6-diopter
prisms, the diplopia seen wich 3-diopcer prisms was over­
com e, and vercical fixacion disparicy somecimes recurned со
ics norm al value (O g le and Prangen 1953). W h ile fusional
limics change wich change in vergence dem and, che differ­
ence becween che upper and lower fusional limics (fusional
amplicude) rem ains conscanc (Sccphens and Jo n es 1990).
Pacel et al. (1 9 9 9 ) investigated the dynamic effects ol
sustained convergence. C onvergence on a 6" convergence
target for 3 0 s or m ore reduced rhe peak velocity o f open-
loop divergence by about 25% . The velocity o f convergence
was nor affected. Satgunam et al. (2 0 0 9 ) had subjects co n ­
verge on a 12° convergence target for 5 m inutes. This
decreased rhe peak velocity and amplitude o f divergence
and increased the peak velocity and am plitude o f open-loop
convergence. There was also a m oderate convergent shift in
phoria. It is n o t clear why Patel et al. did n o t find any effect
o f sustained convergence on convergence.
1 0 .2 .5 b V erg en ce A d a p ta tio n and
A c c o m m o d a tio n
Prisms produce much larger changes in fixation disparity
than does changing the actual distance o f t h e visual target
(Jaschinski 1 9 9 7 ). This is because the change in vergence
demand produced by prisms is n o t accom panied by the
change in accom m odation demand chac is encailed by
changing che real distance o f a target.
After subjects inspected a haploscopic display, set ac
maximum tolerated accom m odative value in one direction
and maximum tolerated vergence value in the other direc­
tion, a change in tonic vergence buc no change in tonic
accom m odation occurred (Kran and Ciuffreda 1988). A
change in tonic accom m odation (dark focus) occurred only
when vergence anil accom m odation were congruent or
when vergence was open loop.
O gle c t al. (1 9 6 7 ) reported that about 25 % o f patients
tested in their clin ic had a forccd-vergence curve chac varied
according со whecher vergence was near or far. This same
phenom enon occurred in abouc 40 % o f a sample o f normal
adulcs (W ick 1985). The mosc frequent change was from a
суре I curve wich near convergence to a type II curve with
far convergence, although Saladin and Sheedy (1 9 7 8 ) found
equal frequencies o f суре 11 ac near and far.
W ith a distant visual target, there is greater vergence
adaptation to base-out prisms, which increase vergence
demand, than со basc-in prisms, which decrease
vergence demand. W ich a near cargec, adaptation produced
by base-out prisms is reduced to a magnitude similar to that
produced by basc-in prisms (N orth e t al. 1 9 9 0 ). At least
two factors could contribute to these effects. Base-in prisms
cause a near target to appear more distant and this decreases
the demand on the vergence system because ot the action ot
proximal vergence (see Scction 10.3.2). Secondly, accom ­
modative convergence creates a greater vergence demand
with a near target than with a far target.
Fixation disparicy also changes when posicive o r ncga-
tive lenses are placed before the eyes. The lenses change
accom m odation, which induces a corresponding change in
the resting state o f vergence. Furtherm ore, prolonged exp o­
sure to a particular scacc o f accoinm odacion changes che
rescing state o f accom m odation, the resting scare o f vcr­
gcncc, and che magnicude o f phoria (Sch or 1983a). The
reciprocal coupling becween accom m odacion and vergence
is discussed in Seccion 10.4.
Vergence demand may also be increased by viewing che
world chrough a telestereoscope, w hich effectively increases
or decreases interocular distance. The cffccts are n o t chc
same as chose produced by prisms. Prisms add a conscanc
amounc со vergence over the whole range o t distance,
whereas increased vergence demand produced by a celesce-
reoscope is inversely related to distance (Figure 10.22).
Hosier et al. (1 9 8 9 ) generated forced-vergence curves
with accom m odacion rendered open loop by an artificial
pupil. Relative to the closed-loop con d ition , the curves were
more exophoric on the forced convergence side but were
unchanged on chc forced divergence side. Sem m low and
Hung (1 9 7 9 ) obtained con flictin g results, so the precise
contribution o f accom m odative vergence to fixation dispar­
ity remains C o be clucidaced.
The conic scacc o f che eyes is clearly noc fixed buc adapcs
со chc currenc level o f vcrgcncc, m ore rapidly and com -
plcccly in som e people chan in others. Hung ( 1 9 9 2 b ) devel­
oped a m athem atical model of vergence adaptacion.
1 0 .2 .5 c A d a p ta tio n o f Eye T o rsio n
Maxwell and Sch or (1 9 9 9 ) placed D ove prisms before the
eyes, which rotated the images ot a sccne in opposite
directions about the visual axes. W h en subjects tilted the
head 4 5 ' in one direction the dove prisms introduced a
cyclodisparity that triggered incyclovcrgence. W h en the
head tilted 45° in the opposite direction the prisms' trig­
gered an excyclovcrgcncc. After 1 hour o f alternating exp o­
sure to this coupling betw een head position and
cyclodisparity, subjects dem onstrated a head-position
dependent change in cyclophoria am ounting to up to 13%
ot the cyclodisparity in the training session.
Maxwell et al. (2 0 0 1 ) observed persisting changes o f
2 to 3° in the torsional alignm ent o t the eyes after a 90-m in ­
ute training period in which subjects cracked a 40 " by 40°
grid o f lines as it changed in position while undergoing
changes in cyclodisparity. The aftereffects were measured
while subjects visually tracked the m ovem ents o f a small
test stimulus. A daptation o f cyclovergence was evident both
when the test stimulus was a grid ot lines contain in g a
cyclodisparity signal (closed loop) and concentric circles
containing no cyclodisparity signal (open loop).
Cyclovergence o f 2 or 3° m aintained for periods up to
150 s took about 5 s to decay in the dark but decayed more
quickly in the presence o f a zero-disparity stimulus (Taylor
c t al. 2 0 0 0 ).
1 0 .2 .6 N O N C O N C O M IT A N T V E R G E N C E
A D A P T A T IO N
10 .2 .6 a N o n c o n c o m ita n t A dap tation
A change in vergence demand is con com itan t when it is the
same for all directions o f gaze. It is nonconcom itant when it
varies with angle ot gaze. W hen the eyes change their conver­
gence from a near pointdirectly ahead to a point in an oblique
direction on the same trontal plane, they must execute an
appropriate vertical vergence to bring the images o f the newly
fixated object onto the foveas (see Figure 10.17). They must
also execute an appropriate change in horizontal vergence.
M idline
b.Rurc Ю.17. U nequal version) n eed ed fo r o bliq u e guze. W h e n chc gaze m oves
from a straight-ah ead a t О , со an ob liq u e p o sitio n . P. chc eves muse
execu te a vertical vergence m ovem en t to b rin g th e im ages o f P in to
vertical corresp on d en ce. T h is is because P Q su bten ds a larger angle, в ,
со o n e eye than to the ocher eye. The eyes m ust also execute unequal
h orizon tal m ovem en ts, since angle 0 К is larger chan angle <f>L.
For instance, a vertical vcrgcncc o f three prism diopters is
required to binocularly fixate a point 24° up and 24° to one-
side on a frontal plane, at a distance o f 3 3 cm (O gle and
Prangen 1 9 5 3 ). Furtherm ore, the required vergence for a
given direction o fg aze varies with the discancc o f the fron­
tal plane.
W h en the gaze was directed to a target w ithout error
feedback, che visual axes intersected on the target with an
error ot no more than 0.25° tor any direction or distance ot
the target (Sch o r et al. 1994). This suggests that vergence
movements are preprogrammed tor changes in gaze direc­
tion or distance.
N on con com itan t vergence demand is induced by spec­
tacle lenses with unequal m agnification in the two eyes; a
condition known as optical aniseikonia (Section 9 .9 ). This
happens when the tw o eyes require different amounts o f
optical correction. W hen the gaze is directed away from the
optic axes o f a spectacle lens, the lens acts like a prism, which
increases in power as a tunction o t the angle o t gaze. It
the lenses do not have the same power the eyes must move
different am ounts to m aintain fusion. A person can co m ­
pensate for the effects o f spectacles by turning the head so
that the eyes look through the centers o f the lenses, and
lenses can be made that optically correct for aniseikonia.
However, m ost people do not need to com pensate in either
o f these ways bccausc they adapt to the n oncon com itant
vergence demand by n onconcom itan t vergence. Thus, a
person used to reading with unequal lenses learns to elevate
the visual axis o f one eye relative to that o f the o ther to bring
the images o t an o b ject onto the fovea. A person who has
made such an adjustm ent o f vergence shows a phoria that
depends on the direction ot gaze when tested with disasso­
ciated viewing. This is n on co n com itan t phoria, or aniso-
phoria (Ellerbrock and Fry 1941, 1 9 4 2 ; Ellerbrock 1948;
Allen 1974). Dynam ic aspects o f adaptation to aniseikonia
are discussed in Section 10.8.3b.
1 0 .2 .6 b The Adaptive Field
W h en a person holds the gaze in one direction while-
adapting the state o f vergence to a prism-induced disparity,
a change in phoria occurs in about 3 0 minutes. Although
the change in tonic vergence is maximal for that direction
o t gaze, it also shows when the eyes look in neighboring
directions along the same meridian. The range o f eye posi­
tions over which a locally applied adaptation o f vergence
spreads is called the adaptive field (H enson and Dharam shi
1982). Changes in phoria after adaptation to a fixed direc­
tion o t gaze were constant over an 18°-wide field, showing
that the adaptive field is at least this wide (Sch o r et al.
1993a).
N on concom itan t adaptation o f tonic vergence to a gra­
dient o t disparity, such as that produced by spectacles, takes
m uch longer than co n com itan t adaptation to constant dis­
parity (Sethi and H enson 1984). W ith nonconcom itant
adapcacion, a specific degree o f adaptation must be applied
at each direction o i gaze along a given meridian.
S ch or ec al. (1 9 9 3 a ) investigated chis process by having
subjeccs adapc со cwo separaced cargecs wich opposice prism-
induccd vercical disparities. They used vercical racher chan
horizoncal vergence because it is not affected by accom m o­
dacion. D ifferential adaptation of vergence was greater with
greater lateral separations o f the targets or w ith smaller
imposed disparities. Thus, the steeper the disparity gradient
between cargecs, che m ore difficult ic becam e со acquire
nonconcom icanc vergence.
Sch or ec al. proposed a tw o-m echanism model o f tonic
vergence adaptation. The first is a global mechanism o f
rapid onset, w hich generalizes to all eye positions along a
given meridian. The second is a slower local mechanism
that adapts to distinct disparities in che visual field. The
local m echanism shows some spread, so that differential
adaptation to objects with d istin ct disparities does noc
occur when the objects are too close together.
In conform ity with this tw o-m echanism model, the
n on con com itan t com ponent o f adaptation of vertical ver­
gence built up more slowly than the con com itan t co m p o ­
nent (M axw ell and Sch or 1 994). C o n co m itan t adaptation
o f vertical vergence to a prism before one eye decayed with a
tim e constant o f about 31 min while n on concom itan t adap­
tation to a lens worn before one eye decayed with a cime
conscanc o f 8 3 m in (G r a f ec al. 2 0 0 3 ). M cC andless ec al.
(1 9 9 6 ) described a model o f che neural processes involved
in n on co n com itan t adaptation o f vertical vergence.
10 .2 .6 c M e rid io n a l S p e c ific ity o f
V c rg c n c c A d a p ta tio n
It seems that n on con com itan t adaptation of tonic vergence
is specific со che meridian along which chc disparicy gradi­
ent is presented. Thus, M axwell and Schor (1 9 9 4 ) adapted
subjects to tw o different vertical disparities presenced along
eicher che horizoncal or vercical meridian. Vergence adapta­
tion, as revealed in postexposure phoria, was n on co n com i­
tant only for the meridian along which the different
disparities had been displayed. It was co n com itan t along
the orthogonal meridian.
S ch or et al. (1 9 9 3 b ) had subjects converge on scacionary
targets at differenc posicions along an optically induced dis­
paricy gradienc. This rcsulced in a posicion-dependenc
phoria and a differential movemenc o f che eyes during visual
pursuic, buc ic did not produce disjunctive saccadcs. The
m echanism responsible for adaptation o f saccadic am pli­
tude in the cwo eyes (Seccion 10.8.2) muse be independenc
o f chat responsible for adapcacion o f scacic vergence and
visual pursuit. Gleason et al. (1 9 9 2 ) developed a model of
rhe processes responsible for adaptation o f static vergence
and disjunctive pursuit.
Sch or and M cC andless (1 9 9 7 ) exposed subjects to ver­
tical disparities that varied according to w hether the gaze
moved in the midsagiccal plane (horizoncal vergence and
vertical version), the frontal plane (horizontal and vertical
version), or che cransverse plane (horizoncal vergence and
horizontal version). Adaptation of vertical vergence, as
indicated by dark phoria, was specific to each o f the three
orthogonal planes. They modeled the results with a matrix
that associated pairs o f eye-position signals with a weighted
output driving vertical vergence.
Maxwell and Schor (1 9 9 6 ) placed either a base-up or
base-down prism before one eye according ro w hether the
head or the whole body was pitched up or down, deviated
to left or right, or rotated left or right about the visual axis.
In each case, 6 0 minutes of alternating changes in head
or body position and prism deviation resulted in a head-
position-dependent change in vertical vergence, which per­
sisted when the prism was removed. This result implies that,
in normal circum stances, changes in vertical vergence co m ­
pensate for the ocu lom otor effects o f vestibular and neck
proprioceptive stimuli arising from movements o t the head
or body. Su bjects can simultaneously adapc vercical vergence
in an cye-posicion-spccific manner, which varies wich head
posicion (M axwell and Sch or 1997). Thus che mechanism
responsible for adaptation o f vertical vergence cakes the
posicions o f boch chc eyes and head inco accounc.
10 .2 .6 d D is ta n c e C u e s f o r V erg en ce A d a p ta tio n
S ch or and M cCandless (1 9 9 5 a , 1995b ) asked subjeccs со
accempc со fuse a cross containing various degrees o f vertical
disparity coupled with variations in various visual cues to
distance, including overlap, loom ing, relative size, and par­
allax. A 2-hour adaptation period did n o t induce any change
in vertical vergence as indicated by postexposure phoria.
However, association o f vertical disparities with different
values o f horizontal vergence as a cue со discance did induce
adaptation of vertical vergence. Thus adaptation o f vertical
vergence occurred in response со associations becween vcr-
cical and horizontal ocu lom otor accivicy buc noc in response
со associacions becween vergence and m onocular cues со
discance.
1 0 .3 V O L U N T A R Y A N D P R O X IM A L
VERGEN CE
1 0 .3 .1 VO LU N TA RY V ERG EN C E
Voluncary vergence is vergence iniciaced when chere is no
cargec scimulus со indicate the required vergence. Ic occurs
in che following circum stances:
1. Mergence to an imagined object Changes in vergence
betw een imagined objects in the dark are voluntary
(M cL in and Schor 1 9 8 8 ). Such vergence movements
are unreliable and poorly correlaced with che imagined
 distances o f the imagined objects (Erkclcns ct al.
1 9 8 9 b ). Vergence induced by an attem pt to fixate o n es
unseen finger in che dark would be voluntary vergence,
although people do noc perform chis cask accuracely.
C hanges in vergence in chc dark seem со be
independent of changes in accom m odation
(Fincham 1962).
2. Deliberate rniseonvergence O n e can learn to diverge or
converge che eyes со make chc images o f an isolaced
objecc disparacc. Also, one can deliberacely misconverge
while looking ac a cexcurcd froncal surface. Ic is rclacivcly
easy со learn со misconverge horizoncally buc chere is no
evidence chac people can learn со misconverge vcrcically
or by rocacing che cwo eyes in opposice directions.
3. Fusion o f stereoscopic images Voluntary vergence is
required when vcrgcncc is changed so as со fuse cwo
widely disparace scimuli beyond che range o f disparicy
dececcors. For example, when looking ac an
aucostereogram, like those discussed in Section 2 4 .1 .6 ,
one must learn to diverge beyond chc plane o f chc
display. O n e must also learn со diverge or converge che
eyes in order со fuse sidc-by-sidc sccrcoscopic images.
(use before, during, and jusc after a vcrgcncc response со
a large binocular disparity step there is a decremenc in che
dcccccabilicy o f an objccc or o f che displaccmcnc or change
in disparicy o f an ob ject (M anning and Riggs 1984; Hung
cc al. 1989, 1990) (Porcraic Figure 10.18). This loss o f
F .Rurc 10. 18. G eorge A*. Hmtg. B o m in Sh an gh ai, C h in a , in 1 9 4 7 .
H e o b ta in ed a B .S c . in m ech an ical b ioen g in eerin g in 1 9 7 0 and P h .D . in
physiological o p tics in 1 9 7 7 , b oth from Berkeley. H e jo in ed the faculty
at R utgers U n iv ersity in 1 9 7 S , where he is now professor o f biom ed ical
engineering.
sensicivicy is analogous to thac associaced wich saccadcs
(M acin 1974; Volkmann ec al. 1 9 7 8 ; Lee and M alpeli 1998).
Suppression helps chc viewer со disregard che inscabilicy o f
images during saccades and vergence. Ic may also help elim i-
nace chc ctfcccs o f spurious disparicy signals during chc cxc-
cucion of large vergence movcmcncs.
1 0 .3 .2 P R O X I M A L V E R G E N C E
The cype o f vergence chac M addox called voluntary vergence
is usually referred to as p roxim al vergence. Ic is evoked by a
scimulus that gives the impression o f being nearer or further
chan che poinc o f convergence, in rhe absence o f disparicy or
accom m odacion cues. In ocher words, che cargec scimulus
contains some informacion abouc che relacive discances ot
che initial and cargec scimuli. Proximal vergence is also inici-
aced by radial opcic flow and by changes in che size o t che
image. Proximal vergence occurs aucomacically when chc
observer acccnds со a particular scimulus. It is cheretore noc
voluncary although ic is evoked by a voluncary change o f
accencion from one o b ject to anochcr.
10 .3 .2 a V c rg c n c c C h a n g e s O v e r L a rg e D ista n c e s
The mechanism thac signs che direccion ol accom m odacion
does noc work for images ouc o f focus more chan 2 D
(Fincham 1951). Furchermore, binocular disparities o f
m ore than about 4° do n o t evoke vergence (Section 10.5.3).
O th er depch cues, such as perspective and m otion parallax,
operace ac distances outside these lim its. Thus, vergence
movements со objeccs ac a distance far removed from
the plane o f initial convergence arc, by definition, proximal
vergence.
C onsider che acc ot changing convergence from a near
o b ject to an objecc in che far discance, or vice versa. The in i­
tial proximal vergence response brings the disparity o f the
o b ject within range o f disparity detectors. Vergence then
comes under the concrol ot absolute disparity. The overall
vergence response and associated accom m odation elim i­
nates the blur and absolute disparity of the images ot the
newly fixated o b ject. Schor c t al. (1 9 9 2 ) devised a feedback
control model o t chesc processes.
10 .3 .2 b P ro x im al V c rg cn cc со C o p la n a r
S ta tic S tim u li
Increasing the size ot chc image o f a playing card was found
со evoke a change in vergence (Iccelson and A m es 1950;
Alpern 1958). Predcbon (1 9 9 4 ) observed vergence induced
by che fam iliar size o f a m onocularly viewed objecc.
Enright (1 9 8 7 a ) found chac subjeccs converged when
chey monocularly fixaced an apparendy near pare o f che
drawing o f a cube, and diverged when chey fixaced an appar-
enclv far pare. In chis case che cue to depth was provided
only by perspective. Vcrgcncc movcmcncs were also eliciccd

i ifu»c Ю.19. Jam esE n rig h t. B o rn in Baker, O reg o n , in 1 9 3 2 . H e o b tain ed a
В .Л . a t U niversity C o lleg e o f L os A ngeles in 1 9 5 7 and a P h .D . w ith
E. NX'. Fagcr at the Scripps Institu te o f O cean o grap h y in 1 9 7 4 .
H e did p o std o cto ra l work w ith J . A s c h o ffa t the M ax P lan ck Institute
fu r V crh altcn sph ysiolog ic, E rln g -A n d ech s, G erm any. H e then join ed
the Scripps In stitu tio n o t O cean o g rap h y a t the U niversity o f C alifo rn ia ,
San D ieg o , where he rem ained u n til he died in 2 0 0 4 .
in the closed eye when the gaze o f the open eye changed
from a pare o f a painting thac depicted a near o b ject со a
part that depicted a far object (Enright 1987b) (Portrait
Figure 10.19). Subjects made large and rapid changcs in ver­
gence when they looked back and forth between two frontal-
plane horizontal fluorcsccnc rods seen ac different distances
in dark surroundings (W ic k and Bedell 1989).
It was claim ed that, because the rods were horizontal, the
only cues to depth were the relative thickness and heighc o f
the rods in the field. However, accom m odation cues were
not elim inated.
Rosenfield et al. (1 9 9 1 ) measured proximal vergence
evoked with accom m odation cues elim inated by having
subjects look through pinholes, and with disparity cues to
depth elim inated by introducinga vertical disparicy between
the images in the tw o eyes. A letter chart viewed in the labo­
ratory was the target for distances up со 6 mecers, and
o b jects such as buildings seen out o f the window were tar­
gets for distances o f up to 1,5 0 0 mecers. Vcrgcncc and
accom m odation changed linearly with increasing distance
o f the cargec, up со abouc 3 mcccrs, after w hich vergence
remained constant.
H orizontal magnification o f chc image o f a random-doc
display in one eye wich respect to that in the other eye cre­
ates an impression o f slant in depth about a vertical axis. As
the gaze shifts horizontally over the surface, vergence
changcs accordingly. A vertical m agnification o f one eyes
image also creates an impression o f a slanted surfacc. This is
O g le s induced effect discussed in Section 2 0 .2 .3 . Sheliga
and M iles (2 0 0 3 ) asked subjects to fixate a point on the
center of such a surfaces and then change their gaze to
another poinc displaced 7.5° со left or righc. W h en chc eyes
began со move, the display was blacked out so that the
response was open loop. During chc change in gaze, vcr-
gence movements occurred that increased in size with
increasing apparent slant of the surface. These movements
occurred even for surfaces containing no horizontal
disparities. The responses had again o t between 0.1 and 0.3
com pared with a gain o f abouc 0.8 for a surface wich a
gradient o f horizontal disparity. The induced cftecc p ro ­
duced by vercical magnificacion o f one image may be can ­
celed by a horizoncal magnificacion o f that image. W hen
subjects changed their gaze over an apparently frontal sur­
face produced in this way, there were no changes in vcr-
gcnce, even though the surface contained a gradient o f
horizontal disparity.
Vergence was also initiated by an impression o f depth
created by m onocular occlusion (see Figure 17.26a), rather
than by binocular disparity (I.iu c t al. 1998).
10 .3 .2 c P ro x im a l V erg en ce w ith
C o n f lic tin g D isp a rity
N orth et al. (1 9 9 3 ) assessed the relative contributions o f
accom m odation, disparity, and proximal cues to vcrgcncc
by introducing three types o f cue discordance. A ccom m o­
dation was made discordant relative со the other cues bv J
having subjects view a display at 4 m through - 0 .7 5 diopter
lenses. Disparity was made discordant by having subjects
view the display through prisms. The proximal cue was
made discordant by having subjects view the display through
both lenses and prisms. They measured che immediate
change in phoria and fixation disparity after a period o f
exposure to each stimulus. Discordance o f disparicy or o f
the proximal cue relative to the o ther cues had sim ilar effects
w hile discordance o f accom m odation had only about one-
third che effect o t a discordance ot either o t the o ther two
cues. H u n g e r al. (1 9 9 6 ) com m ented that, in this experi­
m ent, an absence ot stim uli in the central field created a bias
against accom m odation. They found that proximal cues
had little effect on vergence in the presence o f adequate dis­
parity and accom m odation cues.
W ism eijer et al. (2 0 0 7 ) produced a textured surface in
which linear perspective indicated a slant o f 70° and b in ­
ocular disparity indicated a slant o f 50° in the opposite
direction. Subjects reported that the surfacc alternated
betw een appearing slanted according to perspective and
appearing slanted according to disparity. W hichever way
the surface appeared, the direction o f vergence eye move­
ments produced by changing fixation across the surface was
always in accordance with the disparity-defined slant.
However, perspective bad som e effect because the am pli­ Vergence evoked by optic flow presumably depends on
tude o f vergence with the cues in co n flict was 14% less chan the characteristics o f the underlying m otion detectors.
that when the cucs were in agreement. Here, disparity was W h en a square-wave grating w ith the fundamental fre­
m ore heavily weighted than the perspective, but we will quency missing is moved in W-wavelengch seeps, the odd
now see that this is n o t always the case. harm onics move in the forward direccion and chc even har­
Л concave facc mask appears convex, even with binocu ­ m onics move in che reverse direction (Adelson and Bergen
lar viewing. H otfm ann and Sebald (2 0 0 7 ) tound that sub­ 1985). K odaka ec al. (2 0 0 7 ) caused a concentric missing-
jects converged their eyes on the illusory depth o f the nose fundam ental gracing со expand o r contracc in V\- wavelength
o f the face rather than on its actual location in depth. In the steps. Vergence occurred in the direction o t the 3rd har­
illusion produced by the artist Patrick Huges, concave sur­ m onic, which is the harm onic with the highest concrasc.
faces appear convex and convex surface appear concave, W hen all buc che 3rd and 5th harm onics were removed
even when disparity indicates cheir true orientation. Here from the scimulus, the response was in the direction o f the
also, the eyes converged on the illusory rather than the harm onic with the higher contrast. W h en the contrast ot
actual locations o f p oin ts on the surfaces (W agner et al. one com ponenc was more chan double chac o f chc ocher, che
2 0 0 9 ). In these cases, vergence was controlled by perspec­ response was rotally dom inated by the com ponent with the
tive rather than by con flictin g depth inform ation produced higher contrast. All these features o f the vergence response
by disparity. are consistent with what is known about early processing ot
m otion in the visual cortex.
Pursuit o f a patch on a 2-D display o f dots that
J 0 .3 .2 d V c r g c n c c in d u ccd by L o o m in g S tim u li
created the impression o f a 3 -D rotating sphere (kinetic
Transient proxim al vergence was evoked when the images depth effect) induced the same pattern of divergence and
o f an isolated square changed sinusoidally in size at a fixed convergence as pursuic o f an I.F.I) m oving in an accual 3-D
distance, or varied in disparity but not in size (Erkelens and orbic (Ringach ec al. 1 9 9 6 ). O bservers could noc produce
Regan 1 9 8 6 ). The response to a com bined change in size chis paccern o f eye m ovem ents w ithout an appropriate scim­
and disparity was the linear sum of the two com ponent ulus and could noc entirely suppress vergence movemencs
responses. evoked by che kinetic depch display. Also, monocularly
Biisettini e t al. (1 9 9 7 ) presented subjects with a single viewed forward and backward mocion ot a horizontal grat­
Step o f radial flow in a dot pattern projected o n to an 80 " by ing displayed on a com puter m onitor lying on che ground
80 " screen at a distance o f 3 3 cm . An expanding display elic­ produced nyscagmic horizoncal vergence (Yang ec al.
ited convergence, and a contracting display elicited a smaller 2 0 0 7 ).
divergence. Response am plitude increased as rhe change in Depch cues could drive proximal vergence indireccly by
image size increased trom 1% to 4% . Response latencies evoking a change in accom m odacion (see Takeda ec al.
were sim ilar when the dots changed in density buc not in 1999). Buc chere is confliccing evidence on this poinc.
size. They were also sim ilar with m onocular viewing and M cL in ec al. (1 9 8 8 ) found that the ratio o f vergence to a
when the display was confined to the tem poral hemifields change in stimulus size resembled the ratio o f vergence to
o f both or one eye. In the latter case, the single eye saw lat­ changing accom m odacion (A C /A racio). They concluded
eral m otion in the opposite direction to that in which che chac size changes evoke accom m odacion direcely and ver­
eye moved. This dem onstrates that vergence was n o t simply gence indirectly.
the sum o f two m onocular pursuit movements. However, W ick and C urrie (1 9 9 1 ) com pared vergence and accom ­
the full binocular stimulus produced the largest response. modative responses to prisms and lenses with responses to
Thus, radial mocion specifically triggers vergence in a targets at different distances. They concluded thac proximal
m achine-like fashion. Radial m otion deteccors in M T or vergence can be iniciaced independently o f proximal accom ­
M S T are probably involved (Seccion 5.8.4b ). modacion.
The short-latency vergence response to a step o t radial W hen a binocularly viewed froncal surface increases in
flow was measured as a function o f che angle ac which the size, che edges acquire an uncrossed disparicy because chey
eyes were converged before the vergence response was trig­ becom e m ore discanc from che concave horopter. This
gered (Y a n g et al. 1 9 9 9 ). Response am plitude was inversely change in disparity could concribuce со che divergence pro­
proportional ro the angle o f initial vergence. W ith parallel duced when an objccc increases in size.
gaze (equivalent to infinite viewing distance) the response An experiment should be conducted with an object chang­
was near zero. 'Ih is relationship between vergence and view­ ing size within the curved plane o fth e horopter or within a
ing distance would allow an observer m oving through a fron tal plane at rhe abathic distance, that is, the distance at
natural scene to converge correctly on a distant o b ject and which the horopter lies in the fron tal plane {Section 14.6.2).
ignore loom ing signals arising from nearby objects. Also, according to the above explanation, an object at a far
(Schapero and Levy 1953) had reported a sim ilar relation­ distance where the horopter is convex should induce divergence
ship betw een proximal vergence and vergence angle. when it is made larger.
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Figure 10.21 . S tu art Judge. B o rn in E d in bu rgh in 19-47. H e o b tain ed а В .Л .
in physics and m athem atics in 1 9 6 9 and a P h .D . in co m m u n icatio n
and n cu ro scicn cc in 1 9 7 6 , b o th from K cclc U niversity. H e was lcctu rcr
and then reader in physiology, and a icllow o f S t. A nne's C o lle g e , a t the
U n iv ersity o f O x fo rd , b efore retirin g in 2 0 0 7 .
produce the same result (see Judge 1985) (P ortrait Figure
10 .2 1 ). Hung (1 9 9 7 ) proposed that differences arc due to
nonlinearities arising from the tact that both accom m oda­
tion and vcrgcncc have stimulus thresholds. Larson (1 9 8 2 )
described a procedure for measuring accom m odative co n ­
vergence using a display containing a tusion stimulus.
Since rhe accomm odative state o f an eve is difficult to
measure in routine clinical practice, the AC/A ratio is m ea­
sured with reference to the stimulus to accom m odation, it
being assumed that the accom modative response is propor­
tional to the stimulus. This is the stim ulus AC/A ratio, as
opposed to the response AC/A ratio o b tain ed when accom ­
modation is measured (Alpern et al. 1959). The tw o mea­
sures do not always give the same result (Ripps et al. 1962).
The gain o f accom m odative convergence can be
expressed as the ratio o t the actual vergence change to the
ideal vergence change required to fuse the rargct (Judge and
M iles 19 8 5 ; Judge 1987). This measure provides direct
com parisons betw een subjects with different interocular
distances.
M easurem ent o f the stimulus AC/A ratio is not severely
affected by how long one eye is covered during testing
(Roscnficld c t al. 2 0 0 0 ). Also, the response AC/A ratio is
not affected by adaptation of vergence to base-in or base-
out prisms (R ain cv 2 0 0 0 ). View ing through base-in or
base-out prisms does not alter the change o f vergence
required per unit change in accom m odation, it simply adds
or subtracts a constant vergence at all accom m odation
distances. However, when objects are viewed through a
telestereoscope, as in Figure 10.22, it is as if the eyes were
further apart. The closer the stimulus is to the eyes, the greater
ri*«r« in.ii. A tc/ettcrew topicdevice. T h e effective in tero cu lar distan ce is
increased trom d t o d ' . T h is increases the convergence requ ired when
ch an g in g fixation betw een tw o near o b je c ts , such as A and l i (angle 0
is larger than angle <f>). T h e device also increases the path len gth o f the
light rays, w hich decreases the am ou n t o f a cco m m o d atio n . The ratio o f
con vergen ce to acco m m o d atio n is th erefo re increased.
the vergence demand. This increases the required change in
vergence per unit change in accom m odation. As predicted,
the A C/A ratio increased after subjects had viewed the world
through a telestereoscope for 3 0 minutes (sec next section)
(Judge and M iles 1985). The AC/A ratio did not change
when subjects fixated only one stimulus while looking
through a telestereoscope for 3 0 m in u tes(B obier and M cRae
1996). A simple change in tonic vergence can cater for a fixed
change in vergence demand. However, the AC/A ratio
increased, as it did in the Judge and M iles experiment, after
subjects had alternately fixated two targets at different dis­
tances. A simple change in tonic vcrgcncc cannot cope with
m ore than one convergence distance.
Drugs, such as hom atropine, that increase the effort
required to produce a given accom m odation, increase the
AC/A ratio (C h in and Breinin 1967). Drugs, or viewing
through an artificial pupil, that reduce accommodative effort
have the opposite effect (H erm ann and Samson 1967).
 There have been com peting claim s abouc w hether the
Л С/Л ratio is affected by orth optic exercises (H ofstetter
19 4 5 ; M anas 1 9 5 8 ). Flom (1 9 6 0 c ) controlled for potential
artifacts due to repeated testing and for increases in near
accom m odation and proximal vergence following o rth o p ­
tic exercises. H e found that 3 0 minutes o f orthoptic train­
ing per week over 8 weeks given to 9 4 patients with
exophoria increased the mean Л С/Л ratio by 0 .4 1 . Л co n ­
trol group receiving repeated testing but no orth optic train­
ing showed no change in the AC/A ratio.
Vergence responses o f strabismics and some amblyopes
w ithout strabismus arc sim ilar ro those o f people with
norm al vision but with one eye closed (K enyon et al. 1980a).
Thus, strabism ics show accom m odative vergence but not
disparity vergence.
M yopic children show enhanced accom m odative co n ­
vergence (Jian g 1 995). A child who is esophoric must relax
accom m odation to maincain single vision. The resulting
image blur during near work could induce axial growth ot
the eye and hence myopia (Gw iazda et al. 1 9 9 9 ). Schor
(1 9 9 9 ) developed a model ot these processes.
C onvergence is m ore effectively evoked by disparity
than by m isaccom m odation. For instance, in the monkey,
vergence that was evoked by disparity alone had a smaller
phase lag and higher velocity than vergence evoked by
m isaccom m odation alone (G um m ing and Judge 1986).
A ccom m odation seems to provide a m oderate contribution
to vergence evoked by disparity only when the m ovem ent is
nearly com plete (H u ng et al. 1 9 8 3 ). Furtherm ore, rhe
dynamics o f the initial portion o f a vergence response were
nor improved when a disparity stim ulus was supplemented
by an accom m odation stimulus, although an accom m oda­
tion stimulus did improve the velocity and precision o fth e
final stages o f the vergence response (Sem m low and W etzel
1979). The contributions o f accom m odation and disparity
to vergence are discussed further in Section 10.4.3.
1 0 .4 .2 C O N V E R G E N C E A C C O M M O D A T IO N
H orizontal vergence, however evoked, is accom panied by
an appropriate change in accom m odation. This is known as
con vergence a cco m m o d a tio n (C A ) or vergence accom ­
m odation (V A ).
G um m ing and Judge (1 9 8 6 ) com pared the dynamics o f
C A with those o f accom m odation evoked bv m onocular
blur in monkeys. The stim uli moved sinusoidally at between
0.1 and 1.2 H z. C onvergence accom m odation had higher
gain and lower phase lag than blur accom m odation.
The change in convergence accom m odation per unit
change in eye convergence is the response C A / C ratio. The
change in accom m odation per unit change in the conver­
gence angle o f rhe stimulus is rhe stim u lu s C A / C ratio.
The stimulus tor imposed vergence is the power o f prisms
placed before the eyes, expressed in prism diopters.
Convergence accom m odation is measured when vergence
is changed in the absence o f the blur stimulus to changing
accom m odation. There are three procedures for elim inating
defocus blur.
1. Pinhole viewing An o b ject seen through a pinhole
remains in clear focus whatever its distance and
whatever the accom m odative state o fth e eyes.
However, som e blur remains with pinholes o f a
practical size. The pinhole method has revealed that
accom m odation is a linear function o f convergence. For
young adults, accom m odation in diopters is
approximately equal ro vergence in m eter angles, so rhar
the gain o f convergence accom m odation is 1. The gain
is smaller in older and more presbyopic subjects
(Fincham 19 5 5 ;F in ch a m and W alton 1957).
2. Use o f an interference pattern A speckle interference
pattern form ed on the retina by cwo laser beams
provides an effective stimulus for studying convergence
accom m odation, because such a pattern is independent
o f the state o f accom m odation. Using this procedure,
Kcrsten and Leggc (1 9 8 3 ) found that the average
accom m odation o fth e tw o eyes is linearly related to
vergence angle over rhe eyes’ accom m odative range,
w ith a mean C A / C ratio o f 0.91. The C A / C ratio was
alm ost as high at scotopic levels. A ccom m odation was
found n o t to vary with changes in the angle o f gaze.
3. Use o f a low spatial-frequency stimulus A ccom m odation
can also be made open loop by using a difference o f
Gaussian visual target with a center spatial frequency
o f 0 .2 cpd (Tsuctaki and S ch or 1987). This low
spatial-frequency stimulus did not evoke reflex
accom m odation.
H orizontal convergence increases the horizontal radius
o f curvature o f the cornea, especially in young people
(Lopping and W ealc 1965). This effect is believed to be due
to tension induced in the cornea by con traction o f rhe
medial rectus muscle.
In stereoscopes, flight trainers, o r stereoscopic head-
m ounted display systems, vergence changes when one looks
at different depth planes but, optically, the stimulus remains
at a fixed distance. The resulting conflict betw een vergence
and accom m odation can cause visual fatigue, or asth en o p ia
(W olffsohn et al. 2 0 0 1 ).
1 0 .4 .3 R E L A T IO N B E T W E E N A C A N D CA
1 0 .4 .3 a A C -C A 1in k age
Convergence accom m odation and accom m odative conver­
gence are rwo aspects o f the functional unity o f vergence
and accom m odation. C om m ands tor the two responses
arc issued concurrently and inreract reciprocally. However,
the eyes begin to change vergence before they begin to
accom m odate because chc skeletal reccus muscles respond
more rapidly than the autonom ic ciliary muscles (Allen
1953).
In spite ot this functional unity, accom m odation and
vergence assume independent rcscing staces in the dark
(O wens and Leibow itz 1980). There is conflicting evidence
about whether the resting states o f vergence and accom m o­
dation, although different, are correlated (see G ray et al.
1993c). However, when allowance is made lor differences in
the A C/A ratio between subjects, dark accom m odation may
be predicted trom dark vergence (W o lf et al. 1990; Jiang and
Woessner 1 996). There is probably also some uncorrelated
noise in the two systems. In darkness, vergence and accom ­
modation return to cheir respective resting states because
there is insufficient stimulation to activate the feedback
loops in each system or the cross-links becween the syscems.
People with an unusually high A C/A ratio tend to have
a lower than norm al C A / C ratio. A bnorm ally high AC/A
ratios and low C A /C ratios are accom panied by low adapt­
ability o f rhe resting state o f accom m odation and high
adaptability o t to n ic vergence. Unusually low AC/A ratios in.25. F rederick A lbert M iles. B orn in G rim sby, L n glan d . in 1 9 3 9 . He
arc accom panied by high adaptability o f accom m odation o b ta in ed a B .Sc. in an im al P\physiology from the U n iv ersity o f L eed s in
1 9 6 2 and a P h .D . in ncurophvsiology from the U n iv ersity o f Sussex in
and low adaptability ot tonic vergence (Sch o r 1986, 1988;
1971. H e wav a lectu rer at the U niversitya o f Sussex from 1 9 6 6 to 1 9 7 1 .
S ch or and H orner 19 8 9 ; Polak and Jo n es 1990). In 19 7 1 * he moved to the N atio n al In stitu te o f H ealth in B cthcsda,
W ith increasing age, the C A /C ratio decreases substan­ where he is now ch ief o f the scctio n on o cu lo m o to r co n tro l in the

tially, probably because o f a decrease in the range o f accom ­
m odation. Also, the A C/A ratio increases moderately
(B ru ce cc al. 19 9 5 ; Rosenfield ec al. 1995a), although
Ciuffreda et al. (1 9 9 7 ) found that the increase occurred
only after the age o t 45 years and only tor the stimulus
AC/A ratio.
A telestereoscope increases the effective interocular sep­
aration and the required change in convergence per unit
change in accom m odation. This decreases the required gain
o f AC/A and increases the required gain o fC A / C . Exposure
to a telestereoscope tor 3 0 m inutes produced a mean shift
o f 3 7 % in the AC/A gain, which returned to norm al over a
period ot about 4 hours o t norm al viewing. Periscopic spec­
tacles that bring the visual axes to rhe m idline, reduce the
interocular separation and reduce to zero the change in ver­
gence involved in accom m odating at ditferent distances.
Exposure to periscopic spectacles had very little effect on
AC/A gain (M ile s e ta l. 1987) (Porcraic Figure 10.23).
Exposure to base-out prisms that increase convergence
demand by a constant am ount ac all distances caused a pre­
dicted downward shift in the AC/A curve and upward shift
in the C A / C curve, rather than changes in gain. Basc-in
prisms that reduced vergence demand by a constant am ount
shifted the C A / C curve downward but had no effect on the
AC/A curve (M iles et al. 1 9 8 7 ). Thus, the reciprocal cou ­
plings betw een accom m odation and convergence are sub­
je c t to adaptive changes, although the effects are
asymm etrical. These changes could be due to error-sensing
feedback in the reciprocal control loops, but muscular
fatigue could also make a contribution.
L ab o rato ry o f S e n so rim o to r R esearch o f t h e N atio n al Eye In stitu te. He
received the G o ld en Brain Award o f t h e M in erv a F ou n d ation in 2 0 0 0 .
Exposure to virtual-realicy displays that place unequal
dem ands on vcrgcncc and accom m odation also changes the
AC/A and C A / C ratios (Eadie et al. 2 0 0 0 ).
There has been some dispute about w hether the linkage
betw een accom m odation and vergence is served by tonic
controllers, by phasic controllers, or by both. Evidence o t a
linkage involving the two controllers has been reported by
E bcnholtz and Fisher (1 9 8 2 ) and Rosenfield and G ilm artin
(1 9 8 8 a , 1988b). However, more recent evidence suggests
that the linkage receives inputs from only the phasic sys­
tems (Sch o r 1992; Jian g 1996).
A t frequencies o f stimulus oscillation below about 0.1
Hz, accom m odation does not respond to changes in ver­
gence, and vergence does n o t respond to changes in accom ­
m odation. As stimulus frequency is increased to about 0.5
H z, the C A / C and A C/A ratios increase in a nonlinear
fashion (Sch o r and Koculak 1 9 8 6 ). The values o f both ratios
are subject to fatigue (S ch o r and Tsuctaki 1987).
In all the studies m entioned so far the AC/A and C A / C
ratios were measured w ith an o b ject in the median plane o f
chc head. For an o b jcct in this plane, accom m odation
expressed in diopters and vergence expressed in meter angles
arc chc same. However, Figure 10.24 shows that, for an
eccentric o b ject, the stimulus for vergence is not the same as
that for accom m odation. As an o b ject moves away from
the m idline along an isovergence locus, the stimulus to
 Iso-vergence locus д Iso-accom m odation locus arises because o f Panum s fusional area. The model accounts
for dilferences in the A C/A ratio determ ined by the phoria
and fixation disparity m ethods.
Reviews o f accommodative vergence and vergence
accom m odation have been provided by Alpern (1 9 6 9 ),
M organ ( 1 9 6 8 ), C iuffreda and Kenyon ( 1 9 8 3 ), and Fry
(1 9 8 3 ). Sem m low and Venkiteswaran (1 9 7 6 ) dealt with
dynam ic aspects o f accom m odative vergence.

1 0 .4 .3 c V erg cn cc-A cco m m o d a tio n C h a rts

For a given intcrpupillarv distance there is a required degree

o f vergence and accom m odation for each viewing distance.
W h en plotted on a chart, as in Figure 10 .2 0 Л , the required
accom m odation for each vergence angle is known as the
dem and line. The actual vergence for various degrees o f
accom m odation for disassociated targets plotted on the
same chart indicates the magnitude o f phoria. A similar
Fijwt nt.ii. I ’e rg n tic ,m d м ш н т оЛ лй оп in ceccn trifgaze. F o r o b jccc A in plot with associated targets represents fixation disparity.
th e m ed ian plane, v crg cn cc in m eter angles and acco m m o d atio n in The same chart can be used to plot the range o t vergence
d io p ters arc the sam e. A n e cce n tric o b je c t В w ith th e sam e vcrgcncc as
before loss o f fusion and the insufficiency or excess o f co n ­
o b jc c t A w ould have to b e in p osition С to have the sam e stim ulus for
acco m m o d a tio n as o b jc c t А . (л<ир«<1(томNguy<n« ji. ioog), vergence and o f divergence in relation to accom m odation.
The range o f accom m odation and the range o f vergence
possible w ithout excessive error in either define the zone o f
cle a r single b in o cu la r vision. Figure 10 .2 0 Б shows a repre­
accom m odation increases. As an o b ject moves out along an
sentation o f this zone (Fry 1939). The width o f the zone
equal accom m odation locus, the stimulus to convergence
represents the range o f vergence w ithin which accom m oda­
decreases, ('h an g in g the cross-links betw een the A C /A and
tion remains tolerably precise, and is approximately c o n ­
СЛ/А ratios could com pensate for the change betw een ver­
stant at all levels o f accom m odation. W ith training, people
gence and accom m odation. It could also be compensated
can learn to dissociate vergence and accom m odation, and
for by changing the accom m odation bias or by changing the
thereby broaden the zone o f clear vision (H o fstcttcr 1945;
vergence bias (phoria). Nguyen e t al. (2 0 0 8 ) measured
H eath and H ofstettcr 1952). The range over w hich accom ­
AC/A and С A/A ratios tor stimuli on the m idlinc and at
m odation and vergence can be achieved w ithout discom ­
eccentricities o f 17.5* and 30°. The AC/A ratio decreased
fo rt is known as the com fo rt zone. The right-hand boundary
with increasing gaze eccentricity, especially in subjects with
represents rhe lim it o f convergence, and the slope o f the
a high ratio at the m idline. T h e C A / C ratio did not change,
boundary indicates that the person can achieve higher
but the open-loop accom m odation bias increased to about
degrees o f vergence when aided by near accom m odation
0 .8 4 1) at an eccentricity o f 30°. This m inim izes accom m o­
(th e AC/A ratio).
dation errors tor eccentrically viewed objects.
The situation is com plicated by the fact that strong co n ­
vergence evokes an excessive accom m odative response
1 0 .4 .3 b M o d els o f th e A C - C A linkage through the m ediation o f convergence accom m odation
(Sem m low and H eerem a 1979b ). The distance along the
M odels o f interactions betw een accom m odation and ver­
vergence axis between the demand line and the lim it o t ver­
gence have been developed by Sch or and K otulak (1 9 8 6 ),
gence is known as the vergence reserve. The degree o f
Polak and Jo n es (1 9 9 0 ), Sch or c t al. (1 9 9 2 ), and Sch or
phoria, tor cach value o f accom m odation, is represented by
(1 9 9 2 ). The symbols and units used in these models are
a line parallel to the sides o f the zone o f clear vision.
described in Section 3.3. Sch or and K otulak’s model, shown
Vergence/accomm odation charts are used in clinical
in Figure 1 0 .3 9 , contains separate controllers for phasic and
practice (see H ofstettcr 1 9 8 3 ; G oss 1995).
tonic vergence and accom m odation. The cross-links serving
accomm odative convergence and vergence accom m odation
occur after the phasic controllers but before the tonic co n ­
10.4.3d Vergence A cc o m m o d a tio n in
trollers. I lung (1 9 9 7 ) developed a nonlinear model. O n e
Stereo sco p ic V ie w in g
nonlinearity is the dead space in the accom m odation
system, which arises because o f tolerated blur. A second In a scene viewed in a stereoscope, accom m odation and
non linearity is the dead space in the vergence system that image blur arc fixed by the distance o f the dichoptic images
lim ited by the faster signal. Tin is suggests that vergence
dynamics are determ ined by m onocular m otion signals
before inputs from the two eyes are com bined.
Previous experim ents from the same laboratory had
shown that vergence evoked by a step displacem ent o f the
image in one eye relative to the stationary image in the other
eye produced m otion o f both eyes (B u settin i c t al. 2 0 0 1 ). In
this case, vergence was evoked by changing disparity rather
than by each eye tracking its own image. M asson et al.
argued that step displacem ents do not contain m otion sig­
nals required tor m onocular control o f response dynamics.
1 0 .5 .2 P R O C E S S IN G D IS P A R IT Y F O R
С О N T R О L О F V E R G E N С F.
Disparity signals are first generated in the primary visual
cortex. At that level, disparity detectors respond only to
absolute local disparity (G um m ing and Parker 1 9 9 9 ). The
absolute disparity in the o b je ct that one intends to fixate
indicates the direction and m agnitude o f the change in
horizontal vergence required to binocularly fixate it. A
change in disparity over the whole binocular field or in the
images ot a fixated o b ject induces an autom atic change in
vergence.
Duwaer and van den Brink (1 9 8 1 b ) determ ined the
sm allest disparity required to initiate vertical vergence, as
indicated by displacem ent o f nonius lines. Since vertical
vergence is not under voluntary control it provides a clean
measure o f rhe dispariry/vergence threshold. For stim uli
presented tor 2 s at eccentricities ot up to 4°, vergence was
initiated by a disparity o f about 1 arcm in. The threshold
was higher tor stim uli presented tor only 160 ms at eccen­
tricities greater than 4 ю. These disparity thresholds were
much smaller than the disparities at which singleness ot
vision was lost.
A disparity o f about 4° generates the m ost rapid ver­
gence movements, bu t horizontal vergence is evoked even
by disparities o t up to 9°. These are larger disparities than
those to which single cortical cells have been found to
respond (Section 11.4).
Normally, the steady state o f vergence is determ ined by
the distance o t a fixated o b ject. The fixated o b ject is nor­
mally the o b ject to which we are paying attention. W hen
we switch attention to an o b ject at another distance, the
required change in vergence is determ ined by the disparity
o f the new o b ject. W h en the disparity o f the new o b ject is
beyond the detection range, vergence is determ ined by
o ther distance cues. Thus, we normally exercise voluntary
control over vergence through the m ediation o f a change in
attention and gaze to a new o b ject. People m ust learn to
change vergence voluntarily while keeping their attention
on an o b ject at a fixed distance.
The disparity/vergence threshold should be determined
with an objective method o f recording eye mo vements, and
compared with that used for coding o f depth.
Signals that control transient and sustained vergence are
discussed turther in Section 10.5.10.
Symmetrical vergence m ovem ents w ithin the midsagit-
tal plane are instigated by stimuli that p roject images to
opposite cerebral hemispheres. There is evidence that the
d etection o f large disparities betw een such images depends
on interhem isphericconnections routed through the corpus
callosum (see S ection 1 1.9). This idea is supported by the
fact that a patient with section o f the corpus callosum failed
to produce vergence m ovem ents to targets in the visual
m idline but responded when the images were projected to
the sam e hem isphere (W estheim er and M itchell 1969). The
im portance o f the callosal pathway for the control o f ver­
gence is also indicated by the m isalignm ent o f the eyes in
callosectom ized cats (Payne et al. 1981).
To in itiate a change o f vergence, rhe images in the two
eyes need n o t be similar in contrast, orientation, or size.
However, a vergence state is not m aintained when the
images of a fixated o b ject have opposite contrasts or differ
widely in orientation or size (Section 10 .5 .1 0 ).
A pseudo square-wave grating lacks the fundamental
frequency and contains odd harm onics with amplitudes
inversely proportional to frequency. Identical dichoptic
gratings o f this type with a 90" phase disparity produce a
disparity between the 3rd harm onics that is the same as that
betw een the 5th harm onics. Short-latcncv horizontal or
4
vertical vergence was evoked in the direction of the stronger
3rd harm onic. However, the m agnitude o f horizontal ver­
gence was n o t as great as that produced by two sine-wave
gratings o f the same two frequencies (Sheliga et al. 2 0 0 6 ).
There was thus a m inor contribution from rhe higher har­
m onics o f the pseudo square-wave gating. W e will see in
Section 17.1.1 that the way the visual system links images
for stereopsis is also determ ined by the dom inant spatial-
freque ncy com ponen ts.
W h en one spatial-frequency com ponent had a contrast
m ore than 2.2 tim es that o f rhe other, initial vertical ver­
gence responses were governed wholly by the com ponent
with the higher contrast. For horizontal vergence, the co n ­
trast ratio had to exceed 4.5 before one com ponent gained
com plete dom inance over responses (Sheliga et al. 2 0 0 7 ).
Both horizontal vergence and vertical vergence are
evoked by m odulations o f disparity o f a luminance-defined
grating. However, only horizontal vergence was evoked by a
grating defined by m odulations o f contrast, with mean
lum inance constant (Stevenson 2 0 0 2 ).
1 0 .5 .3 RANGE OF VERG EN CE
The angle o f vergence changes abou t 14° when the gaze is
moved from infinity to the nearest distance for com fortable
convergence at about 2 5 cm . Vergence changes about 36°
when the gaze moves to the nearest point to w hich the eyes
can converge. A bout 9 0 % o f this total change occurs when

Fijpr* 10.1 s. H an C otfcw ijn. Born in A m sterd am in 1 9 3 5 . H e obtain ed
л degree in m ed icin e in I 9 6 0 and a P h .D . in n cu ro b io lo g y in 1 9 6 3 ,
from the U n iv ersity o f A m sterd am . H e then held a research fellow ship
a t C a lifo rn ia In stitu te of T ech n olog y. In 1 9 6 7 he o b tain ed an
ap p o in tm en t in the D e p a rtm e n t o f Physiology a t Erasm us U n iv ersity in
R o tterd a m , where he rem ained u ntil he retired in 2 0 0 0 .
Fi*orc Ю.16. C asper Joh an n es E rkden s. B o rn in Baccnburg, chc N etherlan d s,
in 1 9 5 0 . H e o b ta in ed a B .S c. in physics from chc C a th o lic U n iv ersity
o f N ijm eg en in 1 9 7 3 and was a high sch o o l ccachcr becw een 1 9 7 3 and
1 9 7 8 . In 1 9 8 3 he o b ta in ed a P h .D . in d en ta l physics from U trech t
U niversity. H e con d u cted p o std o cto ra l w ork in the d ep artm en t o f
physiology at Erasm us U n iv ersity in R otterd am and jo in ed the faculty
th ere in 1 9 8 5 . In 1 9 9 2 he was ap p oin ted professor in the D ep artm en t o f
Physics o f M an a t U tr c c h t U niversity. H e was d ire cto r o f the H elm h oltz
In stitu te a t U tr c c h t U niversity betw een 1 9 9 4 ad 2 0 0 0 . In 2 0 0 6 he was
appointed head o f the D ep a rtm en t o t Physics and A stronom y.
Jon es (1 9 7 7 ) Found chat in ahouc 20 % o f subjects with
otherwise normal binocular vision, the vergence response
to briefly exposed stimuli was asym m etrical; som e subjects
did not respond to stim uli with crossed disparities, while
others did not respond to stimuli with uncrossed disparities
wich respect to che rescing scace o f vergence. Figure 10.36
shows chc vergence amplicude/disparicy profile ot a person
who responded со a line scimulus only when ic had an
uncrossed disparicy. These subjects showed anomalous
asymmetries in stereopsis produced by b rief stim uli, like
chose reporced by Richards (1 9 7 1 ) (Seccion 3 2 .2 .1 ).
However, che cwo cypes o f asymmetry were only loosely
relaced. Som e subjcccs wich a scereo anomaly did noc show
asymmetrical vergence. Also, wich longer scimulus dura-
cions, asymmetrical responses showed only as slight differ­
ences in latency and velocity.
The initial disparities used by Jo n es were outside che
fusion range. Fredenburg and Harwerch (2 0 0 1 ) found
asymmecries in che inicial vergence response со briefly
exposed G abor patches wich disparicies o f 3 0 arcm in or less.
Alchough vergence asymmetry was correlated with perfor­
mance on a scereo discrim inacion cask, subjcccs wich ver­
gence asymmecries showed normal scereopsis lo r fine
disparicies. They concluded chac vcrgcncc and scereopsis
share an inicial disparicy-seleccive mechanism buc chac che
cwo responses arc subscqucndy processed by d istinct m ech­
anisms.
Convergence anom alies, such as convergence insuffi­
ciency, fixation disparity, and convergence inaccuracy, may
be alleviated by refractive correction (Dwyer and W ick
1995). Refraccive correction improves che abilicy to detect
binocular disparities thac provide che error signal for ver­
gence.
In o rth o p tic therapy, pacicncs are trained со fuse cargecs
in a synopcophore. There is general agreem ent chac training
is effective in im proving the range o t near vergence but is
less effective in increasing far vergence (D aum ec al. 1988).
For example, che range o f vergence, especially in the direc­
cion o f convergence, was increased by orthopcic training for
10 minutes per day over a period ol a few weeks, although
the effect had m ostly dissipated 6 monchs later (Daum
1982).
10.5.4 S T A B I L I T Y OF V E R G E N C E
10 .5 .4 a F lu ccu acio n s o f V ergen ce
The sm all random m ovem ents o f an eye are alm ost as large
with binocular fixation as wich m onocular fixation (Sc C.vr
and Fender 1 9 6 9 ). D isjunctive m otions o f che eyes produce
a corresponding variation ot disparity tor all objects in the
binocular field. M otter and Poggio (1 9 8 4 ) found that for
about 60 % o f the cime che eves
/ o f a m onkcv/ were miscon-
verged by more chan 7 arcm in in boch che horizoncal
and vertical directions when the animal was fixating a
Ю СК
vcrgcncc increased when chc display moved in chc opposicc
direccion со chac o f che bar. Mocion o f che surrounding dis­
play did noc affect chc sceady-scace amplicudc o f vergence.
This suggescs thac che open-loop com ponenc o f vergence is
based on dynam ic disparicy signals extracted over a large
area buc that the steady-state response is governed by the
disparity o f che local cargec.
‘Ih c range o f horizontal vergencc w ithin w hich a cen-
crally placed scimulus can be held in a fused scace is increased
slightly by rhe addition o f m ore peripheral stim uli, buc only
it che added scimuli are in a nearby depch plane. Peripheral
stimuli wirh disparities above about 0.5" did not contribute
to che maincenance ot excreme posicions ot vergence in fix­
ating a cencral scimulus (Jo n es and Scephens 1989).

1 0 .5 .5 S T I M U L U S S U M M A T IO N F O R
H O R IZ O N T A L V E R G E N C E

] 0 .5 .5 a A real S u m m a tio n o f D isp a ritie s

1c is noc difficult со fuse che images o f a central objecc in the

presence o f horizoncal disparities in scimuli in the periph­
eral visual field (Ludvigh et al. 1 965). However, we saw in
che previous seccion chac binocular fixacion o f a ccncral
cargec can be influenced by changes in the disparity ot
Figu.t io.2 “. Stim ulus a n d j.w ip /e vergencc response. (A ) Su b jcccs looked at
neighboring images. This suggescs chac, under cercain cir­ the lin e as the h o riz o n ta l disparity o f the display was m od u lated a t 1.0
cum stances, horizoncal disparities are incegraced over a cer- o r 0.1 H z w ith am plitude 0.5°. (B ) A sam ple response superim posed on
cain area со provide the signal tor vergence. The areal the sinusoidal stim ulus m od u lation . IIowkJ<tul 2<xx>>

su m m ation o f d isp arities may he defined as che area o f a

cexcured scimulus above which che gain o f vergence in
response to a tem poral m odulation o f disparicy does noc
increase.
Howard cc al. (2 0 0 0 ) measured che gain and phase lag
o f horizontal vergence to sinusoidal m odulations ot h ori­
zontal disparicy o f a cexcured display chrough an amplicude
o f 0.5°. The display is shown in Figure 10.27Л . Ic can be
seen in Figure 10.28 chac vergence gain was jusc as high and
phase lag was jusc as low for a scimulus subcending 0.75* as
for larger displays modulaced in disparicy ac 0.1 or 1 Hz.
Thus vergence tracking is as precise tor a small display as for
a large display. Therefore, chc scimulus incegracion area is
very small for horizoncal vergence cracking o f an isolated
scimulus.
For vercical vergence, che scimulus incegracion area
defined in chis way is several degrees o f visual angle in diam-
ecer (Seccion 10.6.3b). The area is larger still for cyclover-
gence (Section 10.7.5).
Popple et al. (1 9 9 8 ) measured che incegracion area for
com posice scimuli in che following way. They exposed, for
2 5 0 ms, a random -doc scereogram containing a cencral disk
wirh 12.5 arcm in o f crossed disparicy. Subjeccs initially co n ­
verged on a cencral doc in che plane o f che surround. The
magnicudc o f chc inicial vergence response со chc disk, as
assessed by a forced-choice nonius procedure, increased
as che diamecer ot che disk was increased up со about 6°.
This suggescs thac scimuli oucsidc a 3° radius do noc atfccc
the initial open-loop com ponent o f vergence. No conclu ­
sions can be drawn from this result about how mixed dis­
parities are integrated for maincaining horizontal vergence.
People cannoc fuse che images o t a cencral objecc in che
continued presence o f a large vertically disparace display in
chc periphery (Seccion 10.6.3).
1 0 .5 .5 b V o lu m e S u m m a tio n o f D isp aricies
Disparicy intormacion for chc concrol o f vcrgcncc may also
be integrated over a lim ited range o f disparicies in a given
small region. This m aybe called volu m e su m m ation o f d is ­
paricies for vergence concrol. Scimulus integration area
multiplied by integration depth defines che stim ulus incc-
gration volume.
M alloc ec al. (1 9 9 6 ) measured che vergence scace after
tw o planes o f random docs 18 arcm in in fro n co fan d beyond
a prefixacion target were presenced for 2 3 0 ms. W hen che
planes concaincd equal numbers o f docs wich chc same c o n ­
crasc, che eyes remained converged midway becween chem.
W h en one plane concaincd more docs or docs wich higher
concrasc, che eyes moved со a poinc nearer chac plane. Thus
vcrgcncc was cliciccd by a disparicy signal derived from a
weighced mean o f chc disparicies in che cwo planes, wich
 Howard et al. (2 0 0 0 ) found that disparity modulation

а> o f an annular textured display confined to the peripheral

Frequency 0.1 Hz
£ 1.0 * — #" -f------------------------------ —i retina produced a response with lower gain and greater
а>
Е1 phase lag than m odulation o f a display o f equal area co n ­
* 0.8
Frequency 1.0 Hz fined to the central retina.
2
§ 0.6 so Differences betw een centrally and peripherally evoked
У
vergence could be due to any o f the following interrelated
! 0 .4 factors.
О

J 0.2
1. Acuity, including stereoacuity, declines with increasing
eccentricity (Section 18.6.1).
25 35 43 50 56 61 67
S tim ulus dia m e te r (deg) 2. Panum s fusional area increases in the periphery so that,

A with more eccentric stim uli, the tendency o f the eyes to

return to the position o f dark vergence induces a larger
100r
fixation disparity w ithout loss o f fusion (I.udvigh and
80 M cK inn on 1966). Thus, the peripheral retina tolerates
Frequency 1.0 Hz larger disparities w ithout triggering vergence than does
S’ 60 the central retina.
TP,
O*
S2 40 3. Peripheral disparity detectors have a smaller internal'
00 loop gain (vergence signal per u n it steady-state
CTJ
20 Frequency 0.1 Hz disparity) than do those serving the central retina.

4 . The transient character o f disparity detectors may

increase as one moves into the peripheral retina.
-2 0
25 35 43 50 56 61 67
S tim ulus dia m e te r (deg) The greater effectiveness o f central stimuli in evoking

В horizontal vergence is advantageous because vergence is

ь.цшс H orizontal vergen ce a s a fu n ction ofstim u lu ta rca. T h e h o r iz o n ta l
d is p a r ity o f th e s tim u lu s in F ig u r e 9 . 2 7 w a s s in u s o id a lly m o d u la t e d
th r o u g h a p c a b t o - p c a k a m p litu d e o f 0 .5 ° . T b c d is p la y h a d a d ia m e te r
b e tw e e n 0 . 7 5 a n d 6 5 ° . ( A ) S h o w s v c r g c n c c g a in a s a f u n c t i o n o t
s tim u lu s d ia m e te r . ( B ) S h o w s p h a s e la g a s a f u n c t i o n o t s tim u lu s
d ia m e te r . (R c d ra * * from H o w n d <» л1 2000 )
designed to bring the images o f objects o f greatest interest
o n to corresponding retinal points so that residual dispari­
ties can be coded as depth. Cyclovergence is evoked ju st as
effectively by peripheral stim uli as by central stimuli
(Section 10.7.4). But the purpose of cyclovergence is to
bring the whole visual scene into register, not particular
images.

greater w eight given to the plane containing more dots or

higher contrast dots. Since neither stimulus area nor dispar­
ity separation between the planes was varied, this experi­
m ent does n o t indicate the area or range o f disparities over
which disparity averaging occurs.
1 0 .5 .6 E F F E C T S O F S T IM U L U S P O S IT IO N
The velocity and magnitude o f horizontal vergence induced
by disparity steps or ramps has been found to be greater for
stim uli presented in the center o f the visual field than for
those presented 3° in the periphery (H ung et al. 1991).
A stimulus with a given disparity becam e less effective in
m aintaining an accurate state o f vergence as it moved into
the peripheral visual field (Francis and O w ens 1983;
H am pton and Kcrtcsz 1983). Furtherm ore, a large dispa­
rate stimulus was m ore effective in evoking vergence than
was the same stimulus with the central 10"-wide region
occluded by an artificial scotom a (Bom an and Kertesz
1985).
10.5.7 VERGENCE LATENCY
Human horizontal vergence made in response to a 2° step
change in disparity o f a small stimulus has a mean latency ot
betw een 130 and 2 5 0 ms, a m ean velocity o f about 1 0 % ,
and take about 1 s to com plete (Rashbass and W estheimer
1961a). Sim ilar values have been reported for the monkey
(C um m ing and Judge 1 9 8 6 ).
C onju gate saccadic eye movements are so rapid that
they are n o t affected by new sensory intorm ation arriving
between 8 0 ms before the saccade starts and its com pletion
(Becker and Jurgens 1975). In contrast, the duration o f ver­
gence movements is long enough to allow new visual in tor­
mation to guide the response to its goal. Because o f internal
delay, any error correction is n o t effective during the initial
rapid phase o f a vergence m ovem ent, w hich lasts about 100
ms. The initial phase ot the response is therefore open loop.
During the final phase, error correction brings the eyes onto
the target.
 There has been some debate abouc che relacive laccneics
o f convergence and divergence. Sem m low and W etzel
(1 9 7 9 ) reported that divergence had a longer latency than
convergence (1 8 0 m s versus 2 0 0 m s). Hung et al. (1 9 9 7 )
agreed w ith Sem m low and W etzel. Krishnan et al. (1 9 7 3 a )
found the reverse (2 5 0 ms versus 2 1 0 ms). However, they
determ ined the start o f a response by linear extrapolation
from the constant velocity phase. This overestimates rhe
latency ot convergence because convergence has a higher
velocity than divergence. A lso, convergence has a shorter
rise-time to peak velocity, a shorter tim e constant, and
shorter total duration than divergence (Z u ber and Stark
19 6 8 ; M itchell 1 9 7 0 ; Krishnan et al. 1 9 7 3 b ; Hung et al.
1997).
A nother com plicating factor is that the dynamics o f
divergence vary with the starting position o f chc response
(Alvarez et al. 2 0 0 5 a ). Figure 10 .2 9 A shows a typical diver­
gence response to a 4" step change in binocular disparity
trom a near initial vergence ot 18° (2 2 cm ) and trom a tar
initial vergence o f 8 ” (5 0 cm ). The response from the near
position has a shorter latency and higher velocity than that
from a far position. Responses from a near position are
presumably aided by the larger tonic innervation o f the
A m otion ot a visual target, a vergence m ovem ent started even
Time (s)
В was greater when the stimulus was presented just after the
Fipuc Ю.29. E ffect o f startin g position on rergence dynam ics. The eye.v
diverged (A ) or converged ( B ) by 4° iro m л p osition o f 8 ° (ta r) or 18°
(n e a r). These results fo r on e su b ject arc typical o f th o se from rhe four
su bjects. (Redn»n lu-a» ЛКмхе/c« jl. IWSi)
extraocular muscles. Figure 10.29B shows that the dynam­
ics o f a 4° convergence step are n o t atfected by the initial
state o f vergence.
The phase lag o l vergence in response to a sinusoidal
m odulation o f disparity is m uch smaller than one would
predict from the 160 ms latency to a step stimulus. Although
sinusoidal m odulations o f disparity produce shorter latency
responses than irregular m odulations, che difference is not
large enough to account tor the difference betw een sinusoi­
dal and step stimuli (Z u ber and Stark 1968; Krishnan et al.
1973b ). But the difference between phase lag and latency is
a mystery only if one believes that vergence is controlled by
a single-channel linear system. In a nonlinear system the
phase lag to a sm oothly varying stimulus can n ot be pre­
dicted trom that to a discretely varying stimulus. Large and
small disparities tap distinct channels in the disparity-
codingsystcm , and these channels may have different laten­
cies (Section 11.4.1).
In the above studies, phase lag was less tor a sinusoidal
m odulation o f disparity than for an unpredictable sm ooth
m odulation. This suggests that the vergence system has a
prediction operator. A step change in disparity compared
with a tem poral modulation o f disparity should reveal the
presence o f a predictor more clearly. Krishnan et al. (1 9 7 3 b )
found that vergence latencies to unpredictable step changes
in disparity o f a vertical bar were betw een 130 and 2 5 0 ms.
Latencies to regular (predictable) square-wave changes in
disparity were considerably shorter. The advantage o f pre­
dictable stimuli was greatest ac a frequency o f disparicy
m odulation o f 0.5 H z. At this frequency, vergence responses
som etim es anticipated the changes in a regular stimulus.
Kum ar c t al. (2 0 0 2 ) tound that many subjects made
anticipatory vergence responses to step changes in depth o f
an L E D that occurred at regular intervals o f 1.25 s.
A nticipatory responses were rare ro irregular step changes
in depth.
W hen subjects initiated, and therefore ancicipaced the
before the scimulus moved (E rkelen secal. 1989a). However,
when subjects manually tracked a vergence stimulus moving
sinusoidally in depth at various frequencies, vergence lag
was no smaller than when the target was tracked by ver­
gence alone (Koken and Erkelens 1993).
Vergence latencies o f less than 6 0 ms have been reported
in monkeys in response to step disparities in textured stimuli
subtending 4 0 by 40° (Busettini et al. 1 9 9 6 ). These short-
latency responses were not due to the independent response
o f each eye to the m otion o f its retinal image, because both
eyes responded even when image m otion was confined to
one eye. The initial acceleration o f the vergence response
monkey had made a 10” conjugate saccadic eye movemenc.
A version movement is also speeded up after a saccadc.
Postsaccadic enhancem ent depended at least in part on reti­
nal m otion arising from a saccadc. Thus, it occurred after
 W ith large textured displays, the velocity o f the initial
100 ms o t vergence depended on the size ot chc disparity
step (B u settin i e t al. 1 996). However responses to steps
greater than about 2° tended to be in the convergence direc­
tion whatever the sign o f the disparity. This was probably
because sign o f disparity in a textured display becom es
ambiguous with large disparities. Convergence must be a
default response to an am biguous stimulus.
Sym m etrical vergence to a target m oving along the m id­
linc in natural visual surroundings kept up with the stim u­
lus with an accuracy o f abou t 98% tor stimulus velocities up
ro about 4 0 7 s (Erkelens et al. 1989a). At higher stimulus
velocities, vergence progressively failed to keep up with the
stimulus. However, perform ance was better when the move­
m ent o f the stimulus was controlled by the su bject rather
than by the experim enter. W h en vergence was evoked by a
voluntary to-and-fro m otion ot the su b jects head and
upper torso with respect to a stationary target, vergence
velocity kept up to stimulus velocity w ith an accuracy o f
over 9 0 % for stimulus velocities up to lOOVs. Erkelens et al.
did n o t move the su b jects head passively, so we do not
know w hether the extension o f high gain to higher veloci­
ties was due to the voluntary
d m otion o f the head or to a
contribution from stim ulation o f the vestibular system. The
vergence velocities reported by Erkelens et al. are much
higher than those reported by I.udvigh and M cK innon
(1 9 6 8 ) for an isolated bar under the control o f the
experimenter.
Pobuda and Erkelens (1 9 9 3 ) explored the relationship
between vergence velocity and stimulus velocity bv com ­
paring closed-loop responses to a stim ulus that changed in
disparity by 8 “ in 1 s, either sm oothly or in tw o, four, or
eight steps. The pattern o f changing vergence was approxi­
mately a low-pass filtered version ot the change in disparity
with a lag o f one reaction time. Vergence was not sensitive
to the velocity o f changing disparity as such, since the time
course o f the overall response was sim ilar in the sm ooth
and stepped conditions. Л m odel o f the vergence system
based on these features o f the response is discussed in
Section 10.5.11.
Appropriate vergence m ovem ents were evoked when
the stim uli in the tw o eyes differed in lum inance by up to
1.6 log units, although vergence velocity decreased as the
luminance difference increased further (M itch ell 1970).
1 0 .5 .8 b O p e n -I.o o p V ergen ce
The dependence ofvergence velocity on the initial disparity
o f the stimulus can also be investigated by an open-loop
procedure, in which vergence and disparity are linked so as
to keep disparity con stan t. W ith steps o f up to about 1°,
velocity o f open-loop vergence was approximately propor­
tional to the size o f disparity (Rashbass and W estheim er
1961a). O n e su bject showed a 10°/s increase in velocity for
each Г increase in disparity. In the initial phase o f a normal
closed-loop response, before feedback had tim e to be
effective, vergence velocity was approximately proportional
to disparity up to a value o f about 4°. This suggests that the
open-loop transfer function o f the vergence system involves
the conversion o f the initial disparity signal into a velocity
signal. Mays et al. (1 9 8 6 ) suggested that, as the response
proceeds, the velocity signal is integrated into the position
signal required ro m aintain the eyes in their new state o f
vergence.
Erkelens (1 9 8 7 ) used open-loop crossed-disparity steps
from 0.25 to 10° for a vertical bar, a cluster o f random dots,
and the inner region o f a random -dot stereogram. For all
stimuli, maximum velocity ot convergence increased steeply
with increasing disparity up to about 3" and continued to
increase up to a disparity ot about 4*, after which it declined
to zero at about 9° (Figure 10.32). Although vergence veloc­
ity differed widely betw een subjects, the shape o f the fu n c­
tion relating velocity to disparity was much the same for all
subjects. W h en large angles o f convergence were reached,
velocity decreased until vergence saturated betw een 25° and
35°. Responses to open-loop disparities o f more than 2°
were n o t sustained. Convergence was faster than diver­
gence.
Figure 10.33 shows convergence to open-loop steps in
disparity from an initial value o f about 2.5° obtained by
Pobuda and Erkelens (1 9 9 3 ). Vergence velocity to each step
was initially constant and then declined to produce a co n ­
stant m aintained angle o f vergence. Both the initial velocity
and the magnitude o f m aintained vergence increased with
increasing size ot the disparity step.
Retinal disparity (deg)
Figure 10.32. I train ee velocity an d open-loop disparity. Peak vcrgcncc velocity
as a function o t steps o f crosscd disparity between rctinally stabilized
images o f a vertical bar (dotted line) and a random -dot stimulus (line).
Bars are standard deviations (N = 5). < K c J r»w o fr«.m F A c {c m i**?)
 peak amplitude o f disparity m odulation o f t h e stimulus.
This is the closed-loop gain. The gain and phase lag o t ver­
gence o f a young su bject made in response to boch predicc-
able and unpredictable sinusoidally changing disparity o f
amplitude 3.5° in a pair o f vertical lines at a m ean distance
o f 1.75 in are shown in Figure 10.34. G ain was close to 1
(zero decibel loss) tor frequencies up to about 1 Hz and fell
o ff above 1.5 Hz (K rishnan cc al. 1973b ). Phase lags were
considerably less with predictable than with unpredictable
changes in disparity.
Erkelens and C'ollewijn (1 9 8 5 c ) measured the gain and

Tim e (s)
phase lag o f vergence responses evoked by sinusoidal oscilla­
tion o f horizontal disparity ot the whole ot a random -dot
Figure ЮЛЗ. T im e course ofop en -loop tergence. T im e cou rsc o t sym m etrical stereogram. The stereogram had a 15° by 15” area wich a
o p e n -lo o p vcrgcncc to d isparity steps up to 1.5*. (*f t l l l l Erkclrnt 1993
I V .U o Ji J l lli
crossed disparity o f 3 6 arcm in with respect to a 30° by 30°
w i t h l .in J p c r e s м а н г о f r o m S f u i a g c r S o e n c c - f t B u u n m M e J w i )

background. For amplitudes o f disparity modulation

between 1° and 5 Cthe gain o f vergence was between 0.8 and
1 at a frequency o f 0 .2 5 Hz (Figure 10.35). There was an
1 0 .5 .S c A d a p ta tio n o f V c rg c n c c V c lo c itv accelerating drop in gain with increasing stimulus am pli­
tude. A t a certain magnitude o f disparity, chac varied from
Vergence dynamics to a given disparity stim ulus may be
su bject to subject, che response suddenly scopped. Gain was
modified by preceding responses. Repetitive convergence
more closely relaced со scimulus peak velocicy o f image
ro large step stim uli increased the peak velocity o f subse­
oscillation than to frequency or am plitude. The change o f
quent responses to smaller step stimuli. Repetitive conver­
closed-loop gain with changing am plitude demonstrates
gence or divergence to small step stim uli decreased the peak
that the system is nonlinear. The phase lag o f vergence was
velocity o f convergent or divergent responses to large
about 20° at a frequency o f 0.25 Hz and increased to about
step stim uli (Yuan and Sem m low 2 0 0 0 ; Alvarez et al.
100° ac a frequency o f 1.5 Hz in much the same way
2 0 0 5 b ). In both cases, peak velocity rapidly returned to its
norm al level.
M unoz e t al. (1 9 9 9 ) induced large errors in vergence by
introducing a 4° disparity step while subjects changed co n ­
vergence in response to a pair ot vertical lines changing in
disparity ac 16°/s. Betw een five and ten convergence or
divergence training trials produced an increase in the veloc­
ity and magnitude o f response to a test stimulus consisting TJ.
o f a simple 4° step. The effect faded after about 5 responses s
ЛЗ

to the test scimulus. Sim ilar changes were evident when the
test step was exposed for only 100 ms and removed before
che eye movemenc began. This shows chac chc adapcacion
was in the initial open-loop phase o fth e vergence response.
Takagi et al. ( 2 0 0 1 ), also, induced adaptive changes in
convergence. In the 30-m in u te training session the stimulus-
stepped from 2 to 1 m and then, w ithin the 2 0 0 ms open-
loop reaction tim e ro chis stimulus, it stepped to eicher
0 .7 m (signal increase) or со 1.4 m (signaldecrease). Training
wich che signal increasing caused che duration o f accelera- % -5

cion ot che initial response to a 2 to 1 m step to increase. | -1 0

Training wich the signal decreasing decreased che peak
-1 5
acceleration o f che initial response.
-20
0. 01 0.1 1.0 10
1 0 .5 .9 V E R G E N C E G A IN A N D P H A S E LA G Frequency o f disparity m odulation (Hz)

1 0 .5 .9 a C lo s c d -L o o p V c rg cn cc G a in Figwc m.v». C ain a n d p b a ie la g o f vergence. Phase lag and gain o f vcrgcncc

to p redictable and unp redictable sinusoidal changes in disparity as a
For a sinusoidal variation in stimulus disparity, vcrgcncc fu n ctio n o f tem p o ral freq u en cy o f disparity m od u lation a t am plitude
gain is defined as peak am plitude o f vergence divided by 1.7 5 m eter angles (N = 1). {R«lr««n r»>mKmbum « J.

P e a k velocity o f im a g e v e r g e n c e (d e g 's )
10. 35 . lo g a s c c g a in a n d stim ulus r elm sty. V clocicv gain o f h orizon tal
v crg cn cc a s a fu n ccion o f p eak v elocity o f im age v crgcncc for three
am plitudes o f im age v crgcncc (N = 4 ) . (Redraw/romErUmMilCollcwijn IVBSc)
for all amplitudes. This suggests that phase lag results from
a constant delay o f about 2 5 0 ms.
The influence o f stimulus area on vergence gain was dis­
cussed in Section 10.5.5.
10 .5 .9 b O p e n -L o o p Vergence G ain
There are two types o f open-loop gain; that determ ined for
the initial response and that determ ined for a persisting
response. For about the first 2 0 0 ms ot a vergence response
the response is n o t affected by changes in changes in rhe
disparity o f the stimulus. The response is therefore open
loop during this initial period. The am plitude o f the initial
response divided by the am plitude ot initial stimulus dis­
parity is the open-loop gain o f the initial response (Jon es
1980). The peak amplitude o f vergence to a 200-m s flashed
vertical line increased nonlinearly with increasing stimulus
disparity with respect to the position o t tonic vergence,
reaching a maximum at a disparity betw een 2 and 3° (Figure
10.36). The m agnitude o f the initial response is indepen­
dent o f stimulus duration (Sem m low et al. 1993).
An open-loop vergence gain ot a persisting vergence
response can be obtained by coupling the stimulus disparity
C rossed U ncrossed
V ergence a m p litude (deg)
ь*пгс io. w. lirg cn tc am plitu de a n d disparity. T h e peak am p litu d e o f
vcrgcncc in response to a 200-m s flashed stim u lu s as a fu n ctio n o f
b in o cu lar disparity. C u rv e A is from a su b ject show ing a sym m etrical
response to crosscd and uncrossed stim u li. C u rv e В is from a su b ject
w ho responded on ly to uncrossed disparities. [™<, svso)
to the vergence response so that disparity remains constant
during the response. In this case, the constant disparity acts
as a persisting error signal, which drives the response to
large amplitudes (see Section 3 .3 ). W e return this question
in the next section.
1 0 .5 .1 0 T R IG G E R A N D F U S IO N -L O C K
COM PON EN TS
1 0 .5 .1 0 a B asic Facts
Vergence can be triggered by stim uli with large disparities
even when the stimuli occur on opposite sides o f the mid-
line so that they project to opposite cerebral hemispheres
(W inkclm an 1953). I lowevcr, responses to large disparities
are transient when the images are n o t sim ilar in shape.
Vcrgcncc is m aintained on an o b jcct to w ithin about 2
arcmin only when the images are sim ilar and fall within
Panum s fusional area (Riggs and N ichl 1960). The transient
and sustained com ponents o f vergence will be referred to as
the trig g er co m p o n e n t and the fu sio n -lo ck co m p o n e n t
respectively.
The two com ponents arc seen m ost clearly in responses
to open-loop disparity. For instance, Erkelens ( 1 9 8 7 ) found
that open-loop disparities o f up to 2°, in both line and ran­
dom -dot stereogram s, caused the eyes to converge between
15 and 2 5 е and remain in the converged position for as long
as the stim ulus lasted. Thus, for open-loop disparities up to
2° the response was sustained. O pen-loop disparities o f 2 to
5° drove the eyes to a convergence o f up to 35°, but the eyes
drifted back to a vergence o f less than 5". In this case, the
initial response was transient. For disparities larger than 5°,
the eyes moved to a less extreme position and the response
was also transient and som etim es did not occur.
Like Jo n es (1 9 8 0 ), Erkelens found that the disparity at
which vcrgcncc becam e transient was the same as that at
which the images were no longer fused. Thus, transient ver­
gence is initiated by disparities well outside the fusional
range, and vergence is m aintained by disparities small
enough to provide a fusional lock.
Erkelens also found that a transient response to a large
open-loop disparity reduced response velocity to other
stimuli presented subsequently, but only when they had
similar disparities. Thus, the short-term adaptive process
responsible for the transience o f the trigger com pon ent to a
given disparity is restricted to a given range o f disparities.
1 0 .5 .1 0 b F u n ctio n s o f Trigger and
F u sio n -L o ck Vergence
Transient vergence to large disparities serves useful fu n c­
tions. In rhe first place, the initial high-velocity response ro
a step change in disparity rapidly brings the gaze close to the
target plane, where small fixation errors can be easily
detected. A second rapid vergence response may occur
when chc initial response docs noc bring fixacion near chc
target plane. Alvarez cc al. (2 0 0 0 ) produced evidence chac
second rapid responses arc evoked by che sense o f eye posi­
tion rcalfcrcnce rather chan by a visual error signal.
W h en a person decides со change convergence, che large
disparities in the target plane trigger an appropriate tran­
sient response. O n ce the images o f objects in the target
plane have been fused, large disparities arising from objects
in other depth planes should be ignored until a decision has
been made to change convergence again. I f large disparities
in nontarget depth planes were not ignored, the vergence
system would never be able со settle down inco a desired
scace. Subjects have no difficulty in making appropriate ver­
gence movcmcncs со voluncarilv selected parts o f random -
doc scereograms, even chough chis causes nonselected
elem ents со becom e disparate (Erkelcns and Collew ijn
1991).
A fter locking onco a cargec chc vergence syscem should
concinue со respond со small disparities due to movements
o f t h e target or to vergence drift. If disparities are averaged
over a local spacial region che eyes may noc converge pre­
cisely on an o bjecc when chere are neighboring objcccs in
nearby depth planes. This should n o t m atter because small
vergence m ovem ents would noc cause images o f a fixaced
o bjecc to fall outside Panum s fusional area, and would not
disturb detection o f relative disparities in the visual scene.
Also, vergence changes betw een neighboring objects
should help observers to build a representation o f the
3-dim ensional structure o f che local region.
1 0 .5 .1 0 c T ra n sie n t V erg en ce со
D iss im ila r S tim u li
Vergence can be triggered by stim uli that differ in shape, but
chc response is noc m aintained in chc absence o f m atching
features that provide an error signal for fine vergence co n ­
trol (W escheim er and M itchell 1 9 6 9 ; Jo n es and Kerr 1971;
Jon es 1 9 8 0 ). For instance, dichopcic vertical lines with 2° o f
horizontal disparity evoked sustained vergence, buc the
response was transienc when one ot the lines was horizontal.
The response to dissimilar stimuli is transient even for
disparities that normally evoke a sustained response. B rief
exposure to a pair o f sim ilar stimuli and long exposure to a
pair o f dissimilar stimuli evoke the same transient response,
which is n o t m aintained because neither pair o f stim uli is
fusible. The sim ilar stim uli do not fuse because o f the b rief
exposure, and the stimuli w ith long exposure do not fuse
because thev are dissimilar.
W estheim cr and M itchell used only one pair o fd ich o p -
tic images and their subjects may have converged volun­
tarily. Jon es and Kerr (1 9 7 2 ) overcame this problem by
using a vergence compecicion paradigm in which one eye
saw a foveal scimulus and chc ocher eye saw scimuli on boch
sides o f chc fovea. Thus, che subject had chc ch o ice o f c o n ­
verging or diverging. They presenccd a pair o f similar and a
pair o f dissimilar dichopcic images briefly ac chc same time.
It was found that a transient response was just as likely to be
triggered by chc dissimilar pair as by che sim ilar pair (Jon es
1 9 8 0 ; Jo n es and Kerr 1 9 7 2 ; Scm m low ec al. 1986).
Transient vcrgcncc со dissimilar dichopcic scimuli, such
.is horizontal and vertical lines, may be triggered by che
com m on low spacial-frequency com ponencs o f che scimuli.
Edwards ec al. (1 9 9 8 ) invescigaced chis issue using che ver­
gence compecicion paradigm. Subjeccs were prescnccd for
5 0 0 m s wich a G abor foveal pacch to one eye and a pair o f
G abor patches to the o ther eye, one 2.5° to the left and the
other an equal distance to che righc o f che fovea. The d ich o p ­
cic pair ot images wich the highesc mean lum inance contrast
determ ined che direccion o f vergence, even when chc images
differed in concrasc. Vergence was also decermined by che
pair o f images chac concained che lowest spatial frequency.
Thus, cransienc vergence is decermined by dichopcic images
wich che highesc com bined contrast w ithin a low-pass
spatial-scalc channel.
Pope ec al. (1 9 9 9 ) used the same compecicion paradigm.
They found chac, although an orthogonal pair o f (labor
patches or a pair wich opposice luminance polaricy could
induce vergence, chere was a bias in favor ot responding со
images chac macched in oriencacion or polaricy. As chc inicial
disparicy o f che images increased from 2.5° to 5°, the vergence
system became increasingly indifferent to whether the images
matched in orientation or luminance. The system was most
selective for orientation ac a spacial frequency o f 2 cpd.
D earw orth ec al. (2 0 0 5 ) conducccd a sim ilar experimenc
on monkeys. They were prescnccd for 5 0 0 ms wich cwo
idencical scereoscopic scimuli, one nearer anil che ocher an
equal discancc beyond a prcfixacion stimulus. All the m on­
keys showed a bias coward converging on che near scimulus.
As the luminance contrast ot the tar stimulus was increased
relative to that o f the near scimulus, chc m onkeys began со
respond со che far scimulus. Also, response latency was less
for whichever stimulus had che higher contrast.
The above evidence suggests that transient vergence is
evoked by a low spatial-frequency signal derived from che
contrast envelope o f the stimuli. Sato et al. (2 0 0 1 ) asked
how similar in size the contrast envelopes o f G abor patches
with 3.8° o f crossed disparity must be to evoke transient
vergence when in com petition with G abor patches with
3.8° o f uncrossed disparity. The probability o f vergence to
the G abor patches decreased as the ratio o f the sizes o f che
envelopes increased from 1:1 со 1:8. Initially, chc lum i­
nance-defined gracings (carriers) in che dichopcic G abor
patches were orthogonal, and their spatial frequencies were
scaled by envelope size. This ensured chac chere was no scim­
ulus for sustained vergence. However, changing the relative
envelope size had the same effect whatever the relative o ri­
entations or spatial frequencies o f t h e carriers. Thus, tran­
sient vcrgcncc is determ ined by che relative overall sizes o f
the dichopcic scimuli. The syscem does noc require chc
decailcd structure o f the stim uli to be matched.
interludes were transient responses. Their constant main-
sequence characteristics persuaded Sem m low et al. that
they were preprogrammed, or ballistic, movements based
on sam pling accum ulated disparity in the ramping stim u­
lus, in contrast to the proportional control o f sustained
responses. The main sequence takes account o f only the
first-order com ponent o f the system. Alvarez c t al. (1 9 9 9 )
developed a procedure for revealing che second-order co m ­
ponencs ot che transient and sustained systems. A model o f
these processes is described in Seccion 10.5.11.
W ich rapidly changing disparity ramps, vergence lags
chc scimulus and disparity error accumulates to a level chac
triggers a transient response, which in turn restores the dis­
paricy error со wichin chc range o f che suscained mechanism.
W ith gradual ramps, disparity error does not accumulate to
chc level required со crigger a transient response.
Analogously, voluntary pursuit ot a target moving in the
frontal plane is incerrupced by cacch-up saccades when the
target moves to o rapidly. A lternating fast and slow vergence
does not occur when the stimulus ramp is presented in
open-loop m ode (Erkelens 1 9 8 7 ; Pobuda and Erkelens
1993). U nder these conditions, the disparity error is c o n ­
stant, since the m ovem ent o f the stimulus is coupled to that
of' the eyes.
1 0 .5 .1 0 c S u m m a ry
9
Vergcnce can be triggered by nontusible scimuli or by stim -
uli oucside che fusional range. Buc ic is noc maincained in a
given scace unless che fusion-lock mechanism is engaged by
fusible scimuli. In a norm al environmenc we see a multitude
o f disparate scimuli, each capable ot triggering a vergence
movem ent. W h en we decide со change fixacion from one
distance to another we disengage the fusion-lock m echa­
nism, allow the new visual o b ject to crigger an appropriace
vergence response, and reengage the fusion-lock process. If
a new fusible stimulus does not occur after the trigger
response, vergence is noc m aintained in the new position.
Th e response is therefore cransient. If a fusible scimulus
com es in to view, the fusion-lock m echanism is engaged and
che response is suscained. There is some debace abouc the
differenc dynamics o f the tw o types o f vergence.
Sustained an d transient responses have not been studied
in vertical vergence or cyelovergence.
1 0 .5 .1 1 M O D E L I N G T H E
V E R G EN C E SYSTEM
G eneral m ethods in the construction o f m odels o f senso­
rim otor systems were described in Section 3.3. Rashbass
and W estheim er (1 9 6 1 a ) developed the first model o t the
vergence system. It was a linear model with continuous
feedback and a 160-m s delay elem ent in the feedback loop.
Vergence can be m aintained on a target with reasonable
accuracy in two ways. A neural integrator could derive the
final state ofvergence from the integral o f response velocity.
Alternatively, the system could have a high internal-loop
gain, defined as eye velocity per unic image disparicy, which
would allow small error signals со bring vergence close со ics
desired scace. Krishnan and Scark (1 9 8 3 ) also developed a
linear model under continuous sensory con trol, unlike the
ballistic saccadic system. The model incorporates two paral­
lel controllers. The firsc has fasc, cransicnc (derivacive)
dynamics with an eye-velocicy output proportional to the
instantaneous magnitude o f disparity one reaction cime
earlier. This com ponenc contributes to the initial response
only. The ocher com pon ent has slow, conic dynamics (cime
conscant 15 s) with a leaky output related to the integral o f
eye velocity. The leaky oucpuc accounts for the slow drift o f
the eyes back to a resting state in the dark. Each controller
has its own internal-loop gain, and the cwo are com bined
with a pure delay o f 160 ms.
O n e weakness o f Krishnan and Stark s model is th at it
produces too slow a response to step inputs when the in ter­
nal-loop gain o f the integral controller is set low, and pro­
duces oscillations when it is set high. Perform ance could be
improved by making che concrollcr responsive со che pre­
dicted posicion o f che cargec, but this would work only for
predictable movements. It has already been pointed out
that vergence stability does n o t depend on whether the
stimulus is predictable. Perhaps the phase lag o f one o f che
control elements, when operating in a continuous tracking
mode, is less than would be predicted from the latency o f
vergence in response to disparity steps, and thi s may account
for the otherw ise puzzling stability of the real vergence
syscem (Rashbass 1981).
Krishnan and Stark s model deals with the nonlinear
asymmetry between divergence and convergence by adding
an asymmetry in the internal-loop gains. The compressive
nonlinearicies o f che vergence syscem in chc form ofsacurac-
ing levels o t velocity and amplitude, and nonlinear interac­
tions between vergence and version are noc incorporaced
inco che model. N onlinearities arising trom high-level co n ­
trol ofvergence, as when a person decides to respond со one
ot several disparities, are also n o t in the model.
S ch or and Koculak (1 9 8 6 ) developed a model chac
incorporates interactions betw een vergence and accom m o­
dation (Figure 10.39). Iccon cainsan incegracor wich ashore
tim e constant that accounts tor the initial response and an
integrator wich a long cime constant chac accouncs for adap­
tive changes in tonic vergence. N onlinear saturation ele­
ments turn o ff the integrators when che oucpuc reaches a
certain value, so as to prevent overshoot.
Z ee and Levi (1 9 8 9 ) proposed che model shown in
Figure 10.40, which incorporaces che contribution o f che
saccadic system to vergence and the adaptive plasticity o f
the vergence system (Section 10.2.5). C ova and Galiana
(1 9 9 5 , 1996) proposed a neural model o f interactions
betw een version and vergence that are discussed in the next
section. Patel c t al. (1 9 9 7 ) developed a neural netw ork
 |пРи| Fast C ro s s lin k s T o nic adaptation P la nt O utput
elem ent w ith lim ited input

figure 10.19. M od elo fv erg en te oetotn m odation . M u tu al in tera ctio n s b etw een v crgcncc and acco m m o d atio n system s o ccu r b etw een the phasic and to n ic
neural in teg rators in th e feedforw ard paths. Inputs to the to n ic in tegrators have a satu ration lim it, w hich could p rod u cc am p litu d e-d ep en d en t
n o n lin ca ritics o f A C / A and C A / C ratios. T ran sfer fu n ctio n s arc in d icated by Laplace tran sform s. (Кс-г..™ ь .» Schat Kombk \wi)

V ergence efference
V ergence Del ----------------- < ------------- Plant
angle

Retinal Desired V ergence error

T arget Vergence
disparity vergence
vergence position
+ ) V ergence V ergence
1 burst integrator

V ergence velocity
------------------ * ---------

Figure ю.чо. O utline o f a 7/1o il c l o f th e vergence m echanism . A desired angle o f vergence is derived by adding retinal disparity to the present vcrgcncc angle.
Feed back from cclls carryin g v elocity an d p osition signals (b u rst-to n ic n eu ron s) passes throu gh an in tern al m od el o f the o c u lo m o to r p lan t and
a co m p en satin g tim e delay (H c l). T h e d ifferen ce b etw een desired vergence state and th e feedback signal provides a v crgcn cc-crro r signal, w hich
drives vergence* burst n eu rons. Burst neu ron s provide a v elocity signal to o cu lo m o to r nuclei an d . bv in teg ratio n , a v crgcncc p osition signal w hich
m ain tain s th e desired final state. (ReJn«n бот /сслп.1 Uv. iss?)

model o f horizontal vcrgcncc» w hich takes in to account the
nature o f the inpuc disparity signal and che m otor oucpuc
signal. T h e model incorporates adaptive nonlinear control
involving both position and velocity signals and both open-
and closed-loop responses.
Pobuda and Erkelens (1 9 9 3 ) proposed that vergence
signals arc processed through several parallel channels each
with a gain elem ent and a leaky integrator conferring low-
pass characteristics. The gain o f each channel is specific to a
particular range o f disparity amplitudes. As an eye move­
m ent in response to a given disparity progresses, control
passes from chc channcl sensitive со large disparities to chac
sensitive to small disparities. The channels are insensitive to
the rate o f change o f disparity. Pobuda and Erkelens also
proposed chac the overall lag o f che system is com prised o f a
delay o f betw een 8 0 and 120 ms in chc vcrgcncc-proccssing
loop, plus a lag in che m echanical plane. The lag in che pro­
cessing loop is less chan che 160 ms assumed in chc ocher
models and describes che small phase lag in che response со
sinusoidal scimuli, which ocher models do noc explain. The
model also incorporaces a slow incegracor, like that
proposed by Sch or ( 1979a), to accounc tor adapcacion o f
conic vergence. A lthough each o f the channels is linear,
their com bined action introduces a nonlinearity which
causes che gain o f che response со vary with stimulus
amplitude.
A “dual-m ode” model o f disparity control (Figure
10.41) has been developed from chac o f Z ee cc al. by
Sem m low ec al. (1 9 8 6 ), H unger al. ( 1 9 8 6 ), and H orngec al.
(1 9 9 8 a ). A lasc initial preprogrammed response is produced
by a pulse-scep mechanism wich dynamics chac are indepen-
denc o f scimulus duration or size, since the response does
noc depend on error feedback. The inicial response is fol­
lowed by a slower one under feedback control. The o cu lo ­
m otor musclcs arc represented by a first-order plant with a
m ean tim e constant o f 2 6 5 ms. The output o f the pulse gen­
erator is derived from the ditfcrcncc betw een chc scimulus
seep and a delayed internal feedback signal. The model also
concains a nonlinear racc-limiccr and an amplitude satura­
tion elem ent. The pulse signal feeds directly to the plant
and also drives a leaky step incegracor. The sum o f chc pulse
and step signals drives che muscles.
 The vertical fusion range can be increased by exposure
to prisms that increase vertical vergence demand. Luu et al.
( 2000 ) found that the m ajority o f subjects increased their
total fusional range (b o th directions) by betw een 1 and 2 D
after 15 m inutes o f prism training per day for 1 week. The
change persisted over a period o i 3 m onths. However, som e
subjects showed no change.
I he range o f vertical vergence is the maximum am pli­
o b ject from the point o f convergence. Thus, horizontal dis­
tude o f actual vergence movements. It is best determ ined by parity provides inform ation about relative depth between
measuring the m ovem ents o f the eyes in response to vertical
disparities impressed on dichoptic images presented in a
stereoscope. Kertesz (1 9 8 1 ) used scleral search coils to m ea­
sure vertical vergence evoked by the stimulus shown in
Figure 10.44. For one subject, the maximum vergence in
one direction was 1.9° for a disk subtending 5°, 3.5° for a 1 0°
disk, and 5.2° for a 5 7 .6' disk.
1 0 .6 .2 V E R T I C A L P H O R IA
Many people have a v ertical p h o ria chat m anifests itself as
an elevation o f one eye relative to the o ther when there is no
fusional stimulus. A vertical eye m isalignm ent in the pres­
ence o f a fusional stimulus is a vertical fixatio n d isp arity or
a vertical strabismus (see Section 10.2.4).
Sideways tilt o f the head is accom panied by counter­
rolling o f the eyes and vertical vergence. The eye on the side
o f the lower ear is elevated relative to the other eye
(K ori et al. 2 0 0 1 ). D issociated vertical d eviation (D V D )
is an exaggerated vertical vergence induced by head tilt to
one side (Van R ijn et al. 1 9 9 7 ; Cheesem an and G uyton
1999). It is associated with congenital esotropia. It
seems that it is due to a lack o f binocular control over eye
m ovem ents (Brodsky 1 9 9 9 ). Patients typically tilt the head
to the side away from the eye with the larger am ount o f ver­
tical deviation. This helps to reduce the deviation (Santiago
and Rosenbaum 1 9 9 8 ). People wich normal binocular
vision may show asymmetrical vertical phorias that resem­
ble mild dissociated vertical deviation (Van Rijn et al.
1998). The vertical vergence com ponent o f D V D partially
damps nystagmus associated with D V D (G uyton c t al.
1998).
The eyes o f m onkeys and humans tend to develop a ver­
tical phoria when one eye is occluded for several hours o f
days (V tirre e t al. 19 8 7 ; G ra f et al. 2 0 0 2 ). Also, we saw in
Section 10.6.1 that the vertical alignm ent o f the eyes is
easily modified by wearing prisms.
1 0 .6 .3 T H E S T IM U L U S F O R V E R T IC A L
VERGEN CE
1 0 .6 .3 a The R a n ge o f Vertical Disparities
Th e smallest vertical disparity required to initiate vertical
vcrgcncc, as indicated by displacem ent o f nonius lines, was
about 1 arcmin for stimuli presented for 2 s at eccentricities
o f up to 4°. The threshold disparity was higher for stimuli
presented for only 160 ms at eccentricities greater than 4°
(D uw aer and van den Brink 1981b). U nder all conditions,
the disparity threshold for initiation o f vertical vergence
was much smaller than the disparity at which singleness o f
vision was lost.
H orizontal disparity increases with the depth of the
points in the visual field. The horizontal disparity o f an
o b ject at infinity is 14° relative to an o b ject at 25 cm . Images
with a horizontal disparity o f more chan abouc 0.5 " cannoc
be fused, and a disparity of m ore than about 2 ° cannot be
detected by disparity detectors. O utside the 2 " range, che
horizontal convergence mechanism must therefore use cues
to depth o ther than disparity to bring an o b ject o f interest
w ithin range o f the disparity-detection system. Even when
the eyes are converged on an objecc, che space around che
o b ject may contain objects with a wide variety of horizontal
disparities. For m ost precise detection o f relative disparities
in the region o f interest, one needs to be able to converge on
one o b ject and ignore neighboring disparities. This means
that horizontal vergence must be controlled by disparities
in a local region.
Vertical disparity does n o t vary with distance ior objects
viewed in the normal way in the horizontal plane o f regard
or in the median plane. Therefore, it does n o t provide in for­
macion abouc absolute o r relative depths in these planes.
But vertical disparity increases with eccentricity and
decreases with absolute distance w ithin each quadrant ot
the visual field. Even in extrem e eccentricities, vertical dis­
parities are only about 1.5°, which is within range o f the
disparicy-dececcion system. Thus, unlike horizontal ver­
gence, vertical vergence does not need to be evoked by cues
to depth o ther than disparicy.
For a series o f objects at different distances placed along
a line o f sight in che m edian plane, only che horizontal dis­
parity o f the objects changes with distance. A voluntary
choice must be made about which o b ject to converge the
eyes on. Along an oblique line o f sight, both horizontal and
vertical disparities change with distance, b u t horizontal dis­
parities change m uch more rapidly than vertical disparities.
Vertical vergence will be sufficiently precise if it is evoked by
the mean detectable vertical disparity in a fairly large region.
It is n o t nccessary to have attentional control over the stim ­
ulus evoking vertical vergence.
10 .6 .3 b F.fFects o f S tim u lu s A rea
Howard et al. (2 0 0 0 ) measured the gain and phase lag o f
vertical vergence tor m-scaled random texturcd displays.
The displays ranged in size from a small d ot to one 65" in
diameter. The vertical disparity o f the display was m odu­
lated sinusoidally chrough a peak-co-peak amplitude o f 0 . 5 °
at frequencies ot 0.1 and 1.0 H z. It can be seen trom
 H orizontal vergence (0.1 Hz)
V ertical ve rg e n ce (0.1 Hz)
r C yclove rg en ce (0.05 Hz)
a 0.6
О
0.4
0.2
0.0
1000 2000 3000 4000
S tim ulus area (deg2)
25 35 43 50 56 61 67 71
D iam eter o f ce ntral disc (deg)
Fifurr io.-*2. Л 'с effett o f stim ulus a r ta on rergcn te gain . T h e disparicy o t the
stim uli was m odulated sinusoidally a t the frequ ency ind icated o n cach
curve. T o p tw o curves from H ow ard c t д|. ( 2 0 0 0 ) . B o tto m curve from
H ow ard e t a l . ( 1 9 9 4 ) .
Figure 10.42 chat che gain o f che response increased as che
diam eter o f the display increased со 20 °, above which ic
remained reasonably constant. Phase lag decreased slightly
as stimulus diam eter increased to 20°. A central stimulus
with a diam eter o f 45° produced a response with higher
gain than a peripheral stimulus o f the same area (an annular
stim ulus w ith inner diam eter 4 5 ° and outer diam eter 65").
Thus, a central stim ulus is a more effective stim ulus for ver­
tical vcrgcncc than a peripheral stimulus o fth e same area.
The figure also shows how horizontal vergence and cy clo ­
vcrgencc arc affected by stimulus area.
Vertical disparity in a surrounding display induces per­
sistent vertical diplopia in a small cargec wich zero vercical
disparity (Burian 1 9 3 9 ; H outm an and van der Pol 1982a).
In Figure 10.43 it is impossible to fuse the central horizon­
tal lines when the surround has a vertical disparity. C entral
vertical lines with zero horizontal disparity arc easily fused
in the presence o f horizontal disparity in surrounding tex­
ture elements.
Su bjects could noc hold horizontal or vertical vergence
on a ecntral target when the vertical and horizontal dispari­
ties o f a 7.5° cexcured surround were simultaneously m odu­
lated up to 4 0 arcmin at 0 .1 2 5 Hz (Stevenson et al. 1997).
Induced vertical vergence was the same w hether subjects
attended to the stationary target or to the modulated sur­
round. Induced horizontal vcrgcncc was small when sub­
jects tried to fixate the stationary spot but had a gain o f
about 0.85 when they attended to the surround. This dem ­
onstrates that both horizontal vergence and vertical ver­
gence arc driven by a weighted mean o f com peting signals
from a certain area. People have some control over which o f
two com peting stimuli is used to drive horizontal vcrgcncc
but no control over w hich stimulus drives vertical vergence.
This difference is presumably related to the fact thac vertical
5000
76 80
Ш
* ШЯ i ■
■ v y - v y -л *
• Л 1 ■ V
в
Fi|v< in.-*}. Fusing centra! stun ulus teilb d isp arate surround. (A ) T h e central
h o rizo n tal lines c a n n o t be fused w hen the vertically disparate surround
is fused. ( B ) The cen tral vertical lines arc easy to fuse w hen the surround
has a h orizon tal disparity.
disparities do n o t change as abruptly over the visual field as
do horizontal disparities.
Induced horizontal and vertical vergence in subjects
trying to fixate a stationary point decreased with decreasing
area o r increasing eccentricity o f a textured surround m od­
ulated in horizontal and vertical disparity through 0.25° at
0.5 Hz (Stevenson et al. 1999). The decrease with increas­
ing eccencricicy was similar со che change in chc corcicai
magnificacion faccor.
1 0 .6 .3 c In ceraccio n s b ecw een H o riz o n ca l and
V ercical V erg en ce
The firsc quescion is whecher horizontal and vertical ver­
gence com ponents generated by an oblique disparity are
independent.
Stevenson c t al. (1 9 9 7 ) found that the am plitude o f an
oblique vergence is the sum o f the horizontal and vertical
com ponents measured separately, although they used only a
lim ited range o f vergence amplitudes.
Ram bold and M iles (2 0 0 8 ) used a large random-doc
display w ith a disparicy o f 0 .2 ° along horizontal, vertical, or
oblique directions. F.xposurc o f the stimulus for 150 ms
induced horizontal and vertical vergence responses that
approximately matched the amplitudes o f the tw o co m p o ­
nent disparities. W hen the same disparities were introduced
into a sinusoidal grating, the horizontal vergence remained
m uch the same as the grating changed from vertical to about
 0 — I------------------------------------1-------- 1-1— i— i - i - i - t - i . J -----------------1
0 .0 1 0 .1 0 .5 1 2
Frequency o f disparity m odulation (Hz)

Figure io.4%. 7be range ofverticaldisparity. S tim u lu s used bv P crlm u tccr and
K crtcsz (1 9 8 2 ). ‘

an am plitude o f 65 arcm in. Responses away trom the rest­

ing position were slower than those toward the resting posi­
tion (H outm an and van der Pol 1982b).
Perlm utter and Kertesz (1 9 8 2 ) used the stimulus shown
in Figure 10.44, which subtended 8.5°. An open-loop step
o f vertical disparity o f 14.8 arcmin produced a vertical ver­
gence with a reaction tim e o f 180 ms and a velocity o f
3 9 .6 7 s . The final amplitude o f 54 arcmin was maintained Frequency o f disparity m odulation (Hz)

tor 2 5 0 ms. T h e velocity ot vertical vergence was propor­

Fi4«rc io.-is. C ain an d phase lag o f v ertical vergence. G ain and phase lag
tional to the m agnitude o f disparity, as Rashbass and o f vertical v crgcncc as a fu n ctio n o t the freq u en cy o f sinusoidal
W csthcim cr (1 9 6 1 a ) had found tor open-loop horizontal m od u lation o f vertical disparity o f a 6 5 ° texturcd display. G in is plotted
vergence. The stim ulus shown in Figure 10.44 consists to r various am plitudes o t disparity as ind icated on th e curves. Phase
lag is p lo tted to r on ly the 18 arcm in am p litu d e. R esults tor o th er
o t 5 0 notched horizontal lines with an interline spacing o f 10
am p litu d es w ere very sim ilar. N = 4 . (AJ*ptcJfrom HowuJ « al. 1W )
arcmin. At every multiple o f 10 arcmin o f vertical disparity
many segments ot the horizontal lines com e into correspon­
dence and provide a stimulus tor vertical fusion. This stim u­
vertical vcrgcncc resemble the dynamics o f horizontal vcr-
lus is therefore a poor choice for studying vertical vergence.
gence and cyclovergence.
Howard c t al. (1 9 9 7 ) used scleral eve coils to measure
Step changes in vertical vcrgcncc involve disjunctive
the gain and phase o f vertical vergence. The 65° texturcd
saccades (Bush et al. 1 9 9 4 ; Van der Steen and Bruno 1995).
displays were m -scalcd to hom ogenize visibility and were
Furtherm ore, subjects show rapid adaptation o t disjunctive
aperiodic to avoid spurious binocular m atches, as shown in
saccades to unusual patterns o f vertical disparities (Section
Figure 10.27. The vertical disparity o t the display oscillated
10.8.3).
through peak-to-peak am plitudes o f betw een 18 arcmin
and 4° at frequencies betw een 0 .0 5 and 2 H z. The results arc-
shown in Figure 10.45. G ain was near 1 when the stimulus
oscillated through 18 arcm in at 0.1 Hz o r less. As the am pli­ 1 0 .7 CYCLOVERGEN CE
tude o f stimulus oscillation increased, vergence gain
decreased at all frequencies, which is evidence o f a n on lin ­
10.7.1 TYPES OF TO R SIO N A L RESPONSE
earity. G ain declined with increasing stimulus frequency
but was still abou t 0.5 at 2 H z tor an amplitude o t 18 arcm in. C y clo d u ctio n is the torsional state o f a single eye indicated
These results dem onstrate that vertical vergence is designed by the dihedral angle betw een the m edian plane o f the head
to com pensate for small disparities changing at moderate and the plane containing a specified meridian o fth e eye and
frequencies. the visual axis. The usual reference meridian is the normally
Howard et al. also found that phase lag increased vertical meridian as indicated by sclcctcd landmarks on the
from 10" at a stimulus frequency o f 0 .0 5 Hz to betw een 100 eyeball or by the apparent orientation o f the afterimage o f a
and 145° at a frequency o t 2 H z. O verall, the dynamics o f vertical line. Cycloduction is designated incycloduction or
cxcycloduccion, depending on w hether the eye is rotated
top toward or top away from the median plane o f the head.
C ycloversion is the equal com ponent o f che eyes’ cyclo-
ductions. Levocycloversion occurs when the eyes rotate top
to the su b jects left and dcxtrocyclovcrsion occur when they
rotate top right. Cycloversion is evoked under the following
circum stances:
1. R otation o f a frontal textured display around che
fixation point induces optokinetic cycloversion
(B rech er 1 9 3 4 ; C heu ng and Howard 1991).
2. Sm all am plitude cycloversion is evoked by a large
display o f lines or a visual scene tilted from the vertical
in the frontal plane (G oodcnough c t al. 1979; Panscll
et al. 2 0 0 6 ).
3. Cycloversion accom panies vertical vergence.
Left-over-right vertical vergence evokes a top-to-left
cycloversion and vice versa (E n righ t 1 9 9 2 b ; van Rijn
and C ollcw ijn 1994; M ikhacl et al. 1995). This
suggests that vertical vergence is controlled m ainly by
the oblique musclcs.
4. W h en the head tilts to one side, the eyes co u n terro ll
conjugatelv up to about 8" in che opposite direction
(C ollew ijn et al. 1 9 8 5 ; Ferman et al. 1987b ). In the
dark, the response is evoked by signals trom the
vestibular system and has a velocity gain o f about 0 .6 .
In the light, opcokinecic and vcscibular signals com bine
со increase velocicy gain со abouc 0 .7 2 (Leigh ec al.
1 9 8 9 ). In lateral-eyed anim als this reflex occurs in
response со picch o f che head and has a greacer
am plitude chan counterrolling in frontal-eyed
animals. In both cases, the response helps со keep
each image erect w ith respect to the principal
meridian o f che eye.
5. W ich excended practice,cycloversion can be evoked
voluntarily (B a llict and Nakayama 1978).
6. People wich congenital nystagmus exhibit co-and-fro
nyscagmic eye movemencs, predom inantly in the
horizontal plane. They also exhibit torsional oscillations
abouc the visual axes. These eye movemencs degrade
oriencation discrim ination, especially for vertical lines
(Ukw ade c t al. 20 02 ).
C yclovergence is the difference between the eyes’ cyclo-
ductions. Ic is designated incyclovergence or excyclover-
gencc depending on w hether the relative rotations arc
rop-in or top-ou t respectively. Cyclovergence is zero when
two horizontal nonius lines on opposite radii o f a dichoptic
display in che froncal plane appear collinear. Iс is best to use
horizontal rather than vertical nonius lines as a reference
because, under norm al circum stances, corresponding hori­
zontal meridians are parallel while corresponding vertical
meridians have a positive declination o f about 2° (H elm holtz
1909, vol. 3 , p. 4 0 8 ).
Stim ulus cyclodisparity, or d e clin a tio n , is the signed
relative rocation o f dichoptic stimuli in the frontal plane in
external coordinates (O g le and Ellerbrock 1946).
In clin a tio n refers to che slanc o f an objecc in che sagiccal
plane o f the head with respect to chc froncal plane, signed
positive top away. For interpupillary distance a, and obser­
vation distance d , a line in the sagittal plane with inclina­
tion i projects as a pair o f images with declination 9. It is
shown in Section 14.7 that:
Э л tan/ ф а ,„ ( л ^
tan —= — ■ ran—= ----- or (3= 2 arc tan • -----}
2 Id 1 ID I ID )
Forsm all0, 0 = a ГаП1 or / = arctan — in radians
d a
The image cy clo d isp arity o f a pair o f dichoptic images
is their relative orientation with respect to corresponding
retinal meridians, designated positive if the left-eye image is
rotated clockwise and the right-eye image counterclockw ise
with respect со che nearest pair o f corresponding retinal
meridians. D ich op tic images have zero cyclodisparity when
they are parallel to a pair o f corresponding meridians. Ic is
assumed char chey are parallel со corresponding meridians
when chey appear parallel.
The declination o f vertical corresponding meridians
causes che vercical horopcer со be inclined top away by an
am ount chat varies with viewing distance (Scctio n 14.7).
Cyclovergence chac accom panies a change in horizoncal
vergence may also affect inclinacion (Am igo 1 9 7 4 ). It fol­
lows from chese definicions o f disparicy chac, for horizoncal
lines, image cyclodisparity equals stimulus cyclodisparicv
minus cyclovergence. For vercical lines, image cyclodispar-
icy equals scimulus cyclodisparity minus cyclovergence
minus che declinacion o f corresponding vercical meridians.
Several invcstigacors over chc lasc 100 years, including
Hering (see O gle and Ellerbrock 1 9 4 6 ), V erhoeff (1 9 3 4 ),
Kcrccsz ( 1 9 7 2 ), and Krckling (1 9 7 3 ), have denied chac
cyclovergence occurs. The response is noc mencioned in
m ost texebooks. In som e cases, invcscigators changed cheir
m inds when chey used more effeccive scimuli, particularly
scimuli subcendinga visual angle in excess of 25° and con-
caining many horizoncal and vertical elements.
Cyclovergence is evoked by cyclodisparity (Kcrccsz and
Sullivan 1 9 7 8 ) and as a com pon ent o f horizontal vergence
(Allen and C arter 1967) and o f elevation of gaze and vcrci-
cal vcrgcncc (L c C o n cc 1864; F.nrighc 1 9 9 2 b ; C hccscm an
and Guycon 1999). C y clo p h o ria is a corsional misalign-
m cnc o f che eyes in che absence o f cyclofusional stimuli
{W ic k and Ryan 1982). C y clo tro p ia is a torsional m is­
alignm ent o f the eyes in the presence o f fusional stim uli
(Ruccum and Noorden 1983).
 10.7.2 МЕASUREM ENТ О F
CYCLOVERGENCE
The following psychophysical m ethods have been used to
m с as ure eye love rge nee.
1 0 .7 .2 a S e ttin g a L in e in th e M ed ia n
P la n e to V ertical
Th e observer inclines a test line in the m edian plane o fth e
head until it appears to lie in the frontal plane. The method
is based on the assumption that a line seen binocularly
appears vertical it and only it its images tall on correspond­
ing retinal m eridians, and that any error in the vertical set­
ting is due to cyclovergence. However, this assumption is
faulty. The phenom ena o f slant co n trast and norm alization
discussed in Section 2 1 .4 show that a line does n o t neces­
sarily appear vertical when its images fall on corresponding
meridians. Also, this m ethod gives different results depend­
ing on w hether or not a reference plane is provided in the
form o f a frontal circle round the test line (H arker I9 6 0 ).
A nother problem is that an inclined line is a stimulus for
cyclovergence and may therefore contam inate the results.
This problem is at least partially overcome by presenting the
test stimulus briefly, after the stimulus used to induce cy clo ­
vergence has been removed. Ellerbrock (1 9 5 4 ) further m in­
imized the effect o f the test stimulus by setting two points
rather than a line into the apparent frontal plane.
A m igo (1 9 7 4 ) used a similar procedure ro investigate
the vertical horopter. H am pton and Kertesz (1 9 8 2 ) co m ­
pared the psychophysical settings o f a test line w ith an
objective measure o f cyclovergence. Th e perceived inclina­
tion o f the test line was less than that corresponding to the
residual cyclodisparity in the line, and therefore did not
indicate the degree o f cyclovergence. A sequential test stim ­
ulus may overcome one problem, but does n o t solve the
problem s o f slant contrast and norm alization.
1 0 .7 .2 b N u llin g C y c lo d is p a rity in
D ic h o p tic S tim u li
In one form o f this method dichoptic lines are rotated in
opposite directions in the frontal plane until they fuse, or
appear collinear. This m ethod was first used by M cissncr in
about 185 4 ( Le C o n te 18 8 1) and was also used by Volkmann
(see H elm holtz 1 9 0 9 ). C ogan (1 9 7 9 ) pointed o u t that this
measure o f cyclovergence does not agree with that based on
judgm ents o f apparent vertical, since a line does n o t neces­
sarily appear vertical when the images in the two eyes appear
collinear. H e showed that, on average, a line was set within
3° o f true vertical in the median plane whereas two dichop-
tie images in the lrontal plane, one red and one green, had
to be incyclorotated by an am ount corresponding to an
inclination o f 31° to fuse into a single image. Although set­
ting tw o dichoptic images into collinearity may be the
better procedure, it has its own problems. Superimposed
dichoptic images tend to rivalry, and it is difficult to detect
cyclodisparity once the images lie w ithin Panum s fusional
area.
1 0 .7 .2 c T h e N o n iu s M e th o d
In the nonius m ethod, cyclovergence is indicated by the
angle through which a horizontal line presented to one side
o fth e fixation point in one eye has to be rotated in the fron­
tal plane to appear parallel to a horizontal line presented in
the opposite field o f the other eye. A binocular circle sur­
rounding the lines holds horizontal and vertical vergence
steady. This stimulus display is known as Volkmann disks
(see Figure 10.46). This is the torsional equivalent ot nonius
m ethods used to measure horizontal and vertical vergence.
Subjects read off the torsional deviation o f the eyes on a
scale (Sen et al. 1977).
H ofm ann and Bielschowsky (1 9 0 0 ) were the first to use
Volkmann disks systematically. They recorded cyclover­
gence o f about 5°, induced by disjunctive rotation o f tex-
tured displays through 8". V erhoeff (1 9 3 4 ) also used a
nonius m ethod and found cyclovergence to be a slow
response w ith magnitudes o f up to 6“ induced by an 8 :' dis­
junctive rotation o f tcxtured patterns. H e also found that a
greater amplitude o f cyclovergence is induced by texturcd
patterns than by simple line patterns, and more by
cyclodisparity ot horizontal lines than ot vertical lines.
Although su bject ro artifacts, rhe nonius method is the
only satisfactory psychophysical m ethod tor measuring
cyclovergence.
Howard et al. (1 9 9 3 ) superimposed a pair o f nonius
lines on the center o f a 7 5 ° d ichoptic textured display
(Figure 10.47). The images had a static cyclodisparity o f 12°
or were rotated sinusoidally in antiphase through 1 2 °, at
frequencies between 0 .0 5 and 2 H z. Subjects nulled the
apparent offset o f t h e nonius lines in the static display and
nulled their rocking m otion in the dynamic display.
Figure 10.48 shows that, for static cyclodisparity, the
nonius setting was slightly higher than the magnitude ot
cyclovergence measured objectively, using scleral search
coils. W h en the display rotated back and forth , the nonius
Fif»rc in.4*. I'olktn.nitj disks. A n gular m isalign m en t o f chc tw o n o n iu s
lines in the b in ocu lar im age provides a m easure o f t h e d eclin atio n o f
co rresp on d in g vertical m eridians. In m ost people th e corresp on d in g
m eridians arc relatively ex to rted ab ou t 2*.

FiS«.c Ю i7. D isplay u std to m ta$urccydovcrgcw c. D ic h o p tic tcxtu rcd
displays su b te n d in g 7 5 * w ere d isjun ctively Сy d o ro ta ted through various
am plitud es and frequ en cies. C yclo v crg cn cc was m easured w ith scleral
co ils and by alig n in g the c cn tra l n o n iu s lines. (Fio* Howardci *1.1993)
Figure 10.48 . M easures o f eydovergenee* O b jectiv ely m easured cyclovergence
and n on iu sd in c settin g s as a fu n ctio n o f the freq u en cy o f cyclodisparity
m od u lation o f th e display in Figure 9 .4 7 (N = 3 ). (R ed fjn n trooB Howard
lines appeared to rock through a greater amplitude than
predicted trom the m agnitude o t cyclovergence. W ith one
eye closed, the rem aining nonius line appeared to rock in a
direction opposite to that o f the rotating surround. This is
the well-known phenom enon o t induced visual m otion.
W hen both eyes were open, the two m onocularly induced
m otion effects com bined with the effects o f cyclovergence
to create the large apparent rocking m otion o f the nonius
lines. Thus, the nonius m ethod is a reasonably valid m ea­
sure o f cyclovergence, but only for static or slowly changing
disparities.
10 .7 . 2 d O b je ctiv e R e c o r d in g o f Cyclovergence
M ethod s for recording eye movements, such as electroocu ­
lography and the Purkinje eye tracker, do n o t record eve
torsion. Photographs o f the iris or episcleral blood vessels
must be analyzed frame-by-frame (Howard and Evans
1963). V ideo records o f the two irises can be subjected to
autocorrelation to yield a continuous record o f cyclover-
gcncc. Kcrtesz (1 9 7 2 ) used the photographic method but
filled to find cyclovergence because his stimulus was too
small. C.ronc and Evcrhard-Halm (1 9 7 5 ) and H ooten e ta l.
(1 9 7 9 ) used the photographic procedure with a more
adequate stimulus and obtained d e ar evidence of
cyclovergence.
Л scleral search coil m ounted on an annular contact lens
was developed by C ollew ijn et al. ( 1 9 8 5 ), and is available
trom Skalar M edical in Delft. W h en the coil is placed on an
eye within an oscillating m agnetic field, a voltage propor­
tional to the sine o f the torsional position o f the eve is gen­
erated (R obinson 1 9 6 3 ; Collew ijn et al. 1 9 7 5 ; Herman et al.
1987b ). This m ethod provides a low -noisc signal that
continuously registers the torsional position o f an eye to
w ithin a few minutes o f arc. The onlv
J drawback is that the
co n tact lenses can be worn for only about 3 0 m inutes at one
time. Kcrtesz and Sullivan (1 9 7 8 ) used the sclcral-coil pro­
cedure and obtained a cyclovergence o f 3.5° to a + 5° step o f
cyclodisparity in patterned displays subtending 5 0 u.
1 0 .7 .3 D Y N A M IC S O F C Y C L O V E R G E N C E
1 0 .7 .3 a G a in an d P h ase L a g o f C y c lo v c rg c n c c
Howard and Z acher (1 9 9 1 ) used scleral search coils to m ea­
sure gain and phase lag o f cyclovergence as a function o f
frequency and am plitude o f cyclodisparity o f the 75°
dichoptic display shown in Figure 10.47. This stimulus co n ­
tains a broad range of spatial frequencies, has both vertical
and horizontal elem ents to act ascyclofusional stim uli, and
is a good stimulus for keeping horizontal and vertical ver­
gence constant. A regular grid pattern is n o t suitable because
the eyes tend to misconverge on such stim uli. Since the dis­
play was circular and the surroundings black, there were
no stationary lines to provide a cyclofusional anchor. The
dichoptic displays rotated in counterphase about the fixa­
tion point to give peak-to-peak amplitudes of disjunctive
cyclodisparity o f 2 , 6 , or 12°, at frequencies o f from 0 .0 5 to
2 Hz. The gain o f cyclovergence was defined as the mean
peak-to-peak amplitude o f cyclovcrgencc divided by the
peak-to-peak amplitude o f the cyclodisparity o f the stim u­
lus. A sample o f the recordings is shown in Figure 10.49.
G ain declined with increasing stimulus frequency. Phase
lag was imperceptible at a frequency of 0 .0 5 H z, and
increased with increasing frequency o f cyclodisparity,
reaching over 100° at a frequency ot 2 Hz (Figure 10.50).
Cyclovergence is designed to cope with cyclodisparities
of low frequency and am plitude, as indicated by the fact
 ДА/ cW w v w

VyA'VWV

0.05 Hz 0.2 Hz 1 Hz 2 Hz
Frequency o f cyclovergence stim ulus

F.pirc io. C h a r t recording! ofcyelovtrgcn cc. C yclov crg cn cc fo r d ifferen t frequ en cies and am p litu d es o f cyclo disp arity o f the stim ulus show n in
Figure 9 .4 7 . 'Ih c traces represent the d ifferen ce b etw een the opposed cv clo ro tatio n s o f the eyes. Sh arp im pulses arc blinks. { A d ^ c d ^ H.y**»d*nJ
Z*clit» IW1)

chat, in Figure 10.50, gain is highest and phase lag lowest at

C yclodisparity fre qu e ncy (Hz)
C yclodisparity frequency (Hz)
Faftutc io. so. G ain a n d p h a se (ag o fc y d t v e r g e n c e . G a in and phase lag ot
cy clo v crg cn cc as a fu n ctio n o f freq u en cy o f cyclo disp arity for three
am plitud es o f disparity (N = 3 ). (K*dn«. Л»т H<*wrd *nd Z^hc. I99i>
a frequency o f 0 .0 5 Hz and an am plitude o f 2 For one
young adult, the gain o f cyclovergence reached 0.91 at this
frequency and am plitude. Van Rijn et al. (1 9 9 2 ) obtained a
maximum gain o f only 0. 2 , but they used only one fre­
quency o f stimulus rotation o f 0 .2 H z and a scimulus diam ­
eter o f only 28°. Later, they obtained a mean gain o f over
0.4 when they used a 4 8 “-wide display oscillating at 0.15 Hz
(van R ijn et al. 1994a). W c will see in the next section that
the gain o f cyclovergence declines rapidly as stimulus area is
reduced.
The dependence o f cyclovergence gain on the amplitude
o f stimulus cyclorotation shows that the system is n on lin ­
ear, because the gain o f a linear system is independent o f
am plitude for a given frequency. For a stimulus amplitude
o f 6°, the function relating gain in decibels to frequency has
a slope o f 20 db/decade for the five highest frequencies.
G ain in decibels is 2 0 tim es the log o f response amplitude
divided by the log o f stimulus amplitude. This is the value
expected o f a first-order system. However, the phase lag at
the corner frequency corresponding to a gain o f -3 db was
much smaller than expected from cith er a first-order or
second-order svstem.
The high gain and low phase lag for low stim ulus fre­
quencies and small amplitudes is w hat one would expect o f
a system designed to correct for slight rotary misalignments
o f binocular images. M isalignm ents may be produced by
cyclophoria or by torsional drifts o f the eyes that occur as
the gaze moves over a 3 -D scene. Cyclovergence does not
have to deal with rapid external events. Disjunctive cveloro-
tacions o f the whole distal scimulus occur only under very
special circum stances, as, for instance, when one observes an
isolated vertical line changing its inclination. U nder normal
 In
F . * « r * № .* ♦ . A sy m m etr y o f cyxbvergencc. R cco rd s о fc y d o v c rg c n c c o f four
su b jects in response to a + 4 . 6 'o r + 2 .3 “ step in vcrtical-shear disparity
o f а 6 0 ' CCXtured display. T b e stim ulus (d o tted lines) wav m ain tain ed
fo r 10 s. The m agnitud e o f in cyclovergen ce was greater th an th a t o f
cxcy clov crgcn cc in all su b jects. (fUfoww fromH<m*rdм 3 Kwk« ItW).
in vertical-shear disparity o f a tcxturcd display that filled
the binocular visual field. Incyclovergence responses were
larger than cxcyclovcrgcncc responses in their four subjects
(see Figure 10.54). N o subjects had the opposite asymme­
try. Taylor c t al. (2 0 0 0 ) reported the same asymmetry in
their tw o subjects. M axwell et al. ( 2 0 0 1 ) also reported this
asymmetry in each ot their five subjects. This asymmetry
may be due ro the natural predom inance o f horizontal sur­
faces below eve
Ш
level.
The eyes have a tendency to develop an excyclophoria
when one eye is occluded tor some time. Four out o t five
subjects showed a mean excyclophoria o f 1.8 0 after 8 hours
o f m onocular occlusion (C ra t e t al. 2 0 0 2 ). This suggests
that the physiological state o f rest o f cyclovergence is in the
cxcyclovergence direction, and that the stronger response
to incyclodisparity corrects for the tendency o f the eyes to
drift in the direction o f cxcyclovergence. In a sim ilar way,
the tendency for horizontal gaze to becom e exophoric
during m onocular occlusion is balanced by an opposite
asymmetry in the degree o f adaptation o f horizontal ver­
gence (S ch o r 1979a).
10.8 V E R G E N C E - V E R S I O N
INTERACTIONS
1 0 .8 .1 H E R I N G ’ S LA W O F E Q U A L
IN N E R V A T IO N
10 . 8 . 1 a L aw o f Equal Innervation
W h en fixation changes rapidly betw een two points differ­
ing in both depth and direction, vergence is com bined with
a saccade. W h en the eyes track a spot m oving slowly between
points differing in depth and direction, vergence is co m ­
bined with slow pursuit. The following discussion is about
how vergence com bines w ith these two types o f version.
M ovem ents o f a single eye, or ductions, are specified in
terms ot m agnitude, direction, and velocity. Coordinated
m ovem ents o f the two eyes arc specified in terms o f version
and vergence com ponents. Version is an equal m ovem ent ot
the eyes in the same direction, and vergence is an equal
m ovem ent in opposite directions. A circle passing through
the centers o f rotation o f the two eyes and che fixation point
is the path traced by the fixation point as version changes
with vergence held constant. A hyperbola o f Hillebrand is
the path traced by a change in vergence with version held
constant (see Figure 10.10). M athem atically, any movement
o fth e two eyes may be described as the sum o f a version and
a vergence. L et 0 be the version com ponent with move­
ments toward the right signed positive, and let // be the ver­
gence com ponent, with convergence signed positive. For a
pure vergence, the m ovem ent o f each eye equals /i/2 .
In general (after O n o 1 9 8 0 ):
( fl\
в + 1 — = Rotation o fth e left eve
U )
(
0 — — j = Rotation of the right eye
Alhazen, in the 1 1th century, proposed that the move­
m ent o f one eye is accom panied by a m ovem ent o f the other
eye o f equal amplitude and velocity, either in the same or in
the opposite direction. This idea was developed by H ering,
who called it the law o f e q u a l in n e r v a t i o n . Hering (1 8 6 8 ,
p. 17) wrote,
The two eyes are so related to one another that one
cannot be moved independently o f the o ther: rather,
the musculature o f both eyes reacts simultaneously
to one and the same impulse o f will.
H ering did not mean that one eye can n o t move while
the other eve remains stationary. He continued:
* *
It is possible for us to move both eyes sim ultane­
ously about different angles and with different
speeds . . . and even to move one eye outw ard or
inward while the o ther remains still. W e are able to
do this, not because we simultaneously give each eye
a special innervation, but because in these move­
ments each eye receives tw o different innervations.
O n e is л turning m ovem ent o f both eyes to the right
or left and the other is inward or outward turning ot
both eves.
i Since these tw o innervations o f t h e two
eyes work together in one eye and conversely in the
other, the resultant m ovem ent in each eye must nec­
essarily be different.
C onsid er the idealized case, in which the gaze shifts
from point A to point В on the visual axis o f the left cvc.
The m ovem ent may be decom posed in to an equal version
for both eyes o f 9 and a vergence, which in this case moves
the right eye through angle - f l f 2 and the left eye through
angle jU/2. By the above equations they cancel for the left
eye and add for the right eye. The right eye therefore docs
all the moving. People can learn to move an occluded eye
horizontally while keeping the other eye fixated on a sta­
tionary target (M anny 1 980).
H erings law would be a tautology i f it merely stated
that aU eye m ovem ents may be described as the sum o f a
version and a vergence com ponent. It is clear from Hering s
use o f rhe phrase “equal innervation” that he was thinking
o f com pon ent neural processes not merely mathematical
com ponents.
It is not the am plitude or velocity o f the movements o f
the tw o eyes that are equal in H erin g s law, but the am pli­
tude and velocity o f the vergence com ponent in each eye
and o f the version com ponent in each eye. O n e can erect
the hypothesis that, when version and vergence are executed
simultaneously, eye velocity is a linear sum o f the velocities
o f each com ponent movement. Em pirical evidence bearing
on this version o f H erings law is discussed in Scction 10.8.2.
H erings law should perhaps be called the law o f equal
co m p o n e n t in n erv ation s.
H erings law requires that, at any instant, the visual
o b ject that evokes version is also the o b ject that evokes ver­
gence. Chaturvedi and van G isbergen (1 9 9 8 ) presented
two target objects at the same tim e in different positions in
3 -D space. W hichever o b je ct evoked the first saccadic
response was alm ost always the o b ject that evoked the vcr­
gcncc response. W hen rhe saccadic response was to a com ­
promise position, vergence showed a similar com prom ise.
1 0 .8 .1 b N e u ro lo g y o f H e r in g s Law
Hering s law implies that there are tw o centers, one for ver-
gence and one for version, and that, for each center, rhe
same innervation is sent to the two eyes. The simplest
assumption is that the innervations from each center to one
eye are com bined linearly in the final com m on path so that
the m ovem ent o f that eye is the algebraic sum o f the inner­
vations from the tw o centers. But H erin gs law does not
require a linear com bination o f version and vcrgcncc sig­
nals; it only requires that the version signals remain equal
and the vergence signals rem ain equal. For instance, it docs
n o t forbid version signals from being attenuated when com ­
bined with vergence signals.
C onjugate eye m ovem ents o f all types in the horizontal
plane are organized in the paramedian pontine reticular
form ation, or PPRF. C onju gate eye movements in the ver­
tical plane are organized in the mesencephalic reticular for­
m ation, or MRF . These nuclei receive inputs from rhe
superior colliculi, vestibular nuclei, and the frontal eye fields
and p roject m onosynaptically to m otoneuron pools in rhe
o cu lo m oto r nuclei. Each m otoneuron pool innervates
alm ost exclusively
; one extraocular muscle in one eve.
J Those
in the trochlea nucleus innervate the contralateral superior
oblique muscle, those in the abducens nucleus innervate the
ipsilateral lateral rectus, and m otoneuron pools in the ocu l­
o m oto r nucleus innervate the ipsilateral medial rectus, infe­
rior oblique, inferior rectus, and contralateral superior
rectus (Evinger 1 9 8 8 ). M oschovakis et al. (1 9 9 0 ) recorded
from m oroneurons responsible for vertical saccades and
found that they branch to innervate all the m otoneuron
pools that move both eycsconjugately. M oschovakis (1 9 9 5 )
traced the axonal term inations o f prem otor lead burst neu­
rons responsible for initiating horizontal and vertical co n ­
jugate saccades. In each case, the axons term inated in the set
o f m otoneurons that controlled the movements o f both
eyes. This provides a basis for H erin gs law, at least for co n ­
jugate saccades.
Sm ooth pursuit eye movements seem to be organized
by separate com m ands to the eyes. King and Z hou (1 9 9 5 )
found that the pursuit movement o f each eye during the ini­
tial open-loop 100 ms was controlled only by m otion o f the
visual target in that eye, w hether the eye m ovem ent was
conjugate or disjunctive. In their experim ent, any co n trib u ­
tion ot disparity-induced vergence to disjunctive pursuit
must have had a latency longer than 100 ms, but presum­
ably obeyed H erin gs law.
Hering proposed that axons from d istin ct m otoneurons
lo r version and vergence com bine in the muscles. The axons
could converge on the same muscle fibers, or different
muscle fibers could be devoted to each com ponent. Hering
believed in the second possibility and thought he detected
opposed contractions in the muscles o f the stationary eye
during a change ot fixation along that eyes visual axis.
Tam ler c t al. (1 9 5 8 ) claim ed to have detected these co n trac­
tions clectrom yographically in humans.
O th er investigators found no changes in electrical activ­
ity o f muscles o f a stationary eye under these conditions
(B reinin 1 9 5 5 ; Blodi and Van Allen 1957; Allen and C arter
1 9 6 7 ). C ocon tractions could be due to slight saccadic
m ovem ents when vergence changes rapidly along the line o f
sight ot one eye, or to torsional movements that accompany
changes in vergence. M ore recent evidence suggests that
cocontraction o f lateral and medial recti during conver­
gence is due to inappropriate version signals arising in the
abducens nuclei, which are overcome by appropriate signals
arising from centers controlling vergence (G am lin et al.
1989).
Enright (1 9 8 0 ) revealed that there is also a slight lateral
translation o f an eye when vergence changes along that eye s
visual axis. These torsional and translatorv movements are
4
probably incidental to the version and vergence co m p o ­
nents and have no functional significance.
O ’Keefe and Berkley (1 9 9 1 ) produced evidence o f a
coupling o f the movements o f the two eyes mediated by
proprioception. Infusion o f a paralytic agent into the
muscle capsule o f one eye in the anesthetized cat reduced
whecher chc scimulus was aligned with che left or righc visual
axis. This asymmetry was explained in terms o f a displace­
m ent o f t h e cyclopean eye (sec Section 16.7.5} toward the
dom inant eye. Barbeito ct al. (1 9 8 6 ) confirm ed this asym­
metry but produced evidence that displacem ent o f the
cyclopean eye (egocenter) is not the only causal factor.
Furtherm ore, F.nright (1 9 9 8 a ) found that the extent o f the
asymmetry was noc correlaced wich che posicion o f the ego-
center (Section 16.7.2).
O cher invescigators found no evidence o f a clear separa­
tion in tim e between vergence and version com ponents
(Erkelens c t al. 1989b ). Enright (1 9 9 6 ) found rhac m ost
subjects made sm ooth vergence m ovements between tar­
gets in chc median plane or becween cargecs lying on rhe
visual axis ot one eye. W h eth er or n o t this is regarded as
breaking H erings law depends on how che law is inter­
preted.
An extrem e view is that the eyes arc controlled indepen­
dently rather than by the superimposition ot version and
vergence com ponents. Maxwell and Schor (2 0 0 4 ) asked
subjects to make vergence responses to stim uli for which
changes in horizontal disparity were accom panied by
changes in vertical disparity. After training, subjects showed
a change in vertical vergence when tested with a target thac
changed only in horizontal disparity. This aftereffect was
evident for both symmetrical changes in horizontal
vergence and for changes in vergence along the visual axis
o f one eye. But it did not show with conjugate eye
m ovem ents (version). This evidence supports the idea o f
two independent vergence and version com ponents
rather than the view char the two eyes are controlled
independently.
W hen an accom m odative change is induced in one eye
by a lens, with the other eye closed, the closed eye moves but
the open eye moves only slightly o r n o t ac all (M iiller 1829;
Kenyon et al. 1 9 7 8 ; Enright 1992a). Saida e t al. (2 0 0 1 )
found chat boch eyes showed an inicial response со rhe
introduction ot the lens before one eye, but that the open
eye stopped moving while the closed eye concinued to
move. However, under open-loop conditions, in which
m otion o f the visual target was optically stabilized in the
open eye, both eyes moved equally through h a lf the am pli­
cude shown by che closed eye in che closed-loop condicion.
This suggests that, with norm al viewing, the open eye m ain­
tains steady gaze on the cargec by error feedback from reti­
nal slip. W hen this error feedback is removed by opening
the feedback loop, boch eves share in che vergence response
induced by the change in accom m odation.
O cher evidence suggescs thac che control o f vergence,
especially asymm etrical vergence, is m ore complex than a
simple sequential com bination o t rapid version and slow
vergence.
In the first place, the saccadic com ponent is n o t switched
o f f while vergence is occurring. There is thus chc quescion
w hether the saccadic and vergence com ponents com bine
additively when chey occur together. O n o et al. (1 9 7 8 )
found that during the convergence phase o f an eye m ove­
menc evoked by a target chac sceppcd in boch laceral direc­
tion and depth, the differences o f amplitude and velocity
betw een che two eyes were much greater chan predicted
Irom a linear addition o f com ponent velocities. A similar
supra-addicivity o f com ponents occurred when a step
change in the lateral direction o f gaze was superimposed on
a tracking vergence m ovem ent made in response to a target
m oving slowly in depth (Saida and O n o 1 9 8 4 ). Similarly,
when accidental microsaccadcs occurred during a vergence
m ovem ent, the difference in velocity between che cwo eyes
was greater than predicted by simple addition (Kenyon
e ta l. 198 0 b ).
C ollew ijn et al. (1 9 9 7 ) concluded trom their own data
th at version and vergence com ponents o f com posite eye
movements can be executed separately during part o f the
m ovem ent bu t that, in mosc eye movements, the two
com ponents overlap in tim e and interact in a nonlinear
fashion.
The tim ing o f the saccadic com ponent relative to
the vergence com pon ent depends on the direction o f che
change in gaze in 3-D space. W h en gaze changed betw een a
low near point and a tar high point in the m edian plane,
the Saccadic and vergence com ponents reached peak
velocity ac almosc the same cime. However, when gaze
changed betw een a high near point and a tar low point, the
saccadic com pon ent reached its peak velocity up to 66 ms
before vergence reached its peak velocity (Kum ar et al.
2 0 0 5 ).
1 0 .8 .2 b V erg en ce In tru s io n s in S a cca d cs
There is the related question ot cross talk betw een version
and vergence (O n o 1 9 8 3 ). Is the response to a stimulus
requiring pure version devoid o f a vergence com ponent,
and is a required pure vergence devoid o f a version co m p o ­
n en t? D uring fixation the eyes execute m icrosaccadcs ot
betw een 0.2 and 1 .0°. M oller ct al. (2 0 0 2 ) found that all
microsaccades occurred simultaneously and with equal
am plitude in the tw o eyes. Also, for m ost o f them , the d if­
ference in direction was less than 22°. Thus, at least m icro ­
saccadcs are conjugate.
Sm ith et al. (1 9 7 0 ) detected a small lack o f synchrony
betw een the eyes for som e but n o t all saccadcs. Bahill ec al.
(1 9 7 6 ) noted that subjects with norm al vision sometimes
execute unequal saccadcs in the tw o eyes, but they regarded
disconjugate saccadcs as anomalous. W illiam s and Fender
(1 9 7 7 ) found that, in spite o f claim s to the contrary, volun­
tary saccadcs are alm ost com pletely synchronized in the
two eyes.
C ollew ijn et al. (1 9 8 8 a ) found rhar, with horizontal sac­
cadcs along a locus ot isovergcnce, the m otion o f the abduct­
ing eye had a larger am plitude, higher peak velocity, and
shorter duration than the m otion o f the adducting eye
eccentric cargecs or when the natur.il vertical disparities
were nullified by a prism. However the saccadic disconju­
gacy was reduced after several hours during w hich subjects
wore prisms that nulled the disparity (Yggc and Zee 1995).
Spectacles worn to correct unilateral myopia o f rcfrac-
tive origin produce aniseikonia— they enlarge the image in
one eye relative to that in the other (Section 9 .9 ). This is
because spectacle lenses are offset from the cornea and do
not move with the eyes. An oti-axis o b ject seen through
spectacle lenses produces images with ditferent angles o f
eccentricity in the tw o eyes. C o n ta ct lenses do n o t produce
this effect. People w ho wear spectacles to correct for refrac­
tive anisom etropia develop com pensatory asymmetries in
saccadic eye movements (Erkelens et al. 1 9 8 9 c; I.em ij and
C ollew ijn 1991a). M onkeys show the same adaptive
response (O o h ira and Zee 1992).
Figure 10 .5 7 shows a record ot unequal saccadcs made
by a 12-ycar old boy who had worn spectacles tor 7 years to
correct an 1 1 -diopter myopia in one eye. The acquired sac­
cadic asymmetry com pensated for alm ost all the optical
aniseikonia. After 3 m onths ot wearing corrective contact
lenses, which do not produce aniseikonia, saccadcs became
almost equal in size (O o h ira et al. 1991).
Even short periods o f exposure to aniseikonia can pro­
duce appropriate adaptation ot relative saccadic amplitudes
in the tw o eyes. For instance, after 1 hour o f exposure to a
2 -diopter lens in front o f one eye, the am plitudes o f sacca-
des in the tw o eyes differed by the am ount required for bin­
ocular acquisition o f eccentric targets along the horizontal
and vertical meridians (Lem ij and C ollew ijn 1991b ). M ore
powerful lenses caused larger adaptive effects up to a lim it
o f 6 diopters. Six hours o f adaptation to a 6 -diopter lens,
which caused one image ro be m agnified 1 2 %, produced
12 - plane dim inish to zero so that disjunctive saccadcs arc there­
Right eye
10 •
4)
M
■
О
Left eye
с
0 random -dot
1 6 -
2 peripheral target disparate by placing an 8% magnifier in
о 4 - fro n t o f one eye. Even though the target was presented for
N
о only 100 ms on each trial and there was a 1 s interval before
X V ergence
2 -
Tim e (s)
F.nurc 10.57. U n equ aljac carles in A nisom etropia. R ecord o t unequal saccadcs
o f а 12-year-о Id boy adapted to a n iso m etro p ic spectacles, after the
spectacles were rem oved. The visual target was 10° to the right o f in itial
fix atio n . T h e saccadcs ind u ced som e vergence. {Adjf*e4fn>mOolu'j<t«J. 1991)
appropriate saccadic asymmetries. Bucci ct al. ( 2 0 0 1 )
obtained saccadic disconjugacy after 15 minutes, during
w hich tim e subjects made horizontal or vertical saccadcs to
points in a random -dot display magnified in one eye by 2 %.
Disparities produced by images differing in size by 2%
would be within Pan urns fusional lim it.
D isconjugacy o f vertical saccadcs can be induced by
opposite m otion o f identical dichoptic stim uli just after
com pletion o f vertical saccadcs (K apoula et al. 1996a).
However, saccadic disconjugacy is nor induced by posrsac-
cadic m otion o f dichoptic random -dot stimuli that are spa­
tially uncorrelared (Kapoula c t al. 1990). Thus postsaccadic
drift is not induced by opposed m otion o f the images in the
two eyes in the absence o f a recognizable disparity at the
com pletion ot the saccadc.
H orizontal saccadcs becam e disjunctive after subjects
made repeated saccadcs over a period ot 15 minutes to a
Hashed eccentric target with horizontal disparity (Bucci
et al. 2 0 0 0 ). The subjects had no visual error feedback.
Bush c t al. (1 9 9 4 ) projected random -dot patterns in a
stereoscope at a distance o f 3 3 cm . The image in one eye was
magnified 8% relative to that in the other. Saccadcs to a
target superimposed on the display in one eye immediately
produced saccadcs that were unequal by betw een 4 and
7.5% . This response occurred in both humans and monkeys.
Thus, a stronger than usual pattern o f disparity can induce
unequal saccadcs w ithou t adaptation or learning. But this is
not saccadic adaptation, because it occurred immediately
and did n o t persist with m onocular viewing.
Van der Steen and Bruno (1 9 9 5 ) obtained immediate
disjunctive saccades in response to a sim ilar display with
near viewing. However, with far viewing, it took several
minutes to obtain disjunctive saccades. This effect was sac­
cadic adaptation, since it persisted tor some tim e in open-
loop conditions. W ith far viewing, disparities in the frontal
fore not normally required. Bruno et al. (1 9 9 5 ) developed a
model ot saccadic adaptation.
Subjects rapidly adapted relative saccadic amplitudes
when one image was made larger than the o ther or when
the subjects looked back and forth betw een tw o points in a
stereogram (Eggert and Kapoula 1995;
Kapoula c t al. 1996b ). Kapoula et al. (1 9 9 8 ) made a
the saccadc was initiated, subjects learned to make appro­
priate disjunctive saccades with 15 min o f training. The
effect o f training persisted when the target was no longer
disparate but did n o t occur when subjects did not make sac­
cadic eye movements to the disparate target (Kapoula et al.
2000 ).
Saccadic disconjugacy produced by 10% aniseikonia
was reduced when there were m onocular cues rhat rhe
display was frontal (Bu cci et al. 1999).
 A daptation o f conjugate saccades со imposed dysmetria
was specific to the visual meridian along which training
occurred (D eu b el ec al. 1 986). N onconjugate saccadic adap­
tation to aniseikonia has also been found to be specific to
the main orthogonal and oblique directions wichin which
training was applied (Lem ij and C ollew ijn 1992).
A vcrbuch-H cller et al. (1 9 9 9 ) placed a small base-out or
base-in prism in fron t o f one eye so that fixation o f a central
visual target required 5 “ o f convergence or divergence. For
15 m inutes, subjects made 20" saccades from chc central
targec seen through the prism to targets seen to the left or to
che righc oucside che prism. Subjcccs developed a scrongsac­
cadic disconjugacy that persisted during subsequent m on­
ocular viewing. This was accom panied by changes in the
peak velocities o f both eyes and in the relative velocities o f
the eyes. These features o f adapcacion are sympcomacic o f a
binocular saccadic-vergcnce interaction and cannot be
explained by a purely m onocular saccadic adjustm ent. Som e
subjects developed some saccadic disconjugacy in a non-
trained direction along che same horizoncal meridian,
which could be explained only by m onocular adaptation.
Avcrbuch-H cller e t al. concluded th at both binocular sac-
cadic-vergence interaction and a m onocular com ponent
were involved.
1 0 .8 .3 c Adaptation o f Pursuit to A niseikon ia
Schor et al. (1 9 9 0 ) inquired w hether adaptations o f che sac­
cadic and pursuit systems to aniseikonia are independenc.
For pursuit adapcacion, subjects m aintained vergence tor
cwo hours on a pair o f horizoncal dichopcic lines chac moved
up and down ac 1 0 7 s through 20 °, giving a frequency o f
0.25 Hz. For saccadic adapcacion, subjeccs followed seep
vertical displacem ents o f the lines, which occurred every
half-second for 2 hours. H orizontal vcrgcncc was m ain­
tained on a fixed vertical line. The image in one eye was
magnified 10 % so chac che image o f che line in chac eye
moved further than the image in the other eye. Pursuit
adaptation produced a 7 .3 % asymmecry o f pursuic am pli­
tude but onlv
4 about 1% ot saccadic asvmmetrv.
i i Saccadic
adaptation produced a 6 % asymmecry o f saccadic am pli­
tude but only about 2.5% o f pursuit asymmetry. In other
words, adaptation effects were largely specific со che cype o f
eye m ovem ent used in training. No adaptation occurred
when visual error feedback was w ithheld during and jusc
after each eye movement.
10.8 .3 d O c u l o m o t o r Adaptation to Paresis
Saccades and voluntary pursuit adapc со partial paralysis o f
one eye (O pcican ec al. 1985). In one study, a man with
sudden onset o f paralysis o f the left abducens nerve devel­
oped saccadic hypomcrria in his left eye. H is other eye hap­
pened to be scrabismic. Saccadic accuracy o f che left eye,
which he preferred со use tor fixation, recovered after a
while. W hen che parccic eye was pacched, che ocher eye
showed saccadic overshooting (K om m erell ec al. 1976).
A sim ilar recovery o f saccadic orchomecria was reporced
in a patient with sudden onset o f right third-nerve palsy.
D uring the 6 -day recovery period, che left eye was pacched
(A bel et al. 1978).
Paresis induced in the horizontal recti ot one eye o f
monkeys made che eye hypomecric. W ich che good eye
pacched for 6 days, the paretic eye regained orthom etria but
reverted to hypomecria when che pacch was swicched
(O p tican and Robinson 1980).
This capacity со recover from che ctfeccs o f paresis seems
to depend on the integrity o f the cerebellum , since lesions
o f the cerebellum induce perm anent saccadic hyperm edia
(O p tican 1982).
In these studies, the normal eye was noc used or was
kept patched during the recovery period. W hatever adapta­
tion occurred for the parccic eye was also found in che
pacched eye— adaptation was conjugate. The visual system
apparently treats boch eyes alike if chere is no visual
inform ation to indicate that they should be treated
differentially.
Snow et al. (1 9 8 5 ) produced the first evidence that the
saccadic system can adapt to paresis differentially in the two
eyes. In six monkeys, chey weakened the tendon insertions
o f the medial and lateral recti in one eye, w hich caused sac­
cades for chis eye to be hypom etric to a greater or lesser
exccnc. After 3 0 days o f binocular viewing, che racio o f sac­
cadic amplicudes in che cwo eyes recurned со normal in all
six animals, although recovery was faster in those animals
with less inicial hypomecria. After recovery o f balance in
rhe amplitudes o f saccades, saccadic durations were longer
and peak velocities were smaller in both eyes. Furtherm ore,
when the recovered operated eye was patched, its
hypomecria recurned.
Ic was concluded from these tw o facts that recovery o f
saccadic balance depends on changes in neural control and
not merely on recovery o f strength in the operated eye.
V iirre ec al. (1 9 8 8 ) discurbed saccadic balance in m on­
keys by recession (surgical reinsertion) o f a rectus muscle in
one eye. After a period o f binocular viewing, the deviation
ot the operated eye disappeared, and saccades in both eyes
becam e orth om etric in m ost o f the animals. This adapta­
tion did n o t occur after severe weakening ot the muscle.
The experim ents described in chis and che previous sec­
tion dem onstrate that as long as there is appropriate visual
feedback che saccadic syscem can compensace tor aniseiko­
nia or for an unbalanced muscular system by changing the
balance o f innervations to the cwo eyes. Binocu lar visual
inputs also seem со be required jusc for che regular maince-
nancc o f binocular coordination o f saccades. Simply patch-
ing one eye in normal m onkeys for 6 days produced
hypermecria and poscsaccadic drift in thac eye, which rap­
idly cleared up when both eyes were open ( V ilis c t al. 1985;
Viirre et al. 1987).
 1 0 .8 . 3 c Su m m ary
Although version and vergence are d istinct movements,
they sum in a nonlinear fashion when they overlap in cime.
Vergence movements can intrude in to saccadic eye move­
ments со targets thac require only version. This may be due
to loss o f a fusional signal during a saccade or to asymme­
tries in the m echanical properties o f eye muscles. Saccades
o f different amplitudes in the two eyes may intrude into
vergence eye movements. In spite o f these com plexities and
qualifications. H crin g s law remains as a fundam ental state-
men t o f how frontal-eved animals, such as cats and primates,
move cheir eves. They do noc generally move the eyes inde­
pendently like a cham eleon. Also, the tw o visual axes inter­
sect at chc point o f fixacion, and a closed eye moves in
version or in vergence along w ith che open eye.
Relative m otions o ft h e eyes are preprogrammed when
they make saccadic m ovem ents to targets in different direc­
tions and at different distances. The system is rapidly m odi­
fied by the prevailing pattern o f disparities and shows
long-term adaptation when subjects are exposed for some
tim e to unusual patterns o f disparity. Adaptation is largely
specific to the type o f eye m ovem ent involved.
10.9 VERGENCE-VESTIBULAR
INTERACTIONS
1 0 .9 .1 R O T A R V V O R A N D V IE W I N G
D IS T A N C E
W h en che head rotates in the dark around any axis, che eyes
execute conjugate m ovem ents known as rhe vestibuloocu-
lar response (V O R ). The eyes rotate in the head in the
opposite direction ro the head at about the same velocity
(slow phases) with periodic rapid return movements (quick
phases).
Stim uli for V O R arise in the sem icircular canals ot the
vestibular svstem. O n each side o f the head there are three
canals in approximately orthogonal planes. Each canal is
maximally sensitive to rotation o f the head in its own plane.
V O R can be elicited in a horizontal or vertical direction or
about the visual axis (torsional nystagmus), depending on
which canal is in the plane o f head rotation. The V O R is
present in neonates and is basically under the control o f
centers in the vestibular nucleus and cerebellum (see
Howard 1 9 8 6 for a review).
W hen the eyes are open, V O R is supplemented b y o p to -
kinetic nystagmus (O K N ) evoked by m otion o t the image
o f the visual scene (Section 2 2 .6 .1 ). The V O R and O K N
act together to stabilize the retinal image o f the stationary
surroundings as the head rotates.
The velocity o f eye movem ents required to stabilize the
image o f a stationary o b ject when the head rotates about
the m idbody axis varies inversely with viewing distance.
This is because, when the head rotates, the eyes translate
due to their olfset from the axis o f head rotation. For a head
rotation o f в, the rotation o fa n eye, Ф. required to stabilize
the image o f a stationary o b ject at distance D is
n dsinO
0 = 0 + t a n -----------
D
where d is the distance from the axis o f head rotation to the
center o f rotation o f the eye. For a distant o b ject the effect
o f translation is negligible, but for an o b ject at the near
poinr, eye velocity required for image stability is about
double that required at infinity. Thus, the gain ot V O R (eye
velocity divided by head velocity) required for image stabil­
ity increases trom 1 at infinity to 2 for near vision. In illum i­
nated surroundings, the distance scaling o f V O R could be
achieved by visual cues to distance. Ic could also be scaled by
O K N , since O K N is controlled by visual feedback. In the
dark, the scaling could be achieved only it V O R were linked
to the angle o f vergence.
Biguer and Prablanc (1 9 8 1 ) measured V O R gain during
coordinated movements o f the eyes and head to an eccen­
tric visual target. For a near target, V O R had a higher gain
than when the target was far. This was still true when the
target was sw itched o ff ju st before the head started to move,
showing that visual error signals during the m ovem ent are
n o t necessary for distance scaling o t V O R . Biguer and
Prablanc concluded that the m odulation o f V O R gain
depends on visual distance cues seen before the movement
started.
H ine and Thorn (1 9 8 7 ) measured the gain o f V O R
while subjects rotated the head from side to side through
30° and converged on a point o flig h t at various distances.
W hen the target was visible the gain was accurately m odu­
lated by distance. M odulation continued less adequately
after the target was extinguished (see also Paige et al. 1998).
The gain o f V O R was n o t affected by lenses that changed
accom m odation but was affected by prisms that changed
vergence. They concluded that vergence, in addition to
visual distance, provides a signal for distance scaling ot
VOR.
In the monkey, eye velocity increased as the linear co m ­
ponent o f head m otion was increased and as the distance o f
a stationary visual target was decreased (V iirre et al. 1986).
This m odulation o f'V O R was not visually m ediated because
it occurred in the first 20 ms o f the start o f head movement,
which is below the latency o f O K N . The m odulation o f
V O R also occurred at frequencies o f head rotation beyond
the range o f O K N . Presumably, the distance o f the visual
target was assessed before the start o fth e head m otion.
Snyder and King (1 9 9 2 ) had monkeys converge on a
near or far visual target, which was switched o ff just before
the animals were rotated about a vertical axis that was
located either in front o f the eyes or behind the eyes.
The V O R response occurred with a latency o f 2 0 ms.
Initially, ics am plitude was noc affected by convergence or
by the location o f the axis o f rotation. Subsequently, for
both positions o f the axis o f rotation, peak V O R velocity
becam e greater lor near convergence than tor tar conver­
gence. Also, for both angles o f vergence, V O R amplitude
was greater when the axis o i rotation was behind the eyes
than when it was in front. Vergence angle affected the V O R
with a latency o f 4 0 ms, while it took a further 3 0 m s before
the response was modulated by the location o t the axis ot
rotation.
Snyder c t al. (1 9 9 2 ) rotated monkeys around che verti­
cal body axis at betw een 3 0 and 5 0 0 V s for 4 0 ms at various
times j u st before or d uring vergence eye movements between
targets at different distances. The gain o f V O R increased
linearly with increasing vergence angle. The latency o f V O R
was shorter than the latency o f vergence, and the response
showed some m odulation o f gain appropriate to the visual
target on w hich the gaze was not yet directed. This suggests
that che signal for modulation o f V O R is derived from the
cencral m otor com m and related to the shite o f attention to
the new vergence target rather than trom proprioceptive
feedback from extraocular muscles.
Presumably, the m odulation o f V O R gain by either
visually perceived distance or by vergence angle is acquired
through experience. Lewis e t al. (2 0 0 3 ) modified the rela­
tionship between V O R and vergence angle by exposing
observers to diverging prisms as a visual display moved out
o f phase with the head and to converging prisms as the dis­
play moved with the head. After 2 hours o f training, rhe
gain o f V O R changed significantly for each o f the vergence
angles.
1 0 .9 .2 L IN E A R V O R A N D
V I E W I N G D IS T A N C E
A vestibuloocular response is also evoked by sideways
m otion o f the body in the dark (Sm ith 1985; Baloh et al.
1988). This is referred to as lin ea r V O R (L V O R ). The stim ­
ulus in this case arises in the utricles and saccules— the ves­
tibular organs sensitive to linear acceleration. This response
is supplemented by O K N when objects are in view.
Responses to the com bined stimuli stabilize the retinal
image o f the surroundings as the head translates sideways.
W ith linear sideways self-m otion, the angular velocity
o f eye movements required tor image stability is zero for
objects at infinity and increases tor nearer o bjects. For
perfect image stability at viewing distance D s the angular
eye velocity, в , for a linear displacem ent, L , o f the head is
given by
# = arctan—
D betw een L V O R gain and viewing distance was affected
W hen rhe eyes are open, any inadequacy in the L V O R is
com pensated by O K N or by voluntary pursuit, which arc
naturally scaled for viewing distance because the angular
velocity o f a stationary o b ject relative to the moving head is
inversely related to viewing distance. Paige (1 9 8 9 ) found
that eye velocity increased as the visual stimulus was brought
nearer, bu t not rapidly enough to com pensate for the reduc­
tion in distance.
Signals tor V O R ascend from the vcscibular nucleus to
the ocu lom otor nuclei along rhe medial longitudinal fas­
ciculus and the tract o f D eiters. In the monkey, neurons in
che tract o f D eiters increased their response to linear side­
ways mocion o f che head when che animal changed fixacion
from a far со a near o b ject (C h en -H u an g and M cC rea
1 9 9 8 ).
The following experim ental procedures have been used
to reveal w hether L V O R is intrinsically scaled for viewing
distance w ithou t help from visual pursuit.
1. Use o f imaginary targets I he velocity o f 1,V O R in the
dark increased when a linear com ponent was added со a
rotation o fth e head about a vertical axis, and increased
still further when subjeccs imagined chac chey were
looking at a near visual o b ject (G resty c t al. 1987).
The gain o f L V O R in the dark increased when human
subjects imagined that they were looking at a near
visual objecc, even chough chis did noc significantly
increase vergence (Shelham er et al. 1995). However,
L V O R gain was not affected when subjects increased
vergence by means o f auditory feedback. This suggests
that che gain o f linear V O R is governed by a central
signal related to perceived distance rather than by
ertcrcncc or afference signals associated with the
vergence state o f the eyes.
2 . Response after removal o f targets In this procedure,
persisting L V O R is recorded just after the target has
been switched otf. Schwarz and M iles (1 9 9 1 ) measured
the velocity o f L V O R in monkeys in response to linear
sideways acceleration o fth e body, for 200 ms after
sw itching о 1Г a fixation target at one o f several distances
betw een 16 and 150 cm. The velocity o f I.V O R was
inversely proportional to viewing distance. However,
scaling o f velocity to distance was n o t perfect and
varied betw een animals. The mean gain (ratio o fey e
velocity to that required for image stability) was 0 .7 4 at
16 cm and 1.25 at 159 cm .
Paige (1 9 9 1 ) asked human subjects to fixate visual
targets at various distances while their bodies were
oscillated up and down. The gain o f vertical L V O R
continued to be related to viewing distance for some­
tim e after the target was switched otf. The coupling
when subjects viewed the visual targets through prisms
that increased the required vergence, but not when
they viewed the targets through lenses that changed
 chc required accom m odacion. The effect o f viewing
distance on L V O R gain alter the lights were put out
declined as the frequency o f head rotation increased to
4 H z (Paige e ta l. 1 998).
3. Response in (be initial open-loop period G ianna et al.
(1 9 9 7 ) measured the velocity o f the L V O R o f human
subjects to linear sideways accelerations while they
viewed Earth-fixed targets at distances o f 3 0 , 6 0 , or 2 8 0
cm . Eye velocity was inversely proportional to viewing
distance in the initial 130 ms o l acceleration. It was
assumed that visual m otion signals had no effect in this
period.
Tins evidence suggests that L V O R is inversely scaled
for viewing distance w ithout help from visual pursuit.
The scaling could arise Irom visual cues to distance seen
before the m ovem ent starts, from the state ofvergence
during the movem ent, or Irom perceived or imagined
distance.
4 . Dissociation o f cues to distance Inform ation about the
absolute distance o f a visual stimulus is provided by
accom m odation and vcrgcncc (C h ap ter 2 5 ) and by the
purely visual cues o f image size (Section 2 6 .3 ) and
gradients o f horizontal and vertical disparity
(Section 2 0 .5 ).
W ei e t al. (2 0 0 3 ) set o u t to measure the contribution o f
cach cue to the distance scaling o f L V O R . M onkeys were
oscillated from side to side at 5 Hz while fixating a central
target. A large stereoscopic random -dot display was placed
in front o f rhe monkcvs. The L V O R was measured under
the following conditions. (1 ) Purely visual cues to the dis­
tance o f the d o t display (disparity gradients and image size
and density) were varied to sim ulate distances ol between
12 and 102 cm . The m onkey fixated a central target at 32
cm . (2 ) Visual cues to distance were varied along with the
state o f vcrgcncc (determ ined by the overall horizontal dis­
paricy o f the random -dots and the fixation target). Thus,
vergence distance and visual distance cucs were the same.
(3 ) Vergence state was varied, but visual cues to distance o f
the dots were constant at 3 2 cm .
The variations in visual cues had very little effect on the
amplitude o f L V O R when vcrgcncc was constant. Response
amplitude was increased only slightly when visual cues to
distance were added to changes in vcrgcncc (condition 2 )
com pared with when visual cues were held constant (con d i­
tion 3 ). W ei ct al. concludcd that vcrgcncc provides the
m ajor cue for distance scaling o f L V O R . They suggested
that this m ight be because visual cucs to distance take longer
to process than vcrgcncc inform ation.
W ei et al. seem to have overlooked an im portant factor.
The purpose o f distance scaling o f L V O R is to stabilize the
image o l the attended o b ject, w hich is the o b ject on which
the gaze is centered, not objects in a different depth plane.
O p to kin etic nystagmus is evoked only by moving stim uli in
or near the plane o f convergence, that is, by stim uli with
near-zero disparity (Section 2 2 .6 .1 ). It is therefore not sur­
prising that the am plitude o f L V O R remained large when
the random -dot background was visually removed from the
depth plane o f the fixation target. O n e could just as well
conclude from their results that distance scaling o f L V O R is
controlled by the o b ject to which the animal is attending,
w hich is norm ally the one that the animal is fixating.
W ith passive movement of the body, the velocity of
L V O R was larger than required for far viewing and smaller
than required for near viewing. However, with accive move­
m e n t distance scaling of L V O R has been reported to be
more adequate. M ost studies involving passive m ovem ent
used a single light, while studies involving active movement
used a richer visual display. Wei and Angelaki (2 0 0 4 ) co n ­
cluded trom their earlier studv/ that visual cues to distance
arc not responsible for the difference betw een passive and
active movement. They found that L V O R velocity was­
her ter adjusted to viewing distance when a rotational co m ­
ponent was added to the linear m otion ot monkeys. They
concludcd that sim ultaneous activity o f the otoliths and
canals improves distance scaling o f L V O R .
Iiusctcini et al. (1 9 9 1 ) found that the velocity o f the ini­
tial open-loop portion o f O K N evoked by linear m otion o f
a texturcd display past a stationary m onkey was inversely
related to viewing distance. However, the gain o f closed-
loop O K N was independent o f viewing distance. They
assumed that this effect was produced by depth cues such as
vcrgcncc and accom m odation. However, there could per­
haps have been a direct neuromuscular eflect ol vergence
state on eye velocity in the period before visual feedback
becam e operative. They suggested thac, ac near viewing,
the increase in the peak velocity o f O K N is offset by a
nonlinear speed saturation in the L V O R system.
In a subsequent paper trom the same laboratory, Kawano
c t al. (1 9 9 4 ) measured the initial optokinetic response o f
monkeys to a 4 0 7 s sideways m otion o f a 29°-wide central
random -dot display. The O K N response was enhanced
when a stationary random -dot display surrounding the
stimulus had an uncrossed disparity, which made it appear
more distant than the moving central display. The O K N
response was attenuated when the surround display was stc-
rcoscopicallv nearer than the central display. Presumably,
the central display appeared nearer when the surround dis­
play was far and more distant when the surround display
was near.
Sim ilar results were obtained with human subjects,
although the dependence o f the initial velocity o f O K N on
viewing distance varied with stimulus velocity and other
factors (B u settin i c t al. 1994).
In o u e e ta l. (1 9 9 8 ) found that some cells in M S T o fth e
alert m onkey increased their response to visual m otion as
vergence increased, w h ileother cells increased their response
as vergence decreased.
 1 0 .9 .3 V E R G E N C E I N D U C E D BY Each cxtraocular muscle has an outer o rb ita l layer and
FO RW A RD M O T I O N an inner global layer. Each layer has tw o main types o f
muscle fibers. The first type consists o f singly innervated
Forward m otion o f the body with the head facing in the
fibers. Each fiber receives one m otor axon that ends in a
direction o f m otion evokes a convergence eye movement.
cluster o f neuromuscular ju n ction s at a restricted locus on
Backward m otion o t the body evokes divergence.
the muscle fiber ( en plaque endings). These fibers are fast
In the dark, the stim uli for these responses arise in the
acting. The second type o f muscle fiber arc smaller with
otolith organs. Angelaki and M cH enry (1 9 9 9 ) had m on­
many neuromuscular ju n ction s distributed over the their
keys fixate a visual target at a distance o f 2 0 cm . Ju st after the
whole length [en grappe endings). These fibers are slow
target was switched off, the animals were subjected to an
acting but can m aintain con stan t states o f tonic co n trac­
impulsive linear m otion. Forward m otion induced conver­
tion. It is n o t known whether these m ultiple endings arc
gence with a latency o f 7.1 ± 9 .3 ms. Backward m otion
derived from one o r several m otor axons. The two types o f
induced divergence with a latency o t 1 2.5 ± 6.3 ms for the
muscle fibers form distinctive subtypes within both the
adductingeye and o f 18.9 ± 6.3 ms for abducting eye. These
orbital and global layers (see Spencer and Porter 1988;
latencies were sim ilar to those they obtained for version
Porter and Baker 1992). There are distinct types o f efferent
induced by lateral m otion o f the head.
nerve fibers. Som e have a mean diam eter o f 2.5 pm and are
W hen the eyes arc open, vcrgcncc induced by forward
unmyelinated, while others have a mean diam eter ot about
body m otion is influenced by the loom ing o f the image o f
9 ym and arc myelinated (Alpern and W olter 1956).
the visual scene (Section 10.3), by changing lens accom m o­
A fferent nerve fibers convey signals from sensory cells in
dation (Section 1 0 .4 .1 ), and by the changing binocular dis­
specialized muscle fibers (muscle spindles) and Golgi
parity o f the images (Section 10.5.2).
tendon organs. M any o f the smaller sensory or m otor axons
The coupling between vergence and body m otion could
innervate blood vessels.
be learned through the association o t visually induced vcr-
N eurons in the oculom otor nuclei that project to the
gence and vestibular stimuli. If.so, one should be able to train
rectus muscles are segregated into three groups: A , B, and
the vergence system to respond to types o f body m otion that
C . C ells in group С have smaller cell bodies and thinner
do n o t norm ally induce vergence. S ato et al. (2 0 0 4 ) rewarded
axons than those in groups A and В and p roject to smaller
monkeys for tracking a spot that approached when the body
and slower muscle fibers (P orter et al. 1 9 8 3 ). It has been
was pitched forward 5° and receded when the body pitched
suggested that grou p -C cells form a d istinct pathway for
upward 5°. D uring 1 hour o f training the gain o f vergence
vergence (Jam pel 1967; Biittner-Ennever and Akert 1981).
increased and its phase lag decreased. Before training, body
However, Keller and Robinson (1 9 7 2 ) recorded the activ­
pitch in the dark did not induce vergence. After training,
ity o f cells in rhe abducens nucleus o f rhe m onkey and
body pitch induced a significant degree o f vergence.
showed that no type o f eye m ovem ent was the exclusive
It should be possible to reverse the sign o f vergence induced
product o f a particular set o f neurons. By their own admis­
by linear motion o f the body in the dark by training in which
sion, their electrode may have tailed to record the activity o f
forw ard body motion is coupled with a receding visual target
small cells exclusively devoted ro vergence. W c can n ot be
an d backward body motion with an approaching target.
sure that integration ot version and vergence signals is
achieved in the ocu lom otor nuclei rather than in the mus­
cles through the mediation ot distinct efferent fibers.
10.10 PH YSIO LO G Y OF VERG EN CE
The m otoneurons from the ocu lom otor nuclei to the
extraocular eve muscles are known as the final com m on
10.10.1 О С V L O M О Т О R N E RVES i

path (R obinson 1 9 7 5 ). It is supposed that signals from

AND NUCLEI
Th e three pairs o f extraocular muscles shown in Figure 10.1
receive innervation from three cranial nerves: the third
(ocu lom o to r), the fourth (trochlear), and the sixth
(abducens) nerve. Each nerve originates in a brainstem
nucleus o f the same name. Together, the three nuclei are
callcd the ocu lom otor nuclei, w hich is confusing because it
is also the name o f one o f them . The superior recti and supe­
rior obliques receive an exclusively contralateral innerva­
tion from the ocu lom otor and trochlear nuclei respectively.
The other muscles receive an exclusively ipsilateral innerva­
tion. Inputs to the inferior rectus and inferior oblique arc
from the oculom otor nucleus and those to the lateral recti
are from the abducens nucleus (P orter c t al. 1983).
higher centers com bine into com m on signals, which gener­
ate a m achine-like response in the muscles tor all types o f
eye movement. Relationships between m otoneuron firing
rates and instantaneous eye positions have been modeled by
a simple transfer function (R obinson 1981). W e will now
see that recent evidence has cast doubt on these ideas.
10.10.2 S U B C O R T I C A L C O N T R O L
OF V E R G E N C E
1 0 .1 0 .2 a Terminal Signals for C o n ju g a te
Eye M o v em e n ts
It was com m only believed until the early 1950s that, while
convergence required active contraction o f extraocular
rate specifically during convergence, and a few specifically
during divergence. W h ile m ost o f them responded during a
change in vergence or during a change in accom m odation,
some responded only to changes in vergence and some only
cochanges in accom m odation (Z h an g et al. 1992). Vergence-
angle cells responded with m onosynaptic latencies to an ti­
drom ic stim ulation ot m edial rectus m otoneurons in the
ipsilateral ocu lom otor nucleus but not in the contralateral
o cu lo m oto r nucleus (Z h a n g et al. 1991). Thus, convergence
does not involve efferent pathways th at cross the m idline.
Vergence-angle cells have also been found in a su bcorti­
cal region dorsal to the nucleus o f t h e third nerve in alert
monkeys that were trained to track a visual target as it
moved sinusoidally to-and-fro along the visual axis o f one
eye at 0.1 or 0 .2 H z (Judge and G um m ing 1986). O n aver­
age, the firing rate o f these cells increased or decreased by 16
spikes/s for each degree o f change in vergence. Like the cells
described by Mays, m ost o f them increased their firing rate
during convergence rather than during divergence. There
was no response when the eyes moved conjugatelv, and
m ost cells responded in the same way with both eyes open
as with only one eye open. The cells had a mean phase lag o f
34° relative to the stimulus. This is greater than the phase lag
o f 16.8" reported for cclls in the o cu lo m oto r nuclei. Delay
betw een a cell firing and the start o t a vergence movement
varied betw een 35 and 7 0 ms. W h en a cell in this region
was electrically stim ulated, a response occurred with a mean
delay o f about 3 0 ms.
Mays et al. { 1 9 8 6 ) discovered another class o f vergence-
related cells in the same area, just dorsal and lateral to the
ocu lom otor nucleus, and in a m ore dorsal area extending
into the pretectum . These cells responded with a burst ot
activity just before and during vergence movements, which
alert m onkeys had been trained to make to stimuli that
stepped in depth or moved along a depth ramp. The firing-
rate profile o f these cells was related to the velocity profile
ofv erg en ce, and the total number o f spikes in a burst was
related to the size o f vergence. These v erg en ce-b u rst cells
responded in the same way when the anim al tracked a depth
ramp, thus m aintaining the stimulus in a state o t near zero
disparicy. From this, it was argued that these cells respond
to eye velocity rather than to the velocity o f changing dis­
parity. O n average, the response o f a ccll preceded the eye
m ovem ent by 22 ms.
Som e cells in this region showed a burst o f activity
related to response velocity and a tonic response propor­
tional to che angle o f maincained vergence. The tonic
response showed only tor larger movements, presumably
because only a large m ovem ent brought the eyes to a posi­
tion o f gaze for w hich a sizeable tonic innervation was
needed to prevent them from drifting back to their resting
state. These are vergen ce b u rst-to n ic cells. M ost o f rhe
burst and burst-tonic cells responded only to convergence,
but a small num ber o f divergence burst anil burst-tonic
cells were found. Burst cells presumably torm the neural
substrate o f transient vergence (Section 10.5.10). Burst-
tonic cells in the prepositus hypoglossi are involved in the
generation o f unequal saccadcs (Sylvestre et al. 2 0 0 3 ).
In many people with phoria, the tonic imbalance
betw een the eyes returns to its prccxposurc value during a
period o f exposure to base-in o r base-out prisms (Section
10.2.5). M orley c t al. (1 9 9 2 ) recorded from cclls in the
region dorsal to the oculom otor nucleus in the alert monkey,
before and after the animal had been exposed for some time
to visual targets at one o f various accom m odation and ver­
gence distances. O nly a tew o f the cells retained the same
relationship betw een firing rate and vergence angle, so
whatever mechanism is responsible tor the adaptation ot
phoria to changed vergence demand must lie outside chis
region.
1 0 .1 0 .2 d V c rg cn cc C o n tr o l bv th e C e re b e llu m
an d N R T P
The vermis o f che ccrcb ellu m is involved in che concrol o f
both version and vergence (K eller 1989). Patients with cer­
ebellar dysfunction have poor ocular alignm ent com bined
with esophoria or, in many cases, esotropia. These patients
also show disconjugate saccadic dysmetria (Versino cc al.
1 9 9 6 ; Takagi et al. 2 0 0 3 ). There is conflicting evidence
about w hether there is reduced adaptation to prism-induced
phoria (M ild er and Reinecke 1983; Hain and Luebke
1990).
C ells have been found in che poscerior interposed
nucleus ( IP) o f the monkey cerebellum that increase their
activity during either divergence or far accom m odation,
both when the responses are elicited by m isaccom m odation
or by disparicy (Z h an g and G am lin 1998).
The nucleus reticularis tegm enti pontis (N R T P ) receives
afferents from the frontal eye fields in che froncal lobes and
has reciprocal connection s with the cerebellum . It is
involved in the control o f conjugate saccadic and pursuit
eye movements. Som e cells in the N R T P increase their
activity as vergence and accom m odation move to far view-
ingor to near viewing (G am lin etal. 1996). M icrostim ulation
o f these cells produces a com bined far response or near
response. Their activity is n o t related to conjugate eye m ove­
ments (G am lin and Clarke 1 9 9 5 ). Thus, chese cclls in che
N R T P are part o f the corticocerebellar pathway controlling
vergence and accom m odation.
1 0 . 1 0 .2 e V erg en ce C o n tr o l by th e
S u p e r io r C o llic u lu s
The deeper m otor layers o f the rostral superior colliculus
are im plicated in the jo in t concrol o f vergence, accom m oda­
cion, and pupil diamecer (che near criad response). Corcicai
areas involved in control o f accom m odation and vergence
p ro ject to this region o fth e superior colliculus and then ro
the pretectum and other subcortical areas controlling
accom m odacion and vcrgcncc (Ju dge and G um m ing 1986;
O hcsuka and Nagasaka 1 999). Lesions o f the prctectum
produce vergence defects (Lawler and Cow ey 1986).
Stim ulation o l a saccadc-producing site in the rostral supe­
rior colliculus o f the alert monkey n o t only stopped a visu­
ally evoked saccade but also reduced a pure vergence
response or a vergence response associated with a saccade
(C haturvedi and Van Gisbergen 1 9 9 9 ,2 0 0 0 ).
This evidence suggests that saccadc-relatcd collicular
cells in the colliculus arc tuned ro both che direccion and
depth o t stim uli. But the saccade-vcrgcnce interactions
could be due to stim ulation o f brainstem om nip ause neu­
ron s that are active between saccades (G u itto n 1999). In
any case, stim ulation o f the colliculus does not produce
pure vergence responses.
W alton and Mays (2 0 0 5 ) confirmed that the spike fre­
quency o t cells in the monkey colliculus during a saccade is
reduced when che saccade is accompanied by vergence.
However, none ot the collicular neurons showed a pattern o f
discharge expected o f a cell that controls both directional and
in-depth changes o f gaze. They concluded that the superior
colliculus mostly provides signals for conjugate saccades.
10.10.3 CORTICAL CONTROL
OF V E R G E N C E
Cells in V I respond ro local absolute disparities rather than
to relative disparities (Scction 11.4.1). C ells that respond to
che relacive disparicy becween che images o f cwo objects have
been found in V 2 (Thom as et al. 2 0 0 2 ). Relative disparities
are im portant for the perception o f che 3 -D scruccure o f che
scene. They are noc required to control vergence when we
change fixation from one objecc со another. However, rela­
tive disparities may allow us to preprogram changes in ver­
gence required to scan over a surface curved in depth.
Experiments are required to determine whether people can
execute a pattern o f vergence movements to a series o f points in
depth just after the points have been removedfrom view.
Beyond V 2 , visual processing becom es parcidoned into
the dorsal and ventral streams (Section 5 .8 ). The following
evidence suggests that disparity processing for the control
o t vergence is perform ed in the dorsal stream and in the
superior colliculus.
C clls in the suprasylvian area o t the parieto-occipital
cortex (C lare-B ishop area) in cats respond со accom m oda­
tive stim uli, changes in binocular disparity, and m otion-in-
depth (Bando et al. 1 9 8 4 , 1 9 9 6 ; Toyama et al. 1986). These
are all stimuli for vergence. Electrical stim ulation o f cells in
the caudal part o f this area evokes vergence movements
(T o d a e t al. 1991) . Bilateral lesions in rhe suprasylvian area
reduced the am plitude and velocity o f vcrgcncc movements.
Unilateral lesions affected only the contralateral eye,
resulting in asymmetrical vergence (T a k a d a ct al. 2 0 0 0 ).
Accivicy o f som e cells was correlated wich che peak veloc­
ity o f vergence, while activity o f others was correlated with
the peak velocity or amplitude o f accom m odation, and that
o f others with both responses (Takagi et al. 1993).
M ore details abouc che roles o f ditferenc regions o f che
suprasylvian area in the control ot vergence are provided by
T o d a e t al. ( 2 0 0 1 ,2 0 0 6 ) .
C ells in the medial superior temporal cortex ( M S T ) o f
the monkey are involved in the control o f vergence. Sakata
et al. ( 1 9 8 3 ) found that 7 7 % o f cells in the m onkey poste­
rior parietal area, w hich includes M S T , responded during
conjugate (fro n tal) pursuit eye movements. A bou t 16% o f
the cells responded when the animals pursued a point o f
light moving in depth toward or away from che head.
Takem uraet al. (2 0 0 1 ) recorded from M S T cells in alert
m onkeys 5 0 to 110 ms after horizontal disparity steps o f
varioussizes were applied to a random -dot pattern. Disparity
tuning functions o fth e cells resembled those o f cells in V I ,
as described in Section 11.4.1. The mean disparity-tuning
function o f all the cells fitted the curve describing vergence
magnitude as a function o f disparity step size. Takemura
et al. concluded that the m agnitude, direction, and time
course o t the initial vergence response to disparity steps are
determ ined by the sum o f activity o f disparity-sensitive cells
in M S T .
M ore recently, Akao et al. (2 0 0 5 b ) found that 61 % o f
cells in M S T o fth e monkey responded only during co n ju ­
gate pursuit o f a light spot, 2 1 % responded during either
frontal pursuit or vergence tracking, and 18% responded
only during vergence cracking. Abouc a third o f che vcr-
gence-rclated cells also responded when the monkey fixated
a stationary spot while a second spot moved back-and-forch
in depch. These cells cherefore, responded со che disparicy
vergence signal even when the eyes did not move. About
3 0 % o f vergence-related cells discharged ac lease 20 ms
before the onset o f the response, which suggests that these
signals initiate vergence eye movements.
Responses ot cells in the area L IP on the lateral bank ot
the intraparietal sulcus o f the m onkey (Section 5.8 .4 c) are
related to rapid changes o t gaze in 3-D space (G n ad t and
Mays 1995). These m ovem ents involve both saccadic and
vergence com ponents. Each cell responded differentially to
the position o f a visual target in a frontal plane and this d if­
ferential response was independent o f the distance o f the
frontal plane from the monkey. However, som e cells
responded best when the stimulus remained in the same
frontal plane as the initial fixation, others when the target
was stepped toward the monkey, and others when it stepped
away. For many cells, depth tuning could be evoked by
either an accomm odative cue to distance or by binocular
disparity, but m ost cells responded best when both cues
were available. The cells responded in a sim ilar fashion after
the eyes had moved in response to targets that had been
switched o ff before the movement began. Thus, responses
were related to the difference between current eye position
and the desired eye position rather than to the position o f
retinal images at the tim e o f the response. This means that
inform ation abouc changes in eye position, derived from
proprioception or m otor outflow, feeds in to chese cells.
Hum ans are able со make com bined vergence-version
eye m ovem ents to rem embered targets after intervening
changes o f fixation (K rom m enhoek and Van Gisbergen
1994). These cells in L IP therefore generated a prem otor
signal for rapid eye movements in 3-D space relative to the
fixation plane.
Many disparity-tuned cells in area L IP o f the rhesus
m onkey project to the m otor map o f the superior colliculus
(G nadt and Beyer 1 998). They also p roject to the frontal
eye field.
Positron emission tomography (P F .T ) revealed that,
when human subjects pursue an approaching o b ject with
vergence eye m ovem ents, neural activity occurs bilaterally
in the tem porooccipital cortex. This is consistent with
single unit data trom animals. Activity also occurred in the
right fusiform gyrus (hum an analog o f V 4 ) in the ventral
pathway o f cortical processing (H asebe et al. 1999).
The frontal eye fields o f the cerebral cortex are involved
in the control o f saccades and pursuit eye movements
(G am lin e t al. 1 996). Jam pel ( i 9 6 0 ) elicited vergence
responses in the m onkey by stim ulation o f a frontal eye
field. G am lin and Yoon (2 0 0 0 ) found a region in the frontal
eye fields, ju st anterior to the saccade-related region, which
is involved in the co n tro l o f vergence and accom m odation.
Ferraina et al. (2 0 0 0 ) found cells in a frontal eye field that
respond to coarse disparities.
The frontal eye fields have strong reciprocal connections
with medial superior temporal area (M S T ), which is involved
in processing visual m otion and binocular disparicy.
Many cells in the frontal eye fields o f macaque monkeys
m odulate their firing during pursuit eye movements. O f
these cells, 2 5 % responded only during pursuit o f a light
spot in the frontal plane, 66 % responded during either
frontal pursuit or vergence tracking ot a spot m oving in
depth, and 9% responded only during vergence tracking
(Fukushim a et al. 2 0 0 2 ). Responses o f these cells during
frontal or vergence tracking persisted during intervals when
the stimulus was blanked. This indicates that the responses
have a m otor com pon ent that is independent o f sensory
inputs during the m ovem ent. For about h a lf the cells that
responded during vergence tracking, response amplitude
increased linearly with peak vergence velocity over a m od­
erate range o f velocities. Also, abouc h alf the vergence-
tracking cells discharged at least 20 ms before the onset ot
vergence. M any vergence-tracking cells also responded to a
spot o f light moving in depth, with eyes stationary. Som e
cells showed a tonic discharge related to the stationary angle
of vergence. The response frequency of convergence-related
neurons increased as vergence angle increased, while the
response frequency o f divergence-related neurons increased
as vergence decreased (A kao et al. 2 0 0 5 a ).
Thus many cells in che frontal eye fields code eye move­
m ents in 3 -D coordinates and produce signals for tracking
an o b ject in 3 -D space. The com plex signal must be d ecom ­
posed so that distinct brainstem m echanism s for version
and vergence receive correct signals. We have already seen
that the nucleus reticularis tegm enti pontis (N R T P ) in the
brainstem receives afferents from the froncal eye fields. This
nucleus is involved in the control ol saccades, pursuit eye
movements, accom m odation, and vergence (G am lin ec al.
1 9 9 6 ). Thus, the frontal eye fields and the N R T P arc-
involved in the control o f all voluntary eye movements,
conjugate and disconjugate.
10.10.4 PH Y S I О LO G Y О F С YC 1. 0 V E R G E N С E
L ittle is known about the neurology o f cyclovergence. The
rostral interstitial nucleus o f th e m edial lon g itu d in al
fascicu lu s ( M l . F ) is involved in the control o f torsional and
vertical saccades, and the in terstitial n u cleus o f C a ja l is
involved in slow torsional and vertical gaze control, includ­
ing torsional and vertical vestibuloocular responses. Eye
torsion and head deviation were induced bv* stim ulation o f
the nucleus o f C ajal in monkeys (W estheim er and Blair
1 9 7 5 ) and in humans (Lueck et al. 1991) . The nucleus o f
C ajal receives inputs lrom the paramedian pontine reticular
form ation ( P P R F ) , a center concerned with the coord ina­
tion o f all rapid eye movements, and projects to the o cu lo ­
m otor and trochlear nuclei. Neurons in the right nucleus o f
C ajal responded when the eyes rotated clockwise from the
point o f view o t the animal. Those in the left nucleus
responded when the eyes rotated counterclockw ise. C ells in
the same nucleus responded when the eyes executed vertical
saccades. Both up and down movements are represented
in both left: and right nuclei (V ilis et al. 1 9 8 9 ). M icro ­
stim ulation o f cells in the interstitial nucleus o f C ajal in the
monkey induced conjugate saccadic torsional eye m ove­
m ents, which obeyed the same clockwise-counterclockw ise
rule (Craw ford et al. 1991).
Unilateral inactivation o f the interstitial nucleus o f
C ajal in monkeys elim inated ipsilateral rapid torsional eye
movements, torsionallv displaced the eyes (and o f L istings
plane) to the contralateral side, and produced an ipsilater-
ally beating torsional nystagmus with a vertical com ponent.
Unilateral inactivation also caused a slowing o t rapid
downward eye movements, indicating a failure o f the neural
integrator (Craw ford and Vilis 1 9 9 2 ). Inactivation o f both
interstitial nuclei o f C ajal restored torsional balance and
removed the torsional nystagmus, but left a vertical
nystagmus (H elm chen e t al. 1998).
Unilateral inactivation o f rhe M L F produced contralat-
crally beating torsional nystagmus. Bilateral inactivation
elim inated the saccadic com ponents o f torsional and
vertical eye movements (Suzuki e t al. 1995).
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by m icro g lia P ro c N a tl A c a d S e t 1 0 0 1 5 9 8 3 - 8 | 5 .5 -lf,6 .4 .2 d ]
A b b o tt L F , D ayan P ( 1 9 9 9 ) The effect o f correlated variability
o n th e accu racy o f a p op u lation co d e N eu ra l С о т р и t 11 9 1 - 1 0 1
[4 .2 .5 a ]
A b b o tt L F , Scjn o w sk i T J ( 1 9 9 9 ) N e u r a l co d es a n d d is tr ib u te d rep rc se n ta -
tio n s :fo u n d a tio n s o f n e u r a l co m p u ta tio n M I T Press, C am b rid g e, M A
( 4 .2 .6 b , 5 .6 .5 ]
A b b o tt, M L , S ch m id K L , S tra n g К С ( 1 9 9 8 ) D ifferen ces in th e a cco m ­
m o d atio n stim u lu s response curves o f adulc m yopes and cm m ctm p es
O p / M P h y sio l O p t 1 8 1 3 - 2 0 (9 .6 .2 a]
A b el L A , Sch m id t D , D c ll’O sso L F, D a r o ff R B ( 1 9 7 8 ) Saccad ic system
p lasticity in h um ans A n n N eu r o l 4 3 1 3 - 1 8 [ 1 0 .8 .3 d J
A bel P L . O 'B r ie n B J % O lavarria J F ( 2 0 0 0 ) O rg an izatio n o f callosal
linkages in visual area V 2 o f m acaque m on k ey / C o m p N e u r o l 4 2 8
2 7 8 - 9 3 [5 .3 .5 ]
A b ram ov I, G o rd o n J , H en d rick so n A , c t al. ( 1 9 S 2 ) The retin a o f
n ew born hum an in fa n t S cien ce 2 1 7 2 6 5 - 7 (6 .3 .2 a )
A ckroyd C, H um ph rey NK, W arrin g to n EK (1 9 7 4 ) Lasting
effects o f early blin d n ess A case s t u d v ^ ^ r / f E x p P sy ch ol 2 6 1 1 4 - 2 4
[8 .1 .3 ]
A dam s L )L , H o rto n J C ( 2 0 0 2 ) Shad ow s cast by retinal blood vessels in
p rim ary visual c o rte x S cien ce 2 9 8 5 7 2 - 6 (6 .7 .2 d ]
A dam s D L , H o rto n J C ( 2 0 0 3 ) C ap ricio u s expression o f co rtical
co lu m n s in the prim ate brain N a t N c u r o s d 6 1 1 3 - 1 4 [5 .7 .2 f 1
A dam s D L , H o rto n J C (2 0 0 6 a ) M o n o cu la r cells w ith o u t ocu lar
d om in an ce colu m n s J N eu ro p b y sio l 9 6 2 2 5 3 - 6 4 [ 5 .7 .2 f ]
A dam s D L , H o rto n , J C (2 0 0 6 b ) O cu la r d om in an ce colu m n s in
strabism us V is N cu ro sd 2 3 7 9 5 [ 5 - 7 .2 f ]
A dam s D L , Z e k i S ( 2 0 0 1 ) Fu n ctio n al org an ization for m acaque V 3 for
stereoscop ic d ep th J N etiro p b y sio l 8 6 2 1 9 5 - 2 0 3 [5 .8 .2 b ]
A d am s D L , S in c ic h L C , H o rto n J C ( 2 0 0 7 ) C o m p le te p attern o f ocu lar
d om in an ce co lu m n s in hum an prim ary visual c o rtc x / N c u ro sd 2 7
1 0 3 9 1 - 4 0 3 [5 .7 .2 a ]
A dam s JP , D u d ck SM (2 0 0 5 ) L atc-p hasc lo ng -term p o ten tia tio n :
g ettin g to the nucleus N a t R ev N e u r o u i 6 7 3 7 - 4 3 [6 .4 .4 Г ]
A d am s M M , H o f P R , G actass R , c t al. ( 2 0 0 0 ) V isual co rtica l p ro jectio n s
and eh cm o a rch itcccu rc o f m acaque m on k ey pulvinar J C o m p N eu ro l
4 1 9 3 7 7 - 9 3 | 5.5.4b , 5 .9 .1 ]
A dam s R J, C o u ra g e M L , M ercer M E ( 1 9 9 1 ) D eficien cies in human
n eon ates’ c o lo r vision : p h o to rcccp to ra l and neural exp lan ation *
B t b a v B ra in R es 43 109-14 (7.2.1 с j
A dam s W J , Banks M S , van F.c R ( 2 0 0 1 ) A daptation to three-dim ensional
d isto rtio n s in hum an vision N a t N cu ro sd 4 1 0 6 3 - 4 [9 .9 .3 ]
A d clson F.H , Bergen J R ( 1 9 8 5 ) Sp atio tem p o ral energy m odels fo r the
p ercep tio n o f m o tio n / O p t S o c A m A 2 2 8 4 - 9 9 [5 .6 .4 c , 1 0 .3 .2 d ]
A d o rjan P, L ev itt J B , L u n d J S , O b crm ay cr К ( 1 9 9 9 ) A m od el fo r the
in tra co rtica l o rig in o f orien ta tio n preferen ce and tu n in g in m acaquc
striate c o r tc x V is N e u m c i 1 6 3 0 3 - 1 8 15.5.6a)
A d rian F.D, M a tth ew s R ( 1 9 2 7 ) T h e a ctio n o f light o n th e eye J P h y sio l
6 3 3 7 8 - 9 0 [5 .1 .4 a ]
A crtscn A M H J, G crstcin G L , H abib M K , Palm G ( 1 9 8 9 ) D yn am ics o f
n eu ron al firing co rre la tio n : m o d u latio n o f “effective co n n e ctiv ity "
J N eu ro p b y sio l 6 1 9 0 0 - 1 7 [4 .3 .4 a ]
A ggarw ala K R , N o w b o tsin g S , K ruger P B (1 9 9 5 a ) A cco m m o d atio n to
m o n o ch ro m atic and w h ite-ligh t targets In v es t O p h th a l Vis S et 3 6
2 6 9 5 - 7 0 5 [9 .8 .2 d ]
Aggarw ala K R , K ru ger F.S, M ath ew s S , K ruger P B (1 9 9 5 b ) Sp ectral
bandw idth and o cu lar acco m m o d atio n / O p t S o c A m 12 4 5 0 - 5 5
|9.S.2d)
A ggou n -A ou aou i D , K ip cr D C , In n o cen ti G M ( 1 9 9 6 ) G ro w th o f
callosal term in al arb ors in prim ary visual acres o f the cat E u r J
N cu ro sd 8 1 1 3 2 - 4 8 |6.4.6d)
A g m o n -S n ir H , С а п C E , Rinzel J ( 1 9 9 8 ) T h e role o f d en d rites in
a u d ito ry co in cid e n ce d e te ctio n N a tu r e 3 9 3 2 9 8 - 7 2 (4 .2 .2 ]
A gu iloniu s F ( 1 6 1 3 ) O p ticoru m lib r t s e x P lan tin A n tw erp (2 .1 0 .3 b ]
A gu lh on C , F iacco Т А , M c C a rth y K D ( 2 0 1 0 ) H ip p ocam p al sh ort- and
lo ng -term p lasticity are n o t m od u lated by astro cy te С а Ч signaling
S cien ce 1 2 5 0 - 4 [5-5-1 f ]
A hissar E , V aadia E , A hissar M , cc al. ( 1 9 9 2 ) D ep en d en ce o f co rtical
plasticity o n correlated activ ity o f single neu ron s and o n behavioral
c o n te x t S cUtjcc 2 5 7 1 4 1 2 - 1 5 ( 4 .3 .4 f ]
Ahlvcn G , L in d strom S , Lo F - S ( 1 9 8 5 ) In teractio n b etw een in h ib ito ry
pathways to principal cells in th e lateral gen icu late nucleus o t the cat
E xp Brain R es 5 8 1 3 4 - 4 3 (5 .2 .2 a ]
A h m ari S L , B u ch an an J , S m ith S J ( 2 0 0 0 ) A ssem bly o f presynaptic active
zones from cy to p lasm ic tran sp ort packets N a t N c u r o s d 3 4 4 5 - 5 1
(6 .4 .4 a )
A hm ed B, A n d erson J C , D ou glas R J, e t a l. ( 1 9 9 4 ) Polvncuronal in n erv a­
tio n o f spiny stellate n eu ron s in cat visual co rtex / C o m p N e u ro l 3 4 1
3 9 - 4 9 [5 .5 .1 d]
A iello A , W right K W . B o rch e rt M ( 1 9 9 4 } Independence o t o p to k in etic
nystagm us asym m etry an d b in o cu larity in in fan tile esotrop ia A rch
O p h th a l 1 1 2 1 5 8 0 - 3 (8 .4 .5 c ]
A izen b erg A , T k a ch e n k o A , W ein e r S , e t al. ( 2 0 0 1 ) C a lc itic m icro lenses
as part o t the p h o to re ce p to r system in bricclcstars N a tu r e 4 1 2
8 1 9 - 2 2 ( 6 .1 .2 ]
A k a o T , K urkin S A , F u k u sh im a J, Fukushim a К ( 2 0 0 5 a ) V isu al and ver­
gence eye m ovem ent*related responses o t pursuit n eu ron s in the
caudal fro n ta l eye fields to m o tio n -in -d ep th stim u li E x p B r a m R es
1 6 4 9 2 - 1 0 8 [ 1 0 .1 0 3 1
A kao T , M ustari M J, F u k u sh im a J, c t al. ( 2 0 0 5 b ) D ischarge с ha rac t eris­
tics o f pu rsu it neu ron s in M S T d urin g vergence eye m ovem ents
J N e u r o p b y s io l9 3 2 4 1 5 - 3 4 (1 0 .1 0 .3 ]
A k crm an C J,S m y t h D , T h om p son I D ( 2 0 0 2 ) V isual experien ce before
ev e-op en in g and the d evelopm en t o f th e rctin o g cn icu la tc pathw ay
N eu ro n 3 6 8 6 9 - 7 9 18.2.2b )
A kh tar M W ', R ain g o J, N elson El> , ct al. (2 0 0 9 ) H isto n c
d eacctylascs 1 and 2 form a dev elop m en tal sw itch th at co n tro ls e x cit­
a to ry synapse m atu ratio n and fu n ctio n / N eu ro sci 2 9 8 2 8 8 - 9 7
(6.6. 1a)
A lb an o JF ., M arrero A ( 1 9 9 5 ) B in o cu la r in teractio n s in rapid saccadic
ad ap tation Vis R es 3 5 3 4 3 9 - 5 0 [1 0 .8 .3 a ]
A lb ert M K ( 2 0 0 0 ) T h e g en etic view p oin t assum ption an d Bayesian
in feren ce P ercep tio n 2 9 6 0 1 - 8 (3 .6 )
A lb in R I ., Sakuraai SY , M ak o w icc R I ., cc al. ( 1 9 9 1) E x cita to ry am in o
acid s, G A B A A and G A B A B b in d in g sites in hum an striate c o rtcx
C crcb C o rtc x l 4 9 9 - 5 0 9 [5 .5 .2 c )
A lb rc c h t D G ( 1 9 9 5 ) V isual c o rtc x neu ron s in m on k ey and cat: effect o f
c o n tra st o n the spatial and tem p oral phase transfer fu n ctio n s Vis
N eu ro sd 1 2 1 1 9 1 - 2 1 0 [5 .6 .4 b ]
A lb rc c h t D G , 1 lam ilcon D B ( 1 9 8 2 ) Striate co rtex o f m on key and cat:
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A lb rig h t I 'D ( 1 9 9 2 ) F orm -cu c in varian t m o tio n p rocessing in prim ate
visual c o r tc x S cien ce 2 5 5 1 1 4 1 - 3 [5 .8 .4 b ]
A lb rig h t T D . D esim o n e R ( 1 9 8 7 ) L o ca l precision o t visu otopic o rg an i­
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A lbu s K . W o lf W ( 1 9 8 4 ) Early postn atal developm en t o f neuronal
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A lexand er I, C o w ey A ( 2 0 0 9 ) The co rtic a l basis o f global m o tio n d etec­
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A lh azen K itiib a l-m ^ w a z ir (B o o k o f o p tics) In I h e o p tics o f Ib n
a l-H a y th a m 2 volum es ( Translated by A l Sab ra) W arburg In stitu te,
U n iv ersity o f L o n d o n 1 9 8 9 [2 .2 .4d 2 j
A lk o n d o n M , Pereira E F A , E iscn b crg H M , A lb u qu erq u e E X ( 2 0 0 0 )
N ic o tin ic recep to r activ ation in hum an ccrcb ral co rtical in tcm cu -
rons: a m ech an ism for in h ib itio n and d isin h ib itio n o t neuronal
n etw ork sJ N eu ro sd 2 0 6 6 - 7 5 [5 .5 .2 g , 5.9.1 ]
A llen D , B an k s M S , N o rc ia A M ( 1 9 9 3 ) D o cs ch ro m a tic sensitivity
d evelop m ore slow ly than lu m in an cc sensitivitv? V is R es 3 3 2 5 5 ^ - 6 2
[7 .2 .1 c ]
A llen D , Tyler CV\", N o rcia Л М ( 1 9 9 6 ) D ev elo p m en t o f gratin g acuity
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hum an in fa n t V is R es 3 6 1 9 4 5 - 5 3 [7 .2 .1 a ]
A llen D C ( 1 9 7 4 ) V ertical prism adaptation in an iso m etro p cs A m J
O f to m P h y sio l O pt 51 2 5 2 - 9 [ 1 0 .2 .6 a ]
A llen D C { 1 9 3 7 ) A test fo r an iseik on ia by the use o f cen tral fixation and
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A llen M J ( 1 9 5 3 ) A n investigation o f th e tim e ch aracteristics o f a cco m ­
m od ation and convergence o f t h e eyes A m J O p tom A rch A m A ca d
O f to m 3 0 3 9 3 - 4 0 2 [1 0 .4 .3 a ]
A llen M J, C a rte r J H ( 1 9 6 7 ) T h e torsion al co m p o n e n ts o f the near reflex
A m ) O f tom A rch A m A c a d O fto m 4 4 3 4 3 - 9 [10.1.2d» 1 0 .7 .1 ,10.8.1b)
A Hen doer Ier K L , Sh atz C J ( 1 9 9 4 ) T h e su bp late a transient n co co rtical
stru ctu re: its role in the d evelopm en t o f co n n e ctio n s betw een
thalam us an d c o rte x A m i R ev N eu ro sd 1 7 1 8 5 - 2 1 8 [6 .4 .5 c )
A llcm lo crfcr К I., C a b c lli R J, Rseandon F., et al. ( 1 9 9 4 ) R eg u lation o f
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A lliso n D\V, G clfa n d V I. S p ccto r I, C ra ig A M ( 1 9 9 8 ) R ole o f actin in
a n ch o rin g postsynaptic recep to rs in cultured h ip p ocam p al neurons:
d ifferen tia l a tta ch m en t o f N M D A versus A M P A recep to rs ] N eu ro sd
I S 2 7 2 3 - 3 6 [5 .5 .2 b ]
A lliso n R S , H ow ard IP, Fang X ( 2 0 0 0 ) D e p th selectivity o f vertical
fusional m echanism s V ision R es 4 0 2 9 8 5 - 9 8 110.6.3c]
A lliso n R S , H ow ard IP, Fang X ( 2 0 0 4 ) Stim u lu s in tegratio n for
h o riz o n ta l v crg cncc E x p B r a in R es 1 5 6 3 0 5 - 1 3 ( I0.5.*4b]
A llm an J M , M eizin F, M cG u in n css F L ( 1 9 8 5 ) D irectio n - and velocity-
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A lo n so J M , U srcy \ V M , Reid R C ( 1 9 9 6 ) Precisely co rrelated firing in
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A lpern M ( 1 9 4 6 ) Tlie a fte r -e tfc c t o f lateral d u ctio n testin g o n subse­
q u en t p h oria m easu rem ents A m / O p tom A rch A in A c a d O ptom 2 3
4 4 2 - 7 ( 1 0 .2 .5 1
A lpern M ( 1 9 5 8 ) V crgcn cc and a cco m m o d atio n 1. C a n change in size
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A lpern M ( 1 9 6 9 ) Types o f eye m ovem en t. In 7h e e y e (ed H D avson)
V ol 3 pp 6 5 - 1 7 4 A cad em ic Press, N ew York [ 1 0 .1 .3 b , 10.4.3b ]
A lpern M , Ellen P ( 1 9 5 6 ) A quantitative analysis o f the h o rizo n tal m ove­
m en ts o l the eyes in th e exp erim en t o f Jo h a n n es M u ller A m J O fh t h a I
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A lpern M , H o fstcttcr H\V ( 1 9 4 8 ) T h e effect o f prism o n eso tro p ia— a
case rep o rt A m J O p tom A rcf) A m A c a d O p tom 2 5 8 0 - 9 1 [ 1 0 .2.2c]
A lpern M , L arso n B F ( I 9 6 0 ) V crgcn cc and accom m od acion I V Effect o f
lu m in an cc q u a n tity on the A C / A A m J O p h th a l 4 9 1 14 0 - 9 [ 1 0 .4 .1 )
A lpern M , W o ltc r J R ( 1 9 5 6 ) The relatio n o f h o rizo n tal saccadic and
vcrgcncc m ov em en ts A rch O p h ih a l 5 6 6 8 5 - 9 0 ( 10 .1 0 .1 ]
A lpern M , K in caid \V M , L ubeck M J ( 1 9 5 9 ) V crgcncc and acco m m o d a­
tio n : III. Proposed d efin itio n s o f the A C /A ratios A m J O p h th a l 4 8
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A lcm ann L , Lu h m an n 11J, G rcu cl J M , Sin ger \\" ( 1 9 8 7 ) Fu n ctio n al and
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Alvarez T L , Sem m low J L . Yuan W , M u n o z P ( 1 9 9 9 ) D y n am ic d etails o f
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Alvarez T L * Sem m low J L , Yuan W , M u n oz P ( 2 0 0 0 ) D isp arity vergence
dou ble responses processed bv in tern al erro r Vis R es 4 0 3 4 1 - 7
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Alvarez T L , Sem m lo w JL , P ed ron o С (2 0 0 5 a ) D ivergen ce eye
m ov em en ts arc d ep en d en t o n in itia l stim ulus p osition Vis R es 4 5
1 8 4 7 - 5 5 5 110.5.71
Alvarez T L , Bhavsar M . Sem m low J L . c t al. (2 0 0 5 b ) S h o rt-term predic­
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Alvarez V A , S ab atin i B L ( 2 0 0 7 ) A n ato m ical and physiological plasticity
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A lv arcz-M au bccin V, G a rc ia -H c rn in d cz F, W illia m s J T , Van B ock staclc
E J ( 2 0 0 0 ) F u n ctio n al co u p lin g b etw een neu ron s and glia J N eu ro sd
2 0 4 0 9 1 - 8 [ 5 .5 .I f ]
A m ed i A , M alach R , H e n d le r T .c t a l .( 2 0 0 1 ) V isu o -h a p tico b je ct-re la te d
activ ation in th e ventral visual pathw av N a t N e u r o s d 4 3 2 4 - 3 0
[5 .8 .3 c ]
A m es A ( 1 9 4 5 ) The space e ik o n o m eter test fo r an iseikon ia A m / O p h th a l
2 8 2 7 8 - 6 2 [9 .9 .2 b ]
A m igo G ( 1 9 7 4 ) A vertical h o ro p te r O ft ic a A cta 21 2 7 7 - 9 2 [1 0 .7 .1 ,
10.7.2a)
A m igo G , F io rcn tin i A , P irch io M , Sp in clli D ( 1 9 7 8 ) B in o cu la r vision
tested w ith visual evoked p o ten tials in ch ild ren and in fan ts In v est
O p h th a l V is Set 1 7 9 1 0 - 1 5 [7 .6 .3 )
A ndersen R A ( 1 9 9 7 ) M u ltim o d al in tegratio n fo r tin* rep resen tation o f
space in th e p osterior parietal c o r tc x P h il T ran s R oy S o c ft 3 5 2
1 4 2 1 - 8 [5 .8 .4 c ]
A n dersen R A , B u n co C A ( 2 0 0 2 ) In ten tio n al maps in p o sterio r parietal
c o rtcx A n n R ev N eu ro sd 2 5 1 8 9 - 2 2 0 [5 .S .4 c ]
A n dersen R A , M o u n tcastlc V B ( 1 9 8 3 ) The influ en ce o f th e angle o f gaze
u p o n the excitab ility o f th e light-sensitive neu ron s o f th e p osterior
p arietal c o rtc x / N eu ro sd 3 5 3 2 - 4 8 [5 .8 .4 c ]
A n dersen R A , Z ip ser D ( 1 9 8 8 ) T h e role o f the p o sterio r parietal c o rtc x
in co o rd in a te tran sform ation s for visual-m otor in tegration C a n J
P h y sio l P h a r m a c o l 6 6 4 8 8 - 5 0 1 [4 .5 .6 ]
A ndersen R A , В race well R M , Barash S ,c c al. ( 1 9 9 0 ) E y c-p o si cion c ffccts
on visual m em ory an d sa c ca d c -rcla tc d activ ity in areas L IP and 7 a o f
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A nderson C H , Van Essen D C ( 1 9 8 7 ) Sh ifter c ircu its: a com p u tation al
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A n d erson J C . M a rtin K A C , W h ittcrid g c D ( 1 9 9 3 ) Form fu n ctio n and
in traco rtical p ro je c tio n s o f n eu ron s in the striate c o r tc x o f the
m on key M acacu s n em estrin u s C crcb C o rtex 3 4 1 2 - 2 0 [5-5.1 c)
A n d erson J C , Bin zcggcr T , M artin K A C . R ocklan d K S ( 1 9 9 8 ) T h e c o n ­
n ectio n from co rtica l area V I to V 5 : a light and electro n m icro scop ic
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A n d erson J S , L am pcl 1, G illesp ie D C , F crstcr D ( 2 0 0 0 ) The co n trib u ­
tion o f n oise to co n tra st invariance o f orien tatio n tu n in g in cat visual
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A n d erson К С , Siegel R M ( 2 0 0 5 ) T h ree-d im en sio n al stru ctu re-from -
m o tio n selectivity in the an te rio r superior tem p oral polysensory area.
 S T Pa, o f th e behaving m on kcv C e r e b r a l C o rtex 1 5 1 2 9 9 -3 0 7
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A n d erson S A . E isen star D D , Shi L , R u b en stcin J ( 1 9 9 7 ) Intern eu ron
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[9 .9 .2 b ]
B crgh u is P. R a jn icck A M , M o ro zo v Y M . et al. ( 2 0 0 7 ) H ardw iring chc
b rain : cn d ocan n ab in oid s shape n eu ron al co n n ectiv ity S cien ce 3 1 6
1 2 1 2 - 6 [6 .4 .5 b ]
B irn h o lz I C ( 1 9 8 1 ) T h e d ev elo p m en t o f hum an fetal eye m ovem en t pat­
tern s S cien ce 2 1 3 6 7 9 - SO f 7 .3 .4 ]
B ish o p D L . M isgcld T , W aK h M K , ec al. ( 2 0 0 4 ) A xon b ran ch rem oval at
d ev elo p in g synapses by axoso m e shed d ing N eu ro n 4 4 6 5 1 -6 1
1 6 .4 .4 c]
B ish o p K M . R u b en stcin I .R . O 'L e a ry D D M ( 2 0 0 2 ) D istin c t actio n s o f
IL m xly lim x ly and P a x 6 in reg u latin g the sp ecificatio n o f areas in the
developin g n c o c o rte x / N eu roses 2 2 7 6 2 7 - 3 8 (6 .4.2л ]
B ish o p P O , Davis R ( 1 9 5 3 ) B ilateral in tera ctio n in the lateral gen icu late
body S cicn cc 1 1 8 2 7 1 - 3 (5 .2 .3 a ]
B ish o p P O . Pettigrew J D ( 1 9 8 6 ) N eural m c c h a n is m s o f b in o cu lar vision
V is R es 2 9 1 5 8 7 - 6 0 0 ( 2 .1 0 .5 0 ]
B ish o p P O , H en ry G H , S m ith C J ( 1 9 7 1 ) B in o cu lar in teractio n fields o f
single u nits in th e c a t s striate c o r tc x / P h y sio l 2 16 3 9 - 6 8 [ 5 .7 .2 c ]
B isti S . C a rm ig n o to G ( 1 9 8 6 ) M o n o cu lar deprivation in k itten s differ*
c n tly affects crossed and uncrossed visual pathways Vis R es 2 9 8 7 5 -8 *1
[8 .4 .2 a ]
B lackie C A , H ow land H C ( 1 9 9 9 ) A n exten sion o t an accom m od ation
and convergence m od el o f em m etrop ization to inclu de the cffccts o f
illu m in ation in ten sity O p h th a l P h y sio l O p t 19 1 1 2 - 1 2 5 [9 .6 .2 a ]
Blackw ell H R ( 1 9 5 2 ) Stu d ies o f psychophysical m eth od s to r m easuring
th re sh o ld s/O p fS o c A m 4 2 6 0 6 - 1 6 (3 .1 .1 c ]
B lais B S , Sh ouval H Z . C o o p e r LN ( 1 9 9 9 ) Ih e role o f prcsynap tic
activity in m on ocu lar deprivation: com parison o t hom osynaptic and
heterosynap tic m ech an ism s P r o i N a tl A c a d .SV/96 1 0 8 3 - 7 (6 .7 .2 1 ]
Blake R . H irsch H V B ( 1 9 7 5 ) D e fic its in b in o cu lar depth p ercep tion in
ca ts after altern atin g m o n o cu la r d eprivation S cien ce 1 9 0 I I 1 4 - 1 6
| 8.2.5b. 8 .4 .1 ]
Blake m ore С ( 1 9 6 9 ) B in o cu la r d ep th d iscrim in ation and th e nasotcm -
poral d ivision./P h y s io l2 0 5 4 7 1 - 9 (5 .3 .4 ]
B lakem ore С ( 1 9 7 6 ) Ih e co n d itio n s requ ired for th e m ain ten an ce o f
b in o cu la rity in th e k itte n s visual c o rte x / P h y sio ! 2 9 1 4 2 3 -4 4
(8 .2 .5 b ]
B lakem ore C , C am p b ell FW r ( 1 9 6 9 ) O n the existence o f n eu ron e* in the
hum an visual system selectively sensitive to th e o rien ta tio n and size o f
retinal im ages / P h y sio l 2 0 3 2 3 7 - 6 0 ( 4 .2 .5 b , 4 .4 .1 b]
B lakem ore C , C o o p e r G F ( 1 9 7 0 ) D ev elo p m en t o f t h e brain depend s on
the visual en v iron m en t N a tu re 2 2 8 4 7 7 - 8 [6 .6 .4 b ]
B lakem ore C , H aw ken M J ( 1 9 8 2 ) Rapid resto ration o f fu n ctio n a l input
to th e visual c o rte x o f che c a t after b r ie f m o n o cu lar deprivation
J P h y s b l 3 2 7 4 6 3 - 8 7 [8 .2 .3 c ]
B lakem ore C , P rice D J ( 1 9 8 7 a ) T h e org an ization and p o s t-n a ta l devel­
o p m e n t o f area 18 o f the c a ts visual c o rtc x / P h y sio l 3 8 4 2 9 3 - 9 2
[6 .7 .1 ]
B lakem ore C . P rice D J ( 1 9 8 7 b ) E ffects o f dark rearing o n th e develop­
m en t o f area 18 o f th e c a t s visual c o rtcx / P h y sio l 3 8 4 2 9 3 - 3 0 9
[8 .1 .1 c ]
B lakem ore C , Van Sluy tcrs R C ( 1 9 7 4 ) Reversal o f the physiological
c ffc c ts o f m on ocu lar deprivation in k itten s: fu rth er cv id cn cc fo r a
sensitive period / P h y sio l 2 3 7 1 9 5 - 2 1 6 [8 .3 .1 c ]
B lakem ore C , Van Sluytcrs R C ( 1 9 7 5 ) Inn ate and en viron m en tal factors
in th e d ev elo p m en t o f chc k itte n s visual co rte x / P h y sio l 4 8 2 6 6 3 -
7 1 6 [6 .6 .4 a , 8 .2 .3 d ]
B lakem ore C . V ita l-D u r a n d F ( 1 9 8 6 a ) E ffects o f visual deprivation on
th e d evelopm en t o f t h e m o n k ev s lateral gen icu late nucleus / P h y sio l
3 8 0 4 9 3 - 5 1 1 ( 6 .3 .5 b . 8 .2 .2 b . 8 .2 .2 c ]
Blakem ore C , V ita l-D u r a n d F ( 1 9 8 6 b ) O rg an izatio n and p o s t-n a ta l
d ev elo p m en t o f t h e m o n k e y s lateral gen icu late nucleus J P h y sio l 3 S 0
4 5 3 - 9 1 [6 .3 .5 c ]
Blakem ore C . van Sluytcrs R C . Peck C K , \ I o n A ( 1 9 7 5 ) D ev elop m en t
o f c a t visual co rtex follow in g ro ta tio n o f o n e eve N a tu r e 2 5 7 5 8 4 - 7
18.2.5a]
B lakem ore C , G arey L , V ita l-D u r a n d F ( 1 9 7 8 ) Ih e physiological effects
of m o n o cu la r d eprivation and th eir reversal in che m o n k e y s visual
c o r tc x J P h y s io l 2 8 3 2 2 3 - 6 2 [8 .3 .2 ]
Blakem ore C . H aw kcn M J. M ark R F ( 1 9 8 2 ) B r ie f m o n o cu la r dcpriva*
tio n leaves su bth rcsh old synaptic inpur on n eu ron es o f th e c a t s visual
cortex./ P h y sio l 3 2 7 4 8 9 - 5 0 5 1 8 .2 .3 c. 8 .2 .7 d ]
B lan k A A ( 1 9 5 3 ) L u n cb u rg th e o ry o f b in o cu la r visual space / O p t S oc
A m 4 3 7 1 7 - 2 7 (4 .7 .2 ]
B lan k A A ( 1 9 5 8 ) A nalysis o f experim en ts in b in o cu la r space perception
J O p t S o c A m 4 8 9 1 1 - 2 5 [4 .7 .2 ]
Blasdcl G G ( 1 9 9 2 a ) D ifferen tial im aging o f ocu lar d o m in an ce and o ri­
en tatio n selectiv ity in m o n k cv striate co rtex / N eu ro sd 12 31 1 5 - 3 8
15.4.3a. 5 .7 .2 a )
Blasdcl G G ( 1 9 9 2 b ) O rie n ta tio n selectivity preferen ce and c o n tin u ity in
m on k ey striate co rtex J N eu ro sd 12 3 1 3 9 - 6 1 [5 .7 .1 ]
Blasdcl G G . C am p b ell D ( 2 0 0 1 ) F u n ctio n al retin o to p y o f m on k ey visual
co rte x /N e u r o s c i 15 8 2 8 6 - 3 0 1 [5 .5 .4 c ]
Blasdcl G G . Fitzp atrick D ( 1 9 8 4 ) Physiological organ ization o f layer 4
in m acaque striate c o rtc x / N eu rosci 4 8 8 0 - 9 5 [5 .5 .3 ]
Blasdcl G G . Pettigrew J D ( 1 9 7 9 ) D eg ree o f in tcro cu lar synchrony
required fo r m ain ten an ce o f b in o cu larity in k itte n s visual co rtex
/ N eu ro p h y sio l4 2 1 6 9 2 - 7 1 0 [8 .2 .5 b ]
Blasdcl G G . Salam a G ( 1 9 8 6 ) V oltage-sensitive dvcs reveal a m odular
organ ization in m on k ey striate c o rtc x N a tu r e 3 2 1 5 7 9 - 8 5 15.7.1]
Blasdcl G G , Lund J S , Fitzpatrick D ( 1 9 8 5 ) In trin sic c o n n e c tio n s o f
m acaque striate c o rte x : axon al p ro jectio n s o f cells ou tsid e lam in a 4 C
/ N eu ro sci 5 Я Я 5 0 -6 9 (5 .8 .2 a )
Blasdcl G G , O berm ayer K , K iorp es L ( 1 9 9 5 ) O rg an izatio n o f ocu lar
d o m in an ce colu m n s in the striate co rte x o f n eon atal m acaque m o n ­
keys Vis N eu ro sci 1 2 5 8 9 - 6 0 3 (5 .7 .1 .6 .7 .1 ]
Blevins E, Jo h n se n S ( 2 0 0 4 ) Sp atial vision in th e c ch in o id genus
E c h in o m c t r a J E x p R io t 2 0 7 4 4 9 - 5 3 [6 .1 .2 ]
Bliss T V , G ard n cr-M cd w in A R ( 1 9 7 3 ) L o n g -lastin g p o ten tia tio n o f syn­
ap tic transm ission in the d en tate area o f th e u nanaesthetized rabbit
follow in g .stim ulation o f t h e p crfo ran t path / P h y sio l 2 3 2 3 3 1 - 5 6
[6 .5 .1 a ]
B lo d i F C , Van A llen M W ( 1 9 5 7 ) Electrom yograph y o t che extraocu lar
m uscles in fusional m ovem ents Л м J O p h th a l 4 4 1 3 6 - 4 4 [1 0 .8 .1 b ]
Blum R ( 1 9 8 3 ) T h e cy clo stcreo sco p c S te re o W o rld Ju n e 2 9 - 3 1 [2 .1 1 .4 ]
Blu m R , K afitz KWr, K o n n crth A ( 2 0 0 2 ) N cu ro tro p h in -cv o k cd depolar­
ization requires chc sodium ch a n n el N a v i.9 N a tu re 4 1 9 6 8 7 - 9 3
[6 .4 .3 d ]
В lum en fe Id W ( 1 9 1 3 ) U n tersu ch u n g cn iib cr die sch cin b arc G ro ssc im
Sch rau m c Z P sy ch ol 6 5 2 7 1 - 4 0 4 (4 .7 .2 )
B lu n t W ( 1 9 7 0 ) W e d r e a m k in g Hamivh H a m ilto n , L o n d o n (2 .1 0 .5 ]
B o b ic r W 'R t B rad d ick O J ( 1 9 8 5 ) E ccen tric p h o to re fra ctio n : op tical
analysis and em p irical m easures A m / O p tom P h y sio l O pt 6 2 6 1 4 - 2 0
(9 .2 .4 d )
B o b icr W R , M c R a e M ( 1 9 9 6 ) G ain ch an g e in the accom m od ativ e c o n ­
vergence cross-link O p h th .d P h y sio l O p t 1 6 3 1 8 - 2 5 (1 0 .4 .1 ]
B o b icr W R , C am p b ell M C . H in ch M ( 1 9 9 2 ) T h e in flu en ce o f ch ro ­
m atic ab erration on th e static accom m od ativ e response Vis R es 3 2
8 2 3 - 3 2 (9 .8 .2 b ]
B o b icr Vi’ R , G u in ta A . K u rtz S , H ow land H C ( 2 0 0 0 ) Prism induced
acco m m o d atio n in in fan ts 3 to 6 m o n th s o f age V is R es 4 0 5 2 9 - 3 7
[7 .3 .6 ]
B o d c -G r c u c l K M , Sin ger W ( 1 9 8 9 ) T h e d ev elo p m en t o f N - m c t h y l-
D -a s p a rta te rcccpcors in ca t visual c o r tc x D e v e l B r a in R es 4 6 1 9 7 -
2 0 4 (6 .7 .2 a )
B o fi K R . K aufm an L . T h o m a s J P ( 1 9 8 6 ) I la n d b o o k o f p ercep tion and
perfo rm an ce. V ol I Sen sory processes and p ercep tio n W ile y N ew
York 11.3]
B oire D , M o rris R . P tito M . c t a l . ( 1 9 9 5 ) E ffects o f n eo n atal sp littin g o f
the o p tic eh iasm a on th e d ev elo p m en t o f felin e visual callosal c o n n e c ­
tio n s E x p B ra in R es 1 0 4 2 7 5 - 8 6 [6 .4 .6 d ]
B o ll F ( 1 8 7 7 ) Z u r A n a to m ic u nd Physiologic der R etin a A rch P h y sio l
4 - 3 7 ( 2 .6 .1 ]
B o llm an n J 1 1. E n g ert F ( 2 0 0 9 ) Su b ccllu lar top og rap h y o f visually driven
d en d ritic activ ity in the vertebrate visual system N eu ro n 6 1 8 9 5 - 9 0 5
[6 .5 .5 ]
B o ltz R L , 1 larw erth R S ( 1 9 7 9 ) Fu sional vergence ranges o f the m on key:
a behavioural study E x p B r a in R es 3 7 8 7 - 9 1 [ 1 0 .5 .3 ]
B om an D K . K crtesz A E ( 1 9 8 3 ) In teractio n b etw een h o rizo n tal and ver­
tical fu sion al responses P ercep t P sy ch op hy s 3 3 5 6 5 - 7 0 [1 0 .6 .3 c ]
B o m an D K . K crccsz Л Е ( 1 9 8 5 ) H o riz o n ta l fusional responses to scim uli
co n ta in in g artificia l sco to m a s h u r s t O p b th a l Vis S ci 2 9 1 0 5 1 - 6
(1 0 .5 .6 ]
B o m b a P C ( 1 9 8 4 ) The d ev elo p m en t o f oriencacion categories betw een 2
and 4 m onchs o f a g e / E x p C h ild P sy ch o l 3 7 6 0 9 - 3 6 [7 .2 .2 ]
B o n d s A B , M a cL eo d D IA ( 1 9 7 8 ) A displaced Stiles-C raw ford effect
associated wich an c c ccn cric pupil In v est O p b th a l Vis S ci 1 7 7 5 4 - 6 1
[5 .1 .2 a ]
B o n clli M L R . S h e a W R ( 1 9 7 5 } R ea so n , ex p er im e n t, a n d m ysticism
M acm illan , L o n d o n (2 .5 .4 )
B o n h o c tfe r T , G rin vald A ( 1 9 9 3 ) T h e layout o f isooricn catio n dom ains
in area 18 o f cat visual c o rc c x : o p tica l im aging reveals a pinw heel
organ ization / N eu ro sci 1 3 4 1 5 7 - 8 0 [5 .7 .1 ]
B o n h o c tfe r T , H u f J ( 1 9 8 5 ) P osicion -d epen dcn c properties o f retinal
axons and th e ir grow th c o n es N a tu re 3 1 5 4 0 9 - 1 0 [6 .3 .4 a ]
B o n in V, M a n tc V. C a ra n d in i M ( 2 0 0 5 ) T h e suppressive field o f neurons
in laccral geniculace nucleus / N eu ro sci 2 5 1 0 8 4 4 - 5 6 [5 .2 .2 b ]
B o n n c h Y S . Sagi D , Polat U ( 2 0 0 4 } L ocal and n o n -lo cal d eficits in
am blyop ia: a cu ity and spacial in tera ctio n s V is R es 4 4 3 0 9 9 - 1 1 0
[8 .4 .3 b ]
B o o th M C A , R olls E T ( 1 9 9 8 ) V icw -inv ariant rep resentations o f fam il­
iar o b je c ts by neu ron s in th e in ferio r tem p o ral visual c o rtc x C er eb
C o rtex S 5 1 0 - 2 3 [5 .8 .3 b ]
B o o th e R G , W illia m s R A , K iorp es L , Teller D Y ( 1 9 8 0 ) D evelopm en c o f
c o n tra st sensitivity in in fa n t M a e a e a n e m e s tr in a m o n k ey t S c ic n c c 2 0 8
1 2 9 0 - 2 [7 .2 .1 a ]
B o o th e R G , D o b so n V, Teller D Y (1 9 X 5 ) Postnatal developm ent of
vision in hum an and n on h u m an prim ates A n n R ev N eu ro sci 8 4 9 5
5 4 5 1 7 .3 .1 ,7 .4 .1 c )
B o rg -G ra h a m L J, M o n ie r C , Frcgnac Y ( 1 9 9 8 ) V isual input evokes tran ­
sien t and stron g sh u n tin g in h ib itio n in visual neu ron s N a tu re 3 9 3
3 6 9 - 7 3 [5 .5 .2 c ]
B org h u is B G . R atclifF C P , S m ith R G , c t al. ( 2 0 0 8 ) D esign o f a neural
array./N e u r o s c i 2 8 3 1 7 8 - 8 9 [5 .1 .4 c ]
B o rin g E G ( 1 9 3 0 ) A new am bigu ous figure A m / P sy ch o! 4 2 4 4 4 - 5
[4 .5 .9 л ]
B o rin g E G ( 1 9 4 2 ) S en sa tio n a n d p e rc e p tio n in th e h isto ry o f e x p e r im e n ta l
p sy ch o lo g y A pple to n —C e n t u г y—C ro fts, N ew York [2 .5 .2 ]
B o rin g E G ( 1 9 5 0 ) A h isto ry o f e x p e r im e n ta l p sy ch o lo g y A p p lc to n -
C c n tu r v -C r o fts , New York (4 .2 .4 .c ]
B o rn R T , T o o tell В H ( 1 9 9 2 ) Segregation o f glo bal and local m o tio n p ro ­
cessing in prim ate m iddle tem p oral visual area N a tu r e 3 5 7 4 9 7 - 9
[5 .8 .4 b ]
B orn xtcin M H , K rin sk y S J, B cn asich А Л ( 1 9 8 6 ) Fine orien tatio n dis­
crim in a tio n and shape co n sta n cy in young in fan ts J E x p C h ild P sychol
41 4 9 - 6 0 ( 7 . 2 . 2 ]
B o rrcll V. C allaw ay E M ( 2 0 0 2 ) R eo rg an ization o f ex u b eran t axonal
arb o rs co n trib u tes to che d ev elo p m en t o f lam in ar sp ecificity in fen ce
visual co rtex J N eu ro sci 2 2 6 6 8 2 - 9 5 [6 .4 .5 a ]
B o n c lli E , N cstlcr E J, A llis C D , Sa.vsonc-Corsi P ( 2 0 0 8 ) D e co d in g che
cp ig cn ccic language o f neuronal plasticity N eu ron 60 9 6 1 -7 4
[6 .6 .1 c ]
В о гColot со 7. A , B ash ir Z I , D avies C H , C o llin g rid g c G L ( 1 9 9 4 ) A
m olecu lar sw itch activated by m eta b o tro p ic glu tam ate recep tors
regulates in d u ctio n o f lo ng -term p o ten tiatio n N a tu re 3 6 8 7 4 0 - 3
[6 .5 .1 b ]
B o sk in g W 1 1 , Z h a n g , Y, Schofield B , Fitzp atrick D ( 1 9 9 7 ) O rie n ta tio n
selectiv ity and chc arran gcm cn c o f h orizon tal c o n n e ctio n s in cree
shrew striate corcex /N e u r o s c i 1 7 2 1 1 2 - 7 [5 .5 .6 a , 5 .5 .6 b ]
B o ss V C , S c h m id t J T ( 1 9 8 4 ) A ctiv ity an d che form atio n o f o cu lar d o m ­
inance p atch es in duallv innervated ccccum o f goldfish / N eu roses 4
2 8 9 1 - 9 0 5 [6 .7 .3 b ]
B ossom aicr T , Snyd er A W ( 1 9 8 6 ) W h y spacial freq u en cy processing in
th e visual co rcex ? Vis R es 2 9 1 3 0 7 - 9 (3 .2 .6 a ]
B ou m a H ( 1 9 7 0 ) In tera ctio n effects in parafoveal le tter reco g n itio n
N a tu re 2 2 6 1 7 7 - 8 [4 .8 .3 a ]
Boum an M A , van den Brink G ( 1 9 5 2 ) O n the integrate capacity in rim e and
space o l the human peripheral rccinaJ O pt S o cA m 4 2 6 1 7 - 2 0 [3.1.2]
Hour L J ( 1 9 8 1) T h e in flu en ce o f th e spacial d istrib u tio n o f a targ et o n the
dynam ic response and Huccuacions o f che acco m m o d atio n o f chc
hum an eve V is R es 21 1 2 8 7 - 9 6 [9 .6 .4 d ]
B o u rd ct C , O lavarria JF , Van Sluvtcrs, R C ( 1 9 9 6 ) D istrib u tio n o f visual
callosal neu ron s in n orm al an d strab ism ic cacs J C o m p N eu ro l 3 6 6
2 5 9 - 6 9 |6.4.6d , 8 .2 .3 b ]
B ou rg eois J P. R akic P ( 1 9 9 3 ) C h an g cs o f synaptic d en sity in chc prim ary
visual c o rtcx o f the m acaque m on k ey from fetal to adulc stage /
N eu roses 1 3 2 8 0 1 - 2 0 [6 .4 .5 d ]
B ou rg eois JP , R ak ic P ( 1 9 9 6 ) Synapcogencsis in chc o ccip ita l corccx o f
m acaque m on kcv devoid o f retin al in p u t from early em b ry o n ic stages
F u r J N eu rosci 8 9 4 2 - 5 0 [6 .4 .5 c ]
B ou rgeois JP , G o ld m a n -R a k ic P S , R akic P ( 1 9 9 4 ) Synap togenesis in the
p refron tal c o rtcx o f rhesus m on keys C e r e b C o rtcx 4 7 8 - 9 6 f6 .4 .2 d ]
B o v o lcn ta P. M ason С ( 1 9 8 7 ) G ro w th co n e m o rp h o lo g y varies with
p o sitio n in the d ev elo p in g m ouse visual pathw ay from retin a to first
targets / N eu roses 7 1 4 4 7 - 6 0 [6 .3 .4 a ]
Bow er T G R ( 1 9 6 6 ) Slan t perception and shape co n stan cy in intancs
S cien ce 151 8 3 2 - 4 [7 .4 .2 a ]
Bow er T G R , B rou gh to n J M , M o o re M K (1 9 7 0 a ) In fan t responses to
ap p ro ach in g o b jcccs: an in d icato r o f response со d istal variables
P ercep t P sy cbop by .<9 1 9 3 - 6 [7 .4 .1 c ]
Bow er T G R , B rou gh to n J M , M o o re M K ( 1 9 7 0 b ) D em o n stratio n s o f
in te n tio n in chc reach in g behavior o f n con acc hum ans N a tu r e 2 2 8
6 7 9 - 8 1 (7 .4 .1 a ]
B ow ers В (2 0 0 1 ) S ir C h a r le s W h e a ts to n e l:R S I $ 0 2 /Л75 T h e Inscicucion
o f E lectrical En gin eers, L o n d o n [ 2 .1 1.2b]
B o w n c SF ( 1 9 9 0 ) C o n tra s t d iscrim in ation ca n n o t exp lain spatial fre­
q u en cy o rien ta tio n o r tem p oral freq u en cy d iscrim in ation Vis Re< 3 0
4 4 9 - 6 1 (3 .1 .4 a , 4 .2 .8 c ]
B o y co tt B , W ’i sslc H ( 1 9 9 9 ) Parallel p rocessing in the m am m alian retina
In v es t O p b th a l Vis S c i 4 0 1 3 1 3 - 2 8 [5 .1 .3 ]
Boyd J , M atsubara J ( 1 9 9 4 ) T a n g en tial org an ization o l callosal c o n n e c ­
tiv ity in th e c a ts visual co rtex ./ C om p N e u ro l 3 4 7 1 9 7 - 2 1 0 [5 .3 .5 ,
6 .4 .6 d ]
Boyd с A , Jo n e s S J, Taylor M L , et al. ( 1 9 9 0 ) F lu orcsccn cc in th e tandem
scan n in g m icro scop e / M icros 15 7 3 9 - 4 9 [5 .4 .1 b]
Boydcn E S , Z h an g F, B am b erg E , ct al. ( 2 0 0 5 ) M illisccom l-tim cx calc,
gen etically targeted o p tica l co n tro l o f n eu ral activity N a t N eu rosci 8
1 2 6 3 - 8 ( 5 .4 .4 ]
Boyle R ( 1 6 8 8 ) A d isqu isition a b o u t th e final causes o f natural th in g s J
Taylor, L on d on See R o b e rt Boyle th e w orks (cd T B irc h ) V ol 5 O h m ,
H ildcshcim [2 .1 0 .3 c ]
B o y n to n R M ,O n lc y J W ( 1 9 6 2 ) A critiq u e o ft h c s p c c ia l status assigned
by B rin d ley со "psychop hysical lin k in g hypotheses'* o f “class A " Vis
R es 2 3 8 3 - 9 0 [3 .1 .1 a ]
Bozzi Y, Pi/zorusso T . C rcm isi F, c t al. ( 1 9 9 5 ) M o n o cu lar deprivation
decreases the expression o f m essenger R N A for brain-derived ncu-
ro tro p h ic facto r in th e rat visual c o rtc x N eu ro sci 6 9 1 1 3 3 -4 4
| 8 .2.7f]
Braastad B O , H cggclu nd P ( 1 9 8 5 ) D e v elo p m en t o f spatial rc c c p tiv c -
field org an ization and o rien ta tio n selectiv ity in kitccn set iacc c o rtc x /
N eu ro p h y sio l S i 1 1 5 8 - 7 8 [6 .6 .4 a , 8 .1 .1 c ]
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C allaw ay E M ( 1 9 9 8 a ) L ocal circu its in prim ary visual c o rte x o f the
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h orizon tal c o n n e c tio n s in cat striate c o r te x / N eu ro sd 1 0 1 1 3 4 - 5 3
[6 .4 .6 b ]
C allaw ay E M , K atz L C ( 1 9 9 1 ) E tfects o f b in o cu lar deprivation o n the
d ev elo p m en t o f clustered h o rizo n tal c o n n e ctio n s in c a t striate co rtex
P r o c N a t l A c id S ci 8 8 7 4 5 - 9 ( 6 .4 .6 b , 8.1.1 b]
C allaw ay E M , K atz L C ( 1 9 9 2 ) D ev elop m en t o f axon al arb o rs o f layer 4
spiny neu ron s in cat striate co rtex J N eu ro sci 1 2 5 7 0 - 8 2 [6 .4 .6 b ]
C a m in iti R ( 1 9 9 5 ) Spacial v ision and m ovem en t in the parietal lobe
Ce>‘c b C o rtc x 5 N 5 Special Issue [5 -8.4e]
C am p b ell A W ( 1 9 0 5 ) H istolog ical stu dies o n the localizatio n o f t h e
cereb ral fu n ctio n C am brid ge U n iv ersity Press, C am b rid g e [2 .6 .2 ]
C am p b ell F W ( 1 9 5 4 ) T h e m in im u m q u a n tity o t light requ ired to e licit
th e acco m m o d atio n reflex in m an / P h y sio l I 2 3 3 5 7 - 6 6 %9 .6 .4 d ]
C am p b ell F W ( 1 9 5 7 ) T h e d ep th o f field o f t h e hum an eye O p tica A cta 4
1 5 7 - 6 4 [9 .6 .4 a , 9 .6 .4 b , 9 .6 .4 c ]
C am p b ell F W ( 1 9 5 9 ) H ig h -sp e e d in fra -re d o p to m e te r / O p t S oc A m
4 9 2 6 8 - 7 2 [9 .2 .4 d ]
C am p b ell F W ( I 9 6 0 ) C o rre la tio n o t acco m m o d atio n b etw een th e tw o
eyes J O pr S o c A m 5 0 7 3 8 [ 9 .7 .1a)
C am p b ell F W , G u bisch R W ( 1 9 6 6 ) O p tica l qu ality o f th e hum an cvc /
P h y sio l 1 8 6 5 5 8 - 7 8 [9 .1 .3 a , 9 . 1 . 5 . 2 , 9 .6 .4 c 1
C am p b ell F W , Prim rose JA F . ( 1 9 5 3 ) The state o t acco m m o d atio n o f t h e
hum an eve in darkness T rans O p h th a l S o c U K 7 3 3 5 3 - 6 1 [9 .3 .1 ]
C am p b ell F W , R ob so n J G ( 1 9 6 8 ) A p p lication o f Fourier analysis to the
v isibility o f gratings / P h y sio l 1 9 7 5 5 1 - 6 6 [3 .2 .5 , 4 .4 .1 a , 5-6.3]
C am p bell F W , W csth eim cr G (1 9 5 8 ) Sensitivity o f the eve to differences
in focu sJ P h y sio l 1 4 3 1 8 P [ 9 .6 .3 .9 .7 .1 a ]
C am p b ell F W , W csth eim cr G ( 1 9 5 9 ) Factors in flu en cin g a cco m m o d a­
tion responses o f the hum an eye J O pt S o c A m 4 9 5 6 S - 7 1 (9 .8 .1 ,
9 .8 .2 c ]
C am p b ell FW”, W csth eim cr G ( 1 9 6 0 ) D y n am ics o t acco m m o d atio n
responses o f the hum an eve / P h y s io l 151 2 8 5 - 9 5 [9 .5 , 9 .7 .2 a ,
9 .7 .2 b ]
C a m p b ell F W , R o b so n J G , W esth eim er G ( 1 9 5 9 ) F lu ctu atio n s o f a cco m ­
m o d atio n under steady view ing c o n d itio n s / P h y sio ! 1 4 5 > 7 9 - 9 4
[9 .7 .1 л ]
C a m p b ell 1: W , H ess R F , W atson P G , B an k s R ( 1 9 7 8 ) P relim in ary results
o f a physiologically based trea tm en t o f am blyopia B r J O p b th a l 6 2
7 4 8 [8 .4 .6 c ]
C a m p b ell M C W , I larrison E M .S im o n c t P ( 1 9 9 0 ) Psychophysical m ea­
su rem en t o f the blur o n th e retin a due со o p tica l ab erration s o f the
eye Vis R es 3 0 1 5 8 7 - 6 0 2 f 9 . 1 .2 b . 9 .8 .2 a )
C a m p o s E C ( 1 9 8 0 ) A n om alo u s rcrin ai corresp on d en ce A rch O p b th a l
9 8 2 9 9 - 3 0 2 (8 .4 .6 a ]
C a m p o s E C , C h icsi С ( 1 9 8 3 ) B in o cu la rity in c o m ita n t strabism us: II
O b je ctiv e evalu ation w ith visual evoked responses D oc O p b th a l 5 5
2 7 7 - 9 3 (8 .4 .6 a ]
C a m p o s П С , B ed ell H E , E n o ch J M , Fitzgerald C R ( 1 9 7 S ) R etinal
rcccp tiv c fie ld -lik e properties and S tile s -C ra w fo r d effect in a
p atien t w ith a trau m atic ch o ro id al ru pture D o c O p b th a l 4 5 3 8 1 - 9 5
15.1.2a]
C a m p o s IJ* L an gcr A , C row itz A ( 1 9 7 0 ) C ard iac responses on th e visual
c lif f in p rclo co m o to r hum an in fan ts S c ien et 1 7 0 1 9 6 - 7 (7 .4 .1 b ]
C a n d y T R , Bharadw aj S R ( 2 0 0 7 ) ‘Ih e stab ility o f steady state a c co m ­
m o d a tio n in hum an in fan ts / Vis 7 ( 1 1 ) A rticle 4 (7 .3 .1 ]
C a n g J* K an ck o M , Yam ada J , c t al. (2 0 0 5 a ) E p h rin -A s guide th e fo rm a­
tio n o f fu n ctio n a l m aps in th e visual co rtex Л rcu ro n 4 8 5 7 7 - 8 9
[6 .4 .3 c ]
C a n g J , R en teria R C . K anck o M . e t al. ( 2 0 0 5 b ) D ev elo p m en t o f precise
m aps in visual c o r tc x requ ires p a ttern ed sp o n tan eou s activ ity in the
retina N eu ro n 4 8 7 9 7 8 0 9 [6 .6 .2 ]
C a n n o n M W , Fu llcnkam p S C ( 1 9 9 3 ) Spatial in teractio n s in apparent
co n tra st: individual d ifferen ces in en h an cem en t and suppression
effects Vis R es 3 3 1 6 8 5 - 9 5 (5 .5 .6 c ]
C a o A , S ch ille r P H ( 2 0 0 3 ) N eu ral responses to relative speed in the
prim ary visual co rtex o f rhesus m on key Vis N eu ro sci 2 0 7 7 - 8 4
[5.6.4a]
C a p u to G , G u erra S ( 1 9 9 8 ) A ttcn tio n a l selection by d istra cto r suppres­
sion Vis R es 3 8 6 6 9 - 8 9 (4 .8 .1 c ]
C a ra n d in i M , H eeger D J ( 1 9 9 4 ) Su m m ation and division by neu ron s in
prim ate visual co rtex S cien ce 2 7 6 1 3 3 3 - 6 [4 .2 .8 c , 5 .5 .3 ,5 -5.6c]
C a ra n d in i M , B arlow H B , O 'K e e fe LP, c t al. ( 1 9 9 7 ) A d ap tation to c o n ­
tin gen cies in m acaque prim ary visual c o rtcx P h ilo s T r R S o c 3 5 9
1 1 4 0 - 5 4 [4 .2 .9 c ]
C a ra n d in i M , H eeger D J , Scn n W ( 2 0 0 2 ) A synaptic exp lanation o f sup­
pression in visual co rtex / N eu rosci 2 2 1 0 0 5 3 - 6 5 [5 -5 .6 c]
C ard er R K , Jo n e s F.G, H en d ry S H C ( 1 9 9 1 ) D istrib u tio n o f glutam ate
neu ron s and term in als in striate c o rte x o f norm al and m on ocu larly
deprived m onkeys S o c N eu ro sci A b str 1 7 115 [8 .2 .4 ]
C a rd in J A , Palm er L A , C o n tre ra s D ( 2 0 0 5 ) S tim u lu s= d cp cn d cn t у
( 3 0 - 5 0 H z ) o scilla tio n s in sim ple and com p lex fast rh ythm ic bu rst­
in g cclls in prim ary visual c o rtc x J N eu rosci 2 5 5 3 3 9 - 5 0 [4 .3 .2 ]
C ard o so de O liv eira S, T h iele A , H offm an n P K ( 1 9 9 7 ) Sy n ch ron ization
o f n eu ron al activ ity d urin g stim ulus ex p ectatio n in a d irectio n d is­
crim in a tio n cask / N eu rosci 1 7 9 2 7 8 - 6 0 [4 .3 .4 b , 4 .3 .4 c , 5.9.1 ]
C a ric D , P ricc D J ( 1 9 9 9 ) Evidence chat the lateral gen icu late nucleus
regulates the n orm al d ev elo p m en t o f visual c o rtic o co rtica l p ro jec­
tion s in chc c a t E x p N eu ro l 1 5 6 3 5 3 - 6 2 | 6.4.6c)
C a rk c c t A . L evi, D M , M anny R E ( 1 9 9 7 ) D ev elo p m en t o f vern ier acuity
in ch ild h oo d O p tom V is Set 7 4 7 4 1 - 5 0 (7 .2 . Ic ]
C a rlc to n E H , M adigan l.F ( 1 9 3 7 ) R elation sh ip s b etw een an iseikon ia
and am etrop ia A rch O p b th a l 18 2 3 7 - 4 7 [9 .9 .1 a ]
C arlso n S ( 1 9 9 0 ) V isually guided b eh avior o f m on k ey s after early b in ­
ocu lar visual deprivation In t] N eu ro sci 5 0 1 8 5 - 9 4 [8 .1 .2 ]
C arlso n S , 1 lyvarinen L , R a n in cn A ( 1 9 8 6 ) Persistent behavioural b lin d ­
ness after early visual deprivation and active visual reh ab ilitatio n : a
case rep o rt B r J O p b th a l 7 0 6 0 7 - 11 (8 .1 .3 ]
C arlso n S , Pcrtovaara A ,T a n ila 11 ( 1 9 8 7 ) L ate effects o f early b in o cu lar
visual deprivation on the fu n ctio n o t B rod m an n s area 7 o f m onkeys
[M a c a a i a rc to id es) D c r e l B ra in R es 3 3 1 0 1 - 1 1 [8 .1 .1 b]
O r i s o n V R ( 1 9 6 2 ) Size co n sta n cy ju d gm en ts and perceptual co m p ro ­
m ise J E x p P sy ch o l 6 3 6 8 - 7 3 (4 .7 .2 J
C a rm ig n o to G , V ic in i S ( 1 9 9 2 ) A c tiv ity -d e p e n d e n t d ecrease in N M DA
recep to r responses d urin g developm ent o f th e visual co rtex S cien ce
2 5 8 1 0 0 7 - 1 1 (6 .7 .2 a ]
C a rm ig n o to G , C a n c lla R , C a n d co P, e t al. ( 1 9 9 3 ) E ffects o f nerve
grow th fa cto r o n n eu ron al p lasticity o f the k itten visual co rtcx
J P h y sio l 4 6 4 3 4 3 - 6 0 ( 8 .2 .7 f ]
C a rm ig n o to G , Pizzoi usso T , T ia S , V ic in i S ( 1 9 9 7 ) Brain-derived ncu-
ro tro p h ic fa c to r and nerve grow th fa c to r p o ten tia te ex cita to ry synap­
tic tran sm ission in the rat visual co rtex / P h y sio ! 4 9 8 1 5 3 -6 4
(6 .5 .1 c )
C aro n A J , C a ro n R F , C arlson V R ( 1 9 7 8 ) D o in fan ts see o b je c ts o r reti­
nal im ages? Shape co n stan cy revisited I n fw t B eh a ir D c r e l 1 2 2 9 - 4 3
17.4.2a]
C aro n A J, C aro n R F, C arlson V R ( 1 9 7 9 ) In fan t perception o f the
in varian t shape o f o b je c ts varying in slant C h ild D c v d 5 0 7 1 6 - 2 1
|7.4.2a]
C arp en ter M K , C u i X , H u Z , c t al. ( 1 9 9 9 ) In v itro expan sion o f a m ulti-
p o te n t p op u lation o f hum an neural p ro g en ito r cells E x p N e u r o l 1 5 8
2 9 5 - 7 8 | 6 .4 .2 d ]
C a rp e n te r R H S ( 1 9 8 8 ) M ov em en ts o f t h e eyes P io n , L o n d o n 11 0 .1 .1 ,
1 0 .1 .3 b ]
C arro ll R C , Z u k in S ( 2 0 0 2 ) N M D A -rc c c p to r traffickin g and targ etin g :
im p licatio n s for svnaptic tran sm ission and p lasticity T I N S 2 5 5 7 1 - 7
|6.5.1a]
C arro ll R C , N ico ll R A , M alen ka R C ( 1 9 9 8 ) E ffects o f P K A and P K C
on m in iatu re ex citato ry postsynaptic cu rren ts in C A 1 pyram idal cells
J N eu ro p h y sio l * 0 2 7 9 7 - 8 0 0 [6 .5 .1 a ]
C a rro ll R C , B eattie E C , Z astrow M von, M alen ka R C ( 2 0 0 1 ) R ole o f
A M PA recep to r en d o cy to sis in synaptic p lasticity N a t R ev N eu rosci 2
3 1 5 - 2 4 (6 .5 .1 a ]
C a rte r B A R ( 1 9 7 0 ) Perspective In I h e O x fo rd co m p a n io n to a r t (c d H
O sb o rn e ) pp 8 4 0 - 6 1 C laren d on Press» O x fo rd (2 .9 .3 ]
C a rte r D B ( 1 9 5 8 ) Studies o f fixation disparity. II. A pparatus, procedure
and the problem o f co n sta n t error A m J O ptom A rch A m Ac*xA O ptom
3 5 5 9 0 - 8 [1 0 .2 .4 b ]
C a rte r D B ( 1 9 6 3 ) E ffects o f prolon ged w earing o f prism A m J O ptom
P h y sio l O p t 4 0 2 9 5 - 7 3 [ 10 .2 .5 a ]
C a rte r D B ( 19 6 4 ) Fixatio n disparity w ith and w ith ou t foveal f usion c o n ­
tou rs A m J O p tom A rch A m A c a d O p tom 4 1 7 2 9 - 3 6 [ 1 0 .2 .4 g ]
C a rte r D B ( 1 9 6 5 ) Fixatio n disparity and h ctcro p h o ria fo llo w in g p ro ­
longed w earing o f prism s A m J O p tom A rch A m A ca d O p tom 4 2
1 4 1 - 5 2 [1 0 .2 .5 a ]
C a rte r T F ( 1 9 5 5 ) T h e in v en tion o f p rin tin g in C h in a and its spread
westward T h e R o n ald Press, N ew York [2 .2 .2 ]
C a i tc rc ttc E C . Friedm an M P ( 1 9 7 4 ) H a n d b o o k : o f p erc ep tio n Vol II
P sy ch op h y sicalju d g m e n t M id m ea su rem en t A cad em ic Press, N ew York
[3 .1 .1 a ] ‘
C asagran d c V A , B r u n s o -B c c h to ld J K ( 1 9 8 8 ) D ev elo p m en t o f lam ina­
tio n in lateral gen icu late nucleus: c ritic a l facto rs In A dv an ces in n eu ra l
a n d b e h a v io r a l d ev elo p m en t (ed P G S h in k m a n ) V ol 3 pp 3 3 - 7 8
A b lex, N o rw o o d N J [5 .2 .2 a , 6 .3 .5 c )
C asagran d c V A , C o n d o G J ( 1 9 8 8 ) Is b in o cu lar c o m p e titio n essential for
layer form atio n in th e lateral gen icu late n u cleu s? B ra in B e b a v E v o l Ъ\
1 9 8 - 2 0 8 [6 .3 .5 a ]
C asan ova C , Freem an R D , N ord m an n J P ( 1 9 8 9 ) M o n o cu lar and b in ­
o cu lar response p rop erties o f cells in th e striate-recip ien t zon e o f the
c a ts lateral postcrior-pu lvinar com p lex J N eu ro p b y sio l 6 2 5 4 4 - 5 7
[5 .5 .1 b ]
C ase L C , T cssicr-L av ign c M ( 2 0 0 5 ) R eg en eration o f th e adult cen tral
nervous system C u r r B io l 15 R 7 4 9 - 5 3 [6 .4 .2 d ]
C astanada* C astellan o s D R , K ricg stcin A R ( 2 0 0 4 ) C o n tro llin g neuron
n u m b er: does N um b do the mach ? N a t N eu ro sci 7 7 9 3 - 6 [6 .4 .5 b ]
C astcllan i V, B o ltz J ( 1 9 9 7 ) M em bran e-associated m olecules regulate
the form atio n o f laver-specific co rtica l circu its P ro c N a t l A c a d S ci 9 4
7 0 3 0 - 5 16.4.6a]
C astclli В ( 1 6 6 9 ) D iscorso sop ra la v ista S ee A rio tti 1 9 7 3 [2 .5 .2 ]
C astrcn E, Z afra F, T h o e n cn H . L in d h olm D ( 1 9 9 2 ) Lighc regulates
expression o f brain-derived n eu ro tro p h ic fa c to r m R N A in rat visual
co rte x P r o c N a t l A c a d S ci 8 9 9 4 4 4 - 8 [8 .1 .1 b ]
C a ta la n o S M , Sh atz C J (1 9 9 # ) A ctiv ity -d cp cn d cn t co rtica l target sclec-
tio n by th a la m ic axon s S cien ce 2 8 1 5 5 9 - 6 2 [6 .4 .5 c ]
C a ttc ra ll W A , Few Л Р ( 2 0 0 8 ) C a lciu m ch an n cl regu lation and prcsyn-
ap tic p lasticity N eu ro n 5 9 8 8 2 - 9 0 1 [ 6 .4 .3 f )
C avanagh P { 1 9 8 2 } F u n ctio n al size invariance is n o t provided by the co r­
tical m agn ificatio n fa c to r V i s R es 2 2 1 4 0 9 - 1 2 [5 .5 -4 d ]
C avanagh P ( 1 9 8 7 ) R eco n stru ctin g the third d im en sio n : in teractio n s
b etw een c o lo r textu re m o tio n b in o cu lar disparity and shape C o m p u t
V is G r im P ro c 3 7 1 7 1 - 9 5 [4 .5 .7 c ]
C avanagh P. A rgu in M , Trcism an A ( 1 9 9 0 ) E ffect o f surface m edium on
visual search for orien ta tio n and size features / lix p P sy ch ol I I P P 1 6
4 7 9 - 9 1 [4 .2 .6 c ]
Cave K R , Z im m erm an J M ( 1 9 9 7 ) F lex ib ility in spatial a tte n tio n before
and after p ractice P sy ch o l S ci 8 3 9 9 - 4 0 3 (4 .8 .3 d ]
C avincss V S , T ak ah ash i T . N ow akow ski R S ( 1 9 9 5 ) N u m bers tim e and
n c o c o rtic a l n eu ro n o g cn csis: a general d evelopm ental and evolution*
a ry m odel T IN S 1 8 3 7 9 - 8 3 (6 .4 .5 b ]
C a v o n iu s C R , Estevez О ( 1 9 7 5 ) C o n tra st sensitivity o f individual colou r
m ech an ism s o f hum an vision / P h y sio I 2 4 8 6 4 9 - 6 2 [5 .1 ,2a]
C a y o u cttc M> R atFM ( 2 0 0 2 ) A sy m m etric segregation o f N u m b : a m ech ­
anism tor neural specification from D ro so p h ila to m am m als Л fat
N eu ro sci 5 1 2 6 5 - 9 [6 .4 .5 b ]
C c lc b rin i S , N ew som e W T ( 1 9 9 4 ) N euronal and psychophysical sensi­
tiv ity to m o tio n signals in extrastriate area M S T o f the m acaque
m o n k e y / N c u ro sd 1 4 4 1 0 9 - 2 7 [5 .8 .4 c ]
C c lc b rin i S . T h o rp e S , T r o tte r Y, Im bert M ( 1 9 9 3 ) D yn am ics o t o rie n ta ­
tio n co d in g in area V I o f th e awake p rim ate V is N eu ro sci 1 0 8 1 1 - 2 5
[5 .6 .2 c ]
C h a lfic M ,T u Y , Euskirchcn G , c t al. ( 1 9 9 4 ) G reen flu o rcsccn t p ro tein as
a m arker for gene expression S cien ce 2 6 3 8 0 2 - 5 [5 .4 .2 a ]
C h a lla co m b c Jl\ Snow D M * L ctou rn eau P C ( 1 9 9 6 ) R o le o tc y to s k c lc -
ton in grow th co n e m o tility and axon al elo n g atio n S a n N eu ro sci 8
6 7 - 8 0 [6 .4 .3 b ]
C haltip a L M , L ia В ( 1 9 9 1 ) ТЪ с n asotcm p oral division o f retinal gan­
glion cells w ith crosscd and uncrossed p ro jectio n s in th e fetal rhesus
m o n k ey / N c u ro sd 11 1 9 1 - 2 0 2 [6 .3 .4 b ]
C h alu p a L M , W illia m s R W , H end erson Z ( 1 9 8 4 ) B in o cu lar in teractio n
in the fetal c a t regulates th e size o f the ganglion ccll population
N eu ro sci 1 2 1 1 3 9 - 4 6 (6 .3 .3 b , 8 .2 .6 a ]
C h a n J A , Balasubraraanian S , W it t R M , c t al. ( 2 0 0 9 ) P roteoglycan
in tera ctio n s w ith S o n ic H ed g eh o g sp ecify m ito g c n ic responses N o r
N eu ro sci 1 2 4 0 9 - 1 7 [6 .4 .4 b ]
C h a n S O , G u illery R W ( 1 9 9 3 ) D ev elop m en tal ch anges produced in the
rctin o fu g a l pathw ay o f rats an d ferrets by early m o n o cu la r en u cle­
a tio n s: the effects o f age and the d ifferen ce b etw een n orm al and
a lb in o anim als/N e u r o s c i 1 3 5 2 7 7 - 9 3 [6 .3 .4 a , 8 .2 .6 a ]
C h a n S O , G u illery R W ( 1 9 9 4 ) C h an g es in fiber o rd er in the
o p tic nerve and tract o f rat em b ry os / C o m p N eu ro l 3 4 4 2 0 - 3 2
[6 .3 .4 a ]
C h a n -P a la y V , P a la y S L , B illin g s -G a g lia rd i S M ( 1 9 7 4 ) M cv n crt cc lls in
th e prim ate visual co rtex / N eu ro cy to l 3 6 3 1 - 5 8 [5 .7 .1 ]
C h a n ce F S , N elson S B , A b b o tt L F ( 1 9 9 9 ) C o m p le x cclls as co rrically
am plified sim p le cells N m N eu ro sci 2 2 7 7 - 8 2 [5 -5 .3 ]
C h a n d n a A , P cn n cfa th cr P M , K ovacs I, N o rc ia A M ( 2 0 0 1 ) C o n to u r
in tegratio n d eficits in an iso m etrop ic am blv op ia In v est O p h th a l Vis
S ci 4 2 8 7 5 - 8 [8 .4 .3 c ]
C h a o D L , M a L , Sh cn К ( 2 0 0 9 ) T ra n sien t c e ll- c e ll in teractio n s in neural
c irc u it form atio n N a t R ev N eu ro sci 1 0 2 6 2 - 7 1 [6 .4 .3 ]
C h a o M V ( 1 9 9 2 ) N eu ro tro p h in reccp tors: a w indow in to n eu ron al d if­
feren tiatio n N eu ro n 9 5 8 3 - 9 3 [6 .4 .3 d ]
C h a o M V ( 2 0 0 3 ) N cu ro tro p h in s and th e ir recep to rs: a convergence
p oin t for m any sign alling pathways N a t R ev N eu ro sci 4 2 9 9 - 3 0 9
(6 .4 .3 d , 6 .7 .2 d j
C h a o -y i L , C rcu tz fcld t О ( 1 9 8 ч ) The rep resen tation o f co n trast and
o th e r stim ulus param eters by single n eu ron s in area 17 o f the cat
P Jlu g crs A r e h g e s P h y sio l 4 0 1 3 0 4 - 14 (5 .6 .1 ]
C h ap m an B , Stry k er M P ( 1 9 9 3 ) D ev elop m en t o f orien tatio n selectivity
in ferret visual c o rtc x and effects o t deprivation / N cu ro sd 13
5 2 5 1 - 6 2 [8 .1 .1 c )
C h ap m an R .Z a h s K R , Stryker M P ( 1 9 9 1 ) R elatio n o f co rtica l cell orien ­
tation selectivity to alig n m en t o f receptive fields o f the g cn icu lo co rti-
cal afferen ts that arb orize w ith in a single orien tatio n co lu m n in ferret
visual co rte x /N e u r o s c i 11 1 3 4 7 - 5 8 [5 .6 .2 b ]
C h arm an \VN ( 1 9 7 9 ) Sp eckle m ovem en t in laser refractio n . 1. T h eo ry
A m ] O p tom P h y sio l O p t 5 6 2 1 9 - 2 7 [9 .2 .4 b ]
C h arm an \VN ( 1 9 9 1 ) O p tic s o f the hum an eye In V ision a n d v is u a l d y s­
fu n c tio n Vol 1 V isu a l o p tics a n d in stru m en ta tio n (cd \XfN C h arm an )
pp 1 - 2 9 M a cM illa n . L o n d o n (5 -1 .1 ]
C h arm an W N , I leron G ( 1 9 7 9 ) Spacial frequ ency and th e dynam ics o f
the acco m m o d atio n response O p tica A cta 2 6 2 1 7 - 2 8 [9 .6 .4 c ]
C h arm an W N , H eron G ( 1 9 8 8 ) F lu ctu atio n s in a cco m m o d atio n : a
review O p h th a l P h y sio l O pt 8 1 5 3 - 6 4 [9 .7 .1 a ]
C h arm an W N , H eron G ( 2 0 0 0 ) O n the lin earity o f acco m m o d atio n
dynam ics V is R es 4 0 2 0 5 7 - 6 6 [9 .7 .2 b ]
C h arm an W N , Jen n in g s JA M ( 1 9 7 6 ) O b je ctiv e m easu rem ents o f the
lo n g itu d in al ch ro m a tic ab erratio n o f the hum an eye V is R es 1 6 9 9 9 -
1 0 0 5 [9 .1 .2 a ]
C h arm an W N , T u ck er J (1 9 7 7 ) D ep en d en ce o t acco m m o d atio n
response on th e spatial freq u en cy spectru m o f t h e observed o b jc c t Vis
R es 1 7 1 2 9 - 3 9 [9 .6 .4 c ]
C h arm an W N , T u ck er J (1 9 7 8 a ) A cco m m o d a tio n as a fu n ctio n o f o b je c t
form A m J O ptom P h y sio l O pt 5 5 8 4 - 9 2 [9 .6 .4 c ]
C h arm an W N , T u ck er J ( 1 9 7 8 b ) A cco m m o d atio n and co lo r / O p t S oc
A m 6 8 4 5 9 - 7 0 ( 9 - 1.2b , 9 .6 .4 c ]
C h arn w o od L ( 1 9 5 1 ) T h e diagnostic and th erap eu tic use o f m on ocu lar
o cclu sio n B r it ] P h y s io l O pt 8 4 3 - 5 6 [1 0 ,2 ,3 a , 8 .3 .3 a ]
C h atficld С ( 1 9 9 7 ) I h c a n a ly sis o ft it n c scries C h ap m an an d H all, L on d on
[3 .5 ]
C h atu rv ed i V , van G isb ergen JA M ( 1 9 9 7 ) S p ecificity o t saccadic
ad ap tation in th ree-d im en sion al space Vis R es 37 1 3 6 7 -8 2
[1 0 .8 .3 a )
C h a tu rv e d i V> van G isbergen JA M ( 1 9 9 8 ) Shared target selection tor
C om bined version-vcrgcncc eye m ov em en ts / N eu ro p h y sio l 8 0
8 4 9 - 6 2 [1 0 .8 .1 a ]
C h atu rv ed i V, van G isbergen JA M ( 1 9 9 9 ) P ertu rb ation o f co m b in ed
saccad c-v crgcncc m ovem ents by m icro -stim u latio n in m o n k ey supe­
rio r c o llic u lu s / N eu ro p h y sio l8 1 2 2 7 9 - 9 6 [ 1 0 .1 0 .2 c ]
C h atu rv ed i V, van G isbergen J A M ( 2 0 0 0 ) S tim u latio n in the rostral pole
o t m on key su p erior co llicu lu s; cfFccts o n vergence eye m ovem ents
E x p B ra in R es 1 3 2 7 2 - 8 (1 0 .1 0 .2 c ]
C h au d h u ri A , M atsu bar a JA » C y n ad cr M S ( 1 9 9 5 ) N eu ro n al activ ity in
prim ate visual c o rte x asscsNcd by im m u n ostain in g for th e tran scrip ­
tion factor Z if 2 9 8 Vis N c u r o s d 1 2 3 5 - 5 0 (5 .4 .3 a , 5 .7 .2 a , 6 .6 .1 c ]
C haw anya T , A oyagi T , N ishikaw a 1, c t al. ( 1 9 9 3 ) A m od el fo r feature
lin kin g via co llcctiv c oscillation s in the prim ary visual c o rtc x B io l
C y b er 6 8 4 8 3 - 9 0 | 4.3.4g]
C h ccscm a n EW , G u yton D L ( 1 9 9 9 ) V ertical fusion al vergence: the key
to dissociated vertical d ev iatio n A rc h O p h th td 1 1 7 1 1 8 8 - 9 1 [1 0 .6 .2 ,
10.7.1]
C h e n C , R cg ch r W G ( 2 0 0 0 ) D ev elop m en tal rem od elin g o f th e rc tin o -
g cn icu latc synapse N eu ro n 2 S 9 5 5 - 6 6 [6 .4 .4 c ]
C h e n D F , Sch n eid er G E , M a rtin o u [ C , T oncgaw a S ( 1 9 9 7 ) B cI-2 p ro ­
m o tes regen eration o f severed axons in m am m alian C N S N a tu re 3 8 5
4 3 4 - 9 (6 .4 .3 c , 6 .4 .7 b ]
C h e n G , S im a J , Jin M ,e c al. ( 2 0 0 8 ) Scm ap h o rin -3A gu ides radial m igra­
tion o f co rtic a l n eu ron s d u rin g d ev elo p m en t N a tu re N eu ro sci 11
3 6 - 4 4 (6 .4 .5 a )
C h e n H X . O tm a k h o v N . Strack S , c t al. ( 2 0 0 1 ) Is p ersisten t activ ity o f
calciu m / calm o d u lin -d cp en d cn t kinase required for th e m ain ten an ce
o t L T P ? / N eu ro p h y sio l 8 5 1 3 6 8 - 7 6 [6 .5 .1 a]
C h e n L K ruger P B . 1 lo fcr { I ,c t al. ( 2 0 0 6 ) A cco m m o d atio n wirh highcr-
o rd er m o n o ch ro m atic ab erration s corrected w ith adaptive op tics
/ O p t S o c A m A 2 3 1 - 8 [9 .8 .2 c ]
C h e n L , A rta l P. G u tierrez D , W illia m s D R ( 2 0 0 7 ) N eural com p en sa­
tion for che best ab erratio n co rrectio n / Vis 7 ( 1 0 ) A rticle 9 [9 .6 .5 a ]
C h e n X , H e S ( 2 0 0 4 ) L ocal facto rs d eterm in e the stabilization o f m o n ­
o cu lar am bigu ou s and b in ocu lar rivalry stim uli C u rr B io l 14
1 0 1 3 - 1 7 [4 .5 .9 b ]
C h c n -H u a n g С , M c C r c a RA ( 1 9 9 8 ) V iew in g distan ce related sensory
processing in th e ascen d in g tra c t o f D eiters v cstib u lo -ocu lar reflex
pathw ay J V estih R es 8 1 7 5 - 8 4 [ 1 0 .9 .2 ]
C lu n g H , C h in o Y M , S m ith E L . c t al. ( 1 9 9 5 ) T ran sfer ch aracteristics o f
X L G N n eu ron s in cats reared w ith early d iscord an t b in o cu lar vision
J N eu ro p h y sio l 7 4 2 5 5 8 - 7 2 (8 .2 .2 c )
C h e n g 11 M , S in g h O S , Kw ong K K . e t al. ( 1 9 9 2 } Shape o f the m yopic eye
as seen w ith h ich -reso lu tio n m ag n etic reson an ce im ai’ini’ O p tom 17s
S c i 6 9 6 9 8 - 7 0 1 [9 .2 .1 ]
C h e n g K . H ascgaw a T , Saleem K S , T an a k a К ( 1 9 9 7 ) C o m p a riso n o f
neuronal selectivity for stim ulus speed length and co n trast in the pre*
striate visual c o rtic a l area V 4 and M T o t the m acaque m onkey
J N eu ro p h y sio l 7 1 2 2 9 9 - 8 0 [5 .8 .3 a ]
C h e n g K . W aggoner A , T an aka K , ( 2 0 0 1 ) H um an o cu lar d om inan ce
colu m n s as revealed by high*field fu n ctio n a l m agn etic reson ance
im agin g N eu ro n 3 2 3 5 9 - 7 4 [5 .4 .3 f. 5 .7 .2 a ]
C h e n g L C , Pastrana E , Tavazoie M , D o ctsch 1: ( 2 0 0 9 ) m iR -1 2 4 regu­
lates ad ult n eu rogcn esis in the su bventricu lar zon e stem cell n ich e
K i t N eu ro sci 1 2 3 9 9 - 4 0 8 [6 .4 .2 d ]
C h e n g X , B rad ley A , H o n g X .T h ib o s L N ( 2 0 0 3 ) R elation sh ip betw een
refractive erro r and m o n o ch ro m a tic ab erration s o f th e eye O p tom Vis
Av 8 0 4 3 - 9 [9 .6 .2 a ]
C h crn iss H ( 1 9 3 3 ) G alen and P osid oniu s’ th e o ry o f vision A m f P h ilo l
5 4 1 5 4 - 6 1 [2 .1 .4 ]
C h e ru b in d’O rlea n s P ( 1 6 7 1 ) L a d io p tiq u e o cu lairc o u la th c o riq u c la
positive c t la m cch an iq u c de I o cu la irc d io p tiq u e c n to u tes ses cspeces
Jo lly c t B cn a rd , Paris [ 2 . 1 1.2a]
C h e ru b in d ’O rlca n s P ( 1 6 7 7 ) La vision p artaite ou Ics c o n c o u rs d c s d c u x
axes dc la vision cn un scul p o in t d c lo b je t M u rb rc-C ra n io isv , Paris
[2 .1 1 .2 a ]
C h csscld cn W ( 1 7 2 8 ) A n a cco u n t o f som e ob serv atio n s made by a young
gentlem an w h o was b o rn blin d o r lost his sight so early that he had n o
rem em bran ce o f ever having seen and w as co u ch ed betw een 13 and
14 years o f age P h ilo s T r R S oc 3 5 4 4 7 - 5 0 |8.1.3]
C h e u n g B S K , H ow ard IP ( 1 9 9 1 ) O p to k in e tic to rsio n : dynam ics and
relation to circu lar vection Vis R es 31 1 3 2 7 - 3 6 (1 0 .7 .1 )
C h cv a lcy rc V ,C a stillo PE ( 2 0 0 4 ) E n d ocim n abin oid -m cd iatcd m ccaplas-
ticity in the h ipp ocam pus N eu ro n 4 3 8 7 1 - 8 1 [6 .5 .3 )
C h ia n g C , L itin g tu n g Y , L ee E , c t al. ( 1 9 9 6 ) C y clo p ia an d defective axial
p a ttern in g in ra icc lackin g S o n ic h ed gehog gen e fu n ctio n N a tu r e 3 8 3
4 0 7 - 1 3 [6 .4 .2 a ]
C h ic h iln isk y E J, Baylor D A ( 1 9 9 9 ) R cccp tiv c-ficld m icro stru ctu re o f
blue-yellow ganglion cells in prim ate retin a N a t N eu ro sci 2 8 8 9 - 9 3
[5 .1 .4 a ]
C h ich iln isk v E J, K alm ai R S ( 2 0 0 2 ) F u nctio nal asym m etries in O N and
O F F ganglion cells o f prim ate retina / N eu ro sd 2 2 2 7 3 7 - 4 7 [5 .1 .4 a ]
C h in N B , B rein in G M ( 1 9 6 7 ) R a tio o f accom m od ativ e con v ergen ce to
a cco m m o d a tio n A rch O p h th a l 7 7 7 5 2 - 6 [ 1 0 .4 .1 )
C h in o Y M ( 1 9 9 7 ) R cccp tiv c-ficld p lasticity in the adult visual co rtc x :
d ynam ic signal rerou tin g o r exp erien ce-d ep end ent p lasticity S a n
N e u r o sc i9 3 4 - 4 6 [5 .5 .6 c )
C h in o Y M , K aplan E ( 1 9 S S ) A b n o rm al o rien ta tio n bias o f L G N n eu ­
ron s in strab ism ic cats In v est O p h th a l Vis S ci 2 9 6 4 4 - 8 [8 .2 .3 a ]
C h in o Y M , S h an sky M S . 1 lam asaki D1 ( 1 9 8 0 ) D ev elop m en t o f recep ­
tive field properties o f retinal ganglion cells in k itten s raised with
convergent sq u in t E x p B r a in R es 3 9 3 1 3 - 2 0 [8 .2 .1 ]
C h in o Y M , Sh ansky M S . Jan k ow sk i W L , B an ser FA ( 1 9 8 3 ) E tfects o f
rearing k itten s w ith con v erg en t strabism us on the d ev elo p m en t o f
receptive field properties in striate co rtex neu ron s / N eu ro p h y sio l 5 0
2 9 5 - 8 6 [ 8 .2 .3 f ]
C h in o Y M , Ridder W H .C z o r a EP ( 1 9 8 8 ) E tfects o f convergent strabis­
m us on sp atio-tem p oral response properties o f neu ron s in c a t area 18
E x p B r a in R es 7 2 2 9 4 - 7 8 18.2.3a]
C h in o Y M , S m ith E L . W ada H , c t al. ( 1 9 9 1 ) D isru p tion o f binocularly
correlated signals alters the postn atal d ev elo p m en t o f spatial p ro p er­
ties in cat striate co rtic a l neu ron s J N a tr o p h y s io l 6 5 8 4 1 - 5 9 [8 .2 .3 a ]
C h in o Y M . K aas J H , S m ith E L , e t al. ( 1 9 9 2 ) Rapid reo rgan ization o f
co rtic a l m aps in ad ult cats follow in g restricted d caftcrcn tatio n in
retina V is R es 3 2 7 8 9 - 9 6 [5 .5 .6 c ]
C h in o Y M , C h e n g H , S m ith E L ,c f al. ( 1 9 9 4 a ) Early d iscord an t b in o cu ­
lar vision disrupts signal transfer in the lateral gen icu late nucleus P ro c
N a d A c a d S ci 9 1 6 9 3 8 - 4 2 [8 .2 .2 c ]
C h in o Y M . S m ith E L . Yoshida K , c t al. ( 1 9 9 4 b ) B in o cu lar in teractio n s
in striate co rtica l neu ron s o f cats reared w ith d iscord an t visual inputs
J N eu ro sci 1 4 5 0 5 0 - 6 7 [8 .2 .3 a ]
C h in o Y M . S m ith E L , I la tta S, C h e n g I i ( 1 9 9 7 ) Postn atal d ev elo p m en t
o f b in o cu la r disparity sensitivity in neu ron s o f th e prim ate visual
co rte x / N eu ro sci 1 7 2 9 6 - 3 0 7 [6 .6 .4 a , 6 .7 .1 .8 .3 .2 )
C h in o Y M , S m ith E L , Z h a n g B , et al. ( 2 0 0 1 ) R ecovery o f b in ocu lar
responses by co rtical n eu ron s after early m o n o cu lar lesions N a t
N eu ro sci 4 6 8 9 - 9 0 [5 .5 .6 c ]
C h iu C , W elikv M ( 2 0 0 2 ) R elation sh ip o f correlated spon tan eou s activ ­
ity to fu n ctio n al ocu lar d om in an ce colu m n s in th e developin g visual
c o rtc x N eu ro n 3 5 1 1 2 3 - 4 |6.7.2d]
C h k lo v sk ii D B ( 2 0 0 0 ) B in o cu lar disparity can explain the orien tatio n o f
ocu lar d om in an ce strip es in prim ate p rim ary visual area ( V I ) V is R es
4 0 1 7 6 5 - 7 3 1 5 .7.2c]
C h o u d h u ry B P , W h itte rid g e D , W ilso n M E ( 1 9 6 5 ) Ih e fu n ctio n o f t h e
callosal c o n n e ctio n s o f the visual c o r tc x J £ u a r t J E x p P h y sio ! 5 0 2 1 5 -
19 [5 .3 .5 ]
C h o w K L ( 1 9 7 3 ) N euronal ch anges in the visual system follow in g visual
deprivation In H an d b oo k o t sensory phvsiologv (cd R lu n g) Vol
V I 1/3A pp 5 9 9 - 6 3 0 Springer. N ew York [8 .1 .1 a , 8 .2 .2 d ) ’
C h ristak o s C N ( 1 9 9 4 ) A nalysis o f syn ch ron y (co rre la tio n s) in neural
p op u lation s by m eans o f u n it-to-aggregate co h eren ce co m p u tatio n s
N eu ro sci 5 8 - * 3 - 5 7 [4.3.4g|
C h risto p h erso n K S , U llian E M , e t al. ( 2 0 0 5 ) 'Ih ro m b o sp o n d in s are
astro cy tc-sceretcd p ro tein s th a t p ro m o te C N S synaptogenesis C e ll
1 2 0 4 2 1 - 3 3 16.4.4c]
C h u b b C , Sp erling G ( 1 9 8 8 ) D rift-b alan ced random stim uli: a general
basis fo r studying n o n -F o u rier m o tio n p ercep tio n / O pt S oc A n t A 5
1 9 8 6 - 2 0 0 7 [4 .4 .4 ]
C lu ib y k in A A , Atavoy D , E th crto n M R ,c t a l . ( 2 0 0 7 ) A ctiv ity -d cp cn d cn t
validation o f ex cita to ry versus in h ib ito ry synapses by neuroligin-1
versus n cu ro lig in -2 . N eu ro n 5 4 9 1 9 - 3 1 (6 .4 .4 b )
C h u n g S T L , Li R W , L evi D M ( 2 0 0 8 ) L earn in g со id en tify n car-th rcsh -
old lu m in an ce-d efin ed and con trast-d efin ed letters in observers w ith
am blyopia V is R es 4 8 2 7 3 9 - 5 0 (8 .4 .6 c )
C h u rch land P S , Sejn ow ski T J ( 1 9 8 8 ) Perspectives on cogn itive n eu ro ­
scien ce S cien ce 2 4 2 7 4 1 - 5 [ 5 . 4 . 3 f )
C ia n i L , Salin as P C ( 2 0 0 5 ) W N T s in the v ertebrate nervous system :
from p attern in g to n eu ron al co n n ectiv ity N a t R e v N eu ro sci 6 351 - 6 2
(6 .4 .2 a )
C ic c o n c D N , Su H . H cvi S. c t al. ( 2 0 0 9 ) K D M IB is a h isto n e H 3 K 4
dcincthylu.sc required to establish m aternal g en o m ic im p rin tsN a totre
4 6 1 4 1 5 - 8 [6 .6 .1 a ]
C.incr F.B, Sch cim an M M , S c h o n c l-K lits c h E ( 1 9 8 9 ) Stereop sis testin g
in 1 8 - to 3 5 - m o n t h - o ld ch ild ren using operant preferential lo ok in g
O p tom Vis S ci 6 6 7 8 2 - 7 [7 .6 .1 c ]
C in c r E B , S c h a n c l-K lits c h E , Sch cim an M M ( 1 9 9 1 ) S tereo acu ity devel­
o p m en t in young ch ild ren O p tom V is S ci 6 8 5 3 3 - 6 [7 .6 .1 c ]
C in c r E B , S c h a n c l-K lits c h E , H c r z b c r g C ( 1 9 9 6 ) Stereoacu ity d evelop­
m en t: 6 m o n th s to 5 years A n ew to o l fo r testin g an d screen in g Opto?n
V is S ci 7 3 4 3 - 8 [7 .6 . Ic]
C itri A , M alcn k a R C ( 2 0 0 7 ) Sy nap tic p lasticity : m ultiple form s, fu n c­
tio n s, and m ech an ism s N eu ro p sy ch o p h a rm a co lo g y R ev iew s. 1 - 2 4
[6 .5 .1 a ]
C iu ftrcd a K J ( 1 9 9 1 ) A cco m m o d atio n and its an om alies In V ision a n d
v isu a l d y sfu n ction V ol I V isu al o p tics and in stru m en tatio n (cd W N
C h a rm a n ) pp 2 3 1 - 7 9 M a cM illa n , L o n d o n (9 .2 .3 )
C iu ftrcd a K J , I lo k o d a S C ( 1 9 8 3 ) Spatial freq u en cy d ependence o f
accom m od ativ e responses in am blyop ic eyes Vis R es 2 3 1 5 8 5 - 9 4
18.4.5a, 9 .6 .4 c ]
C iu ftrcd a K J, I lo k o d a S C ( 1 9 8 5 a ) E ffect o f in stru ctio n an d h igh er level
co n tro l on th e accom m od ativ e response spatial freq u en cy profile
O p h th a l P h y sio ! O pt 5 2 2 1 - 3 (9 .6 .4 c )
C iu ftrcd a K J , H o k o d a S C ( 1 9 8 5 b ) Su b jectiv e vergence erro r a t near
d urin g active head rotation O p h th a l P h y sio l O p t 5 4 1 1 - 1 5 ( 1 0 .5 .4 a )
C r.iskc В , Craw shaw M ( 1 9 7 4 ) A daptive ch an g cs o f o p p o site sign in rhe
o c u lo m o to r system s o f the tw o eyes Q u a r t} E x p P sy ch ol 2 9 1 0 6 - 1 3
H .5 .7 jl
C ra to n L G . Yonas A ( 1 9 8 8 ) Infants* sen sitiv ity to bou n d ary flow in fo r­
m ation for depth a t an edge C h ild D ev el 5 9 1 5 2 2 - 9 [7 .4 .2I>]
C raw ford J D . V ilis T ( 1 9 9 2 ) Sy m m etry о f o cu lo m o to r burst neuron
coord in ates ab ou t L is tin g s plane / N eu ro p h y sio l 6 S 4 3 2 - 4 8
[1 0 .1 0 .4 )
C raw ford |D . C a d cra W , V ilis T ( 1 9 9 1 ) G e n e ratio n o f torsion al and ver­
tica l ey e p osition signals by th e in terstitial nucleus o f C a ja l S cien ce
2 5 2 1 5 5 1 - 3 ( 1 0 .1 0 .4 )
C raw ford M L J ( 1 9 9 8 } C o lu m n spacing in n orm al and visually deprived
m o n k ey sE x p B r a in R e s 1 2 3 2 8 2 - 8 [8 .2 .3 a ]
C raw ford M L J, H arw crth R S ( 2 0 0 4 ) O cu la r d o m in an ce colum n w idth
and c o n tra st sensitivity in m on keys reared w ith strabism us or an i­
so m etro p ia In v est O p h th a l V is S ci 4 5 3 0 3 6 - 4 2 [8 .2 .4 a ]
C raw ford M L J, N oord en G K von ( 1 9 7 9 ; The effects o f sh ort-term
exp erim en tal strabism u s on the visual system in М а ш а m u la tta
In v es t O p h th a l V is S ci 1 8 4 9 6 - 5 0 4 [8 .2 .2 c ]
C raw ford M L J , N o o rd en G K v on ( 1 9 8 0 ) O p tica lly induced c o n c o m i­
ta n t strabism us in m on kcv s In v est O p h th a l V is S ci 19 1 1 0 5 -9
[8 .2 ,5 a ]
C raw ford M L J, N oord en G К von ( 1 9 9 6 } Sh rin kage and recovery o f cells
o f the lateral gen icu late nuclei w ith prism -rearing in m acaques B eh a i'
B r a in R es 7 9 2 3 3 - 8 [8 .2 .2 c ]
C raw ford M L J , N oord en G K von , M ch a rg L S , c t al. ( 1 9 8 3 ) B in o cu lar
n eu ron s and b in o cu la r fu n ctio n in m onkeys and ch ild ren In v est
O p h th a l Vis S c i 2 7 4 9 1 - 5 [8 .2 .5 a ]
C raw ford M L J, Sm ith E L , H arw crth R S , N o o rd en G K v on ( 1 9 8 4 )
S tcrco b lin d m onkeys have few b in o cu la r n eu ron s In v es t O p h th a l Vis
S ci 2 5 7 7 9 - 8 1 [8 .2 .5 a !
C raw ford M L J, D e Faber J T , H a rw crth R S , e t al. ( 1 9 8 9 ) T h e effects o t
reverse m o n o cu la r d eprivation in m onkeys. 11. Elcctroph ysiological
and a n a to m ica l stu d ies E x p B r a in R es 7 4 3 3 8 - 4 7 [8 .3 .2 ]
C raw ford M L J , H a rw crth R S , S m ith EL> N o o rd en G K von ( 1 9 9 6 a )
L oss o f stereopsis in m on keys follow in g prism atic b in o cu lar dissocia­
tion d urin g in fan cy B c h a v B r a in R es 7 9 2 0 7 - 1 8 [8 .2 .5 a ]
C raw ford M L J, Pcsch T W ', N o o rd en G K von (1 9 9 6 b ) E x c ita to ry neu­
rons arc lost follow ing p rism atic b in o cu lar d issociation in in fan t
m onkeys B c h a v B r a in R es 7 9 2 2 7 - 3 2 [8 .2 .5 a ]
C rcu t/ fcld t O D ( 1 9 7 7 ) G e n e ra lity o f th e fu n ctio n a l stru ctu re o f the
n eocorcex N a tu ru -issen sch a fu n 6 4 5 0 7 - 1 7 [5 .5 .1 b]
C rcw th cr D P , C rcw th cr S G , Pettigrew J D ( 1 9 7 8 ) A role for extraocu lar
afferent*' in p o s t-c r itic a l period reversal o f m o n o cu lar deprivation
/ P h y sio l 2 8 2 1 8 1 - 9 5 [8 .2 .3 c ]
C rc w th c r S G , and G rc w th c r D P ( 1 9 9 3 ) A m blyopia and suppression in
b in o cu lar c o rtic a l n eu ro n es o f strab ism ic c a t N eu ro rep o rt 4 1 0 8 3 - 6
[8 .2 .3 a , 8 .2 .3 b ]
C rc w th c r S G , C rc w th c r D P , Peek C K , Pettigrew J D ( 1 9 8 0 ) V isu al c o r ti­
c a l effects o f rearing cacs w ith m o n o cu lar o r b in o cu lar cyclo to rsio n
/ N eu ro p h y sio l 4 4 9 7 - 1 1 8 (7 .5 ]
C rcw th cr S G , G rcw ch cr D P , M itc h e ll D E ( 1 9 8 3 ) The effects o f sh o rt­
term occlu sion therapy o n reversal o f th e an ato m ical and p hysiologi­
cal e ffe c ts o f m o n o cu la r d eprivation in chc lateral gen icu late nucleus
and visual co rtex o f k itten s E x p B r a in R es 51 2 0 6 - 1 6 8 .3 .1 c ]
C rcw th cr S G , G rc w th c r D P ,C ld la n d B G ( 1 9 8 5 ) C o n v e rg en t strab ism ic
am bly op ia in c a ts E x p B ra in R es 6 0 1 —9 [ 8 .2 .2 c )
C rick F ( 1 9 8 4 ) F u n ctio n o f the th alam ic reticu lar co m p lex : the search­
light hypothesis P r o c N a t l A c a d S et 8 1 4 5 S 6 - 9 0 15.2.2b )
C ric k F, K och С ( 1 9 9 0 ) Tow ards a n eu ro b io lo g ical th e o ry o f con scio u s­
ness S em in a rs in th e N eu roscien ces 2 2 9 3 - 7 5 [4 .3 .4 c )
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Fredj N B , B u rron c J ( 2 0 0 9 ) A resting p ool o f vcvielcs is responsible for
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Fredj N B . H am m on d S, O tstin a H , e t al. ( 2 0 1 0 ) Synaptic activ ity and
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Freed M A ( 2 0 0 5 ) Q u a n ta l c n c o d in g o f in fo rm atio n in a retinal ganglion
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Freedm an D J, R icscn h u b cr M , P o g g io T , M iller F.K ( 2 0 0 2 ) V isual ca te­
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Freedm an D J , R icscn h u b cr M . P o g g io T , M ille r E K ( 2 0 0 3 ) A C om p arison
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Freedm an D J, R icscn h u b cr M , P oggio T , M ille r E K ( 2 0 0 6 ) Experience-
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Freedm an M S , Lucas R J, S o n i B , c t al. ( 1 9 9 9 ) R eg u lation o f m am m alian
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Freem an AW', N guyen V A , Jo lly N ( 1 9 9 6 ) C o m p o n e n ts o l visual acuity
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Freem an M , G u rd o n J B ( 2 0 0 2 ) R eg u latory principles o t developm ental
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Freem an R D , B rad ley A ( 1 9 8 0 ) M o n o cu larly deprived hum ans: n ondc-
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1 8 .2 .3 П '
Freem an R D , Oh/.awa I ( 1 9 8 8 ) M o n o cu larly deprived cats: b in o cu lar
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Freem an R D , T su m o to T ( 1 9 8 3 ) A n eleccroph ysiological com p arison o f
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Freem an W ( 1 9 7 5 ) M a ss a c tio n in th e n erv o u s system A cad em ic Press,
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Freem an, W T ( 1 9 9 4 ) T h e gen eric v iew p oin t assum ption in a fram ew ork
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Fregnac Y. Sh u lz D ,T h o r p e S , B icn cn sto ck E ( 1 9 8 8 ) A cellu lar analogue
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Freiwald W A , К re ite r A K , Sin ger W ( 1 9 9 5 ) Stim u lu s depend ent inter-
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Frenkel M Y , Bear M F ( 2 0 0 4 ) H ow m o n o cu lar deprivation sh ifts ocular
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Freund T F , M a rtin К А C , Soltesz I, c t al. ( 1 9 8 9 ) A rb o rizatio n pattern
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Freund T F , K a to n a I, P io m clli D ( 2 0 0 3 ) R ole o f en d ogen o u s eannabi-
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G u illcry R W . M ason C A , Tavlor J S H ( 1 9 9 5 ) D evelop m en tal d ctcrm i-
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G u ld enagel M , A m m crm u llcr J , Fcigcnspan A ,c t a l . ( 2 0 0 1 ) V isual tran s­
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G u o H G , Ingolia N T * W cissm an J S , B a rtel D P ( 2 0 1 0 } M am m alian
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G iicig R , So in p olin sk y H ( 2 0 0 6 } T h e tcm p o tro n : a neuron that learns
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H a m p to n D R , K crtesz A E ( 1 9 8 2 ) H um an response to cy clo fu sion al
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[1 0 .7 .2 a |
H am p ton D R , K crtesz A E ( 1 9 8 3 ) Fusional vergence response to local
peripheral stim u la tio n / O pt S oc A?n 7 3 7 - 1 0 [1 0 .5 .6 ]
H anashim a C , S h c n L , L i S C , Lai E ( 2 0 0 2 ) B r ia n F a cto r-1 co n tro ls
th e p roliferation and d ifferen tiation o f n co c o rtic a l p ro g en ito r
cclls through in d ep en d ent m ech an ism s / N eu ro sci 2 2 6 5 2 6 - 3 6
[6 .4 .5 b ]
H anashim a C , L i S C , Sh cn I., c t al. ( 2 0 0 4 } F o x g ! suppresses early
co rtic a l ccll fate S cien ce 3 0 3 5 6 - 9 [6 .4 .5 a ]
H anganu I L , B cn -A ri Y, K hazip ov R ( 2 0 0 6 ) R etin a l waves trigger spin ­
d le Ь и ш л in th e n eon atal rat visual co rtex / N eu ro sci 2 6 6 7 2 8 - 3 6
[6.6.2]
H iinny P, von der H cvd t R ( 1 9 8 2 ) T h e effect o f h o riz o n ta l-p la n e
en v iro n m en t o n the d evelopm ent o f b in o cu lar recep tive fields o f cells
in cat visual c o r te x / P h y sio l 3 2 9 7 5 - 9 2 [7 .5 ]
H anover J L , H u an g Z J , Toncgavva S , Stryk er M P ( 1 9 9 9 ) Brain-dcrivcd
n eu ro tro p h ic faccor oveiexprcssion induces p reco ciou s c ritic a l period
in m ouse visual c o rte x /N e u r o s c i 19 R C 4 0 | 8 .2.7f]
H ansen M J, D alla l G E , Flanagan J G ( 2 0 0 4 ) R etinal axon response со
cp h rin -A s show s a graded, co n cen tra tio n -d ep en d en t tran sitio n trom
g row th p ro m o tio n со in h ib icion N a tr o n 4 2 7 1 7 - 3 0 [6 .4 .3 c ]
I la o 1 1. R ivkccs SA ( 1 9 9 9 ) T h e b iolog ical c lo ck o f very prem ature pri­
m ate in fan ts is responsive Co light P ro c N a t l A c a d S ci 9 6 2 - 4 2 6 -9
[6 .3 .2 b ]
H ara N , Steffen H , R o b erts D C , Z e e D S ( 1 9 9 8 ) E ffects o f h orizon tal
vergence on the m o to r and sensory co m p o n e n ts o f vertical fusion
In v est O p h th a l Vis S ci 3 9 2 2 9 8 - 7 6 ( 1 0 .6 .1J
H araca N C , C h o i S , Pyle J L , et al. ( 2 0 0 6 ) Frequ cncy-depcnd enc
kin etics and prevalence o f kiss-and-run and reuse a t h ipp ocam pal
synapses stu died w ith novel q u en ch in g m eth od s N eu ro n 4 9 2 4 3 - 5 6
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I iarauzov A , Sp o lid o ro M , D i C risto G , c t al. ( 2 0 1 0 ) R ed u cin g in craco r-
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H arris A E , E rm cn tro u c G B , Sm all S I . ( 1 9 9 7 ) A m od el o f ocu lar d o m i­
n an ce colum n d ev elo p m en t by co m p e titio n for tro p h ic facto r P ro c
N a tl A c a d S ci 9 4 9 9 4 4 - 9 [ 6 .7 .2 f ]
H arris G G ( 1 9 6 0 ) Binau ral in teractio n s o t im pulsive stim uli and pure
to n es/ A cou st S o c A m 3 2 6 8 5 - 9 2 [4 .5 .7 d ]
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o f reversible figures A m J P sy ch ol 9 3 4 4 5 - 5 7 [4 .5 .9 c ]
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H arris P, M acFarlanc A ( 1 9 7 4 ) T h e grow th o f th e effective visual field
from b irth to seven w eeks/ E x p C h ild P sy ch ol 1 8 3 4 0 - 8 [7 .3 .5 ]
H arris W A ( 1 9 8 4 ) A xon al pachfinding in che absen ce o f norm al pach-
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H arsanyi K , Fricdland er M J (1 9 9 7 a ) T ran sien t synaptic p o ten tia tio n in
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H arsanyi K , Fricdlander M J (1 9 9 7 b ) T ran sien t synaptic p o ten tiatio n in
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H arter M R ,S c ip le W H , Salm on L ( 1 9 7 3 ) B in o cu lar sum m ation o t visu­
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H a r tig JK , H u erta M F , H a sh ik a w a T , L icsh o u t D P ( 1 9 9 1 ) P ro jectio n o f
the m am m alian superior co llicu lu s u pon th e dors.il lateral gcnieulate
nucleus: org an ization o f tc cto g cn icu ia tc pathways in nin eteen
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H artlin e H K ( 1 9 3 8 ) The response o t single o p tic nerve fibres o f th e ver­
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H artlin e H K ,G r a h a m C H ( 1 9 ^ 2 ) N erve im pulses from single recep to rs
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H artlin e P H , H urley A C , Lange G D ( 1 9 7 9 ) Eye stab ilization by vtato-
cvst m ediated o c u lo m o to r reflex in N a u tilu s J C om p P h y sio l A 1 3 2
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H artm an n E E , B an k s M S ( 1 9 9 2 ) Tem p oral co n trast sensitivity in hum an
in fan ts V is R es 3 2 1 1 6 3 - 8 [7 .2 .3 a ]
H artm an n E U , Su cco p A , Buck S L .c t al. ( 1 9 9 3 ) Q u a n tifica tio n o f m o n ­
o cu lar o p to k in e tic nystagm us asym m etries and m o tio n perception
w ith m o tio n -n u llin g tech n iq u es / O pt S o c A m A 10 1 8 3 5 -4 0
[8 .4 .5 c ]
H art veil F., R am berg S I, H cggchm d P ( 1 9 9 3 ) Brain stem m o d u latio n o f
spatial rcccptivc field properties o f single e e lk in the dorsal lateral
gen icu late nucleus o f th e c a t/ N eu ro p h y sio l 7 0 1 6 4 4 - 5 5 [5 .2 .2 d ]
H aru ta M , H ara Y ( 2 0 0 7 ) E x p ericn cc-d riven ax o n retractio n w ith ou t
b in o cu lar im b alan ce in developin g visual c o rtc x С ю г B io l 1 7 3 7 - 4 2
[8.2.7c1
H arvey A R ( 1 9 8 0 ) A physiological analysis o f su b co rtical and co m m is­
sural p ro jectio n s o f areas 17 and 18 o f th e cat / P h y sio l 3 0 2 5 0 7 - 3 4
[5.3.51
H arvey C D , Sv ob od a К ( 2 0 0 7 ) L ocally d yn am ic synaptic learn in g rules
in pyram idal n eu ron d en d rites N a tu r e 4 5 0 1 1 9 5 - 2 0 0 [6 .5 .5 ]
I larv cy L O ( 1 9 7 8 ) Sin gle rep resen tation o f th e visual m id lin c in hum ans
N eu ro p sy ch o lo g ia 1 6 6 0 1 - 1 0 [5 -3 .5 )
H arw erth R S , S m ith E L . B o ltz R L , C raw ford M L J, N o o rd en G K von
(1 9 8 3 a ) Behavioral studies on th e effect o f a b n o rm al early visual
experien ce in m onkeys: spatial m o d u latio n sensitivity Vis R es 2 3
1 5 0 1 - 1 0 [8 .4 .2 a ]
H arw erth R S , S m ith E L . B o ltz R L , cc al. (1 9 8 3 b ) B eh avioral stu dies on
the effect o f ab norm al early visual experien ce in m onkeys: tem p oral
m o d u latio n sensitivity Vis R es 2 3 1 5 1 1 - 1 7 [8 .4 ,4 b ]
H arw erth R S , S m ith E L , O ku n d ayc O J ( 1 9 8 3 c ) O b liq u e effects vertical
e ffe c ts and m erid ion al am blyopia in m on kcv s E x p B ra m R es 5 3 14 2 -
5 0 [8 .4 .2 b ]
H arw erth R S , S m ith E L , C raw ford M L J. N o o rd en G K von ( 1 9 8 4 )
E ffects o t en u cleation o t the n on d cp riv cd eye on stim ulus depriva­
tio n am blyopia in m onkeys In v es t O p h th a l V is S ci 2 5 1 0 - 2 5 [8 .3 .2 ]
H arw crth R S , S m ith E L , D u n can G C , cc al. ( 1 9 8 6 a ) E ffects o f en u cle­
a tio n o f chc fixating eye on strab ism ic am blyopia in m on k ey In v est
O fljt b a J Vis S ci 2 7 2 7 6 - 5 4 [8 .4 .6 a ]
H arw crth R S , S m ith E L , D u n can G C . c t al. (1 9 8 6 b ) M u ltip le sensitive
p eriod s in chc d evelopm ent o f the prim ate visual system S cien ce 2 3 2
2 3 5 - 8 [8 .3 ]
H a rw crth R S , S m ith ILL, C ra w fo rd M L J, N o o rd cn G K von ( 1 9 9 0 )
B eh av ioral stu dies o f the sensitive p eriod o f d ev elo p m en t o f visual
fu n c tio n s in m on keys B e b a v B r a in R es 41 1 7 9 - 9 8 [8 .3 .2 ]
H arw crth R S , Sm ith E L , Paul A D , c t al. ( 1 9 9 1 ) F u n ctio n al effects o f
b ilateral form d eprivation in m on keys In v est O p h th a l Vis S ci 3 2
2 3 1 1 - 2 7 [8 .1 .2 ]
H a rw crth R S , S m ith E L , S id e ro v J ( 1 9 9 5 ) B eh avioral stu d ies o f lo cal stc-
reopsis and d isp arity vcrgcncc in m onkeys Vis R es 3 5 1 7 5 5 - 7 0
[1 0 .5 .3 ]
H a rw crth R S , S m ith E L , C ra w fo rd M L I, N oord cn G K von ( 1 9 9 7 )
S tereop sis and d isp arity v crg cncc in m onkeys w ith subnorm al
b in o cu lar vision Vis R es 3 7 4 8 3 - 9 3 18.3 .2]
H a scb c H , O h tsu k i H , K o n o R , K a k a h ira Y ( 1 9 9 8 ) B io m etric co n firm a­
tio n o f the H irsch b crg ratio in strabism ic ch ild ren In v es t O p h th a l Vis
S ci 3 9 2 7 8 2 - 5 [ 1 0 .2 .3 b ]
H ascb c H , О yam ada H , K in om u ra S , c t al. ( 1 9 9 9 ) H um an co rtical
areas activated in relatio n to v crgcncc eye m ov em en ts— a P E T studv
N eu ro im a g e 1 0 2 0 0 - 8 [ 1 0 .1 0 .3 ]
H aslw antcr T ( 1 9 9 5 ) M a th em a tics o f th ree-d im en sion al eye ro tatio n s
V is R es 3 5 1 7 2 7 - 3 9 [1 0 .1 .2 d ]
H asson U> H cn d ler T , B en B ash at I ) , M alach R ( 2 0 0 1 ) Vase o r facc?
A n eu ral correlate o t shape* selective grou ping processes in th e hum an
brain / C o g N e u ro s d 1 3 7 4 4 - 5 3 [5 .8 .3 c )
H ata Y, S try k er M P ( 1 9 9 4 ) C o n tr o l o f th alam o co rtical afferen t rear­
rangem ent bv postsynaptic activ ity in developin g visual c o rte x S cien ce
2 9 5 1 7 3 2 - 5 (8 .2 .7 c )
H ata Y, T su m o to T , S a to H , c t al. ( 1 9 8 8 ) In h ib itio n co n trib u tes to o rie n ­
tation selectiv ity in visual c o rte x o f cat N a tu r e 3 3 5 8 1 5 - 7 (5 .6 .2 b |
H ata Y, T su m o to T , S a to H , c t al. ( 1 9 9 3 ) D ev elo p m en t o f lo cal in terac­
tion s in cat visual c o r tc x studied b y c ro s s-co rre la tio n analysis
J N cu ro p h y sio l 6 9 4 0 - 5 6 [6 .4 .6 b ]
H ata Y, T su m o to T , Stryker M P ( 1 9 9 9 ) S electiv e p ru n in g o f m ore active
afferen ts w hen c a t visual c o rtc x is ph arm acologically in h ib ited
N eu ro n 2 2 3 7 5 - 8 1 [8 .2 .7 c ]
H ata Y, O h sh im a M , Ichivaka S, c t al. ( 2 0 0 0 ) Brain-derived n cu ro tro p h ic
fa c to r expands ocu lar d o m in a n ce co lu m n s in visual c o rtc x in m o n ­
ocu larlv deprived and n ond cprivcd k itten s but d ocs n o t in adult cats
J N eu rosci 2 0 R C 5 7 | 6.7.2d , 8 .2 .7 f ]
H atan ak a Y , M u rakam i F ( 2 0 0 2 ) In v itro analysis o f t h e o rig in , m igra­
to ry behavior, and m atu ratio n o f co rtical pyram idal cells / C om p
N eu ro l 4 5 4 1 - 1 4 [6 .4 .5 b ]
H a tto ri M , O stcrficld M , Flanagan J G ( 2 0 0 0 ) R egulated cleavage o t a
co n ta ct-m ed ia ted axon rep ellen t S d c n c e 2 8 9 1 3 6 0 - 5 [6 .4 .3 c]
H aw kcn M J, Parker A J ( 1 9 8 4 ) C o n tra s t sensitivity and o rien ta tio n selec­
tivity in lam ina IV o f the striate c o rte x o f old world m onkeys E x p
B r a in R es 5 4 3 6 7 - 7 2 ( 5 . 6 . 1 ]
H aw kcn M J, Shapley R M , G r o s o f D H ( 1 9 9 6 ) T cm p o ral-frcq u cn cy
selectiv ity in m on k ey visual c o rtc x V is N eurosci 1 3 4 7 7 - 9 2 [5 .6 .4 b ]
I law kcn M J, B lak em ore C , M o r lc y J W ( 1 9 9 7 ) D e v elo p m en t o f co n tra st
sensitivity and tcm p o ra l-frcq u en cy selectiv ity in prim ate lateral
g en icu la te nucleus E x p B ra in R es 1 1 4 8 6 - 9 8 [6 .3 .5 c ]
H ay J C , Pick H L , R osser E ( 1 9 6 3 ) A d ap tation to ch ro m atic aberration
by the hum an visual system S cien ce 141 1 6 7 - 9 [9 .6 .5 c )
I laydar T F , W a n g F , Sch w artz M L , R a k ic P ( 2 0 0 0 ) D ifferen tial m odu la­
tio n o f p roliferation in th e n co co rtica l ventricular and subvcntricular
zon es /N e u r o s d 2 0 5 7 6 4 - 7 4 [6 .4 .5 a , 6 .4 .5 b ]
H aydar T F , A n g E , R akic P ( 2 0 0 3 ) M ito tic spindle rotation and m ode o f
ccll division in the d ev elo p in g telen cep h alon P ro c N a t l A ca d S et 1 0 0
2 8 9 0 - 5 [6 .4 .5 b ]
H avdon P G ( 2 0 0 1 ) G lia : listen in g an d ta lk in g N a t R ev N eu ro sci 2 1 8 5 —
9 3 [5.5.1 f ]
H ayes R M ( 1 9 8 9 ) 3 rD m ovies A h isto ry and film ography o t stereoscop ic
cin em a M cF arlan d . L o n d o n [2 .1 1 .4 ]
Наупсч H , W h ite B L . H eld R ( 1 9 6 5 ) V isual acco m m o d atio n in hum an
in fa n ts S d e n c e 1 4 8 5 2 8 - 3 0 [7 .3 .1 ]
H e H Y , H o d o s W , Q u in la n E M ( 2 0 0 6 ) V isual deprivation reactivates
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H e J C , B urns S A , M arcos S ( 2 0 0 0 ) M o n o ch ro m a tic ab erratio n s in chc
acco m m o d ated hum an eye Vis R es 4 0 41 - 8 [ 9 .1 .1 ]
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locus o f visual aw areness N a tu r e 3 8 3 3 3 4 - 7 [4 .8 .3 b ]
H e S , C o h e n E R , H u X ( 1 9 9 8 ) C lo se co rrelatio n b etw een activ ity in
brain area M T / V 5 and the perception o t a visual m o tio n aftereffect
C u r r B io l S 1 2 1 5 - 1 8 [5 .8 .4 b ]
H earn D , B aker M P ( 1 9 8 6 ) C o m p u te r g ra p h ics P ren tice-H all, Englew ood
C liffs N J [3 .7 .4 ]
H eath G G (1 9 5 6 a ) C o m p o n e n ts o f acco m m o d atio n A m / O p tom 3 3
5 6 9 - 7 9 [9 .2 .1 )
H eath G G (1 9 5 6 b ) The influ en ce o f visual acu ity on accom m odative
responses o t the cv c A m / O p tom A rch A m A c a d O p tom 3 3 5 1 3 - 2 4
[9 .3 .1 )
H eath G G ( 1 9 5 6 c ) A ccom m od ativ e responses o t to tally co lo r blind
observers A m J O p tom A rch A c a d O ptom 3 3 4 5 7 - 6 5 [9 .6 .1 ]
H eath G , H o fs te ttc r H W ( 1 9 5 2 ) T h e effect o f o rth o p tics o n the zon e o f
b in o cu lar vision in in te rm itte n t exotrop ia a ease study A m J O ptom
A rch A m A c a d O p tom 2 9 1 2 - 3 1 ( 1 0 .4.3c]
H cb b D O ( 1 9 4 9 ) I h e o r g a n iz a tio n o f b e h a v io r W ile y , N ew York [4 .3 .4 f,
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H eb bard F W ( 1 9 6 2 ) C o m p ariso n o f su bjective and o b jectiv e m easure­
m en ts o t fixation d isparity / O pt Soc A m 5 2 7 0 6 12 [ 1 0 .2 .4 d ]
H eb bard FW" ( 1 9 6 4 } E ffect o f blur on fixation disparity A m J O ptom
A rch A m A c a d O p tom 41 5 4 0 - 4 8 [ I 0 .2 .4 g ]
H e c h t H , van D o o m A , K o cn d crin k J J ( 1 9 9 9 ) C o m p ressio n o t visual
space in natural scenes and th eir p h o to g rap h ic co u n terp arts P ercept
P sychophys 6 1 1 2 9 9 - 8 6 ( 4 .7 .2 ]
H c ch t S , M int/ E U ( 1 9 3 9 ) T h e v isib ility o f single lines at various illu m i­
n ation s an d the retin al basis o f visual resolu tion / G en P h y sio l 2 2
5 9 3 - 6 1 2 [3 .1 .2 ]
H c c h t S , S ch la er S , P iren n e M H ( 1 9 4 2 ) Energy, q u an ta, and vision
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H ccg cr D J ( 1 9 9 2 a ) N orm alization o f ccll responses in ca t striate co rtex
Vis N eu ro sci 9 181 - 9 7 [4 .2 .8 c , 5 .6 .4 c )
H ccg cr D J (1 9 9 2 b ) H alf-sq u arin g in responses o f c a t striate cells Vis
N eu ro sci 9 4 2 7 - 4 3 ( 5 .5 3 )
H ccgcr D J ( 1 9 9 9 ) L in k in g visual p ercep tion w ith hum an brain activity
C u n O ptn N e u r o b io l 9 4 7 4 - 9 [ 5 .4 .3 f ]
H cclcy D\V, B u ch an a n -Sm ith H M ( 1 9 9 6 ) M ech an ism s specialized tor
the p ercep tion o f im age geom etry 1Ъ R es 3 6 3 6 0 7 - 2 7 [5 -5 .6 c]
H cgd c A N , D iA n to n io A ( 2 0 0 2 ) U b iq u itin and the synapse N a t R ev
N eu roses 3 8 5 4 - 6 1 (6 .4 .3 c , 6.5.1 a]
H cgd c J , Van Essen D C ( 2 0 0 0 ) Selectiv ity for com p lex shapes in prim ate
visual area V 2 J N eu ro sd 2 0 R C 6 1 [ 5 .8 .2 a ]
H cgd c J , Van Essen D C ( 2 0 0 3 ) Strategics o f shape rep resentation in
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H cggclu nd P, A lbus К ( 1 9 7 8 ) O rie n ta tio n selectiv ity o t single cells in
striate co rtex o f cat: the shape o f o rien ta tio n cuning curves V is R es 1S
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H cid er B , M csk cn aitc V, Peterh an s E ( 2 0 0 0 ) A n ato m y and physiology o f
a n eu ral m ech an ism d efin in g depth o rd er and c o n tra st p olarity at
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H eld R ( 1 9 8 1 ) A cu ity in in fan ts w ith norm al and an om alou s visual exp e­
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a n d v isu a l d y sfu n ction Vol 9 B in o c u la r v isio n (cd D R eg an) pp 1 7 0 - 8
M a cM illa n , L o n d o n [7 .6 .4 )
H eld R ( 1 9 9 3 ) T w o stages in the developm en t o f b in o cu lar vision
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1 7 .6 .2 ] ^ ' u n certain ty H s R es 3 7 3 1 4 5 - 6 1 [8 .4 .3 c ]
H eron G . C h a rm a n W N . G ray L S ( 1 9 9 9 ) A cco m m o d atio n responses
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H eron G , C h arm an W N , S c h o r С ( 2 0 0 1 ) D yn am ics o f chc acco m m o d a­
tio n response to ab ru p t ch a n g cs in target vcrgcncc as a fu n ctio n o f
age Г и R es 4 1 5 0 7 - 1 9 [7 .3 .1 ]
H errera 11, B row n L . A ruga J , e t al. ( 2 0 0 3 ) Z ic 2 p attern s b in o cu lar vision
by specifyin g the uncrossed retin al p ro je c tio n C e ll 1 1 4 > 4 5 - 7
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H errera E , M arcus R . L i S , W illia m s S E . c t al. ( 2 0 0 ч ) Foxd I is required
lo r proper form atio n o f the o p tic ch iasm D ev elo p m en t 131 5 7 2 7 - 3 9
[6 .3 .4 b ]
H ersh berger W ( 1 9 7 0 ) A ttach ed -sh ad ow orien tatio n perceived as
depth by c h ick en s reared in an en v iron m en t illu m inated from below
J C om p P h y sio l P sy ch o l 7 3 4 0 7 - 1 1 (7 .4 .2 d 1
H ersh k o A , C ic c h a n o v c r A , H eller H . H aas A L , R ose 1A ( 1 9 8 0 )
Proposed role o f A F P in p rotein breakd ow n: co n ju g atio n o f p rotein s
w ith m ultiple ch ain s o l th e polypep tid e o f A T P -d c p c n d c n t p ro teo ly ­
sis P ro c N a t l A c a d S c i 7 1 7 8 3 - 6 [6 .4 .3 c ]
H ere A , S u L c r B , K une R , van H cm m cn J L ( 1 9 8 9 ) H eb bian learning
recon sid ered : rep resen tation o f static and d yn am ic o b je cts in associa­
tive n ets B io l C y b er 6 0 4 5 7 - 6 7 [ 4 . 3 . 4 f )
H erzo g M H , Fahle ( 1 9 9 7 ) T h e role o f feed b ack in learn in g a vernier
d iscrim in ation ta sk Vis R es 3 7 2 1 3 3 - 4 1 [4 .9 .2 b ]
H cslcr J , P ickw cll D , G ilc h rist J ( 1 9 8 9 ) The accom m od ativ e c o n trib u ­
tio n to b in o cu la r vergence eve m ovem ents O p h th a l P h y sio l O p t 9
3 7 9 - 8 4 1 1 0 .2 .5 b ]
H ess D T , Edwards M A ( 1 9 8 7 ) A n a to m ica l d em o n stratio n o f o cu la r veg-
regation in the retin o g en icu lo co rtica l pathw ay o l the N ew W orld
cap u ch in m on k cv {C eb u s a p e /la ) / C o m p N e u ro l 2 9 4 4 0 9 - 2 0
[ 5 .7 .2 f )
Hcsv R F ( 1 9 8 0 ) A p relim inary investigation o f neural fu n ctio n and dys­
fu n ctio n in am blyop ia. I. Size-selective ch an n els V is R et 2 0 7 4 9 - 5 4
(8 .4 .3 )
H ess R F, A nd erson S J ( 1 9 9 3 ) M o tio n sensitivity and spatial undcrsam -
p lin g in am bly op ia Vis R es 3 3 8 8 1 - 9 6 [8 .4 .4 c )
H ew R F, Baker C L ( 1 9 8 4 ) A ssessm ent o f retinal fu n ctio n in severely
am blyop ic individuals V is R es 2 7 1 3 6 7 - 7 6 [8 .4 .1 ]
H ess R F , Bradley A ( 1 9 8 0 ) C o n tra st p ercep tio n above threshold is only
m inim ally im paired in hum an am blyopia N a tu re 2 8 7 4 6 3 - 4 [8.4.2a)
H ess R F . D c m a n in s R ( 1 9 9 8 ) C o n to u r in teg ratio n in an iso m etrop ic
am bly op ia Vis R es 3 8 8 8 9 - 9 4 [8 .4 .3 c ]
H ess R F, Field D J ( 1 9 9 4 ) Is th e spatial deficic in strab ism ic am blyopia
d u e to loss o f cells o r an u ncalib ratcd disarray o f cells V is R es 3 4
3 3 9 7 - 4 0 6 [8 .4 .3 ]
H ess R F, Field D J ( 1 9 9 5 ) C o n to u r in tegratio n across depth V is R es 3 5
1 6 9 9 - 7 1 1 [4 .5 .2 b ]
H ess R F . H ollid ay I ( 1 9 9 2 ) T h e spatial localizatio n d eficit in am blyopia
V is R es 3 2 1 3 1 9 - 3 9 [8 .4 .3 ]
I less R F, J low cll E R ( 1 9 7 7 ) The threshold co n tra st sensitivity fu n ctio n
in strab ism ic am blyopia: ev id en ce to r a tw o type classification
V is R es 1 7 1 0 4 9 - 5 5 [8 .4 .2 a ]
H ess R F, P o in ter J S ( 1 9 8 5 ) D ifferen ces in the neural basis o f hum an
am blyop ia: th e d istrib u tion o f the an om aly across chc visual field
V is R es 2 5 1 5 7 7 - 9 4 [8 .4 .5 c , S .4 .6 a ]
H ess R F, C a m p b ell F W , G rce n h a lg h T ( 1 9 7 8 ) O n che nature o f the
n eu ral ab n o rm a lity in hum an am blyop ia; neural ab erration s and
neural sensitivity loss P fiu g ers A rc h g es P h y sio l 3 7 7 2 0 1 - 7 [8 .4 .3 ,
8 .4 .3 c ]
H ess R F, C a m p b ell F W , Z im m c rn R ( 1 9 8 0 ) D ifferen ces in th e neural
basis o t hum an am bly op ia: th e effect o t m ean lu m in an ce Vis R es 2 0
2 9 5 - 3 0 5 [8 .4 .2 a ]
H ess R F, France T D , T u lu n ay -K ccscy U ( 1 9 8 1 ) Residual vision in
hum ans w ho have been m on ocu larly deprived o t p attern stim u lation
in early life E x p B r a n t R es 4 4 2 9 5 - 3 1 1 [S .5.1 ]
H ess R F, H ayes A , K ingd om FA A ( 1 9 9 7 a ) In tegratin g co n to u rs w ithin
and throu gh depth Vis R es 3 7 6 9 1 - 6 (4 .5 .2 b ]
H ess R F , M cllh ag g a W . Field D J ( 1 9 9 7 b ) C o n to u r in tegratio n in strabis­
m ic am blyop ia: the sufficiency o f an exp lan ation based on p osition al
H ess R F, D c m a n in s R , B ex P J ( 1 9 9 7 c ) A reduced m o tio n aftereffect in
strab ism ic am blyopia V is R es 3 7 1 3 0 3 - 11 [8 .4 .4 c ]
H ess R F, W an g Y Z , D cm an in s R , ct al. ( 1 9 9 9 ) A d eficit in strabism ic
am blyopia for glo bal shape d etectio n Vis R es 3 9 9 0 1 - 1 4 [8 .4 .2 a .
8 .4 .3 c ]
H ess R F. D ak in S c .T c w fik M . Brow n В ( 2 0 0 1 ) C o n to u r in teractio n in
am blyop ia: scale selectio n 4 s R es 41 2 2 8 5 - 9 6 [8 .4 .3 b ]
H ess. R F. P o in ter |S, Sim m ers A , B ex P ( 2 0 0 3 ) B o rd er d istin ctn ess in
am blyopia Vis R es 4 3 2 2 5 5 - 6 4 [8 .4 .2 a , 9 .6 .5 a ]
H cth erin g to n PA , Sw indale N V ( 1 9 9 9 ) R eceptive field and orien tatio n
scatter studied by tetrod e recordings in cat area 17 Vis N eu ro sci 1 6
6 3 7 - 5 2 ( 5 .7 .1 ]
H eu er H , O w en s D A ( 1 9 8 9 ) V ertical gaze d ire ctio n and th e resting pos­
ture o f the eyes P ercep tio n 1 8 3 6 3 - 7 7 (1 0 .2 .1 ]
H eu er H . D u n k e l-A b e ls G , B riiw cr M , c t al. ( 1 9 8 8 ) Ih e e ffe cts o f sus­
tain ed vertical gaze d eviation o n th e resting state o t the vergence
system V is R es 2 8 1 3 3 7 - 4 4 1 10.2.1 ]
H cu m an n D . R ab in ow icz T ( 1 9 8 2 ) Postn atal developm en t o t th e visual
co rte x o f the m ouse after en u cleatio n at b irth E x p B ra in R es 4 6
9 9 - 1 0 6 18 . 1.4a]
H e u s e rJ ( 2 0 0 3 ) M v little sp o n tan eou s blips S cien ce 3 0 0 1 2 4 8 [2 .6 .1 ]
H c v n c r R F, W on g-R iley M T T ( 1 9 9 3 ) M ito ch ro n d ria l and nuclear gene
expression for cy to ch ro m e oxidase su bu n its arc d isp rop o rtion ately
regulated by fu n ctio n al activ ity in n eu ron es / N eu ro sci 13 1 8 0 5 - 1 9
[8 .2 .4 b ]
H cy n cn A J, Yoon B J, Liu C H , c t al. ( 2 0 0 3 ) M o lecu lar m cch an ism for
loss o f co rtical responsiveness follow in g b r ie f m on ocu lar deprivation
N a t N eu ro sci 6 8 5 4 - 6 2 [8 .2 .7 c ]
H cyw ood C A , C o w ey A , N cc o m b c F ( 1 9 9 1) C h ro m a tic d iscrim in ation
in a co rtica llv co lo u r blind o b serv er E u r J N eu ro sci 3 8 0 2 - 1 2
[5 .8 .3 a ]
H cyw ood C A , G a d o tti A , C o w c y A ( 1 9 9 2 ) C o rtic a l area V 4 and its role
in th e perception o f co lo r J N eu rosci 1 2 4 0 5 6 - 6 5 [5 .8 .3 a ]
H ick ey T L ( 1 9 7 7 ) Postn atal developm en t o f th e hum an lateral gen icu ­
late nucleus: relation sh ip to a critica l period for the visual system
S cien ce 1 9 8 8 3 6 - 8 [6 .3 .5 a ]
H ick ey T L , Sp ear P D , KratZ A E ( 1 9 7 7 ) Q u an titativ e studies o f cell size
in th e c a t s dorsal lateral gen icu late n u cleu s follow ing visual depriva­
tio n / C o m p N e u ro l 1 7 2 2 9 5 - 8 2 [8 .2 .2 b ]
H icta n cn J K , Perrecc D I ( 1 9 9 6 ) M o tio n sensitive cells in th e m acaque
superior tem poral poly sensor у area: response d iscrim in ation betw een
self-generated and extern ally generated pattern m o tio n B e h a v B ra in
R es 7 6 1 5 5 - 6 7 [5 .8 .4 ]
H ig g in b oth am H R , G lccso n G ( 2 0 0 7 ) T h e cen tro so m e in neuronal
d ev elo p m en t T IN S 3 0 2 7 6 - 8 3 [6 .4 .3 b ]
H iggins KF., D au gm an J G , M ansfield R JW ( 1 9 8 2 ) A m b ly o p ic co n tra st
sen sitiv ity: insensitivity to unsteady fixation In v est O p b th a l Vis S ci 2 3
1 1 3 - 2 0 [8 .4 .2 a ]
H igh m an V N ( 1 9 7 7 ) S tereop sis and an iseikon ia in u nipolar aphakia
B r i t J O p b th a l61 3 0 - 3 3 [9 .9 .1 c ]
1 li g o N .O i s h iT , Y a m ash itaA .M atsu d a К . 1 layashi M ( 2 0 0 0 ) Expression
o f G A P -4 3 an d S C G I 0 m R N A s in lateral gen icu late nucleus o f
n orm al and m on ocu larly deprived m acaque m onkeys / N eu rosci 2 0
6 0 3 0 - 8 | 8.2.7f ]
H ill D K , K eynes R D ( 1 9 4 9 ) O p a c ity ch an g cs in stim u lated nerve
J P h y sio l 1 0 8 2 7 9 [5 .4 .3 a ]
I li ll is J M , Ernsc M O , B an k s M S , L an d y M S ( 2 0 0 2 ) C o m b in in g sensory
in fo rm a tio n : m an d ato ry fusion w ith in , but n o t b etw een , senses
S cien ce 2 9 8 1 6 2 7 - 3 0 [4 .5 .7 b ]
H in c T . T h o rn F ( 1 9 8 7 ) C o m p e n sa to ry eye m ovem ents d urin g active
head rotation fo r near targets: ctfccts o t im agin ation rapid head
o scillatio n and v crgcncc Vis R es 2 7 1 6 3 9 - 5 7 [1 0 .9 .1 ]
H in k le D A , C o n n o r C E ( 2 0 0 2 ) T h ree-d im en sio n al orien tatio n tu n in g
m m acaque area V 4 N a t N eu rosci 5 6 6 5 - 7 0 [5 .8 .3 a ]
H in to n G E (1 9 8 7 ) Ih e h orizon tal-vertical delusion P ercep tio n 16
6 6 7 - 8 0 [4 .6 .3 g ]
Jia n g В С ( 1 9 9 6 ) A ccom m od ativ e v crgcncc is driven by the phasic c o m ­
p o n en t o f th e accom m odative* c o n tro lle r f ls R es 3 6 9 7 - 1 0 2
1 1 0 .4 .3 a ]
Jia n g B C ( 1 9 9 7 ) In teg ration o f л sensory co m p o n e n t inro the a cco m ­
m od ation m od el reveals d ifferen ces b etw een cm m ctro p ia and lacc-
onscc m yopia In v est O p h th a l Vis S ci 3 8 1 5 1 1 - 6 [9 .6 .2 a ]
Jia n g B C , W ocssn cr W M ( 1 9 9 6 ) D ark focu s and dark vergence: an
experim ental verification o f t h e con fig u ratio n o f the dual-interactive
feed b ack m od el O p h th a l Physiol O p r 16 3 4 2 - 7 1 1 0.4.3a]
Jia n g B C , G ish K W , L cib ow itz I l\Xr ( 1 9 9 1 ) E ffe c t o f lu m in an ce o n the
relation b etw een a cco m m o d a tio n and convergence O p tom V is S ci
6 S 2 2 0 - 5 [9 .3 .1 ]
Jim e n e z J R . O liv ares J L , P cre z -O co n F, d el B arco L J ( 2 0 0 0 ) A ssociated
phoria in relatio n to stereopsis w ith ran d om -d ot stereogram s
O p tom Vis S e i 7 7 4 7 - 5 0 [ 1 0 .2 .4 g )
J in D Z , D rag oi V, S u r M , S cu n g H S ( 2 0 0 5 ) 'l ilt aftereffect and adapca*
tio n -in d u ced changes in orien tation tu n in g in visual co rtex
J N eu ro p h y sio l 9 4 4 0 3 8 - 4 0 5 0 - [ 5 .6 .2 a J
Jo h an sso n C B , M o m m a S , C la rk e D L , c t al. ( 1 9 9 9 ) Id en tificatio n o f a
neural stem ccll in the a d u lt m am m alian cen tral nervous system
C e ll9 6 2 5 - 3 4 [6 .4 .2 d ]
Jo h an sso n G ( 1 9 7 3 ) V isu a l p ercep tion o f b iolog ical m o tio n and a m odel
lo r its analysis P crccp t P sychophys 1 4 2 0 1 - 1 1 [4 .5 .2 c ]
Jo h an sso n R S , B irzn ieks ( 2 0 0 4 ) First spikes in ensem bles o f hum an
tactile afferen ts c o d c co m p lex spatial even ts N a t N eu ro sci 7 1 7 0 - 7
[4 .3 .3 c ]
Jo h n so n B , B eck L F ( 1 9 4 1 ) The d evelopm ent o f space p ercep tion :
1. Stereo sco p ic vision in p reschool ch ild ren f G en et P sy ch o l 5 8
2 4 7 - 5 4 v [7 .4 . Id ]
Jo h n so n C A ( 1 9 7 6 ) E ffects o f lu m in an ce and stim u lu s d istan ce on
acco m m o d atio n and visual resolu tion ) O pt S o c A m 6 6 138- 4 2
[ 9 .3 .1 ,9 .6 .4 d ]
Jo h n so n C A , Post R B , C halu p a L M , L ee T J ( 1 9 8 2 ) M o n o cu lar depriva­
tio n in hum ans: a study* o f id en tical tw in s In v est O p h th a l Vis S ci 2 3
1 3 5 - 8 [ 8 .2 .3 f ]
Jo h n so n J S , O lsh au scn B A ( 2 0 0 5 ) T h e re co g n itio n o f p artially visible
natural o b je c ts in chc presence and absence o f th e ir occlu d ers V is R es
4 5 3 2 6 2 - 7 6 [4 .5 .2 c ]
Jo h n so n R R , B u rkh alter A ( 1 9 9 7 ) A polysynaptic feed b ack circu it in rat
visual c o rte x J N eu ro sci 1 7 7 1 2 9 - 4 0 [5-5-1 b]
Jo h n s to n J C , Pashler H ( 1 9 9 0 ) C lo se b in d in g o f id e n tity and lo ca tio n in
visual feature p ercep tion / E x p P sy ch ol H P P 1 6 8 4 3 - 5 6 [4 .5 .4a|
Jo n e s D C , van Slu y tcrs R C , M urphy K M ( 1 9 9 1 ) A co m p u tatio n al m od el
for th e overall p attern o f o c u la r d o m in an ce / N eu ro sci 11 3 7 9 4 - 8 0 8
[5 .7 .2 c ]
Jo n e s H F., W an g W , S illito A M ( 2 0 0 2 ) Spatial organ ization and
m agnitud e o f o ricn tacio n co n tra st in teractio n s in p rim ate V I
/ N eu ro p h y sio l 8 8 2 7 9 6 - 8 0 8 [5 .6 .7 a ]
Jo n e s JP , Palm er L A ( 1 9 8 7 ) A n evalu ation o f th e tw o-d im en sion al
G a b o r filter m od el o f sim ple receptive fields in c a t striate co rtcx
J N eu ro p h y sio l 5 8 1 2 3 3 - 5 8 [ 4 .4 .2 ,5 -5 .3 ]
Jo n e s K R , Berkeley M A ( 1 9 8 3 ) Loss o f tem p oral sensitivity in dorsal lat­
eral gen icu late nucleus and area 18 o t th e cat follow in g m on ocu lar
d eprivation / N eu ro p h y sio l4 9 2 5 4 - 6 8 1 8 .2.3c)
Jo n e s K R , K alil RF., Spear P D (1 9 8 4 a ) F.ttccts o f strabism u s on
rcsponsivicy spatial resolu tion and co n tra st sensitivity o f ca t lateral
g en icu la te n eu ron s J N eu ro p h y sio l S I 5 3 8 - 5 2 [8 .2 .2 c*
Jo n e s K R , Spear P D , T o n g L ( 1 9 8 4 b ) C ritic a l periods to r effects o f
m on ocu lar d ep riv ation : d ifferen ces b etw een striate and extrastriate
c o r t e x /N e u r o s c i 4 2 5 4 3 - 5 2 [8 .3 .1 a ]
lo n cs L S ( 1 9 9 6 ) Integrin s: possible fu n ctio n s in the adult C N S T IN S 19
6 8 - 7 2 [6 .4 .3 b ]
Jo n e s R ( 1 9 7 7 ) A n om alies o t d isparity d etectio n in th e hum an visual
system J P h y sio l 2 9 4 6 2 1 - 4 0 [ 1 0 .5 .3 ]
Jo n e s R ( 1 9 8 0 ) Fusional vergence: sustained and tran sien t co m p o n e n ts
A m J O ptom P h y sio l O pt 5 7 6 4 0 - 4 [ 1 0 .5 .1 0 c , 1 0 .5 .9 b ]
Jo n e s R . K err K L ( 1 9 7 1 ) M o to r responses to co n flictin g asym m etrical
vergence stim ulus in form atio n A m J O p tom A m A c a d O p tom 4 8
9 8 9 - 1 0 0 0 [1 0 .5 .1 0 c ]
Jo n e s R , K err KF, ( 1 9 7 2 ) V crgcn cc eye m ov em en ts to pairs o f disparicy
stim u li w ith shape selection cues V is R es 1 2 1 4 2 5 - 3 0 f 1 0 .5 .1 0 c]
Jo n e s R , S tep h en s G L ( 1 9 8 9 ) H o rizo n tal fusion al am plitudes In v est
O p h th a l Vis S a 3 0 1 6 3 8 - 4 2 [ 1 0 .5 .3 ,1 0 .5 .4 b ]
Jo n e s T A , G rccn o u g h W T ( 2 0 0 2 ) B ehaviou ral exp erien ce-d ep end ent
p lasticity o f g lial-n eu ron al in teractio n s In T h e tr ip a r tite sy n a p se (cd A
V o ltcrra, P J M ag istrctti, P G I lavdon ) pp 2 4 S - 6 5 O xfo rd U niversicy
Press, O x fo rd [5 -5 . I f ]
Jo sep h J S , C h u n M M . N akavam a К ( 1 9 9 7 ) A ttcn tio n a l req u irem en ts in
a ‘preattcn tivc* feature scarch task N a tu re 3 8 7 S 0 5 - 7 [ 4 .8 .la ]
Jo u e n F, L cp ccq J C , G a p cn n c O , B erten ch al В I ( 2 0 0 0 ) O p tic flow
sensicivicy in n eo n ates In fa n t В c h a r D eu el 2 3 2 7 1 - 8 4 [ 7 .2 .3 b |
Jo u rd ain P, Fukunaga K , M u ller D (2 0 0 Я ) C alciu m / calm od u lin-
depend ent p ro tein kinase II co n trib u tes to activ ity-d ep en d en t filopo*
dia grow th an d spine fo rm atio n / N eu ro sci 2 3 1 0 6 4 5 - 4 9 [6 .4 .3 f,
6 .5 .1 a ]
Jo v n so n R B ( 1 9 7 1 ) M ic h o tc c s exp erim en tal m cchods B r it / P sy ch ol 6 2
' 2 9 3 - 3 0 2 [4 .6 .3 g ]
Judd C H ( 1 9 0 7 ) Phocographic records o f convergence and divergence
P sy ch o l R et/ P sy ch o lM o n o g r 8 3 7 0 - 4 2 3 [ 10.2.4)
fudge A W ( 1 9 5 0 ) S tereo sco p ic p h o to g ra p h y C h ap m an H all, L on d on
[2 .1 1 .3 )
Ju d g e SJ ( 1 9 8 5 ) C a n cu rren t m od els o t acco m m o d atio n and vcrgcncc
co n tro l acco u n t for chc discrepancies betw een A C / A m easurem ents
m ade by the fixation disparity and p h oria m eth od s Vis R es 2 5
1 9 9 9 - 2 0 0 1 [ 1 0 .4 .1 ]
Ju d g e S J ( 1 9 8 7 ) O p tica lly -in d u c e d changes in co n ic v crgcncc and A C / A
ratio in n orm al m on keys and m onkeys w ith lesions o f the flocculus
and ventral paraflocculti* E x p B ra in R es 6 6 1 - 9 [ 1 0 .4 .1 )
Ju d g e S J ( 1 9 8 8 ) D o target an gular size-change and b lu r cues in teract lin-
carlv in the co n tro l o f hum an acco m m o d a tio n ? Vis R es 2 8 2 6 3 8
[9 .5 ]
Ju d g e SJ ( 1 9 9 1 ) Vergence In V ision a n d v isu a l d y sfu n ction Vol 8 E y e
m o v em en ts (cd R H S C a rp e n te r) pp 1 5 7 - 7 2 M a c M illa n , L o n d o n
[1 0 .1 .3 b ]
Ju d g e S J ( 2 0 0 6 ) R eflectio n m akes sense o f ro tatio n o f t h e eyes Vis R es 4 6
3 8 6 2 - 6 [1 0 .1 .2 )
Ju d g e S J, G u m m in g B G ( 1 9 8 6 ) N eu ro n s in m on k ey m id b rain with
activ ity related to vcrgcncc eye m ovem en t and acco m m o d atio n
J N eu ro p h y sio l 5 5 9 1 5 - 3 0 [ 9 . 2 . 3 , 1 0 .1 0 .2 c , 1 0 .1 0 .2 c )
Ju d g e S J , M iles FA ( 1 9 8 5 ) C h an g es in the co u p lin g b etw een a cco m m o ­
d ation and vcrgcncc eye m ovem ents induced in hum an su b jects by
a lterin g the effectiv e in tcrocu lar d istan ce P ercep tio n 14 6 1 7 - 2 9
(1 0 .4 .1 )
Julesy. В ( 1 9 7 1 ) F o u n d a tio n s o f cy clop ean p erc ep tio n U n iv ersity o f C h ica g o
Press, C h ica g o [ 1 . 3 , 4 .5 .8 b ]
Jules/ B , Bergen J R ( 1 9 8 3 ) T e x to n s th e fu n d am en tal elem en ts on
p reattcn tiv c vision and p ercep tion o f texture B e ll S ystem T ech n ica l
J o u r n a l6 2 1 6 1 9 - 4 5 [4 .8 .1 a ]
Ju n g R ( 1 9 6 1 ) N eural in tegratio n in chc visual co rccx and ics significance
for visual in fo rm atio n In S en sory in teg ra tio n (cd W R oscn b lich )
pp 6 2 7 - 7 4 M I T Press, N ew Y ork [ 3 .1 .la ]
Kaas J H , G u illery R W , A llm an J M ( 1 9 7 2 ) S o m e p rincip les o f organiza­
tion in the dorsal lateral gen icu late nucleus B r a in B e h a v E v o l 6
2 5 3 - 9 9 ( 5 .2 .1 )
Kaas J H , H arcing J K , G u illery RW' ( 1 9 7 4 ) R ep resen tation o f chc c o m ­
pete retin a in che concralaceral superior co llicu lu s o f som e anim als
B r a in R es 6 5 3 4 3 - 6 [5 .3 .1 ]
K a a s JH , L in C S .C a sa g ra n d e VA ( 1 9 7 6 ) The relay o f ipsilatcral an d con-
tralatcral retinal inputs from the lateral gen icu late nucleus to striate
co rte x in che owl m o n k ey : a tran sn eu ron al cransporc study B r a in R es
1 0 6 3 7 1 - 8 [ 5 .7 .2 f J
K aas J H , K ru b itz cr L A , C h in o Y M ,c t al. ( 1 9 9 0 ) R eo rgan ization o t reti-
n ocop ic corcicai maps in adulc m am m als after lesions o f che retina
S cien ce 2 4 8 2 2 9 - 3 1 [5 .5 .6 c ]
K aczm arck L , C hau d h u ri A ( 1 9 9 7 ) S e n so ry regu lation o f im m ediate-
early gen e expression in m am m alian visual c o rtc x : im p licatio n s tor
tun ccion al m apping and n eu ral p lasticity B r a in R es R ev 2 3 2 3 7 - 5 6
[6.6. 1 c]
K aczm arck L , K ossut M t S k an g icl-K raim k a J ( 1 9 9 7 ) G lu tam ate
recep to rs in c o rtic a l p lasticity : m o lecu lar and cellu lar b iology
P h y sio! R ev 7 7 2 1 7 - 5 5 [ 5 .5 .2 c ,6 .6 .3 ]
K agan 1, G u r M , Sn o d d crly M ( 2 0 0 2 ) Spacial org an ization o f rcccpcivc
fields o f V 1 n eu ron s o f alcrc m onkeys: com p arison w ith responses со
gracing»/ N eu ro p h y sio l 8 8 2 5 5 7 - 7 4 [5 .5 .3 ]
K ah n D M . K ru b n itz cr L ( 2 0 0 2 ) M assive cro ss-m o d ality c o rtic a l plastic-
icy an d chc em ergence o f a new c o rtic a l area in dev elop m en tal ly blind
m am m als P r o c N a d A c a d S ci 9 9 1 1 4 2 9 - 3 4 [8 .1 .4 b ]
K ah n J I , Foster DM (1 9 8 1 ) V isual com p arison o f rotated and
reflected ran d om -d ot p attern s as a fu n ccion o f th e ir p osition al
sym m etry and separation in chc field JQ u art / H xp P sy ch ol 33A
1 5 5 - 6 6 [4 .6 .3 c ]
K alarick al G J , M arsh all J A ( 1 9 9 9 ) M o d els o f rcccp tiv c-ficld dynam ics in
visual c o rtc x V is N eu ro sci 1 6 1 0 5 5 - 8 1 [5 .5 .6 c ]
K alil R L ( 1 9 8 0 ) A qu an titativ e study o f che effects o f m o n o cu la r c n u clc'
a tio n an d deprivation on cell grow th in chc dorsal laceral gen icu late
nucleus o f the c a t J C o m p N e u r o l 1 8 9 4 8 3 - 5 2 7 18.2.2a]
K alil R E ( 1 9 9 0 ) 'Ih e in flu en ce o f a ctio n p occn tials on chc developm enc
o f the ce n tra l visual pathw ay in m am m als / E x p B io l 1 5 3 2 9 1 - 7 6
[6 .3 .5 b ]
K alil R E , S p ea r P D , L an gsetm o A ( 1 9 8 4 ) R esponse p rop erties o f striate
co rccx neu ron s in cats raised w ith d ivergent o r convergent strabism us
J N eu ro p h y sio l 5 2 5 1 4 - 3 7 [ 8 .4 .2 a )
K am i дока B> K aczm arck L , C h au d h u ri A ( 1 9 9 6 ) V isual stim u lation
regulates the expression o f tran scrip tion factors and m odulates
th e co m p o sitio n o f A IM in visual co rtex ./ N eu ro sci 1 6 3 9 6 8 - 7 8
[6 .6 .1 c ]
K a m im k a B , K aczm arck i L , C h au d h u ri A ( 1 9 9 7 ) A ctiv ity-d ep en d en t
regu lation o f cy to ch ro m c b gene expression in m on key visual c o rtc x
J C om p N e u r o l 3 7 9 2 7 1 - 8 2 [8 .2 .4 b ]
K a n d lcr K , K atz L C ( 1 9 9 8 ) C o o rd in a tio n o t n eu ron al activ ity in
developin g visual c o rte x by gap ju n ctio n -m cd ia tcd b io ch em ical
co m m u n ica tio n ./ N eu ro sci 18 1 4 1 9 - 2 7 [6 .6 .2 J
K ang H ,S c h u m a n ( 1 9 9 5 ) L o n g -la stin g n cu ro tro p h in -in d u ced e n h an ce­
m e n t o f synaptic tran sm ission in the adult h ipp ocam pus S cien ce 2 6 7
1 6 5 8 - 6 2 [6 .5 .1 c ]
K a n g H , Sch u m an ( 1 9 9 6 ) A req u irem en t for lo cal p ro tein synthesis in
n cu ro tro p h in -in d u ced h ipp ocam pal synaptic p lasticity S cien ce 2 7 3
1 4 0 2 - 6 [ 6 .4 .4 f ]
K a n g K , Shelly M , So m p olin sk y H ( 2 0 0 3 ) M exican h ats and pinw heel*
in visual co rtex P ro c N .i d A ca d S ci 1 0 0 2 8 4 8 - 5 3 15.7.1]
K ano ld P O , Shatz C J ( 2 0 0 6 } Subplace neu ron s regu late m atu ratio n o f
co rtic a l in h ib itio n and o u tco m e o f o cu la r d o m in an ce plasticity
N eu ro n 5 1 6 2 7 - 3 8 [6 .4 .4 d . 8 .2 .7 d )
K a n o ld P O , K ara P, Reid R C , Sharz C J ( 2 0 0 3 ) R o le o fs u b p la tc neurons
in fu n ctio n a l m atu ratio n o f visual co rcical colu m n s S cien ce 301
5 2 1 - 5 [6 .4 .5 c ]
K apadia M K , G ilb e rt C D , \Vcvihcimcr G ( 1 9 9 4 ) A qu an titativ e m ea­
sure fo r s h o r t-te r m corcical p la sticity in hum an vision J N eu ro sci 14
4 5 1 - 7 [5 .5 .6 c ]
K apad ia M K , Ico M ,G ilb e r t C D , W esth eim er G ( 1 9 9 5 ) Im provem en t in
visual sensitivity by changes in local c o n te x t: parallel studies in hum an
observers and in V I o f a lert m on keys N eu ro n 15 8 4 3 - 5 6 15.6.7b ,
5 .9 .3 a ]
K apadia M K , W esth eim er G , G ilb e r t C D ( 2 0 0 0 ) Spacial d istrib u tion
o f co n te x tu a l in teractio n s in prim ary visual c o rtc x and in visual
perception / N eu ro p h y sio l8 4 2 0 4 8 - 6 2 [5 .6 .7 b ]
K aplan D . G lass L ( 1 9 9 5 ) U n d ersta n d in g n o n lin e a r d y n a m ics Springer,
N ew Y ork [3 .5 ]
K aplan I:, Shapley R M ( 1 9 8 6 ) T h e prim ate retin a co n ta in s tw o types o f
ganglion cclls w ith high and low co n tra st sensitivity P r o c N a tl A cad
S c i 8 3 2 7 5 5 - 7 [5 .2 .1 ]
K aplan E , Purpura K . Shapley R M ( 1 9 8 7 ) C o n tra s t affects che transm is-
sion o f visual in form acion th ro u g h che m am m alian laceral gen icu late
nucleusJ P h y s io l3 9 1 2 6 7 - 8 8 [5 .2 .2 b ]
K apou la Z , M ain T C , Z e e D S , R o b in so n DA ( 1 9 8 7 ) A daptive
ch ang es in p o st-sa c ca d ic drift induced by p atch in g o n e eve V is R es
2 7 1 2 9 9 - 3 0 7 [1 0 .8 .2 b ]
K apou la Z , O p tica n L M , R o b in so n D A ( 1 9 9 0 ) R etin al im age m o tio n
a lo n e d o es n oc concrol disconjugacc postsaccadic eye drift
J N eu ro p h y sio l G 3 1 0 0 0 - 9 [1 0 .8 .3 b ]
K ap ou la Z . Eggcrc T , B u cci M P ( 1 9 9 5 ) Im m ed iate saccadc am plitude
d iscon ju gacv indu ced b y u nequ al im ages Vis R es 3 5 3 5 0 5 - 1 8
[1 0 .8 .2 b ]
K ap ou la Z . Eggcrc T , B u cci M P ( 1 9 9 6 a ) D iscon ju g acc adapcacion o f chc
vertical o c u lo m o to r sysccm Vis R es 3 6 2 7 3 5 - 4 5 [1 0 .8 .3 b ]
K ap ou la Z . Bucci M P, Eggcrc T , Z am firescu F ( 1 9 9 6 b ) East disconjugacc
ad ap tation s o f saccades in m icro strabism ic su bjects Vis R es 3 6 1 0 3 - 8
1 1 0 .8 .3 b ]
K ap ou la Z , B u cci M P . E g g crt T , G arraud L ( 1 9 9 7 ) Im p airm en t o f the
b in o cu lar co o rd in atio n o f saccades in strabism us Vis R es 3 7 2 7 5 7 - 6 6
1 1 0 .8 .2 b ]
K apou la Z. B u cci M P. Lavignc-Tom ps F. Z am firescu F (1 9 9 8 )
D isco n ju g atc m cm o rv 'g u id cd saccades to disparate targets: evidence
for 3 D sensitivity E x p B r a in R es 1 2 2 4 1 3 - 2 3 [ 1 0 .8 .3 b )
K apou la Z , B crn o tas M , H aslw anter T ( 1 9 9 9 } L is tin g s plane rotation
w ith con v ergen ce: role o f disparity, a cco m m o d atio n , and depch
p ercep tion E x p B r a in R es 1 2 9 1 7 5 - 8 6 [1 0 .1 .2 d ]
K apou la Z , B u cci M P, B c rn o ta s M , Zam firescu F ( 2 0 0 0 ) M o co r execu­
tio n is necessary to m em orize disparity E x p B r a in R es 131 5 0 0 - 1 0
110.8.3b ]
K ap ral R , Sh o w alter К ( 1 9 9 5 ) C h e m ic a l u /aves a n d p a ttern s Kluw er
N o rw cll M A [5 .7 .1 ]
K ara P, R ein age I P, Reid R C ( 2 0 0 0 ) L ow response variability in sim u lta­
neou sly recorded retinal» th alam ic, and c o rtic a l neu ron s N eu ro n 2 7
6 3 5 - 4 6 [4 .3 .1 b ]
K arm arkcr U R , N ajarian M T , B u o n o m a n o D V ( 2 0 0 2 ) M ech an ism s
and significance o f spike-tim ing d ep en d en t p lasticity B io l C y fiern
8 7 3 7 3 - 8 2 [6 .5 .1 a , 6 .5 .2 ]
K a m a th H O ( 2 0 0 1 ) N ew insigh ts in to chc fu n c tio n s o f the superior
tem p o ral co rtex N a t R ev N eu ro sci 2 5 6 9 - 7 6 [5 .8 .4 d ]
K arn ath H O , Fcrb cr S , H im m clb ach M ( 2 0 0 1 ) Spatial awareness is a
fu n ctio n o f the tem p o ral n o t the p o ste rio r parietal lobe N a tu r e 4 1 1
9 5 0 - 3 [5 .8 .4 d ]
K asam atsu T ( 1 9 9 1 ) A d ren ergic regu latio n o f v isu ocortical p lasticity : a
role o f chc locus co cru lcu s svstcm P ro g B ra in R es 8 8 5 9 9 - 6 1 6
(8 .2 .7 h ]
K asam atsu T , Pettigrew J D ( 1 9 7 9 ) Preservation o f b in o cu larity after
m o n o cu lar deprivation in th e striate c o rtc x o f k itten s treated with
6 -h y d ro x y d o p a m in c J C o m p N eu r o l 1 8 5 1 3 9 - 6 1 [8 .2 .7 h ]
K asam atsu T , Pettigrew J D , Л гу M ( 1 9 7 9 ) R esto ratio n o f visual cortical
p lasticity by lo cal m icro p crfu sion o f n orep in ep h rin e / C o m p N eu ro l
1 8 5 1 6 3 - 8 2 [8 .2 .7 h ]
K asam atsu T , Pettigrew J D , Л гу M ( 1 9 8 1 } C o rtic a l recov ery from effects
o f m o n o cu lar d ep riv ation : acceleratio n wich n orep in ep h rin e and
suppression wich 6-h yd roxyd op am in c / N eu ro p h y sio l 4 5 2 5 4 - 6 6
[S .2 .7 h ]
K asam atsu T , W atabc K , H cggclu nd P, S c h o llc r E ( 1 9 8 5 ) P lasticity in c a t
visual c o rtcx restored by electrical stim u latio n o f th e locus cocru lcu s
N eu rosci R es 2 3 6 5 - 8 6 [8 .2 .7 h ]
K asam atsu T , K ita n o M , Su tter E E , N o rc ia A M (1 9 9 8 a ) Lack o f lateral
in h ib ito ry in teractio n s in visual c o rtc x o f m on ocu larly deprived cats
V is R es 3 8 1 - 1 2 [8 .2 .3 c ]
K asam atsu T , Im am ura K , M ataga N , c t al. ( 1 9 9 8 b ) R o le s o f N -m eth yl-
D -asp artate reccp tors in ocu lar d o m in an ce p lasticity in developing
visual c o rte x : re-evaluation N eu ro scien ce 8 2 6 8 7 - 7 0 0 18.2.7c]
K asam atsu T , Polac U . Pectec M W , N o rc ia A M ( 2 0 0 1 ) C o llin ea r facilita­
tio n p ro m o tes reliability o f single-cell responses in ca t striate co rtex
E x p B ra in R es 1 3 8 2 , 1 6 3 - 7 2 [5 .6 .7 b ]
K asch u b c M , W o lf F, G icscl T , Low el S ( 2 0 0 2 ) G e n e tic influ en ce on
q u an titativ e features o f n eocorcical a rch itectu re J N eu ro sci 2 2
7 2 0 6 - 1 7 1 5 .7 .1 ]
K asthurirangan S , V ilu p u ru A S, G lasser A (2 0 0 3 ) A m plitude
depend ent accom m od ativ e dynam ics in hum ans Vis R es 4 3 2 9 4 5 - 5 6
|9.7.2c)
K astn er S , U n gerlcid cr L G ( 2 0 0 0 ) M ech an ism s o t visual acccntion in the
hum an c o rtc x A n n R ev N eu ro sci 2 3 3 1 5 - 4 1 14.8.3d ]
M o o re T , Fallah M ( 2 0 0 4 ) M icro stim u la tio n o f the froncal eye field and
ics c ffc c ts on co v ert spatial a tte n tio n / N cu ro p h y sio l 91 1 5 2 - 6 2
[5 .9 .2 a ]
M o o res ££. F ris b y JP , B uckley D L , F aw cett A ( 1 9 9 8 ) V crgcn cc co n tro l
across saccades in dyslexic adulcs O p h th a l P h y sio l O pt 1 8 4 5 2 - 6 2
[1 0 .2 .2 c ]
M o o scr F, B osk in g W l I, Fitzp atrick D ( 2 0 0 4 ) A m orp h ological basis for
oriencacion tu n in g in prim ary visual co rcex N a t N eu ro sci 7 8 7 2 - 9
[5 .6 .2 b ]
M o rad i F, S h im o jo S ( 2 0 0 4 ) Perceptual b in d in g and p ersisten t surface
segregation Vis R es 4 4 2 8 8 5 - 9 9 [4 .5 .4 a ]
M orales B , C h o i SY, K irkw ood A ( 2 0 0 2 ) D ark rearing alters th e d evelop­
m en t o f G A B A c rg ic transm ission in visual c o rtcx J N eu ro sci 2 2
8 0 8 4 - 9 0 [6 .4 .4 d , 8 .1 .1 b. 8 .1 .4 a , 8.3 .1 b]
M o ran J , D esim on e R ( 1 9 8 5 ) Selectiv e a tte n tio n gates visual processing
in th e ex trastriate c o r tc x S d c n c e 2 2 9 7 8 2 - 4 [5 .9 .1 , 5 .9 .3c)
M ord i J A , C iu ffred a K J ( 1 9 9 8 ) Sta tic asp ccts o f acco m m o d a tio n : age
and presbyopia Vis R es 3 8 1 6 4 3 - 5 3 I9 .2 .2 b ]
M ord i J A , C iu ffred a K J (2 0 0 4 a ) D y n am ic asp ects o f acco m m o d atio n :
age and presbyopia V is R es 4 4 591 •-6 0 1 [7.3.1 ]
M ord i J A , C iu ffred a K J ( 2 0 0 4 b ) D y n a m ic aspects o f acco m m o d atio n :
age and presbyopia. Reply to a le tte r to the e d ito r Vis R es 4 4 2 3 1 5 - 6
19.2.2b ]
M organ H , Sy m m cs D ( 1 9 8 2 ) A m a z in g 3 *D L ittle Brow n C o , B oston
[2 .1 1 .3 ]
M organ M J , H o to p f W H N ( 1 9 8 9 ) Perceived d iagonals in grids and
la t t ic e s / '* / t o 2 9 1 0 0 5 - 1 5 [4 .5 .2 b )
M organ M J, R egan D ( 1 9 8 7 ) O p p o n e n t m odels for lin e in terv al d is­
crim in a tio n : in terval and vernier p erform ance com pared 1Ъ R et 2 7
1 0 7 - 1 8 [ 4 .5 .2 c , 4 .5 .2 d )
M organ M W ( 1 9 4 4 ) A cco m m o d a tio n and its relation sh ip to con v er­
gence A m J O p tom A rch A m A c a d O p tom 21 1 8 3 - 9 5 [ 10.4.1 ]
M o rg an M W ( 1 9 4 6 ) A new th e o ry for the co n tro l o f accom m od ation
A m J O p tom 2 3 9 9 - 1 1 0 (9 .2 .3 ]
M organ M W ( 1 9 6 8 ) A cco m m o d a tio n and v crgcncc A m J O p tom A rch
A m A c id O p tom 4 5 4 1 7 - 5 3 (1 0 .4 .3 b , 9 .5 ]
M organ M W , O lm sted J M D .W a t r o u s W ( 1 9 4 0 ) Sy m p ath etic actio n in
a cco m m o d a tio n for far vision A m J P h y sio l 1 2 8 5 8 8 - [9 .2 .3 ]
M o ri T , M atsu lira K , Z h an g B , c t al. ( 2 0 0 2 ) Elfcct.s o f t h e d u ration o f
early strabism us on th e b in o cu la r responses o f neu ron s in the m onkey
visual c o rtc x ( V I ) In v est O p h th a l V is S ci 4 3 1 2 6 2 - 9 [8 .2 .4 a ]
M orley J W , Lindsey J W , Ju d g e SJ ( 1 9 8 8 ) P rism -a d a p ta tio n in a
strabism ic m on k ey C lin V is S ci 3 1- 8 [1 0 .2 .5 ]
M o rley J W , Ju d g e S J, L in d sey J W ( 1 9 9 2 ) R ole o f m on k ey inidbrain
n c a r-rc sp o n sc neu ron s in p h o ria ad ap tation J N cu ro p h y sio l 6 7
1 4 7 5 - 9 2 [1 0 .1 0 .2 c ]
M orrison L C ( 1 9 7 2 ) Fu rth er stu d ies on the ad ap tation to a rtificia lly -
p rod uced an iseik on ia B r J P h y sio l O pt 2 7 8 4 - 1 0 1 [9 -9 .3 ]
M o rron c M C , Burr D C , F io rcn lin i A ( 1 9 9 3 ) D ev elop m en t o f in fan t
co n tra st sensitivity to ch rom acic stim u li Vis R es 3 3 2 5 3 5 - 5 2 [7 .2 .1 c ]
M o rro n c M C ,T o s c tti M , M o n can aro D ,c c al. ( 2 0 0 0 ) A corcical area chac
responds specifically со o p tic flow, revealed by f M R I N a t N eu rosci
3 , 1 3 2 2 - 8 [5 .8 .4 b ]
M o rro n g icllo B A ( 1 9 8 8 ) Infants* localizatio n o f sounds a lo n g the
horizoncal axis: estim ates o f m in im u m audible angle D ev et P sy ch ol 2 4
8 - 1 3 [7 .7 ]
M o rtcn scn U ( 2 0 0 2 ) A d d itive n oise, W cib u ll fu n ctio n s and th e ap p roxi­
m ation o f p sy ch o m etric fu n ctio n s Vis R es 4 2 2 3 7 1 - 9 3 (3 .1 .1 b )
M oschovak is A K ( 1 9 9 5 ) A rc laws thac govern behavior em bedded in the
stru ctu re o f che C N S ? The case o f i le r in g s law Vis R es 3 5 3 2 0 7 - 1 6
[1 0 .1 0 .2 a , 1 0 .8 .1 b ]
M oschovak is A K , S cu d d cr C A , I lig h stcin S M ( 1 9 9 0 ) A stru ctu ral basis
fo r H c rin g s law : p ro jectio n s to extraocu lar m o to n e u ro n sS cie?ice 2 7 8
1 1 1 8 - 1 9 [1 0 .8 .1 b ]
M oss S J, Sm art T G ( 2 0 0 1 ) C o n stru c tin g in h ib ito ry synapses N a t Rei>
N eu ro sci 2 2 4 0 - 5 0 [5 .5 .2 c ]
M o ttc r В С ( 1 9 9 1 ) B eyond extrastriate co rte x : th e parietal visual system
In V ision a n d v is u a l d isju n c tio n (cd A L L cv cn th al) Vol IV pp 3 7 1 - 8 7
M a cM illa n , L o n d o n [5 .8 .4 ]
M o ttcr B C ( 1 9 9 3 ) F o cal a tte n tio n produces spatially selective
processing in visual corcical areas V I V 2 and V 4 in che presence o f
co m p e tin g stim u li J N cu ro p h y sio l 7 0 9 0 9 - 1 9 15.9.3a]
M o ttc r B C ( 1 9 9 4 ) N eural correlates o f atten tiv e selection fo r co lo r o r
lu m in an cc in extrastriate area V 4 J N eu ro sci 1 4 2 1 7 8 - 8 9 [5-9.3c]
M o ttcr B C , P oggio G F ( 1 9 8 4 ) B in o cu lar fixatio n in che rhesus m on key:
spatial an d tem p o ral ch aracteristics E x p B r a in R es 5 4 3 0 4 - 1 4
1 1 0.5.4a]
M o u n ccastlc V B ( 1 9 5 7 ) M o d ality and to p o g rap h ic p rop erties o f single
neu ron s o f cacs so m atic sensory c o rtc x J N cu ro p h y sio l 2 0 4 0 8 - 3 4
15,71
M o u n ccastlc V B ( 1 9 9 7 ) T h e colu m n ar organ ization o f the n co c o rtcx
B r a in 1 2 0 7 0 1 - 2 2 [5 .7 ]
M o u n tca stlc V B ( 1 9 9 8 ) P erc ep tu a l n eu roscien ce.. T h e c c r e b r a l co rtcx
\larvard U n iv ersity Press, C am b rid g e, M A [6 .4 .2 d ]
M o u n tcastlc V B . Lynch J C , G co rg o p o u lo s A c t al. ( 1 9 7 5 ) Posterior
parietal associacion corcex o f chc m onkey. C o m m a n d fu n ctio n s for
o p eratio n s w ith in extrapersonal space / N eu ro p h y sio l 3 8 8 7 1 - 9 0 8
| 4 .5 .6 .5 .8 .4 c ]
M o u n ts J R W ( 2 0 0 0 ) Evidence for suppressive m echanism s in a tte n tio n al
se lectio n : feature singletons p rod u cc in h ib ito ry surrounds P ercep t
P sy ch o p h y s6 2 9 6 9 - 8 3 (4 .8 .3 d ]
M outou ssis K , K eliris G , K ou rtzi Z , L o g o th ctis N ( 2 0 0 5 ) A b in o cu lar
rivalry studv o f m o tio n perception in the hum an b rain Vis R es 4 5
2 2 3 1 - 4 3 [5 .8 .4 b ]
M ovshon JA ( 1 9 7 6 ) Reversal o f the behavioural effects o f m on ocu lar
deprivation in the k itten J P h y sio ! 2 9 1 1 7 5 - 8 7 [8 .3 .1 c ]
M ovshon J A , B lakem ore С ( 1 9 7 4 ) Fu n ctio n al rcin n crv atio n in kitten
visual c o r tc x N a tu re 2 5 1 5 0 4 - 5 [8 .3 .1 c ]
M o vsh o n J A , D u rsteler M R ( 1 9 7 7 ) E ffects o f b rie f periods o f unilateral
eve closure on the k itte n s visual system / N cu ro p h y sio l 4 0 1 2 5 5 6 5
(8.2.3d)
M ovshon J A , K iorp es L ( 1 9 8 8 ) A n alysis o f the developm en t o f spatial
co n tra st sensitivity in m on key and hum an in fan ts / O pt S oc A m Л 5
2 1 6 6 - 7 2 (7 .2 .1 a ]
M ovshon J A , N ew som e W T ( 1 9 9 6 ) V isual response p rop erties o f striate
co rtica l neu ron s p ro jectin g to area M T in m acaque m o n k cу/ N eu ro sci
1 6 7 7 3 3 - 4 1 [5 .8 .4 b ]
M ovshon J A , T h om p son ID , T o lh u rst D J ( 1 9 7 8 ) Spatial and tem poral
co n tra st sensitivity o f n eu ron es in areas 17 and 18 o f the c a t s visual
c o rte x / P h y sio l 2 8 3 1 0 1 -2 0 ( 5 .6 .3 ,5 .6 .4 b ]
M ovshon J A , Eggcrs H M .G iz z i M S , c t a l. ( 1 9 8 7 ) E ffects o f early u n ilat­
eral b lu r o f che m a caq u es visual system . III. Physiological observ a­
tio n s / N eu rosci 7 1 3 4 0 - 5 1 [8 .2 .4 b ]
M o vsh o n J A , K iorp es L , H aw kcn M J, C avanaugh J R ( 2 0 0 5 ) Fu n ctio n al
m atu ratio n o f t h e m a caq u es lateral gen icu late nucleus J N eu rosci 2 5
2 7 1 2 - 2 2 [6 .3 .5 c ]
M ow er A F, L iao D S , N cstlcr E J, ec al. ( 2 0 0 2 ) c A M P / C a *+ response
elem en t b in d in g p ro tein fu n ctio n is essential fo r o cu lar d om in an ce
plastic icyJ N eu ro sci 2 2 2 2 3 7 - 4 5 [ 8 .2 .7 f ]
M o w er C .D , C h risten W G ( 1 9 8 5 ) R ole o f visual experien ce in activating
critical period in cat visual c o rtc x / N cu ro p h y sio l 5 3 5 7 2 - S 9 ( 8 .3 .lb ]
M o w er G D , C h riste n W G ( 1 9 8 9 ) Evidence for an en h an ced role o f
G A B A in h ib itio n in visual co rtical d om in an ce o f cats reared w ith
ab n o rm al m o n o cu la r experien ce D ev cl B ra in R es 4 5 2 1 1 -1 8
[8 .2 .7 d )
M o w er G D , B u rch ficl J L , D u ffy П I (1 9 8 1 a ) The effects o f dark rearing
o n th e d evelopm en t and p lasticity o f chc lateral gen icu late nucleus
D cv cl B ra in R es 1 4 1 8 - 2 7 [8 .1 .1 a )
M o w er G D , B crrv D , B urch ficl J L , D u ffy F H (1 9 8 1 b ) C o m p a riso n o f
the effects o f d a rb rc a rin g a n d b in o cu lar suture on developm en t and
plascicicv o fc a c visual c o rte x B ra in R es 2 2 0 2 5 5 - 6 7 [8 .3 .1 b ]
M o w er G D , C ap lan C J , Lccsou G ( 1 9 8 2 ) Behavioral recovery from
b in o cu lar deprivation in the cat B e h a v B r a in R es 4 2 0 9 - 1 5 [8 .1 .2 ]
M o w er G D C h risten W G , C ap lan C J ( 1 9 8 3 ) Very b r ie f exposure elim i­
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Poslcanzcr K , N ecd lcm a n L A , Bozdagi O , H unrlcv G\V ( 2 0 0 3 )
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P ratt-Johnvon J A , T illso n G ( 1 9 8 1 ) V isu al results a fter rem oval o f c o n ­
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P ratt-Joh n von J A , T ills o n G ( 19 X 3 ) Sen sory results follow ing treatm en t
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P rcd cbon J ( 1 9 9 4 ) C o n v erg en ce responses to m o n o cu larly viewed
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Prcvost A ( 1 8 4 3 ) F.ssai sur la th c o ric dc la vision b in o cu lairc Rambo/.,
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Prcvost P ( 1 8 0 4 ) F.ssais dc p h iloso p h ic OU etu d e d c le sp rit hum ain
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P roffitt D R , G ild c n , D L ( 1 9 8 9 ) U n d erstan d in g natural dynam ics J E x p
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Provinc R R , W esterm an JA ( 1 9 7 9 ) C rossin g the m id lin c: lim its o f early
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Pugh M ( 1 9 5 8 ) V isual d isto rtio n in am blyop ia B r / O p h th a l 4 2 4 4 9 - 6 0
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Purvcs D , L ich tm an J W ( 19 8 5 ) P rin cip les o f n e u r a l d e v e lo p m e n t Sinaucr,
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Pylyshvn Z W ( 1 9 7 3 ) W h a t th e m in d s eye tells the m in d s brain P sy ch ol
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Q a d ir C A ( 1 9 9 0 ) P h ilo so p h y a n d scien ce in th e Is la m ic w o r ld R otitled ge,
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Q iu F T ,S u g ih a r a T ,v o n d er H eyd t R ( 2 0 0 7 ) Figure-ground m echanism s
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Q u a ia C , O p tica n L M ( 1 9 9 8 ) C o m m u tativ e saccad ic g en erator is
sufficient to co n tro l a 3 -D o cu lar plant w ith pulleys./ N eu ro p h y sio l
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Q u creau | ( 1 9 5 4 ) S o m e asp ect o f to rsio n A rch O p h th a l 51 7 8 3 - 8
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Q u ick M W , B o o th e R G ( 1 9 8 9 ) M easu rem en t o f b in o cu lar alig n m en t in
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Q u ick M W ,T ig g c s M , G am m o n J A , B o o th e R G ( 1 9 8 9 ) Early abnorm al
visual experien ce indu ces strabism us in in fa n t m onkeys In v est
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Q u in la n E M , P h ilp o t B D , H u gan ir R L , B ear M F ( 1 9 9 9 ) R ap id , experi­
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Q u in la n E M , L c b c l 1>, B m sh I, Barkai E ( 2 0 0 4 ) A m olecu lar m echanism
for stab ilization o f Icarnin g-in d u ccd synaptic m o d ificatio n s N eu ro n
41 1 8 5 - 9 2 [6 .4 .4 f, 6 .5 .l a , 6 .6 .3 ]
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Radhakri.vhnan H , Pardhan S , C alv cr R I, O ’Leary D J (2 0 0 4 a ) U nequal
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R ain ey B B ( 2 0 0 0 ) T h e e ffe c t o f p rism ad ap tation o n th e response AC/A
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R ak ic P ( 1 9 7 4 ) N eu ro n s in rhesus m on key visual co rte x : system atic rela­
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R ak ic P ( 1 9 7 6 ) Prenatal genesis o f c o n n e c tio n s subserving o cu lar dom i*
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R ak ic P ( 1 9 8 1 ) D ev elo p m en t o f visual cen ters in the prim ate brain
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R ak ik P ( 1 9 8 5 ) L im its o f n cu ro gcn csis in prim ates S cien ce 2 2 7 1 0 5 4 - 6
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R ak ic P ( 1 9 8 8 ) Sp ecificatio n o f cereb ral co rtical areas S cien ce 2 7 1 1 7 0 - 6
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R o sen b la tt F ( 1 9 5 8 ) The p crccp tro n : a p ro bab ilistic m od el for in fo rm a­
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R osenfield M ( 1 9 9 7 ) T o n ic vergence and vergence ad ap tation O p tom t'ls
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Rosenfield M , C iu ffred a K J ( 1 9 9 0 ) D ista n ce h cte ro p h o ria and to n ic
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R osenfield M , C iu ffred a K J ( 1 9 9 1 b ) E ffect of*surround p ro p in q u ity on
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Rosenfield M , G ilm a rtin Б ( 1 9 8 8 a ) A ccom m od ativ e ad ap tation induced
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Rosenfield M , C iu ffred a K J. O n g E , A zin i A ( 1 9 9 0 } P roxim al induced
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Rosenfield M , C iu ffred a К J , H u n g G K ( 1 9 9 1 ) The lin earity o f proxim al-
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Rosenfield M , R ap p o n J M , C arrel M F {20(H )) V crgcn cc adaptation
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R u tstein RP, C o rliss D ( 1 9 9 9 ) R elatio n sh ip betw een an iso m etrop ia,
am blyop ia, and b in o cu larity O p tom Vis S ci 7 6 2 2 9 - 3 3 [ 8.4.1 ]
R u tstein R P , F,skridgc IB ( 1 9 8 4 ) Stereopsis in sm all-an glc strabism us A m
J O p tom P h y sio l O p t 6 1 4 9 1 - 8 [ 10.2.2b ]
R u tstein RP, Fuhr P S ( 1 9 9 2 ) E fficacy and stab ility o f am blyopia therapy
O p tom Vis S ci 6 9 7 4 7 - 5 4 [8 .4 .6 b ]
R u ttu m M , N o o rd cn G K v on ( 1 9 8 3 ) A d ap tation to tiltin g o f the visual
en v iro n m en t in cyclotropia^/w J O p h th a l 9 6 2 2 9 - 3 7 110.7.1*
Rvndcrs M C , N avarro R , Losada M A ( 1 9 9 8 } O b je ctiv e m easurem ent
o f th e o ff-ax is lo n g itu d in al ch ro m atic ab erration in the hum an eye
V is R es 3 8 5 1 3 - 2 2 [9 .1 .2 a ]
Saarela T P . Sayim B , W csth eim cr G , H erzog M H ( 2 0 0 9 ) G lob al
stim u lu s con fig u ration m odulates crow d ing / Vis 9 ( 2 ) A rticle 5
[4 .8 .3 d ]
Saarin en J ( 1 9 9 6 ) L ocalization and d iscrim in ation o f "p o p -o u t targets"
 I N D E X OF C I T E D J O U R N A L S

Acta O phthal A cra Ophthalm okigica A rt History

Acta O phthal Supp A cta O phthalm ologica Supplement A rt Q uarterly
A c u O t o lir p ^ o l Acra OtoLaryngologica A rtif Intell A rtificial Intelligence
Acta Physiol A cra Physiologica A rtcn Percept l4ychophvs A ttention. Perception, and Psychophysics
A cta Psychol A cta Psycho Jog tea Auk Auk
Adv C h illi Dcvcl bchav Advances in C h ik l Developm ent and behavior Aust J O ptom Australian Journal o f O ptom etry
Adv O phthal A dsaiucs in O phthalm ology Aust J Psychol Australian Journal o f Psychology
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Akirvtiquc Z c itschr.lt Akust Z Bchav Biol Behavioural Biology
Aw J Mum G en et American Journal o f 1 luman G enctic* Bchav Ecol Sociobiol Behavioral Ecology and Sociobiology
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Arch Psyehiat Z get Neurol Archiv liu Psychiatric und Zeiisehrift fu r die Com pur Biol Med Com puter* ill Biology and Medicine
gcsaratc Ncuro logic C om put V is G r Im Pnvc C om puter Vision» Graphics and linage Processing
Arch Psychol Archiv es o f Psychology С «ii4r'
V.*Illbl#iж
l
Arch H ist Exact Sci Archive for H istory o f Exact Sciences C u rr Biol Current Biology
Ar<h Mikros Anar Ent Archiv M ikroskopic A natom ic und C u crO p in Ncurobiol Current O pinion in Neurobiology
Entw kikingsm cchanism c Developm ent
A n Bulletin Dcvcl Biology Developm ental Biology
p c v c l Вram Res Developmental Brain Research J Elcctroplwtkil Journal o f Olcctrophyskikigy
D c rc l Psychol Developmental Psychokigy I Exp Anal Behav Journal o fth e Experimental Analysis o f Behavior
Displays J Exp Biol Journal o f Experimental Biology
D o c O phthal D o cu m en t* O phthalm ologica J Exp C h ild Psychol Journal o f Experimental C h ild Psychology
E<ol Pfcyehol Ecological Psychology J Exp Psychol Journal o f Expcrimental Psychology
Ed i lib J Sci Edinburgh Journal o f Scicncc J Exp Psychol Gen Journal o f Experimental Psychology: General
E E C C lin Neurophysiol Elcctn:*cncq»lulography and C h n k a l J Exp Psychol H PP Journal ol Experimental Pssvh"logv: Human
Ne u rophy sk)k | y Perception and Performance
E u rJ Neurosci European Journal o f Neuroscience I franklin Inst Journal o fth e fran klin Institute
Exp Brain Res Experimental Brain Research J Gen Physiol Journal o f General Physiology
Exp Neurol Expсri me 11ral N eurology J G e n Psychol Journal o fG en cral Psychology
Exp Psyvhol M o nog г Experimental Psychology Monograph J Hist Behav Sci Journal o f the H istory o f the Behavioral Sciences
For*ch Z ool l-orchntte der L<x>logic J H itt Med Allied Sci Journal o fth e H istory o f M cdicinc anti Allied
G cr 1 O p h th il G erm an journal o f O phthalm ology Scicnccs
G ro c k s Arch Klin Exp O phthal G racfc* Archiv fitt klintschc und experim ented J H ist Philos Journal o fth e H istory o f Philosophy
O phthalnio logic J !m Sci Tcchr.ol Journal o f Image Science and Technology
} lerpctologica J Inst Elcc Engin Journal o f the Institute o f Electrical Engineers
Hum Factors 1 luman Facto r* J M ath Jmag Vis Journal o f M athem atical Imaging and Vision
Hum O.cnct Human G en et ics I M ath Psychol Journal o f M athematical Psychology
i lum N curobiol I ium an Ncurobiology J M icros Journal o fM k ro sco p y
IE E E T r Part A d Much Intel IE E E Transaction! o n Pattern Analysis and 1 M orphol Journal o f M orphology
M achine Intelligence J M ot Hchav Journal o f M otor behavior
IE E E T r C om put Graph App IE E E Transactions on С о т р и т е Graphics J N at Philo* A m Journal o f Natural Philosophy and Arts
Applications J Navig Journal o f Navigation
lE E E T r Biom cd Engin IE E E Transaction! on Biom edical Engineering J Ncurobkil Journal o f Ncurobiology
IE E E T rS y s Sci C ybcm IE E E Transactions on Systems Scicncc and J Neurochcm Jo u rn al o f Neurochcmistry
Cybernetics J Ncurocyrol Journal o f Ncurocytologjr
IE E E T r M an M ach Cybcrn IE E E Transactions on M an. M achines and J Neurol Journal o f Neurology
Cybernetics J Neurol Ncurosurg Psychiai Journal o f Neurology Neurosurgery and
IE E E T r M an-M ach Syst IE E E Transactions on M an*M achinc Syst Psychiatry
Image Vi» Com p Image and Vision C om puting 1 Neurol Sci Journal o f the Neurological Scicnccs
Infant Behav D c rcl Infant Behavior and Dcvckipm cnt J Neurophysiol Journal o f N cufophyoology
lnt J C om put Vi* Internationa] jo u rn al o f C om puter Vision J Neurosci Journal o f Neuroscience
Int J D c rcl Biol Inter narwnal Journal <»f Developmental J O p r S o c Am Journal o f the O p tical Society <»fAmcrica
Biology JO rn Journal o f O rnithology
lnt j M an-M ach Stud International Journal o f M an-M achine Studies J Pesl O p h th al Strab Journal o f Pcdiatrk O phthalm ology and
l n t j Neurosci I ntc rnat h>nal Jo u m al o f N с иго<с ic nc с Strabismus
Int j Opcom International Journal o f O ptom etry J Person Journal o f Personality
Int J Parr Rccog A ftif Intel 1 International Journal o f Pattern Rcvognirktn and j Physiol Journal o f Physiology
Artificial Intelligence I Psychol Journal o f Psychology
Int J Psychophyaiol International Journal o f Psychophysiology J Soc Motk»n Piet Engirt Journal o f the Society о f M otion Picture
ln t J R o b ot Res Internationa] Jo u m al о f Rob ot ic Rc sc arc h Engineers
Int I V irtu al Reality International jou rn al o f Virtual Reality I S o c Moty»n Piet Tclevis Engin Journal o fth e S ocicty o f M otion Picturc and
Int R cc M ed Q u art Rev O phthal International Record o f M cdicinc and Quarterly Television Engineers
Review o f O phthalm ology I \Xarb C ou rt Inst Journal o fth e Warburg ansi C ourtauld Institutes
In te rn alJ N curosd International Journal o f Neuroscience J Sports Sci Journal o f Sports Science
Invest O phthal Investigative O phthalm ology I Tltcor Biol Journal o f Theoretical Biology
Invest O phthal V b Sci Investigative O phthalm ology and Visual Science J Ultra struct Res Journal o f Ultra struct urc Research
Invest Radio! Investigative Radiology J Vcstib Res Journal ofV cstib u lir Research
b is J Vb Journal o f Vision
J* p Psychol Res Japanese Psychological Research Klin Monar Axigcnhcilk Kliniswhe M onarsbU ttct fur Augenh<iLkunde
J A m In tra -o cu iir Implant Soc Journal o f the American Intra-ocular Implant Lor.d Edin Philos M ag i Sci London and Edinburgh Philosophical Magazine
Society and Journal o f Scicncc
J A bo S o c Psychol Journal o f Abnorm al and Social Psychology Lon Edin D ub Philos M ag J Sci London Edinburgh and D ublin Philosophical
J Acoust S o c Am Journal o f the Acoustical Socicty o f America Magazine and Journal o f Science
J AAPCS Journal o f the American Association o l Pediatric M ar Biol M arine Biology
O phthalm ology and Strabismus M ed Biol Engin M edical and Biological Engineering
J A m O ptom Assoc Journal o f the American Optvimctric Mi d Biol Engin Com put Medical and Biological Engineering and
Association C om puting
J Anat Journal o f Anatom y M ed PnsgTcchnol M edical Pro grew Through Technology
J AudUi Engin Soc Journal o fth e A uditory En/inccring Society M ed Sci Res M edical Science Research
J Audit Rev Journal o f Auditory Research Medieval Studies
J Biom cd O pt Journal o t RiootcdiciJ Opt»*» Mem Am Philos Soc M emoirs o f tb c American Philosophical Society
J C c ll Biol Journal o f C c ll Biology M IT Q iu r t Prog Rep M IT Q uarterly Progress Report
J C c ll C o m p Physiol Journal o f C ellular and Comparative Physiology M olec Neurobio 1 M olecular Neurobiologv
j C hem Physks Journal o f Chem ical Physics M ona: Her Akad M onatsberichtc der Berliner Academic
J C lin Invent Journal o f C linical Investigation M ullers Arch An.it M ullers Archiv for Anatom ic
J C o g Neurosci Journal o f Cognitive Neuroscience Nature Med Nature Medicine
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J C om p Physiol Psychol Journal o f Com parative and Physiological N at Rev N curosd Nature: Reviews Neuroscience
Psychology Natur vr«e nsc ha ft сn
J Com pur A o itr Tomog Journal o f C om puter Assisted Tomography Neural C om put Neural Compucarion
J C om put Neurosci Journal o f Com putational Neuroscience Neural Network* Neural Networks
J dc Physique Journal tie Physique Neuroease
J Display Tcchnol Journal o f Display Technology N cuiocom puting
Ncuro Image Psycho) Stud Psychologic he Studicn (Leipzig)
N curo-O phthal N euro-O phthalm ology Psychonom Bull Rev Psychonomic Bulletin and Review
Psychonom M onogf Supp Psychonomic Monograph Supplements
Neurosci Neuroscience Psychonom Sci Psychonomic Science
N ew o*ci Lett Ncuroscicncc U tw r t Q i u r t ) Exp Physiol Q uarterly JournAl o f Experiment a I Physiology
N cu rotd Res Ncuroscicncc Research Q u ir t j Exp Psychol Q uarterly JonnvAl o f Experiment a I Psychology
New» Physiol Sci News in Physiological Scicncc* Res D cvcl Research D erelapm ent
Nucleic Acids Rc* Nucleic A c k b Research Rev M od Phys Review o f M odern Physics
N Z J feychol New Zealand Journal o f Psychology Rev Neurosci Res icw o f Ncuroscicncc
N Z JZ o o l New Zealand Journal o i Zook)gy Rev Neurol Revue Ncurc»log»oue
O phthal Physiol O pr O phthalm ic ап J Physiological O ptics Scam : J Psychol Scandinavian Journal o f Psychology
O phthal Ren O p h tlu lm ic Research Sci Am Scientific American
O ck jl Act a Scm Neurosci Seminars in Neuroscience
O ptom V is Sci O p tom etry AnJ V ision Scicncc Sen Proc Sensory Processes
Percept M ot Ski! Is Perceptual and M o to r Skilk Sig Prac: Image C om m Signal Processing: Image C o mini in ic ation
Percept Psychophys Perception And Psychophysics S oc Neurosci A bitr So ciety o f Ncuroscicncc Abstracts
Pflugers Arch gcs Phyiiol PHugcr* Archiv fur die gCfcume Physiologic S o c Neurowi Symp Society o f N eurottience Symposium
Philos Stud Philosophise lie Srudicn Spat Vis Spat til Vision
Philos T r R S o c Philosophical Transactions o fth e Royal Society Survey O phthal Survey o f O phthalm ology
London System Z ool Systematic Zoology
Photogram Engin PhotogrAmmctric Engineering A rt Q u irt fb c A rt Quarterly
Photogiam Engin Rem S<ji P hotogram m ctrk Engineering and Remote ’Hie American Cartographer
Sensing Tohoku Psychol Folia T o h o lu PsyehologKA Folia
Photograph f Photographic Journal Tr A m O phthal Soc Transactions o f the American Ophthalm ological
Physiol Bchav Physiology and Behavior Socicty
Physiol Rev Physiological R ev iew T r Am Philos Soc Transactions o fth e American Philosophical
Physiol Z ool Physiological Zoology Society
PogflcndortFs A nn P ln sik C h cm Poggendorif* A nnakn d er Physik iind C hcm ic Tr M icroscop Soc Lon Transactions o fth e M icroscopical So cicty o f
Prim Ate* London
Proc S o c Neurosci Proceedings o fth e Sociccy o f Ncuroscicncc T r O phthal S o c U K Transactions o f the Ophthalm ological S ocicty o f
Р п к Am Philos Soc Proceedings o ftlw Am erican Philosophical the U nited Kingdom
Society Tr Ope S o c Lon T r a n s itio n s o f the M icroscopicil Society o f
Рпк- Aw Rev ncrv I)ii P ro ceed in g o fth e Association for Research in London
Nervous Disease* Tr R S o c Edinb Transaction* o f the Royal Society o f Edinburgh
Proc Intern At S o c O p t Engin Proceedings o fth e International Society o f Tr S oc M otion Piet Engm Transactions o fth e Socicty o f M otion Picture
O p tical Engineers Engineers
Р п к Natl Acad Sci Proceeding* o f (h e National Academy o f Sciences T IN S Trends in Ncuroscicncc
Proc Physics S o c Proceedings o fth e Physics Socicty Trends C o g n it Sci Trends in Cognitive Science
Proc R Soc Proceedings o l the Royal So Сkey London V U C o g n it Visual C ognirion
Рпк* R Soc M c J Proceedings o fth e Royal Society o f M edicine V is Neurosci Visual Neuroscience
Р п к Soc P hoto O pt Instrum Engin Proceeding* o fth e Society o f Photo-optical V i* Res V ision Rrsearsh
Instrumentation Engineers V is Sci S oc Abstracts V ision Sciences S ocicty Abstracts
Proc Physiol Sot- Proceedings o fth e Physiological Socicty Z Exp Angcw Psychol Z citsch rik tor e xp erim en ted und angcwandtc
Prog Brain Ret Progress in Brain Research Psychologic
Prog Ncurobiol Progress in Neurobiology Z G csch Arabi-bkun W isscn Zcitschrift fur G eschiehte der Arabtsclv
Prog Psvcbobiol Physiol Psychol Progrcw in Psychobiology And Physiological h iim b c h cn W is e n t* halt
Psychology Z Naturforsch Zcitschrift for Naturfbrschung
Psychol licit Psychotogisehc Beit rage Z Neurol Psychiit Zcitschrift fur Neurologic und Psychiatric
Psychol Bull Ptychokigical Bulkrin Z Psychol Zcirschrifi tor Psychologic
Psychol Forsch Psychologischc Forschung Z Psycho I Physiol Sinnctorg Zefcschrife fur Psychologic und Physiologic dcs
Psychol M onogr Psychological M onographs Sinncsorganc
Psychol Rcc Psychological Record Z Sinncsphyssol Zcirschrift fur Slnncsphysiologic
Psychol Res Psychological Research Z Г icrpsychol Zcttsclinh fur Tierpsychologie
Psychol Rev P>ychok*gical Review Z VC’isscn P hotog Photophy Photochcm Zcirschrifi tor Vt-'isscnschaltlichc Photographic
Psychol Rev M oiiogr Stipp P a th o lo g ic a l Review Monograph Supplements Photophysik und P hocochcm k
Psychol Sci Pcycliokjgical Science
 PORTRAIT INDEX VOLUME 1

Andersen. R . A. 223 H arw crth. R . S. J± 1 Payne. B. R . 224 W illiam s, IX R .

Aslin. R . N. V”' H e b k D .O . Wi PbLz.U . 267 Vfon5- R i k y ,M .T X 2Ы
Atkinvon. J. ill H e ld R . i ll WufiR. 1L 290
H elm holtz. L L von Л1 Rakic. P. U l Yonas, A . HU
Hear. M . F. jl LL H ering. F,. Ram*5n у C a j* L $ . 38 Yoi »A£, T. ;s
Berkeley, G . 11 Hes*. R . F. Ro^cnKcU. M. :iii
Berman. N. 414 1Norton, J. C . 26S
Birch. L E. ill H ubei. D .L L 2AL Sakata. LL 2 2d
Brewster, D. $2 H u n g.G . K. Л1Z Schactfcl. F. •И6
Schiller, P LL m i
Callaway. t*. M . iii Judge» S . У iiU Sch or. C M . ж :
C a m p b e ll F VC*. m Semmlow,J. L. m
Charm an. N . W. in Kapoula. /.. Shapley. R.
C h in o. Y .M . Kasamatsu. T. 4(M Shatz. C .J- in
C o lk w ijn .il. 507 Kepler. У 22 Sherm an. S . M.
C o ttfy . A. 2^ 1 Кюгрсе, L. a2 R Shim ojo. S. ill
Crawford* Mr L. J. illL K k m .S . A. ill Singer» VC*. 403
C v n aJcr, M 122 Kruger. P. В A bb Sireteanu. R. M£l
Sm ith. L . L Jii
D j£u crrc. L Ы Levi, D . M . 421 Sperry, R . W . 221
Daw. N . W. ill Livin&stonc. 278 Sretavan. D. VC'. ill
iic IU P o tta C . B. 22 Stryker. M . P. 2sa
D o ca rte s. R . ?5 M ach. •И Swindzlc. X . V. H i
D cV alois R . L M aunsell. J. LL R 288
Miles, F. A. 503 Talbot. F. tb.
Gibv^n, E l . M itchell. D E. 417 Tim ncy. B. ^L5
M ounu'atcle. V. B. 2V : Tootell. R . B. LL 2£i
Enright. J . T. M ovthon. A. ш Trcisman. A. L il
Erkelem . С . У 507 M n lk r.J. Ji
Van Essen. I>. C . lii
F ech n crG . F. 41 Newton. L 70 Vesalius. A- ii
Fry. О . A. a iC Niepce. N. Von N oofilen. G . K.
N orcia, A. M . it L
G ilbert, C . D. ?.7a W heatstone* C . 79
G ross, C . G. 22L O rb an , G. A. 2S£ W iesel. T .N . lid
 SUBJECT INDEX

Abelard, Peter. 2 £ Achromatic active search and, 1 * 8 - 7 9 anisom etropia and. 4 6 9 - 7 4 ,4 7 1 /

Aberrations Achromatic ganglion cclls. 2 12 - J 3 assumptions and context i n .l l i x in aphakia. a liL
hkir sign an J lens. 4 6 6 - 6 8 Achromatic lenses. Ц conscious con trol of. 17 9 -КО in a iia l ametropia. 4 7 0 - 7 1
chrom atic. 4 3 7 -3 & , 4 $ 7 f. 4 6 0 - 6 1 . z b b A ctin. 2 j -L grouping o f neighboring shape* and. disparities produced by. 4 7 3 . 4 7ty ’
cotnpcru.it ion o f . i i l fi laments, 3 2 7 - 2 8 m i 99/ o l e cce n trk g a « , ± I i i
dynamic acceinunodacion k u ! ,4 6 7 - 6 S nucleator*. 1 2 Z niulrivrable percepts and. 177., 17 I f eikonom eter measurement of. 471 - 7 2
m onochrom atic. 4 3 5 - J ? treadmill, i l l processing channcl adaptation and. H E . pursuit adaptation t o . i i l i
spherical. 'л--, •»V'y.' i-’^- A ctin binding proteins. 2лХ weighting o f cucs and. 1 7 7 -7 8 space eikonom eter measurement of.
stactc accomm odation and. oiafi A ction potentials. 130—31 Amblyopia. 4 0 5 - 6 . *aJh. 4 7 2 - 7 3 ,4 7 3 /
uavefrone, 4 4 0 -4 1 amacrine veils generating, 211 abnorm al risualty guided movement* types of, 4 6 9 - 7 0
Aberromcrcr, ±A L axon guidance and. lii. in . 4 2 9 - 3 0 vergence adaptation to , 53# ~ 40
A C . A y Accommodative convergence Active elccirolocaiion. i acuity loss and, 4 2 1 - 2 4 A niw -accom m odation. 4 6 4 - 6 5
AC/A ratio, SilLL Active search, 1 7 8 -TV antsomcrropic compared to s o a b s m k . Anisom etropia, 4 6 9
C A / C ratio relationship svith. 5 0 3 - 4 Actirhy-rcgubfecd genes. 357-5H 4 2 1 -2 3 aniseikonia and . 4 6 9 - 7 4 .4 7 1 1
o rth op tic exercises ejfecting, v V Acuity contrast sensitivity loss and. i 2 l - 2 4 rvpcs of, 4 6 9 - 7 0
response, ilLL amblyopia and V.m о f. 421 - 2 4 crowding and. i 2 i . A nisom etropic amblyopia, *a2iL
btimuklls&U- color sensitivity and, 3 6 9 - 7 2 defective stimulus integration and. st rabivmk amblyopia compared to ,
Accclcrating nonlincar.ty. l u l l grating. 2 2 0 . 5 Tty* 4 2 6 -2 7 4 2 1 -2 3
Accidcntal v icwpou)t> lZii. vernier,a i . *7 0 -7 1 development d &4 ) 0 - 3 3 Anisophorta.£&&
Accomm odation Adaptive held, 4 9 5 - 9 6 directional preponderance o f O K N Anomalous retinal correspondence (A R C ).
aberrations and dynamic. 4 6 7 - 6 8 Adaptive opcics dcx icc.d 6Q .464 in.±21L AM.
abcrration# and s ta c k ,млu Adaptive procedure. eccentric bxatkm and, ii2iL A ntagon nt.2aa-
aberration* and *tcp changcs in .iiiiZ Additive noise. L ite. rlxitcr sensitivity loss in. 4 2 7 - 2 8 A nterior intraparietal area (A JP ). 2iLi.
aniso-, 4 6 4 - 6 5 Additive variance hypothesis. llil m otion detection asymmetry and, Anterograde transjx>rt. l i Z .
comparative aspects of. 4 4 4 - 4 5 A dt lard o f Bath. 15. 4 2 S -2 9 Anri'aliasing H ltcr,d i2
cucing, 4 6 5 - 6 9 Adequate stimulus, llii. mocion sensitivity Joss in,ii22i Aphakia, aniseikonia in .a llL
COdcfocUV blur. **6l - 6 5 . id Visfiliation (K ep к i ). 2 2 m otor symptoms of, 4 2 9 - 3 0 Apollonius, l a .
depth o f field and accuracy o f, 4 5 7 - 5 9 Affine geometry. 12*2. 119/ neural com petition a n d .4 3 0 - 3 - A p op to sis. l u i
dynamics of, 4 6 2 - 6 4 Age-specific genes, l i l orientation discrim ination in .4 2 3 - 2 4 Apposition com pound eyes, 3 0 7 - J , 3 0 7 f
far point of, 443 Agonist, response latency in . 4 2 7 A rabic empire, visual science in . 2 0 - 2 4
gain o f . M 2 . 4 6 y Aguilonius. Franciseus spatial distortions and. 4 2 4 - 2 7 A R C .S t t Anomalous retinal
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unequal demand of. 4 6 4 - 6 5 o n P tok m y s work, 6 3 Amplitude gain. lh L A tom ic theory. 1 1
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binocular connections, 2 a Z
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gain. 112. critical period postponem ent in . 4 1 6 - 17
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optical imaging o l, 2 J 2 - 3 3 C en n in i. C cn n i no. 211
P E T for. 222- Cerebellum , vergence conrrol by.2-ал
Renaissance understanding of. a ll C erebral achromatopsia. 2& ±
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Broca. Paul, i l l Channeled feature. 12i2.
Bruncllcschi. Filippo, 5 l - 5 2 . i l / - 5 y Channel homogeneity, 12&
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C L l« В psychophysical procedure, lij.
C U ^ ical period* G reece. 1 0 -1 1
CLuistrum, 2 4 8 - 4 9
C k o m e e le s 2 i
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C loscd-loop gain. 1 1 1 - 1 2
Closed operation, l l i
C oactivation. 2 j j l
C od ing primitives
basis functions and. 1 5 5 - 5 6
Fourier analysis and. 15 6 - 5 8
G abor functions and. 158
spatiaHVe^uency channels and, 15 6 - 5 7
wave Ice theory and. l i &
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C ognitive neuroscience.L iu .
C oh eren ce function. 1 2 2
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depth o f field and. 459
C olor-opponent ganglion cells. 212.
C o lu m n s S t fa fs 0 O cu lar dom inance
columns
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excitation and inhibition balance
In. 265.
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C o m fort zone, i i l i
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C om m on »iet gen es 26^.
Com m utative group. 112L
Com partmcnralracd dendritic plasticity,
3 5 5 -5 6
Com petitive figural grouping, 1 9 8 -2 0 0 ,
199/-20О/
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C om posite eve construction. 2 6 2
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C on com itant strabism us aiLi.
Cones
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types of. 2 0 7 - 8 . 208/'
C on fo cal scanning microscope. 2 2 il
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C on fu sion, 4 3 3 - 3 4
Congruence. 1 1 8 - 1 9 . 119/’
C o n ic* (A pollon ii» ).-U
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C o n ie sections, 1 2 1 - 2 2 , 121/
C onjugate eye movements, 5 4 4 - 4 5
C on nected points. 1 2 2
C o n n e x in s 21 U. 2 a l . 2 1u
Consciousness
attention and, 2 0 1 - 3
levels of. 2Ш .
stream o f. 2 0 2 - 3
C onstant error. 122
C on stant in ius A fric anus. 2 2
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C o n tex t, recognition a n d .liiiL 2 0 iy ’
C ontingent aftereffects, J_Lll
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Солсгм
depth o f field, luminancc and, *i 5 8 - 5 9
orientation tuning independence from,
2 5 9 -6 0
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s e n a r y coding and. 1-<5
Concrasc sensitivity
amblyopia and Io n of, 4 2 1 - 2 4
o f co n ical c e lls 2 5 6 - 5 7
development of. 3 & L 369/-370/
C o n trast sensitivity function (C S F )
blur and. 4 3 5 .4 5 5 / ’
in linear systems, 1 0 8 - 9 , I OS/
C o n tro l theory
error* and. 110
human factors and, 1 10
for Jinear systems, 1 1 0 - 13
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break point ol’ SO?
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insufficiency, 4 8 3 ,5 0 7
near point of. 5 0 7
recovery point ot. 5 0 7
weakness, 4 8 6 , S llli
Convergence accomm odation (C A )
A C relationship w ith, 5 0 2 - 5
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Convergent perspective, 4 9 - 5 0 . >1I/
Convolution function, signal analysis and.
1 0 9 -1 0
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C o p b n a r static stim uli, 4 9 7 - 9 8
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(V csa liu s),?!
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binocular connections in. ^ iZ
corresponding connections of. 2 2 6 . 1 2 7 /
development of. 3 4 6 - 4 8
function» o f .2 2 il
monocular connections in.2^i2
monocular connections of. l l L . 228/
strabismus and, 4 0 1 - 2
transmidline connections of. 22la.227/*
visual pathways and. 2 2 6 - 2 9
Corresponding visual lines
Alha/cn o n .6 6
Ptolemy o n ,6 2 * 6 5
C o rtaetin ,22&
C ortical cclls
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development of, 3 4 8 - 4 9
spatiote rnporal tuning of, 2 6 1 -6 3
types o f. 2X&J'
in visual co rtc*, 2 3 7 - 4 0
C o rtical magnification factor, 2 4 9 - 5 0
C ortical plasticity
catecholam ine* and, 4 14
dendritic spinesand, 4 13
gene trinsw iption and, »l 1 -1 3
I lebbian synapses and, 4 1 0 - J I
intracortical/intcrcortk.il inhibition
and. 4 0 9 - 1 0
mechanisms of, 1 0 8 - 1 4
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a n d .ii£ i
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C o rtic a l responsivity. dark reading and loss
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C orticalsynaptcs
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inter layer, 245. gain and phase lag of. 5 2 8 - 3 0 . 529/ development o f ,3 8 0 - 8 5
in visualcortex. 2 4 0 - 4 6 .2 4 \ f-2 A 2 f. horizontal and shear disparities u ith, Kepler o n . I l l
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C raw ford, Jack. 0Ш/ physiology of, 548 ideal, 1 8 5 -8 6
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elem ent binging proteins types of, 5 2 5 - 2 6 descriptive processes
C riterion level. 9 6 visual stimulus fo*. 5 3 0 - 3 3 Detectability, 9 6
C ritical flicker frequency, 2 2 2 CyclovcrsK>n. 52A Deviation scores, £ 2
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duration of. 4 J 5 - 1 6 Cytocbrom c-oxidasc stripes. 2 8 1.2 8 \ f Dichopcic stimulus. 1 7 6 ,1 7 6 f
in hum ans,4 I S - 19 Cytoplasm . 2 i Z Difference ofC ausstans (D O G ), 15^2* 1 5 9 /
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in subprimates, 4 1 5 - 1 8 l>ale, } lenry. 39 Diophancus. h x
Cross-correlation function* 115 Dam ping function. 112/ Diopters, 443
Cross-m odal effect, Dan del in's proof. 121/ prism, 4 8 2
o f plasticity in blindness. 3 9 5 - 9 6 Dark focus, Л5 0 ,4 83 Dioptrics, 2 2
Cross-m odal innervation Dark light. 2 1 5 / , . « {Descart es) . 2Li
blindness and. 3 9 5 - 9 6 Dark rearing Dioramas. 77
in m o n ocu br deprivation, d M behavioral effects of* 3 9 3 - 9 4 Dipper function», 1 0 2 - 3 .4 5 6 - 5 7
Cross-m o dal m atching, 167 cortical responsiviry loss with, 391 - 9 2 D irectional preponderance, o f O K N in
C ross-m od uhtion products, 1 1*4. U lL с fleets of. 391 - 9 6 amblyopia. a2ii.
Crove*oncntat>on suppression, 259 ocular dom inance columns and. 2 * 1 D irection-of-m ot ion sensitivity. H i .
C ross ratios, 119, 120/ response specificity loss with, 3 9 2 - 9 3 Discrete maps, 136
o f points on a curve, 1 2 1 - 2 2 , 122/ subcortical effects of* liLL Discrimination
Cross-spectral density function, 1 1 5 Dark vcrgcncc, 483 features of, 1 0 1 - 2
Crow ding phoria and. 4 8 7 - 8 8 functions, 1 0 2 - 3 . 102/'
amblyopia and, 4 2 5 Darwin. Charles, hype/acuity and, 102
attention and, 1 9 8 -2 0 0 da V in ci. Leonards» norm and. 1 0 3 -4
com petitive figural grouping and. on binocular vision, &S. perceptual judgement and, 1 8 2 -8 3
1 9 8 - 2 0 0 . 199/ -200/ o n light waves.2& psychophysics and, 1 0 1 -4
hypcraenity and, 198 perspective drawing and. 54/, 5 5 .5 2 .5 8 / * Dishabituation, 3 6 8 .3 8 7
C SK .V er C ontrast sensitivity function vision and writings о К 1& Dissociated vertical deviation (D V D ). 5 2 2
C S P G s. Chondroitin-sulphate Daw. Nigel. 4 15/ Distance. 2
proteoglycans P c c t l o t i o n o f visuil pathways, 2 u . 2 1 2 alky, 194
Cues. S ttd lw M ulticue systems D efoe us b lu r.jd ii perception o f, 3 8 0 - 8 3
accom m odation and, 1 6 5 - 6 9 accomm odation t o ,4 6 1 - 6 5 phoria, 4 8 6
averaging. 17 1 - 7 2 C A and elim ination o f,5112 points, 5 0 , 5 5 . 55/"
confirm ation of. 173 detection of. 4 5 3 - 6 1 to n ic vcrgcncc and c ttc s o f .^ &
deletion*accrerion, л - - neural com pensation tor, 4 5 9 - 6 0 vergence changes over large. a ^ 2
d e p t h .4 - 5 .d i i l sensitivity to change in. ^55 D istortion, 4 2 6
dissociation and alternation of, 1 7 4 -7 5 D e l e ti o n - ,u s r e t i o n c u e * l & a . D istractor signals, 5 0 9 - 10
dom inance of, 174 della Porta. Giovanni Hattitta. 2 9 - 3 0 . 5b. D istributed coding, 185
invariance. 284 del M onte, G uidobakio, 55 Distributed feature. 1 2 1
nature of. 170 Delta function, 108 Distributed representation, 16 6
ret.ilibr.itton of. 175 Delta waves, 234 Disuse hypersensitivity, 355
recruitment o f new, 175 Demand line, 504 Divergence
rcintcrpreution of, J 7 3 - 7 4 D em ocritus, 1 1 с х с с и .4 8 3 ,4 8 6
to n ic vcrgcncc and distance. 4 ib . D endritic shafts, 2 J& weakness, 4 8 6
trading. 3 7 2 -7 3 D en d ritk spines,25& Divergent perspective. *19, 50/
weighting of» 1 7 7 -7 8 cortical plasticity and, 4 1 3 D O G , S ee Difference o f Gaussian*
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C u t o ff frequency* 1 0 # .- 2 £ Deprivation. S ee M onocular deprivation D om ain prior» 116
C yclic group, 11 8 Deprivation amblyopia, 4211 D onders. Frans C o m e bus, 2 5
Cyclodisparity. 5 l £ . Depth D opam ine. 2 u i
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Cyclopean ax » . 65 detest ion o f. I t frontal cortex an d .2^15
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Cyclopean eve. 1 2 o f focus, 4 5 7 M S T and. 2 9 0 - 9 1
Aguilonius o n . 65L Depth o f field M T and , 2 8 8 - 9 0
Cyclopean procedures. 1 7 5 - 7 6 accommodacion accuracy and. 4 5 7 - 5 9 parieto*occipital region in. 2 8 7 - 8 8
Cyclopean vision,il characteristic* o f, 4 5 7 posterior parietal cortex ami, 2 9 1 -9 5 ,
Ptolemy o n , 6 4 - 6 5 color and, 4 5 9 292r
C yclophoria. 4 8 6 . 5 2 ii contrast, luminance and, 4 5 8 - 5 9 prem otor cortex and. 2 9 5 - 9 6
C yclopia, 2 2 * pupil diam eter and, 4 5 7 rostral superior tem poral cortex and, liU -
Cyclostcrcoscope, i l l spatial frequency and, 4 5 7 - 5 8 stimulusrspccific etfects in. 2 0 2
Cyc lotrop u , 5 2 ii Stiles-Craw ford effect and, 4 5 9 V 5 and. 2 8 8 - 9 0
Cyclovergence, * 2 6 .4 8 0 -8 1 stimulus eccentricity and, 4 5 9 ventral pathway interacting w ith,2S&
angle o f g j* c and. 530 Depth perception Dorsal tclcn ccp h alo n .222
asymmetry of» 5 3 2 -3 3 * 533/ avoidaoce o f approaching objcccs and, 3 8 2 D o iv i-d o гчаI stream, 2&2
dynamics of. 5 2 8 - 3 0 c liff avoidance and. 2 iL . Double-pass procedure, a liL
Double-staircase m ethod, 9 6 Explicit descr iptive process 1 9 1 -9 2 Fick system. a22. Gam л и wax'es 234
Du Bois-Rcym ond, Em il. Exponential fu n ctio n s linear systems and. Figural aftcrcKects. JLlI G anglion cclb
D u ction, i 2 i i 1 1 2 - 1 3 .1 1 3 / Figural goodness, 179 achrom atic, 2 1 2 - 1 3
D u M on t, Henri, Express saccadcs, 513 Figural groupings. 1 6 3 -6 5 adaptive coding in . 2 1 4 - 15
Duret; A lbrecht, 55 Exrc realization stim ulus Filopodia, 12L .327/ ' in c a r s 2 1 1 - 1 2
D V D .& r Dissociated vertical dcviorion External noise. 216 Final com m on path. Saa. color-opponent. 2 1 2
Dynam ic range. U L l External relcrencc fram e, ii Fine bam coincidcncc optom eter, 449 com petitive survival of, 3 1 4 - 1 5
Exrcroccprivc rcaftcrcncc, 168 Fixation disparity connections and responses of.
E b m P jfjr u y , ti Extracellular matrix. 2 2 2 . fixation shift an d .4 8 9 - 9 0 2 1 3 -1 4
E C As. S ee Enzyme com plementation assay* Extraocular m u K k i k i measurement of. *iSK -89 displaced. 2 1 5
Eccentric (\ хлаапч£ 2 Я Extravtriatc cortcx, l^ L nonius procedure for. 4$9 photosensitive. 21 5
Ecccntric gaze, vcrtk-il vcrgcncc in . 524 Extromission theory o f vision. 1 7 - 1 К Panurn s fusional area and. 491 - 9 2 receptive field sm , 2 U L 2 l 3 , 2 1 4 /
Ecccntric photorel taction. 4 50 Eye*hand coordination system, 169/ phoria and, 4 9 0 - 9 1 L lA iL iL .3 1 S .3 3 2
Echolocation. L .£ Eye movements. S e e.rfjo Vcrgcncc eve vertical, £12. G ap ju n ctio n s ILlL
£ Hi rence copy, 16 7 movements Fixation shift, fixation disparity and. Gap-overlap effect, 513
Egypt, ophthalm ology history in . 2 avis systems for. 4 7 6 - $ 0 . 477/* 4 8 9 -9 0 Garden school, Greece. LL
Eigenvalues.124 conjugate* 5 4 4 - 4 5 Flicker sensitivity, 2 2 a Gavvcudi, Pierre, 1 2
E»gcnvcctor*,12u geometry of, 478/" amblyopia and low o f. 4 2 7 -2 K Gaussian function
Eikonometer I iclinholtz and Elering debate Dvcr.iiS, Fluorescent dyes, 2 2 ii differentiating, l i i L
i n i t c i b n i a measured by. 4 7 1 - 7 2 Listing's law for. 4 7 7 - 8 0 tracer, 231 G abor function and. 1 5 7 - 5 8
«расе. 472-73.473/ types of. 4 7 5 - 7 6 fM R L S ee Гипсе)*-n i\ M K1 G ene knockout procedure, 1Q&
Elect rok»catvon,l E yes S ee a/so ffe fip c p jr x f Focal at tent km , 196 G enerator p o ten tial.l l l i
a c tiv e ,! Alha/xn on structure of, 23 Focus stim ulator, 448/’ G eneric viewpoint, 179
passive, i alignment o t. 3 7 7 - 7 8 Forccd-vcrgcncc curves. 4 9 2 - 9 4 , 4 9 ^ G ene transcription
fiJem en /so fG eo m erry (hueI id). 12. a m i t rop k', i t s a . 469 forw ard and reverse signaling. 330 cortical plasticity and, 4 1 1 - 1 3
Elevator m ovem ent.3 2 1 apposition com pound. 3 0 7 - 8 ,3 0 7 f Forward loop. 110. I ICy' neural con trol of. 3 5 6 - 5 7
HlfcKjame**0-$l,83f Iaxes o f vertcbrarc. £ . ( f Fourier analysis № 5 -6 G ene translation, neural control о 1.3 5 7
Em anation theory ot*vision. 20 com posite construction of, l iC . coding primitives and, 1 5 6 -5 8 G enom e im printing, 356
Alha/cn rejecting, 21 com pound, 3 0 7 - 8 , 3 0 ^ - 3 0 8 / o f complex patterns, J_ la G eom etric com p o n en ts 181
Em inert * law. 30 counter roll o f. S2£. for vruul system. Iz h . G eom etry
Emmetropic eye. .io .a.469 development of. 3 0 9 - 1 1 , $ Q 9 f Fourier power spcctTum .IQ d o f acco m m o d ate n. 444/'
Em inert opization. 3 1 0 - 1 1 em m etropic. XLL.469 Fourier transform, IQS ariine. 119, 11?/'
Exnpcdoclcs. l i l emm etropization in . 3 1 0 - 1 1 spatiotemporal. 107 analytic. 1 2 5 - 2 7
Empiricist-nativist controversy, 4 2 - 4 7 etew e, 10a. Fovea, 208/' .iiitonsotphs i n .I Z x
Empty lie Id myopia. 451 evolution o f, 3 0 3 - 8 fixation o f image o n . d i d congruence, isometry. sim ilarity as basis
Enantio morphs, ± !& eyespots 3 0 4 - 5 . 304/ ^-30^ sparing. 111! for, I I 8 - 1 9 ,1 1 9 /
m irror image and. 12& genetic con trol o f development o t i l l i Frames о f rc fercncc, psychophysics and. differencial, 1 2 Z
Endocannabinoids, 2 u £ l i i i i . hype rm et ropic. 44 S f i^.99f Euclidian. 1 2 4 - 2 5
Endocytosis. 3 3 0 . l i & . 1£2. image plane o f.2 Q £ Francesca, Piero della. >'i o fey e m ovem ents 4 7 ^ "
Endoplasmic reticulum, 2 1 2 .2 2 1 inverse. a ila frcqucncy*swcpt VEP. 1 liiL invariants in . 1 2 1
Endosom es l i L lews 3 0 5 - 7 Fresnel, AugUStin, I i non-Eucltdian, 1 2 4 -2 5
Enright, Ja m e s 4 98/ myopic, iiiiiu4 4 5f IVitsch. G .. 4 0 principles o f visual 193
Envelope. 152L nondcprired, 4 0 4 - 5 Frontal cortcx. 2£& p ro jc c tn c, 1 1 9 - 2 2 . 120/-122/'
Enzyme com plem entation away* Planer’s diagram of. 12/' Frontal eye fields, 2^5. symmetry and groups in, 118
(E G A s), 2 3 2 Sch cincrs drawing o f. j d . 34/* Frontal plane, Q topology and, 1 2 2 - 2 4 , 12 2 / -1i y %
Epb receptors, 3 1 7 structure o f, 2 0 6 - 7 , 207/' Fry» G lenn , 4 8 3 / types of, 1 1 8 -2 4
Ephrin ligand<.317 superposition com pound, 3M .308/ * fun ctional com ponents, I S 1 o f visual spacc. 1 9 3 - 9 5
E p h m is 3 3 0 transplanted third, i i i l Functional M RI (fM R I), 2 3 5 - 3 6 Gerard o f C rem ona. 2&
E picurus JLL Eyespots., 3 0 4 - 5 . 3 0 4 / -3 0 5 / Funnclm g. 1 0 1 G FP . S et G reen ftuartsccnr protein
intromission theory o f vision and.UL Eye torsion, adaptation of, 4 9 4 - 9 5 Fusiform lace area (F F A ).2Д а G ibson, Eleanor, 1& 1/
Epigenesis 3 5 6 Fusion disparity, 491 G ilb ert, С harks, 2 I iX 27\y
EPSP-spikc potentiation, 33V Га no ratio. lo £ . Fusion-lock соm poncnt G l i a lc c lk 2ALL
Equilibrium structures 1 8 9 -9 (1 ,190/ a I-Farabi. 20 dynamics of, 5 1 8 - 1 9 G lial growth factors, l o b
Equivalent input noise. 216 Feature-bawd attention . 397 functions of, 5 1 6 - 1 7 G lio b la sts.3 2 1
Era$ist rat»i s 1 1 Feature binding» 166 G Hot ransm issk»n, 2lLL
Erkelens. Casper Jo h an n e s SOУ Feature detectors G A B A . S ee y*am ino-butyric ac kl G lobal layer o fcu rao cu lu r m uscle.io a .
Error feedback, 204 construction oftow -level, l i i l G abo r functions G lutam ate, 242.
dynam ic, 4 6 5 - 6 6 definition of, 1 3 9 -4 0 coding primitives and, 1S& Glycoproteins, 3 2 8 - 2 9
Esotropia. 483 dense coding and. liilL Gaussian Я т с г л т and. 1 5 7 -5 8 G n o stic o ccu lt. 2&
Essential nonlincarity, 1 5 9 -6 1 developm ent of. 3 5 9 - 6 0 G abor patch. I5$J/ G olgi, C am illo, 3 8 - 3 9
Euclid. 1 2 -1 4 figural groupings and, 1 6 3 -6 $ G a i n .l M G olgi apparatus. i i Z
books o f, 1 2 -1 3 interaction between. 1 4 0 -4 1 o f к т о т modatio it, o(l L 463/ G olgi met bod, 2 2 i
retinal image and, -JL jo io tly tuned. 2u$. amplitude. 1Ли G proteins, 3 3 2
theorem s of. 1 3 - 1 4 .1 3 * . 14/ modification of. 3 6 0 B ode plot. 112 G rafting, 112.
Euclidian geometry. 12 4 - 2 5 perceptual descriptive processes and. 185 cU»scd-loop, 1 1 1 -1 2 Grandm other c e lls 1 6 6 ,1 8 5
Eudoxus. 1 0 -1 1 population coding and , laiL o f cyclovcrgcncc, 5 2 8 - 3 0 . 5 2 9 / G ratin g acuity. a7fl..370/
EvgU tbtipH tltU b I l i a . 304/* sensory coding and, 1 3 9 -4 1 function, 1 17 G rariolet, lx»urt-Pterre,12.
Europe, 2 9 - 3 6 . S e e л/v Medieval Europe; spatially separated objects a n d .l u i open-loop, 1 1 1 -1 2 Greece
Renaissance Fcature-intcgration theory. 166. 197 velocity, Ш & Alcxandr.an period in. 1 1 - 1 7
Eustachio, 3 1 - 3 2 Feature in v arian t.121 mergence, 5 1 5 - 1 6 .5 l 5 / - 5 1 ^ classical period in, 1 0 - 11
Evcn-crror signal, *165. Fcchncr, Gustav Theodor, ai^42/’ o f vertical vcrgcncc. i l a . 525/ extromission theory o f vision in. 1 7 -1 8
Evetsc eyes, Ж *. Feedback loop, HO, 1 10/' o fV O R .iii Garden school in, 2 L
ExaHercnce. 167 Feldberg. W illiam . 39 G alen, 1 6 - 1 7 .3 9 introm ission th eo ry o f vision in, 1L
Exocytosis. 1 1 2 .3 3 0 FFA. S tt Fusiform face area G all, Franz Joseph, 4 0 Ionian period in. 9 - Ю
E x 0lf0p ia,4S 3 Fibroblast growth factor (F (iF ),2 a ia Galvan i, Luigi. 39 Museum o f Alexandria m , 1 2
interm ittent. 484 Fibronccrin. I2 £ . Gam m a (тс<|испсу, 149 mysticism in . 2

SUBJ ECT I NDEX • 657

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direitos autorais
Linear perspective. 1 1
Linear systems
analysis o f, 1 0 4 - 1 0
con trol theory for. П О - 13
C S F in , I O H -9 ,108/'
exponential functioim aiu!,
ш/
Fourier an.ilysis for, 10 5 - 6
line-spread function an d .lil&
logarithm ic functions and. i l l
nature of, 1 0 4 -5
point-spread function a n d .J M
Signal analysis aild, ) 0 9 —10
stability of. H I
trainfer function and . 1 0 6 -7 , № 6 f
Linear V O R (L V O R ). 5 4 2 - 4 3
Linear zones. 2 I i l
Line-spread function. 1 И Ю 8 - 3 9 ,4 3 9 / '
LIP. S ee Lateral intraparietal area
Listing's law. 4 7 7 - 7 8
consequcnccs o f, l£ £ i
dem onstration o f, 4 7 b f
eye movement* according to . 4 7 7 - 8 0
mechanism o l, 4 7 9 - 80
modified, i 3 .
test o f, 4 78/
Litrings p h n c. i7~
L in n ^ io n c . Margaret. 27fy
Lizards, parietal eye of. L l L
L O C . S ee Lateral occipital cortex
Local cod ing, l o l l
Local properties, 12K
L ocal sign. 115.
Local spectral reverse correlation, 11a.
Location-based attention.
Locus coeruleus, I o l l 12JL
Logarithm ic functions, linear systems
and. I l l
Longitudinal chrom anc aberration*, u l Z
4 37/
Long-term depression ( L T D ).l i i * 3 4 9
I icbbian synapse a n d .l l l l
presynaptic processes in. 3 5 4 - 5 5
Long-term potentiation (L T I>), 1 5 2 - 5 3 .
3 3 8 - 3 9 ,3 4 9
I Jcbbiao synapse a n d .lS ll
prcsynaptic processes in, ^ 5 4 -5 5
L o th a rin j;ia .2 l
Low-pass system, .Ш 1
LTD . S te Long-term depression
L T P S t * Long-fern* potentiation
Lumicrc. Auguste.
Lutrocre, L o u is ilU
Lum inance. * 5 # - 5 9
Luncburg, Rudolf, 1 9 3 -9 4
L V O R . S t* Linear V O R
Lyceum. 1 1
Lvsosonics, i l l
M acroglia,
M ad do w o d rest. aiJC
M .idd»s « v in g t c s t .iS 2 .4 8 y
M A G , ДО.
M agcnd k. Francois.o il
M agic lantern, 7 5 - 7 6
Magnesium ions. 1SH
M agnetic resonance imaging (M R ]),
2 3 5 -3 6
M a gn ctocn с cp halogr aphy, 21a.
M agnocellular system, 1 1 1
Magnus. A lbcrtus. ДЯ
M aim oniJes, 1 ±
M am sequence. 513
M akbranch c, N icholas, 15,
M alleti te s t,4 8 8
M alpighi. M arcello.
Mapmaking, perspective development
through, 4 8 - 4 9
Masaccio. 5 2 - 5 3 . 5 ^ '
M dtbcm A iike s y n d tx u (Ptolem y). 1 4 - 3 5
M.itri \com position, H Z
1 1 2 -1 3 , Matthtesxen ratio, IQ u . 4 4 6
M aunsell, Jo h n . 288/
M a x e l l . Jam es C lerk . Ц
M axwellian viewing system. 4 4 8
M cells. 2 1 2 - 1 3
M -concs. 2 0 7 - 8 . 2 08/
M edial intrjparietal cortex (M IP ), l i i l
M edial longitudinal fasciculus (M L F ), 545
nucleus o K lu X
M edial superior tem poral area (M S T ),
IliLlal
dorsal pathway and , 2 9 0 -9 1
M edial tem poral lobe. 2 8 6 - 8 7
Median plane, ii
M edicine, in medieval Europe, 2 4 - 2 7
Medieval Europe
m edicine in. 2 4 - 2 7
optics in, 2 b
science and technology history in. 2 4 - 2 7
trivium and quadrivium in. 2 ±
M elanopsin. 2 1 1
Memory, Renaissance and. 2 k
M cn a cc h m u v .ll
M eridional afoeal lens, j 2 2
M eridional amblyopia. ^±212
M eridional anisometropia, 469
Mesenccphalic reticular form ation (M RF),
i l l . 54 5 - 4 6
Messenger R N A (m R N A ), ? а З ,Л .Ч
con c growth and. i l l
M ctabotropic glutamate receptors
(m G luR s). 3 5 9
M ctabotropic ligand-gated synapses,
2 4 4 -4 5
M ctabotropic receptors. 152.
M ctabotropic synapses, 1 61
M etam eric sensory systems. I l l
M etam eric s n m iih t s .iiii.l- a l
Metamerism
cause o l. l i i L
detecting, —C .
tunneling and. 1412
imiltiple-ehannel system and, 1 1 2
sensory coding and, 141 - 4 2
Mctaplast icily, 359
M erer angles, 4 8 1- 8 2
M ethod o f adjustm ent. Sia.
M ethod o f constant stim uli. У4.
M ethod o f equivalent n o tfe ,4 2 d
M ethod o f limits, 2_L
M c th y la r io n .lll
M cyncrt cells. 2 2 1
mCihtR*. S t* M eeabo tropic ghiranurc
receptors
M к he Ison contrast, l i i £ . 1 0 б £ п 1 £
M krofilam ents. 2 1 1
M icroglia, 2лИ
M kroiontophorcsis. 2 1 1
M icro RN A s (m iR N A s). 1 2 1
po sttron script ional control o t,l& 2
Microscopy. 2 3 0 -3 1
Mierostrabismus, U L l
M k ro tro p ta .-iill
M icrotubulcs. U S .
M iildlc Eofct,China trade w ith .lU
M >Jdle temporal area (M T ).22£L
dorsal pathways and. 2 8 8 - 9 0
M kIfrontal plane,£
M idget bipolar?, 2 i&
Msdtransverse plane, ia
M iles, Frederick Albert. 503/*
M iniature postsynaptic potentials. I l l
M inkowski. Miccxyslaw. o l
Minvky spiral. 122/’
M l P. S ee M edial intrapaneral cortex
m iRN A s. S e t M icroRN A s
M irror im age,enanbom orphs and .lK &
M irror stereoscope, £И .8(у
Mirror-symmetric pattern. l.V i. 1 1 7 /
M itchell. D onaU E ..4 1 7 /
M itoc h o n d ria .2 2 2
M laminae, 2 1 1
M LF. S ee M edial longitudinal fasciculus
Ш Ы т n c t .1 2 i l .l 2 0 /
M obi us strip. 1 2 2 /
Modal com pletion, l i i i
M odulation transfer function (M T F ).
1 0 6 -7
image quality and, 4 3 9 - 4 0 . \Ji 0 /
Mohammed (P ro p h et),211
M olecular clutch mechanism. *28
M olyneux. W illiam , la .
M olyneux s question, I^l l
Monkeys. S ee л I * / VI
critical period in. i l l
I T in O k ! W orld, 2 8 4 ~ 8 5
ocular dom inance colum ns in New
W orld, 2 7 7 - 7 8
M onochrom atic aberrations, 4 3 5 - 3 7
M onocsi L r eon nect kms, М 2
bL>ckage of. a l i i
M onocular deprivation, i
induction o f. »96
binocular deprivation compared to . *10*1
in cats, 4 0 0 -4 0 1
critical period and. 414
cross-modal innervation m ,M &
LG N an d .3 9 7 - 9 9
m primates. 4 0 5 - 6
retinal effects of. 3 9 6 - 9 7
subcortical effects of. 3 9 7 - 4 0 0
in subprimates, 4 0 0 - 4 0 5
superior colliculuv and. 3 9 9 - 4 0 0
M onocular diplopia, n i l
M onocular enucleation
anatom ical effects of, 4 0 7 - 8
visual etfects ot..uiiL
M onocular indcpcn Jc n c c . i l l
M onocular m otion, as vergence stimulus,
5 0 5 -6
M on o cu br occlusion, subprimates and,
4 0 2 -4
M onofixation syndrome, d £ l
M onopolar detectors, 13 2 - 3 3
Monovifion.anl
Morphogens. 1 2 1
cell differential ion anvi. 1 x 1
M otion
aftereffects, l o l
amblyopia and loss o f sensitivity o £ Д2&
coherence detector, l i i i
detection asymmetry, 4 2 8 - 2 9
induced visual, i l l
monocular, 5 0 5 - 6
perception o f. i
perception o l shape from . l&a.
sensitivity. 3 7 3 - 7 4
shape from, liLL
tparkitempora) tun ing to. 1 6 1
vcrgcncc induced by forw ard,1 1 1
M ountcastlc, Vernon В . 292/
M ovshon, Anthony. 21*11.
M R F. S ee M esenccphalk reticular
formation
M R L S e e M agnetic resonance imaging
m RN A . S et Messenger RNA
M scaling. 2 ^ 2
M•sequence, l l u .
M S T . S et Medial superior temporal area
M T . S ee M iddle tem poral area
M T F . S<e M odulation transfer function
M uller, H cinrich, 3 7 - 3 $
M il Her, Johannes, 1 1 . *i 3/
on horopter. 2 1
Mullcr-Lycr illusion,
M ulticuc judgement. H U
Mulricue systems. ^>r.r/eoCsies
averaging and, 1 7 1 -7 2
complement ars-, 1 2 ±
stability and. 1 2 1
stimulus equivalence in . I l l
trading and. 1 7 2 -7 3
types of. 1 7 0 -7 1
M ultidimensional scaling, L i l
MuIrimodal features. 2 £ 1
M ultiple-channcl system
channel hom ogeneity in, И 9
metamerism and. i l l
for secondary c o Jin g , 1 3 6 -3 9
tim ing functions o f, 1 3 8 - 3 9
M ultiplicative noise,l l H
Mulriplicativc nonlincaritics, 16lL
M ultistable percepts. S t t d lio Ambiguity
ambiguity and, 1 1 2 * V 77/
neural changes related to , 12iiL
types of. 1 2 2
M unk. 1 icrm ann. a il
Museum o f Alexandria, 1 1
Muybridge. Eadweard. 2H
M vcctom y.lU ii
Myelin, 1 1 1
Mvxipia. -Lio. 4 4 5/
empty field, : i H
Lite-onset, a l i .
night, i i i a
Mxvtpk eye, 00-1,445/
M ystetium 0>т <ф лрЬиит (K epler), 1 1
M ysticbm
Alexandrian period, (ire cce a n d .iii
sn < irecce.i
Kepler on scicncc com paied to , 3 2 - 3 3
science and technology history and. 2 4
vision and, 1 - 2
Nasotemporal division. I l l
Nativivt theory. 1 1
Naur a m ethod, 222.
jY.iu d h ,рлтрЛЫ$%Ш х305/
Navigation. 1
N-cadherin. i l l
Near-triad response. SOU
Necker cube. 1 2 1
Neighboring inhibition hypothesis. 2 £ 1
N eocortex. 1 2 1
Nerve growth factor (N G F ). 3 3 1 - 3 2 , - a l l
Nerve imp\ilsc, in sensory coding. 1 3 0 -3 1
Nervous system
detailed structure of, 3 6 - 3 9
development of, 3 2 1 - 2 3
ncurogcnciisand repair in, 1 1 1
Nested sensory systems. 1 6 8 -7 0
Nestorians. 1 8 -1 9
NiTiin.-1.growth facror.ULL
Nerrins, 1 1 L
Nesiral ablation, 2 1 4
Neural activity
controlling, 2 3 6 - 3 7
spontaneous, д1 1
Nesiral anitcikonta. 4 6 9
Neural cre*r cells. I l l
Neural spikes
adapt.it>on and discrim inability of,
n cu rom ctrk function of. 1 4 5 - 4 6
Neural spikes (лш/ n iW )
г с р о л к variability o f .i a i i
tempo ral cod mg o ( 14 5 - 4 6
NciiTobliso,Ш
Ncu/ofi laments, 2 s?
Ncurateflcnt, X2li
Ncuroligins, L15.
Neuro metric function, t i l
o f neural spikes, 1 4 5 - 4 6
N ew » m od ubto i s 1 *2
cortical plasticit v and. -113-14
Neuronа I migration, 1 1 1
Neuron theory, iS .
Ncurophysio logical procedures, 2 2 9 - 3 7
N cu ro p ilin .H L
Nesiro transm itters, 2*1 0 -4 6 ,2 А 1 /-1 4 2 /,
241/
N curotrophins, i l l . 3 3 1 - 3 2
c o r tk a l plasticity and, 4 1 1 - 1 3
development of, 349
ocular dom inance colum ns and
com petition for, 3 6 3 - 6 5
Newton. Isaac, U5.71/’
o n binocular vision, 7 0 -7 1
N ew ron-M ulkr-Giuldcn Lit»', 2 1 1
NGR Nerve growth factor
N ight myopia, o i l
Nisei m ethod, 21iL
N-mcihyl-D-avpartatc (N M D A ), l i i
N onconcom itant strabism us
N oneoncom hant vcrgcncc, 4 9 5 - 9 6
N o n d cp rivcd eve, 4 0 4 - 5
Nonius procedure
for cyclovcrgencc, 5 2 7 - 2 8
for fixation disparity. 489
N onlinear systems
analysts of, 1 1 3 - 1 4
cross-m odulabon products in.JJL L
dynamics of. i l k
N onlinear visual processes. 15 9 -6 1
Nonmirror-symmctric pattern, 2 2 4 .
2 2 7/ -228/
N ontopographic sensory inputs, 1 3 5 - 3 6
N orcia. A nthony М ., 3 & 9 /
Norepinephrine, L lh
N orm , l o l .
discrimination and. 1 0 3 - 4
Normalization
response, L iS .
sensory coding and. L A
tik lu i.
N otch K m
N otch/Delta system, 3 4 8 - 4 9
N K L 359
N R l . 359
N R 1 359
N r - C A M .3 1 7 -1 8
N R T P. S e t N ik leu* reticularis tegmcnt*
pontis
U b L 3 3 i-3 im a s i
M ^ l3 3 1 -3 2
N T -5 . 3 3 1 - 3 2
N ucko*>m e, l l u
Nucleus o f M cyncrt, l a 5 . 2UX.
N o ck m reticularis tcgm cnti ponds
(N R T I ? ) .& l O p tical aniseikonia. 469
N um b protein, JLL&
Nyquist diagram, i l l
Nyquist lim it. IL eI
aliasing and, 4 4 1 - 4 3 .
O bject-based attention, 1 9 6 -9 7
O b je ct blur, 4 3 6 - 3 7 .4 5 3
adaptation to .a tili
O bjectivc-coupled planar illumination
microscopy, H I
O bjective optom etry. o a il
O b jc c t structure, 18<1—81
Obir.|uc effect. 1 5 2
O bserver likelihood function, L L1
Obsec set prior. I I l l
Observer's scimulus domain (O D ) . L La
O cclusion dbparity, L i
O cu lar dom inance colum ns. 2 7 0
dark reading and, L I S
dichoptic interactions a m i.H Z
excitation and inbibirion balance in. iiaS.
in ferrets, 364
induct k>n o f, 3 6 6 - 6 7
mapping, 2 7 4 - 7 5
mode k o f development of. 3 6 5 - 6 6
neurotrophin com petition and. 3 6 3 - 6 5
in New W orld monkeys. 2 7 7 - 7 $
properties of. 2 7 5 - 7 6
scaling. 2 7 6 - 7 7
topology o f. 2~>
in V I . 2 7 4 - 7 5 , 2 7 4 / -2 7 5 /
O cu lom otor system
accom m odation in . 3 7 6 - 7 7
eye alignment and, 3 7 7 - 7 8
growth o f. 3 7 6 - 8 0
pupillary response in .I l l
pursuit eve movements and. 3 7 8 - 7 9
saccadic eye movements and. 379
vcrgcncc eye movements and, 3 7 9 - 8 0
l O D . S ee O bservers stim ulus domain
O d d-crror signal, ajS5.
O F P -b ip o L r cclls. 2 0 9 - 1 0
O F F -c e lb , I L L
O F F -cco tcr rcccptivc field s 2__L
O FF -rcgio ns, 2 4 6 - 4 7
O K N . S e e O ptokinetic nystagmus
O ligodendrocytes, ?-ifl Д1Я
O m nipausc neurons, S - i l
O N «bipolar veils, 2 0 9 - 1 0
O N -cells, I L L
O N -ccn ter receptive field s I L L
O ne-p oin t perspective, 5 5 - 5 6 . 57/’
O N -rcgions, 2 4 6 - 4 7
O pen-loop gain. 1 1 1 -1 2
O pen-loop vcrgcncc. 5 1 a . 5 1 4/ -515/
O perant conditioning, 1& & .387
O phthalm ology. Egyptian history of, ±
O p h tb alm otrop cs 1 2 1 .4 7 7 / '
Opponency, 143—44
O pticas)
o f accom m odation, 4 4 3 - 4 4
axis. 2111
cop.iUbL309/
development of, 3 2 - 3 5
fissure, m . 3 0 9 /
flow, i l l
I leron o f Alexandria o n . 1 ±
history of, i
K ep kr o n . 3 3 - 3 4
in medieval Europe, 1 £
physio logical, i i .
fad iat ions. I l l
stalk, iOSL 3 09/
term inology history of. i l
vcsiclc. 1 0 2 ,3 0 9 /
O p tica) anitophoria, i l L
O p tical imaging, o f brain, 2 3 2 -3 3
O ftiA s ( Newton), 7 0 -7 1
O p tic nerve,1 1 1
growth of. 3 1 3 - 1 5
structure of, 3 1 3 - J 4
O ffu o ru m I jh r iS e x (Aguilonius). & L
68/169/
Optics ( Euclid)» i l •I ^><4
O f m s (Ptolem y), 1 S. 62.63/ *
O p tic tracts. 112*222/ '
growth of. 3 1 3 - 1 5
structure of, 3 1 3 - 1 4
O p t о gene tics, 2 1 1
O ptokinetic nystagmus»(OKN). l.S2_
3 7 3 -7 4 , i l S
amblyopia and directional
preponderance o C i l S .
directional preponderance of. 4 8 4 - 8 5
L V O R and, 5 4 2 - 4 3
stability from. 1 1 ^
subcortical direction-selective
mechanism in. i l l
suppressing, 3 7 8 - 7 9
V O R supplemented by. v i 1
O ptom etry, 4 4 8 - 4 9
O rban, Guy, 2 9 0 /
O rbital layer o fe.strro cu iir muscle. I a 4
O rientation colu m n s H i i
O rientation discrim ination.am blyopia and,
4 2 3 -2 4
O rientation sensitivity, 3 7 2 - 7 3
O rientarion tuning
contrast independence and. 2 5 9 - 6 0
functions of. 2 5 7 - 5 8 , 257/
m echanisms of. 2 5 8 - 5 9
tem poral aspect* of. 25S?
in V I , 2 5 7 - 6 0
O n d v O rigin 0
/ Specie* (D a rw in ),l i l i
O rth o m ctric saccades, 538
O rthoph oria, £&&
O uter plexiform layer. 209
p 7 5 receptors, i l l
PacioJi. Luca. 5 3 - 5 4
P alin o p sij.iliia
Pamx/a. Ь а г г о Ь т с о .а й
Panoram as 1 2 . 78^-79/
Panoramic camera obscura,I S
Panums fusional area, fixation disparity
an d .4 9 I - 9 2
Paper, invention o f . i £
Pappus, lh .
Parallax grating, d i
Parallel alley.ilia .
Parallel processing, 1 6 1
Paramedian pontine reticular {urination
( P P R F ) .ili.5 4 5 .iil
Parameter estim ation by sequential testing
( P E S T ) ,2 £ l
Paresis, i o i i
Parietal c y c .J A i
Pa-ict al-rcae It region ( PR R ). l i l i
Parieto-occipital region. 2 8 7 - 8 8
Partial coherence mtcrtcrometrv (P C I),
ParviKcHular l a m i n a e .l l l
Parvoce llu Ur system, 1 L 1
Passive electrolocation. 5
Patch clamp procedure. I l l
Path integration,5
Payne. Bertram» 2 i y
Payoff matrix, ilu
P cclls. I L L
P C I. S et Partial coherence intcrfcrom ctry
Pedestal, stimulus on. 1 Щ
P ed ie lc.llL i
Pccpshow s 7 6 - 7 7 . 7 6 /
Perception. S ttd lw Depth perception
abilities of, 1
o f distance, 3 8 0 - 8 3
E m p e Jo ck s and theory o f, i l l
Ы m otion, 5.
procedures for studying development
o f shape from m otion.
ol shape from «hading. 385
o f 3-D form. 3 8 3 - 8 5
o f3 *D rotating shapes, 3?s4-85
Perceptive hvpcrcolumn. illX
PefCCpfwJ constancy,^. LLL
judgments and. l u i
stimulus covariance an d .iiali
Perceptual lievcriptive processes
causal scqucnccs, 1V0—VI
descriptive domains and, I КЗ- 8 5
equilibrium structures and. 1 8 9 - 9 0 . 190/
feature d ctcctor* and. L & l
ideal percctscr in, 1 8 5 - 8 6
perceptual judgement and. 1 8 3 -9 3
symbolic. 1 9 1 - 9 3
symm etry and. 1 8 7 - 8 9 . 188/-189/.' 189/
transformation and , 1 8 6 -8 7 ,
Perceptual judgement. a lia Judgem ent
categorization, scaling, identification
a n d .1 8 «
d etection, resolution, discrimination
a n d .1 8 2 - 8 3
percept uaJ descriptive procc*sc* and.
1 8 3 -9 3
types of, 1 8 2 -9 3
Perim eter system. £ 2 2
Pcrincuronal nets, 1 2 k
Permutation group. U JL
Persia. 1 8 -1 9
Pcrspcctira a r t ir ic ia lis il
Perspectiva naturalis. M .
Perspectiva p r a c t k a .i i
Pcrspcctise
A lberti s methods with, 5 3 - 5 4 , 5 1/
anam orphic art and. 51!.60/^61/ iiL
in ancient w orld, 4 7 - 4 9 , 4 ^ -4 9 / *
H runelkschis methods with, 5 1 - 5 2 .
5 1 / -5 У
camera obscura for, 5 8 - 5 9 . 59/
con rcrgcnt. 4 9 - 5 0 , 51/
da Vitwi and, 5 4 / 5 5 .1 2 .5 8 /
development o f responses to , 3 8 2 - 8 3 .
3 83/
devices for drawing in, 5 7 - 5 9 . 5 8 ^ 5 9 /
d e Vries's work o n , 5 5 - 5 6 , 56/
discovery of, 4 7 -6 1
di\tancc points and. 5 i L 5 i . 5
divergent, dSL 50/'
D u k /i work on. 5 ii
in 14tb century, 4 9 - 5 0 , 50/151/
G reece history w ith ,4 7 - 4 8 , 48/*
and roapmaking. 4 8 - 4 9
m athematics of, 5 6 - 5 7
one-point. 5 5 - 5 6 . Ь 7 /
Plato o n painting and. 5 1
in Renaissance. 51 - 5 7 . 51/-52Д 54/15 7 f
retinal image and. 5 1
three-point, 5 ^ . 57/'
trompe local a n d ,5 S .6 ( y
tw o-point, 5 6 .5 7 / '
with vanishing p o in ts 5 2 - 5 3
P ersp titiv t (de \’n cs). 5 5 . 56/
Perspcctivist tradition, 1.JL1-1U
Pcrspcctirity, 1 1 9 -2 0 , 120/
PEST. S « Parameter estim ation by
sequential testing
P ET .S t e Positr<»n*emission tomography
Pettigrew, ^ick. l a .
Petty. W illiam ,
Ph*M 4M 4gprM > Z L
Phantom fringes, alad.
Phase Bode p k » t . i i l
Phase b g
o f accom m odation, d ial
o f c>vJo vergence, 5 2 8 - 3 0 , 529/
o f vertical vcrgcncc. 515-^25/’
РКлъс* locked spectral analysis. 1 1 1 , 21a. P re fe re n tia l lo o k in g , l£ £ » 3 X 6 - К7 sealing procedure** in. iiZ. L O N . pn^pcrticsof. 2 1 X -2 0
Phaic sbilt. iilfc. Preferred d ire c tio n . I l l L signal detection pn^ccdures for. 9 6 - 9 7 orientation sensitisity o f.2 2 ll
Phase spectrum» i i i i Preferred o rie n ta tio n , 2 i l staircase m ethod tor, 9 5 - 9 6 spatiotemporal rcsp<inics of. 2 1 8 -2 0 ,
Phasic K nw rv. Д ± P re m o to r c o rte x . 2 9 5 -9 6 stimulus probes in . 9 7 - 9 8 219/
Pbenakistiscopr. Presbyopia. s ?6 tem poral thresholds an d .lU L Release r s . l i i l
Phenom enological analysts, 9 8 - 9 9 . 9Х/ accomm odation and. *i47 terms o f. 9 2 -9 -i Renaissance
Phoria Prcstriatc cortex» 22Д 2 A F C procedure in. 3 2 brain understanding in» ЗД
■IX4iK JAlivC, 4 8 8 Pre tectum . H I Ptolemy, 1 4 - 1 6 m em ory i n . l i
d a rk vc rg c n c c a n d , 4 8 7 - 8 8 Prcverbal stereo tests, 3 8 6 - 8 7 Alhaxcn on work о :,Ы perspective in. 5 1 - 5 7 . 51Л52/1
l i l At io n lii'p .in r y a n d . 4 9 0 -9 1 Pr*vosr. Pierre, 2 1 o n binocular disparities. ^ 1 M /-S7/
m c M u rc t of. 4 8 6 - 8 7 . 487/ Primary coding. 1 3 3 -3 6 o n binocular siskin. 6 2 - 6 6 , 63/ science and technology history in,
ty p « o f,i£ k labeled-line c o d in g 1 3 4 -3 5 o n corresponding visual lin<*>6 2 * 6 1 2 7 -2 9
vertical. I l l receptor-type coding. 1 3 5 -3 6 o n cyclopean axi\ .u S Representation, 1 8 3 -8 4
P h o rom ctcr.M Z o f stimulus intensity. 11a. o n cyclopean vision. 6 4 - 6 5 R c p u k i o n .i l !
Phosphorylation. 2 i 1 topographk cod ing. 1 horopter contusion o f, 6 5 - 6 6 Rerouting procedure. 308
Photo hllin g.22& Primary f c a t u r c s l l l o n light, IS . Resolution, 4 3 5 - 4 3
Pbotorccepcors, 3 0 3 - 4 secondary features compared to* 1 3 3 -3 4 o n refraction, 1 5 - 1 6 perceptual judgement and, 1 8 2 -8 3
Physiologic л I nyvu^mut, -a2il Primary stim uli. 1 2 X -2 9 Pulvinar. ? Ж ' Ш psychophysics and. 1 0 0 -1 0 1
Physio logical o p tic s 1 1 Primates. S a .r/w M onkeys; VI Pupillary response, 1 2 2 o f secondary features l i ! L
Pinwhccl patterns, 2 7 0 - 7 2 binocular vision in L G N of. 221 P u rk in jc .jo n .lZ o f stim uli» separation, 1 0 0 -1 0 1
Pitch. & m onocular deprivation in . 4 0 5 - 6 Purkinjc-imagc m ethod. ллИ s« idth.ilLLl
P U c < *lk 2 8 £ str abisoiut in , 4 0 5 - 6 Pursuic eye m o v e m e n ts ltiL >87 Response coding. I l l
P laminae, 2 1 2 Principle o f superposition. 1£l1 ocu lom otor system and, 3 7 8 - 7 9 Response dom ain. 9 2 - 9 3 . -LK1
Plasticity Principle o f time invariancc. i i i i Pyramidal cells. 2 3 8 - 3 9 . 238/ Response norm alization, l i f t . 256
blindness and cross-modal. 3 9 5 - 9 6 Principles o f figural organization, 1 Ш . I 8 1/ development o f .l^ X Response resonance. 21a.
branch-spikc. l l u Printing. 1$L temporal dynamics o f.2 S ii Rcsp-ansc specificity, dark reading and k«ss
com partm entalized dendritic. 3 5 5 - 5 6 PrUm in V i . 1 1 ^ ' o t; 3 9 2 - 9 3
cortical. 4 0 8 - 1 4 diopters. a £ l Pythagoras. I l l Retina
cspcricruc-dcpcndenr, 2 0 4 - 5 ГОПк vergence adaptation to , -1 9 2 -9 5 , .ihlation o f temporal,
I Jebbian synapse and. 3 5 0 - 5 2 49I f C^uadris ium , 2л. development of. 3 1 1 -1 3
hctcrosynaptic* 4 0 8 - 9 Probit analysis. 9 4 - 9 5 Q uantal efficiency. 1 L I m onocular dcpnsation and с fleets of,
hom eostatic, 355 Probsxs bundle, 3 4 6 - 4 7 (^uanti/ed signal. Щ 3 9 6 -9 7
hom osyiupcic, 4 0 8 - 9 Progenitor cells, U S . C^L'EST. C^uick estimate by sequential structure of. 2 il2
т с » Капi m * « I neural, 3 4 9 - 5 3 Projection testing Retinal image
m ctabotropk reccptors and. i l l colum ns. Г : 7 2 17/* Q uick estimate by sequential testing coding, i l l
spike tim ing-dependent, 1 1 1 .3 5 3 - 5 4 zonc,22d " ( Q U E S T ) .^ Euclid and. 1 1
o f v ifiu l fiin a io iu , 2 0 3 - 5 Projective geometry. 11 9 - 2 2 .1 2 0 / -122/" kical sign of. I l l
Plateau.Joseph, M7 1W Projcctivcly equivalent stim uli, i l l Radial bias.ISiL pcrspcctivc and nature of, 1 1
P U o ,1 4 .1 2 Pn>jecrivjty, 11 9 -2 0 ,1 2 0 ^ Rai nbow spite m . I l l R c tin J magnification error. U S .
o n perspective in p ain tin g .id. P r o n c u r o tr o p b iiis lll Rakic. Рдпко. 319/ Retinoid cycle, l l i i i
Platter, Felix. 1 1 Proportional control, 5 1 8 ,5 1 X/ R * m c ti.A g M m o .5 £ R c t in o ic o p y .iil
Pliny. 12. Proprioceptive rca& ren cc. lii& Ram on у Caial. Santiago, 3 8 - 3 9 Retraction bulb<.12ia
P lo tin u s i n Prosopagnosia, 2&1 Ramus. Peter. 2A Retractor lenris muscle. 4 4 5
Pecker stereoscope, h L i.K ’y ' Рпксиопх,Ш Rayleigh criterion, i l i i l Retrograde signaling system. 2 ^ 1
Point o f objective equality <P O L ). ± i Protein Reaching movements, accuracy ot» Retrograde transport, 112.
Point o fm b je td v c equality ( P S E ) .£ 1 к ina*CS 2 * 1 * 1 1 1 3 8 0 -S I Reverse correlation procedure» 2 3 3 - 3 4 ,
adaptive procedure and. i l l synthesis. 3 3 2 - 3 3 Reaching procedure. ittiL 2 6 1 -6 2
Point-spread function. l i l i L 4 3 8 - 3 9 tyrosine kinase receptors, i i i i Reaction tin ic .IllL Rcsersc ocular dom inance sKift. J i l l i
Poisson m odel. L iZ Protractor lent is muscle, 4 4 5 Reafference. 1 6 7 -6 X Reverse p itc h in g .a l l
Polar coordinate*, i l l Provioial accom m odation, 4 5 2 - 5 3 , 4 53/ Receiver operating characteristic (R O C ), Rhabdom erk re c e p to rs3 0 3 - 4
Polarity, 1 2 1 Proximal vcrgcncc, 4 9 7 - 9 9 ^ 9 If Rhaws,2a
Polat, U ri. 2 6 ^ * with con dieting disparity. 4 9 8 - 9 9 R cccp tisc Helds, 11a. Rhodopsin, 2QSL
Polyscnsory areas., li^L to coplanar italic stimuli. 4 9 7 - 9 8 o f cells in visual Cortcx, 2 4 6 - 4 8 , l< \ lf Rho G TPascs.
Pontifical c e ll S e t Grandm other cel К loom ing stim uli inducing, in ganglion e e lk 1 1 1 . Г l.L 214/ Rhopalium . l l l l
Pontine reticular f o r m a ti o n ,!^ P R R . S ft ParictaUrcAch region R cccptor*, 1 1 1 Riboso mcs, 2 1 Z H I
Pontine rcricular nu cleus 2£& P SE . S f f Point o ffu b p o iv c equality c ilia ry .3 0 3 -4 Ricco « law. 11a.
Population c o d in g 1.16.7SZ . i '± l Pseudoseope, 81 - 82 potential of. 11I2L RN A polymerase. H I
feature dctccti>n a iu L ia U Psychoanatomical procedures 1 2 1 o n presynaptic т с т Ь г а г к < .1 -ь 1 R ob o r c c c p t o R o u n d a b o u t receptors
Porterfield. W illiam , 1 5 . 2 1 Psychological cxophoria. nZh. rhabdomeric. 3 0 3 - 4 R O C . S ee Receiver operating characteristic
Positron-cmission tomography (P E T ). Psychoractric function, i l l . 9 5/ «(ructufc of. 2 0 7 - 9 , 208/' R o d s 1122
with Weihull function. £ 1 R ccep rofty p c coding. 1 3 5 - 3 6 term inak and synapses of. 2 1 i t 21 ( /
Posterior p ark tal cortcx, 2 9 1- 9 5 . l ± l f Psychophysical linking hypothesis, Receptor-type Labelcd-fanc cod in g .i l i a Ro hault, Jacq u es 1 1
Post*vnaptic Psychophysics Recipient гоп е,I l i a o n binocular vision, 2 L
activity blockage, a l i i basic m ethods o f, 9 4 - 9 5 R ecognition. i £ l visual pathway drawings of. 16.37/ *
density, 2 4 1 beginnings o f, 4 1 - 4 2 context a n d .lU U ,2 0 (/ R oll. 6
potential. H f l,- H i class A procedure i n . £ l Recruitm ent o f resourcce, 2 0 4 - 5 Rosenfield. M ark, n il/
P o M tn m cn p o o iu l control, 1 1 2 class В procedure in, £ ± Rectification. Rostral brainstem. 1 Л
Postulate o f unique parallel. 12u. detection and. 1ca. Rclraction Rostral superior tem poral cortex. 2iLL
Power spectral density Function. U S discrimination and . 101—4 Alhazen o n .2 2 Rou ndabou creceptors i 1V. H I ■ 549
Power spectrum analysis H a . double-nair^asc method for.3& Ptolemy o n , 1 5 -1 6 Rufus o f Ephesus. X b
Poz2o, Andrea. 5 1 . IK frames o f reference and.U il.99/’ Refractive am etrop ia.469
PPRF. S ee Paramedian pontine reticular illiwions an a lm s and, 9 9 - 1 0 0 RelrM tivc an isomet r«ipia, 4 6 9 Saccades, vergence intrusions and, 5 3 6 - 3 8
formation implicit phytic* and. 1 9 0 -9 1 RclarionAl judgem ent, i i i i Saccadic dr^metria. 538
Preattcntivc stage. phenomenological analysis in . 9 8 - 9 9 . Relay c e lls I L L S accad k cse movements, 3 7 9
Precision, iU 98/' arousal responses in, 2 2 u S.sddlc points, 2 2 i-
visual instrum ents. ± L resolution and. 1 0 0 - 101 inputs to . 1UL S a k a ta .H k k o .2 W /

SUBJECT INDEX • 661

Scale shift hfyothcsi*. 4 2 S Sensory c a n n in g , 1 4 7 - 4 8 Spatial undersauipling, 4 2 4 - 2 5 cyclovergence and visual. 5 3 0 - 3 3
Scaling Sensory systems Spatiotem poral Fourier transform , l i i l declination, £ 2 4
M sca lin g, 2 l £ higlvordcr. 1 6 2 - 8 2 Spatiotem poral transfer function, 1M depth o f field and eccen trk ity o f, 4 5 9
multidimensional, 1 4 i incidental stimulus covariance w ithin. Spatiotem poral tuning dichoptic, 1 7 4 17 6 /
ocular dom inance colum ns, 2 7 6 - 7 7 Ш. o f cortical cells. 261 - 6 3 dorsal pathway and effects of, 1
perce p tu a l ju d g e m e n t a n d . - X x ncvtc J . 1 6 8 -7 0 m odels of, 2 6 2 - 6 3 dynamic relationships becween. 145.
psychophysics and. i l l Separable responses. 1 4 iu 2 4 1 to m otion, 2 4 L h oritontal vcrgcncc and, 5 1 0 - 1 1 ,
sensory, I l i i Serial processing, 1 4 2 Specific nerve energies 1 3 4 - 3 5 5 ig / -5 1 1 /
synaptic. 3 5 5 , &L& Serotonin. 2 1 4 S p e cto ck s.2 2 inclination.
Scene Set theory. 1К* Sperry. Roger. 3 2 ^ * intcgfal. h O
semantics, JILL Shadowgraphs, 25.75/ Spherical aberrations. a j j , ••->>/' -пУЧ L G N and effects of, 3 0 0 -3 0 1
structure, 1 8 1 -8 2 Shape constancy. ± i Spherule, 21lL
Schaeffel, fran k , 4 $ 6 f development of, 3 8 3 - 8 4 Sphincter muscles, 4 4 7 on |>ederfal#i a i .
Scbcincr. С Ь п я о р Ь .З ^ .,^ / ’ Shape from m otion. liL L Spike tim ing-dependent plasticity (S T D P )» primary, 1 2 8 - 2 9
Schem ata. 1~N- l S i perception of, 3S-i 1 5 1 3 5 3 -5 4 primary coding for intensity of. 1 Vi
S ch ilk r. Pcrcr 11 . ?K7 Shape from shading, perception o t, 385 Spiking neurons.2a& proxim al vcrgcncc induced by loom ing,
Schuk/c, M ax, liL Sbaplcy, R obert, 2 1 3/ Spin, 4 . 7 f
Schwann. T h eo d o r . XZ Shatz, Carla J.. 3 1 4/ Spiny stellate cells. La& second-order.1 4 1 . 2 6 0 -6 1
Science and technology history Shccdy disparomctCT, 4 8 8 development of, selection of.1214
in A rabic empire, 2 0 - 2 4 Sherm an. Murray S., 43Q f Spurxheim ,Johann Ciaspard. sense organs and. 12 8 - 30
in C h in a. l i i Shifter circu it, S09 Stability sensory processing and. 1 6 2 -6 3
cm p iritttt'im iv i*! controversy in. 4 2 - 4 7 Shim ojo. Shinsukc, 371/' o f cyclovergence. 530 sefarablc, 1 6 2 -6 3
in K u io p c . 1 6 th a n d 1 7th ce n tu ry, 2 9 -3 6 Sight recovery, in humans, i i a . o f linear systems, 1 L 1 synchronized neural activity and tuning
in G re e c e .9 - IK Signal analysis multicue systems and. 1 1 1 o f. 1 4 9 -5 0
in In d ia . 1 £ b a s» functions for, O K N and. iZA. iransduccti.Ukli
o f kn scs and spcctacks, 2 2 convolution function and. 1 0 9 - 1 0 o f vcrgcncc. 5 0 8 - 1 0 undeterm ined. 1Ш.
in medieval Europe, 2 4 - 2 7 linear systems and, 1 0 9 -1 0 Staining procedures, 2 2 9 - 3 0 V I , contrasting concentric. 2 6 6 - 6 7
mysticism and. 2 4 Signal averaging. 1 1 4 - 1 5 .21a. for living cells. 1X L V ] . organization of. 1M .
in Persia. ±& Signal d etection, psychophysics and, Staircase m ethod, 9 5 - 9 6 V I , responses to aligned, 2 6 7 - 6 8
p c n p c c tn t discovery in. 4 7 - 6 1 9 6 -9 7 Static blur, sensitivity to difference in, V ] and eltects of. 3 0 0 -3 0 1
precise measurement and. 4 1 - 4 2 Signal-to-noisc ratio. 1 ift. 21 \ 4 5 5 -5 6 ventral pathway and effects of. 3 0 1 - 2
in Renaissance. 2 7 - 2 9 Silent eye, 2 1 4 S T D P. S ee Spike riming dependent fi>r vertical vergence. 5 2 2 - 2 4 , 523/’
visual ncuroscicncc beginnings in. Silent synapses, J S 1 plasticity visual attention and effects of. 3 0 0 - 3 0 2
3 6 -4 1 Similarity geometry, 1 1 8 -1 9 , 119 / Steady-state b ia s a 4 2 for V O R ,i U .
S-concs, 2 0 7 - 8 . 208/* Simulated emission depletion microscope S T E D . S re Sim uLtcd emission depletion Stimulus binding, synchronous Hringand,
5 D . S f* Stim ulus domain ( S T iD ) .m microscope 1 5 0 -5 1
Secondary coding. 1 3 6 -3 9 Singer, W olf. 4 0 " if Stein ccll*,Jk2ik Stimulus domain (S D ), 114.
m ultipk-channcl system Гог. 1 3 6 -3 9 Singularities. 2 7 0 -7 1 S tereo acu ity .! essential ambiguities o f . l l u
Secondary fcatu res..Lai..La4 Siretcanu, Ruxandra.400/' in a g c d .i£ & fully determ ined. 1 - Z
primary fcat\irc* compared to , 1 3 3 -3 4 S ix B toksm U gbt ,4wf S hade(da V inci). 2 !i amblyopia and. x i i Stim ulus equivalence in mulricue systems,
Second-ordcr stimuli» 1 4 1 * 2 6 0 -6 1 Sifcc c o n sta n cy .H development of, 3 8 6 - S 9 la l
Sellers, C olem an. Sill development ofc 382 Stcreofancascopc. №. Stimulus externalizAtion. 2Щ.
Sem antic nests.ULL Slant* 6 - 7 . 7/ Stereograms. £ l l JJ \ / Stim ulus probes. 9 7 - 9 8
Scniaphorins. -xli- Slits. ДД1-349 Srereophotography. 8 3 - 8 7 , 84/187/ Stimulus reparation. rcv.>huion ot.
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mapping. 2 5 0 -5 1 Visual neuroscience, beginnings. 3 6 - 4 1 Voltage-gated synapses,2 H W ren, Christopher.
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