CHAPTER 11

Attention: behavior and neural mechanisms

K E N N E T H M. HEILMAN Department of Neurology, University of Florida College of
Medicine, and Veterans Administration Medical
ROBERT T. WATSON Center, Gainesville, Florida
Department of Neurology, University of Florida
EDWARD VALENSTEIN College of Medicine, Gainesville, Florida
Laboratory of Sensorimotor Research, National Eye Institute,
MICHAEL E. GOLDBERG Bethesda, Maryland; and Department of Neurology,
Georgetown University School of Medicine, Washington, DC

CHAPTER CONTENTS through static on a radio. It can also select the location
of a certain stimulus. Physiologically, selective atten-
Behavioral Enhancement of Sensory Response as a Physiological tion describes excitability changes limited to some
Analogue of Attentional Processes subset of stimuli within a modality. The selection of
Arousal a stimulus in space (spatial attention) is related to the
Selective Attention
Relationships between selective attention and arousal final property, which is intention. Intention involves
Intention the preparation of the motor system to interact with
Frontal lobes the environment and has also been called activation
Centromedian-parafascicularis-frontocortical-thalamic reticular (113).
nucleus system
Catecholamine systems Arousal, selective attention, and intention may oc-
Hemispheric Asymmetries of Attention and Intention cur serially. To respond meaningfully to a stimulus,
Attention an organism must be aroused so that it can respond
Intention to the entire class of stimuli. It must then attend to a
Summary and Conclusions
specific stimulus, selecting it from the environment
for further processing. Finally, it may channel the
motor system to interact with the stimulus, activating
THE BRAIN RECEIVES more stimuli than it can fully the motor system through the process of intention.
process simultaneously. Some stimuli are of little or These processes can also be interactive. For example,
no importance; others are biologically significant. an aroused organism may become further aroused
Some important stimuli call for action; others do not. when presented with a highly significant stimulus.
Similarly the brain can simultaneously regulate only Organisms frequently attend to a novel stimulus
a limited number of behaviors. The mechanisms by because they have not yet determined its biological
which we prepare to process stimuli, focus on what to importance. Conversely, repeated presentations of a
process, and determine how far it will be processed nonsignificant stimulus will cause it to cease affecting
and whether it should call us to action we call atten- behavior. This waning of response is called habitua-
tion. tion. If the stimulus remains biologically significant,
To study the physiology of attention, we need defi- the organism will respond to it regardless of how often
nitions that can be experimentally tested. Attention it has been presented. Eventually, however, if the
is a complex psychological construct that includes stimulus becomes nonsignificant, the organism ceases
arousal, selective attention, and motor intention. Be- to respond to it; this loss of response to a previously
haviorally, arousal occupies a continuum that ranges significant stimulus is called extinction. A failure of
from the pathological state of coma, in which the the arousal or intentional processes can lead to the
organism may not respond to any stimulus, to the organisms not responding to the stimulus or neglect-
various degrees of waking. Physiologically, arousal ing it. A failure of the selective attentional process
describes the excitability of the nervous system (160). may lead to inappropriate distraction or to failure by
An organism can selectively process one or more prop- extinction.
erties of a complex stimulus, such as music coming Understanding the physiological bases of attention
461
462 HANDBOOK OF PHYSIOLOGY - T H E NERVOUS SYSTEM V
involves knowing which parts of the brain have the
property of altered excitability, under what circum-
stances their excitability is altered, and how that
altered responsiveness is expressed. Studying altera-
tions of excitability is not always sufficient, however,
because many psychological processes such as mem-
ory, perception, and cognition also may share these
properties. Therefore observations of altered behavior
associated with perturbations of specific areas of the
brain are needed to understand the physiology of
attention.
BEHAVIORAL E N H A N C E M E N T OF S E N S O R Y
R E S P O N S E AS A PHYSIOLOGICAL ANALOGUE OF
ATTENTIONAL PROCESSES
The electrophysiological approach to attention has
centered on examining the electrical activity of certain
brain structures and then studying how either manip-
ulating an animal's environment or manipulating an-
other part of the brain changes that neural activity.
The brain structures involved in generating visually
guided eye movements are the areas that have been
most exhaustingly analyzed. We discuss them here
because they not only illustrate the physiological ap-
proach to the problem but help to clarify the differ-
ences among arousal, selective attention, and inten-
tion.
Goldberg and Wurtz (49) first noticed that the
responses to visual stimuli of single neurons in the
superficial layers of the monkey superior colliculus
were affected both by the physical properties of the
stimulus and by the animal's reaction to the stimulus.
Taking recordings from monkeys trained to perform
visuomotor tasks, Goldberg and Wurtz (49) first
worked out the base-line visual properties of single
neurons in the superficial layers of the monkey supe-
rior colliculus and then showed that the responses
were enhanced when the monkey made a saccade to
the stimulus in the receptive field. In this experiment
the monkey was trained to look at a spot of light on a
tangent screen. While the monkey looked at that spot,
a second spot of light could be used to determine the
visual receptive field of the neuron. The monkey was
then trained to make a saccade to the stimulus when
it appeared in the receptive field. The cells responded
more briskly and regularly to the stimulus when the
monkey made a saccade. Conversely, removal of the
stimulus from the receptive field terminated the activ-
ity. The increased activity could not be due merely to
the act of the eye movement that swept the stimulus
across the receptive field, because much of the en-
hanced activity preceded the saccade. This enhance-
ment of the visual response could be due to many
factors, only one of which is attention to the stimulus.
For example, the activity could be confounded by a
motor discharge before the saccade, which is the case
for cells in the intermediate layers of the colliculus
(159) or in the frontal eye field (21). However, cells in
the superficial layers of the colliculus never discharge
before saccades in the absence of a visual stimulus
(49), although the activity of some cells is suppressed
around a saccade (123). The enhancement also could
be due to some general phenomenon associated with
performing a saccade. For example, the pupils dilate
before saccades and the effect could be greater lumi-
nous flux on the retina. Because it is easier for mon-
keys to perform a saccade task than a fixation task,
there may be a difference in arousal between the
saccade and the fixation tasks. Such factors would be
associated with any saccade, not only the saccade to
the stimulus in the receptive field.
To control for these general effects of a saccade, the
response of the neuron to the stimulus in the receptive
field was studied when the animal made a saccade to
a control stimulus that originated outside the receptive
field. If the enhancement were selective for the recep-
tive field of the neuron, it would be absent when the
animal makes a saccade elsewhere. Figure 1 illustrates
this experiment: A shows the response of the neuron
to the simultaneous onset of stimuli in the receptive
field, B shows the enhanced activity when the monkey
makes the saccade to the stimulus in the receptive
field, and C shows that the activity of the neuron was
not enhanced when the animal made the saccade to
CON
.I:;.-:-.
A . . . . . ... - ... . . . * ,. .'*;
.... ..-. ....
. I
. .. .. .. . .
1,
........ ... .. ..-.
-. . . .
I;..
.--"tL & A
~
B ......
--.. . .
l.-&-.
. --.
-.-. ...
I- ..
.....
I -;
..........
F
L *
........
.....
. .
.-.
..
*
.-. . . . . ." 1
:
I . ..- . .. --
. . ... ..... . . . .
.--
. . . . . . . . . .:.'..-
I
W
100 mrec
FIG. 1. Spatial selectivity of enhancement in monkey superior
colliculus. Top, cartoon illustrates receptive field of a collicular
neuron in relationto fovea.RF, stimulusin receptivefield of neuron.
Receptive field outlined by dashed line; FP, fixation point at which
monkey stars, CON, control stimulus outside receptive field. A
response of neuron as raster diagram and histogram to onset of
visual stimuli during a task in which animal looks at fixation point
and does not break gaze when the 2 other stimuli are flashed on
screen; B: enhanced response to appearance of stimulus when
monkey is going to make a saccade to RF,C: lack of enhancement
to appearance of both stimuli when monkey is going to make a
saccade to CON.[From Wurtz and Mohler (161).]
 CHAPTER 11: ATTENTION 463

A .-...._- ....
...._.. _.......
hancement in the monkey frontal eye field is also
._._.-...
. . . . ..........
I.

... saccade specific (Fig. 2).

... ............
--.. . .
. ..........
- .-_. ..........
..........
Evidence for behavioral enhancemqnt of visual re-
- .-...
.............
. . ......
..........
.-_ ..... sponsiveness can also be found in the striate cortex
.-_ .........
........ bI# 8r.k (162). Here, however, the enhancement occurs when-

p:
ever the monkey makes a saccade, whether or not the
B ......... .= . saccade is made into the receptive field of the neuron.
.-. ._ . It also occurs whether or not the stimulus is used as a
. .-._.
-.. - . -
... .. .-.. I target for a saccade or as a cue in the peripheral-
attention task. This global increase in the excitability
of the striate cortex under certain behavioral condi-
tions is consistent with an arousal process but is not
c ...... .%. . consistent with an attentional process, which must be
spatially selective. Figure 3 shows spatially nonselec-
tive enhancement of visual activity in the monkey
L&
striate cortex. It is not consistent with either a selec-
M tive attentional or an intentional process, because it
400 mrec is not specific to either the movement or the stimulus
selection. The striate cortex is a region subject to
FIG. 2. Saccade-related enhancement of visual responsiveness.
A: response of a single neuron in monkey frontal eye fields to onset arousal but not to the selective activation inherent in
of spot of light in its receptive field. Raster and histogram are attention; therefore any excitability changes that op-
synchronized on stimulus onset, signified by vertical line. B re- erate on the entire retinogeniculostriate system must
sponse of the neuron to same spot when monkey makes a saccade also be participating in general arousal mechanisms
to fixate stimulus. Raster and histogram are synchronized on stim- rather than selective attentional mechanisms.
ulus onset. C same trials synchronized on the eye movement.
Significant activity occurs before beginning of saccade. [From Gold- Enhancement also has been shown in the posterior
berg and Bushnell(47).] parietal cortex, area 7 (24, 120). In the parietal cortex

the stimulus outside the receptive field. By exclusion, CON

the enhancement had to be related not to the act of
making a saccade but to the act of making the specific
saccade to the stimulus in the receptive field. Such a
specific enhancement could be related either to the
selective attentional processes associated with choos-
ing that stimulus from the environment or to the FP
intentional processes associated with making the spe-
cific saccade.
To distinguish between selective attention and mo-
tor intention, it is necessary to study the activity of
the neuron in situations where the animal does not
make a saccade to the stimulus but must attend to it.
One such situation is a peripheral-attention task. The
monkey begins the task by looking at a central fixation
point. Another stimulus appears in the receptive field
of the neuron, which presumably does not include the
fovea; a few seconds later, either the small central

1 ?LJ
fixation point or the larger peripheral stimulus dims.
Because the animal must maintain gaze on the fixa-
. . . .. -

I
tion point to perceive its dimming and does not require . ...........
.......
-._-. ..... -.
the fovea to detect the dimming of the peripheral ----
--_-.__-..
.................. -,,,,
stimulus, it tends not to make a saccade to the periph- . '

eral stimulus. Because the animal responds to the L-.4J&

H
stimulus, it must have attended to it. In the superior 100 msec
colliculus the enhancement only occurs when the mon- FIG. 3. Spatially nonselective enhancement of visual activity in
key makes a saccade to the stimulus in the receptive monkey striate cortex. Top, cartoon illustrates location of receptive
field and not when the stimulus is used in the periph- field (RF) and control stimuli (CON) on the screen. FP, fixation
eral-attention task (161). Therefore the enhancement point at which monkey stares. A: cell's iesponse- to stimuli. B:
response when monkey makes a saccade to stimulus in RF. C
in the superior colliculus is specifically related to the response when monkey makes a saccade to CON. [From Wurtz and
act of making a saccade or to motor intention. En- Mohler (162).]
464 HANDBOOK OF PHYSIOLOGY - T H E NERVOUS SYSTEM V

the enhancement is spatially selective, occurring only activity is temporarily stopped 2) if an organism is at
when the monkey attends to the stimulus in the re- rest, muscle tone is increased 3 ) autonomic changes
ceptive field (24, 120). However, it is not movement occur (pupil dilation, increased sweating, peripheral
specific because it occurs when a monkey makes a vasoconstriction or dilation, and alterations in heart
saccade to the stimulus in the receptive field, uses it rate and respiration); and 4 ) sensory thresholds are
as a cue for a peripheral-attention task, or reaches out lowered (93). These general changes are all indepen-
and touches it without making a saccade to the stim- dent of the stimulus evoking the behavior and the
ulus. Figure 4 shows enhancement of a parietal neuron strategy of the specific response. They are the concom-
in saccade and peripheral-attention tasks. Because the itants of arousal.
enhanced signal occurred in association with any of Beck (lo), one of the cofounders of electroenceph-
the tasks examined, the signal could not be specific to alography, noted that a variety of sensory stimuli
any of the different motor strategies. Because the induced a decrease in rhythmic electroencephalogram
monkey attended to the stimulus in all of the cases, (EEG) oscillations. Berger (14) showed in human sub-
Robinson and co-workers (24,120)postulated that the jects that the EEG voltage decreased and frequency
enhancement was related to the processes underlying increased with sensory stimulation. He thought that
selective attention. sensory stimuli induced optimal excitability in areas
We use the results of the preceding group of exper- of the brain that were processing the stimulus, whereas
iments as guidelines for our discussion of the processes the remainder of the cortex was in a state of decreased
involved in attention. Here arousal refers to an in- excitability. Berger also thought that the associated
crease in responsiveness that occurs across an entire reduced voltage of the EEG reflected inhibition and
modality under a given behavioral situation. Selective deactivation. Adrian and Matthews (l),however, sug-
attention refers to an increase in excitability limited gested that the changes in the rhythmic activity de-
to a subset within a modality, e.g., a part of visual pend on the attention to the stimulus.
space. Selective attention must therefore be indepen- Moruzzi and Magoun (101) revolutionized thinking
dent of the behavioral strategy used to deal with the about the process of EEG activation by showing that
attended stimulus. Intention refers more narrowly to electrical stimulation of the reticular formation of the
the response: increased excitability in an intentional mesencephalon in animals would evoke EEG desyn-
system must be limited to the case in which the animal chronization similar to that occurring during natural
deals with the stimulus with one movement but not arousal. Bilateral lesions of the mesencephalic retic-
another. ular formation induced the opposite of arousal, coma.
This was the first demonstration that a seemingly
nonspecific brain area could affect the way the brain
AROUSAL interacted with its environment. The results were used
to explain both arousal and the maintenance of the
When an organism is presented with a novel or waking state.
significant stimulus, it aligns its sensory organs (e.g., During the last 30 years the activating theory has
eyes and ears) with the source of the stimulus. Pavlov received growing criticism. The first problems occur
first called this response the investigating or what in the dissociation of behavior and low-voltage fast
is it? reaction. This orienting response is associated EEG activity. Although low-voltage fast EEG rhythms
with many specific physiological correlates: I ) ongoing usually signal alert wakefulness, they can occur with

FIG. 4. Task-independent, spatially selective enhancement of visual activity in monkey posterior

parietal cortex. A: response to visual stimulus by a parietal neuron when monkey does not have to
respond to stimulus. B: response of same neuron to same stimulus when monkey makes a saccade to
stimulus. C: response of same neuron to same stimulus when monkey attends to but does not make
a saccade to stimulus. Vertical lines, onset of stimulus. [From Bushnell et al. (24).]
 CHAPTER 11: ATTENTION 465

coma (90). Slowing of EEG rhythms usually indicates
decreased arousal. However, atropine induces EEG
slowing without particularly affecting behavior (147).
Evidence is also accumulating that much of the retic-
ular formation has a specific motor function. For
example, the saccade generators for the oculomotor
system are located in the parapontine reticular for-
mation (26) for horizontal saccades and the mesen-
cephalic reticular formation for vertical saccades (83).
Siegel (131) has shown that activity in most pontine
reticular formation neurons can be correlated with the
movement of specific muscles and that specific pairs
of neurons seem to have significant autocorrelation
with each other as well as with movement. Siegel et
al. (133; 134) recently found some behavioral or move-
ment correlation for 95% of the 300 neurons studied.
The arousal and motor functions of the reticular
formation may not be exclusive. When an animal is
in an active state, cortical processing and motor be-
havior both increase. If a by-product of increased
motor activity is increased tonic activation of cortical
sensory or analytic systems, the cortex will function
more efficiently to provide information to the motor
system. Biologically the cortical analytic systems
evolved later than the reticular motor systems; thus
an ascending copy of reticular motor efferent signals
may have assumed the function of arousing the cortex.
This would enable a neuron with a specific motor
signal to function also as a nonspecific tonic activator
of ascending processes (131).
Growing evidence indicates, as Moruzzi and Ma-
goun (101) predicted, that the mesencephalic reticular
formation can affect visual function so as to augment
the excitability of neurons to their natural stimula-
tion. The intensity of gross visual potentials in the
lateral geniculate body of the monkey is increased by
electrical stimulation of the mesencephalic reticular
formation (33); this facilitation is most effective when
the monkey is drowsy. When the monkey is alert,
reticular stimulation has little effect (6),which sug-
gests that the mesencephalic reticular formation
arouses the visual system. If the system is already
aroused, further stimulation is ineffective. Similar fa-
cilitation was also seen in the responses of single
neurons in the monkey striate cortex [Fig. 5; @)I.
Singer (135,136) studied intracellular recordings from
the lateral geniculate of the cat and noted that bursts
of inhibitory postsynaptic potentials (IPSPs) synchro-
nized with slow waves in the EEG. The same mesen-
cephalic stimulation that desynchronized the slow
waves obliterated the IPSPs, an effect that would
allow more effective transmission of visual informa-
tion through the lateral geniculate nucleus. Because
the IPSPs inherent in the visual lateral inhibitory

t STROBOTRON 1
c LOCAL FLASH ON

L L STROBOTRON+MRF

MRF

50 100 150
.B
1 OT

'MRF~
I 1 I
.5 1
I 1

10 20 30
MSEC SEC
FIG. 5. Effect of mesencephalic stimulation on visual responsiveness of neurons in striate cortex.
Three neurons were studied; in each a visual or electrical stimulus of optic tract was presented.
Stimuli were presented alone and also paired with a mesencephalic reticular formation (MRF)
electrical stimulus presented 75 ms before. A: response of neuron to flash (strobotron), MRF
stimulation by flash after 75 ms (strobotron + MRF), and alone (MRF). B: response of another
neuron to optic tract (OT), combined (OT + MRF), and alone (MRF). C response of 3rd neuron to
onset of light (on), onset and MRF stimulation (on + MRF), disappearance of light (off), disappear-
ance combined with MRF (off + MRF), and alone (MRF). [From Bartlett and Doty (7).]
466 HANDBOOK OF PHYSIOLOGY - T H E NERVOUS SYSTEM V

process in the lateral geniculate were also affected by
mesencephalic reticular formation stimulation, Singer
postulated that another effect of mesencephalic retic-
ular formation was to sharpen visual processing by
the lateral geniculate. This suggestion was consistent
with the early observation by Godfraind and Meulders
(46) that mesencephalic reticular formation stimula-
tion increased the size of the excitatory center of
receptive fields in the lateral geniculate of the cat.
There have been several other examples of arousal
demonstrated in' cortical studies. Wurtz and Mohler
(161) showed that neurons in the striate cortex have
enhanced responses before saccades or in association
with a peripheral-attention task. The enhancement
was spatially nonselective and the phenomenon there-
fore related to arousal. Robinson and Fuchs (118)
showed a similar spatial nonselectivity of enhance-
ment for neurons in the prestriate cortex of the mon-
key. Motter and Mountcastle (102) found a similar
effect in the responsiveness of visually responsive or
light-sensitive neurons in the posterior parietal cortex.
They compared the response of these neurons to visual
stimuli when the animal was actively looking at a
fixation point with the response to the same stimuli
when the animal was not actively fixating. The act of
fixation was responsible for a significant increase in
the visual excitability of the neurons (Fig. 6), although
the animal did not respond to the peripheral stimulus
and may not have even been attending to it. This was
not merely a visual interaction with the fixation tar-
get, because if the central fixation target disappeared
for a brief time during active fixation, the increased
excitability of the cell persisted.
There are two separate pathways by which mesen-

NO-TASK MODE TASK MODE A TASK MODE B

I I I I 1 1
I I 111 1 1 I I I 1
I 8 II am I I I
11 I I I1 I I1 1 1
111 I II I I
1 1 1 1 Ill a I I 1
I I Ill I

.!...!..
..
: :
: :

- ...
... ...
.. .. .... ..

FIG.6. Responses of parietal light-sensitive neuron to visual stimuli when monkey was alert but
not actively fixating, compared with those evoked by same stimulus when monkey was actively
fixating. Raster-histograms synchronized by onset of stimulus signified by vertical dotted lines. No-
task mode, monkey alert and resting. Task mode A, monkey fixating a spot of light. Task mode B,
monkey fixating where a spot had been, but for interval of stimulus presentation, fixation point
disappeared. Monkey nevertheless maintained fixation accurately, waiting for reappearance of fixa-
tion point. Black diamonds, bins in which response in no-task mode differs significantly from responses
in both task modes. Dotted lines above solid histograms, SEM for each bin. [From Mountcastle et al.
(1051.1

cephalic reticular activity can affect cortical sensory
processing. No direct connections have been satisfac-
torily demonstrated from the mesencephalic reticular
formation to the cerebral cortex (107, 124). Instead
the mesencephalic reticular formation projects to the
cortex in a widespread but specific fashion, relayed
through the medial thalamus. This has been studied
in the cat, in which Steriade and Glenn (140) showed
that neurons in the centralis lateralis-paracentralis
complex of the cat thalamus project to the ipsilateral
caudate nucleus or cerebral cortex and that 13% of
these cells could be excited monosynaptically from the
ipsilateral mesencephalic reticular formation. Because
of the technical problems involved in exciting all of
the mesencephalic reticular formation, 13%may be a
substantial underestimate. The thalamic projections
to caudate and cortex were quite specific: cells that
could be excited from the caudate could not be excited
from the cortex, and cells that could be excited from
the pericruciate cortex could not be excited from the
middle suprasylvian gyms. Thus different sensory sys-
tems can be facilitated independently by reticular
activation, the pericruciate region being a specific
somatosensory cortical association area (103) and the
middle suprasylvian cortex a visual association area
(110).
The second manner in which the mesencephalic
reticular formation can affect cortical activity is by
influencing the reticular nucleus of the thalamus. Di-
rect cholinergic projections from the mesencephalic
reticular formation to the reticular nucleus of the
thalamus have been demonstrated (11).Scheibel and
Scheibel(l27) first postulated, based on its structure,
that the reticular nucleus of the thalamus could inhibit
modality-specific thalamic nuclei. Waszak and Schlag
(152) noted that the reticular nucleus of the thalamus
had an alternating relationship with primary thalamic
nuclei: when the reticular nucleus discharged, it in-
hibited relay in other thalamic nuclei. Waszak and
Schlag (152) also showed that stimulation of the mes-
encephalic reticular formation in the cat inhibited
spontaneous activity in the reticular nucleus of the
thalamus. These findings suggest that the role of the
mesencephalic reticular formation on the reticular
nucleus of the thalamus is disinhibition.
Many neurons that ascend within the area of mes-
encephalic reticular formation and its environs are
monoaminergic. The locus coeruleus-norepinephrine
system projects diffusely to cortical structures.
Whereas the locus coeruleus originates in the pons,
the area of the mesencephalon stimulated by Moruzzi
and Magoun (101) contains ascending catecholamine
systems, especially norepinephrine. Although this nor-
epinephrine system would appear to be an ideal can-
didate to mediate cortical arousal (76), destruction of
most of the locus coeruleus does not greatly affect
behavioral arousal nor does it change EEG patterns
(71). Moruzzi and Magoun (101) demonstrated that
unilateral stimulation of the mesencephalic reticular-
CHAPTER 11: ATTENTION 467
activating system induced greater desynchronization
ipsilaterally than contralaterally. Unilateral lesions in
the region of the mesencephalic reticular formation
induce EEG and behavioral changes suggestive of
unilateral coma or neglect (117, 154). Conversely,
unilateral lesions of the locus coeruleus do not induce
similar behavioral or EEG changes (R. K. Deuel,
personal communication).
Although the dopaminergic system may be critical
in the intentional systems of the brain (see INTEN-
TION, p. 470), dopamine and serotonin do not appear
to be important transmitters in neural systems me-
diating arousal, because blockade of both synthesis
and receptors does not appear to affect EEG desyn-
chronization (122, 158).
The role of acetylcholine is more complex. Shute
and Lewis (130) described an ascending cholinergic
reticular formation. Stimulation of the midbrain mes-
encephalic reticular-activating system not only in-
duces the arousal response but also increases the rate
of acetylcholine released from the neocortex (78). Cho-
linergic agonists induce neocortical desynchroniza-
tion, and antagonists abolish desynchronization (19).
Unfortunately, however, although cholinergic blockers
such as atropine interfere with EEG desynchroniza-
tion, they do not visibly affect behavioral arousal.
Vanderwolf and Robinson (147) suggest that there
may be two types of cholinergic input to the neocortex,
only one of which is atropine sensitive.
SELECTIVE ATTENTION
Selective attention differs from arousal in that somc
members of a given class of stimuli are treated pref-
erentially by the organism. At the electrophysiological
level, this principle has been shown by the selective
enhancement of the response of sensory neurons to
their appropriate stimuli when that stimulus has some
biological significance for the animal's behavior. The
enhancement of visual responsiveness of visual neu-
rons in the monkey (see Fig. 4) was archetypical of
this phenomenon, which has been studied extensively
in the visual system and to some extent in the soma-
tosensory and auditory systems. In the visual system,
saccade-related enhancement has been demonstrated
in many areas: superior colliculus (49), striate cortex
(162), prestriate cortex (39, 118), posterior parietal
cortex (120, 163), frontal cortex (47, 99), substantia
nigra pars reticulata (64), and pulvinar (121).
The first suggestion that the posterior parietal cor-
tex might be related to attentional processes came
from observations that contralateral inattention de-
veloped in humans and monkeys after temporoparietal
lesions (28,57). Using electrophysiological techniques,
Hyvarinen and Poranen (69) and Lynch, Mountcastle,
and co-workers (92, 106) showed in monkeys that
neurons in area 7 discharged before visually guided
hand and eye movements to interesting stimuli.
468 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM
Mountcastle (104) postulated that those neurons were
involved in directing visual attention. The demonstra-
tion that parietal neurons showed task-independent
enhancement when the monkey attended to the stim-
ulus (24) confirmed the role of the posterior parietal
cortex in selective attentional processes.
The visual properties of neurons in area 7 have been
studied by Robinson et al. (120,122) and Mountcastle
and co-workers (102, 163). The cells have large recep-
tive fields, and although there is some ipsilateral rep-
resentation, more cells respond to contralateral visual
stimuli. Most cells respond better to large bright stim-
uli (120), whereas some seem to be tuned broadly for
specific directions of stimulus movements (93). Some
cells with receptive fields in both the ipsilateral and
contralateral hemifields have directional selectivities
for stimuli moving toward or away from the fovea
rather than in a selective direction for the whole field.
This property has been called opponent-vector orga-
nization (93). Cells expressing this property are likely
to discharge when the animal is moving either forward
or backward through a visual environment. Some vis-
ual cells have their activity gated by the direction of
gaze; a stimulus with a certain retinal position, even
the fovea, will evoke a response when the animal is
looking in one direction but not in another (93).These
cells do not appear to possess specificity for stimulus
orientation, shape, or color, and binocular interactions
do not play an important part in their properties.
These visual properties are precisely what one would
.expect for cells that mediate spatial visual attention.
The posterior parietal cortex is not an exclusively
visual area; it also shows somatosensory and auditory
activity (69, 120). Lesions in posterior parietal and
temporal cortex induce multimodal inattention (57)
in the monkey. Lesions in homologous regions in
humans also produce contralateral multimodal inat-
tention (56).
The activity in the parietal cortex can be viewed as
reflecting an association between visual, somatosen-
sory, and auditory information influenced by nonsen-
sory stimuli that modulate the sensory activity ac-
cording to the importance of the stimulus to the
animal. The nonsensory influence presumably would
be generated from the limbic system, which projects
strongly to the posterior parietal cortex. The anterior
cingulate cortex contains neurons that respond to
biologically significant stimuli and projects to the
posterior parietal cortex (108). In addition, cingulate
lesions in humans and monkeys produce contralateral
inattention (53, 153). These limbic connections may
provide an anatomical substrate by which motiva-
tional activity (such as biological needs, psychological
set, and long-term goals) can influence stimulus pro-
cessing (62). Such interactions between limbic and
sensory projections could produce the attention-re-
lated enhancement of visual responses that has been
demonstrated in the posterior parietal cortex.
Enhancement has also been demonstrated in the
v
somatosensory system. Dubner et al. (34) showed that
neurons in the medullary dorsal horn (trigeminal nu-
cleus caudalis) of the rhesus monkey have two types
of behavioral modulation in their responses. They
trained monkeys to respond differently to noxious
and to warm thermal stimuli. They also trained the
animals on a visual discrimination task and then
compared the response of wide-dynamic-range and
nociceptive-specific neurons with the thermal discrim-
ination task and with thermal stimuli presented as
irrelevant. As the difficulty of the task increased, the
responsiveness of the neurons to the somatosensory
discharge decreased. The same neurons gave an en-
hanced response in the thermal task. However, a
smaller percentage of the somatosensory neurons also
showed task-related responses, discharging in associ-
ation with trial initiation or with detection of a cue
relative to a reward, independent of the modality of
the cue. These task-related responses were not related
to any of the motor aspects of the task. Bushnell et
al. (23) showed that both enhanced and task-related
neurons can be driven antidromically by stimulation
in the thalamus near both the primary somatosensory
nucleus and the medial thalamic group. The results of
the experiments, however, do not clarify whether the
modifiability of sensory responses related more to an
arousal or to a selective attentional phenomenon. For
example, Hyvarinen et al. (70) showed that a few
neurons in the monkey primary somatosensory cortex
appeared to be affected by attentive behavior. These
cells augumented their response to the relevant stim-
uli. Although these results could be cited as an exam-
ple of selective attention, before the vibration a signal
light was turned on in front of the animal. The color
of the light indicated whether the stimulus was rele-
vant or irrelevant. According to Hyvarinen et al. (70),
this task produced nonspecific arousal because it in-
volved anticipation of the relevant stimulus. Such
cortical neural effects would probably be mediated by
the reticular system. The reticular system projects
strongly to the top layers of the cortex, the area where
Hyvarinen et al. (70) found the greatest percentage of
cells with an augmentation response.
In the auditory system, Hubel et al. (68) first ob-
served that neurons in the cat auditory cortex re-
sponded better to novel and interesting stimuli. Such
cells discharged more briskly whenever the cat seemed
to attend to auditory stimuli of interest, such as the
squeaking of a toy mouse or the scratching of finger-
nails on a nearby table. More recent systematic work
in awake monkeys has confirmed these observations.
Beaton and Miller (9) studied the responses of neurons
in the monkey auditory cortex when the animal
worked on a reaction-time task. They interspersed
relevant presentations of the stimulus with presenta-
tions of the same stimulus when it was irrelevant to
the task. Twenty-five percent of cells in auditory
cortex showed an enhancement on the task in which
the frequency of the stimulus was relevant for behav-

ior. In other experiments, Benson et al. (12) found a
mild enhancement of response in a task in which the
monkey had to discriminate between stimuli presented
to the left versus the right ear. Hocherman et al. (65),
also studying the problem, trained monkeys to respond
differentially to tone and noise stimuli, and then cued
the auditory stimulus with light cues. The monkeys
learned to anticipate the auditory stimulus. When the
investigators made the cue less reliable, the monkeys
responded as if they had predicted the auditory stim-
ulus cued by the light. Of neurons responding prefer-
entially to either of the stimuli, 50% enhanced their
activity when the monkeys predicted that the stimulus
was going to occur. In all of the experiments the
specificity of the responses made it unlikely that there
were significant differences in generalized arousal
levels during the task. However, in many of the ex-
periments, the auditory stimulus was cued. These cues
may have altered the behavioral state of the monkey
and thereby altered cellular excitability. It therefore
remains uncertain whether primary sensory cortex can
mediate selective attention (i.e., demonstrate an en-
hanced response to a significant stimulus in the ab-
sence of a cue) or whether these experiments exem-
plify focal activation or local arousal mediated by the
thalamic reticular nucleus, an action discussed in the
next section.
Relationships Between Selective Attention
and Arousal
Selective attention, arousal, and habituation are
closely related and interdependent processes. Sokolov
(139) proposed a neurological model incorporating
Pavlovian concepts of cortical function together with
the postulate that the reticular system may be critical
for mediating the arousal response. According to this
model, afferent stimuli are transmitted to the cortex
by the classic sensory pathways while afferent collat-
erals reach the reticular system. The cortex makes a
model of the stimulus characteristics. If the stimulus
is novel or of biological importance, the cortex induces
excitation of the reticular system and an arousal re-
sponse occurs. If the stimulus is not novel, or is
unimportant, an arousal response does not occur.
Primary sensory areas project to their association
areas, which in turn converge on polysensory areas
such as the superior temporal sulcus (111). Unimodal
association areas may also project directly to the cau-
dal inferior parietal lobule, or alternatively may reach
the inferior parietal lobule after synapse in polymodal
convergence areas (e.g., prefrontal cortex and around
both banks of the superior temporal sulcus) [Fig. 7;
(98)]. These polymodal areas also receive projections
from the cingulate gyms. According to Denny-Brown
and Banker (29), polymodal convergence areas may
also allow polymodal sensory synthesis. Polymodal
sensory synthesis may also be important in polymodal
modeling (detecting stimulus novelty) and together
CHAPTER 11: ATTENTION 469
with limbic input may be important for determining
significance (62, 156).
Support of the Sokolovian hypothesis comes from
physiological, anatomical, and ablation-behavior stud-
ies. One such experiment came from Segundo et al.
(129), who stimulated various portions of the cortex
and found that the parietotemporal region induced
reticular formation evoked potentials.
If an organism receives a lateralized novel stimulus,
it will orient to the side of the stimulus. Although the
organism will show a bilateral arousal response, there
are asymmetries. For example, visual stimuli pre-
sented to one side tend to block contralateral EEG a-
activity more than ipsilateral a-activity (1). Moruzzi
and Magoun (101) demonstrated with unilateral mes-
encephalic reticular-activating system stimulation
that the ipsilateral hemisphere showed greater desyn-
chronization than the contralateral hemisphere. Con-
versely, unilateral lesions of the mesencephalic retic-
ular-activating system induce a contralateral disorder
of attention with loss of the orienting reflex to contra-
lateral stimuli (as measured behaviorally and elec-
troencephalographically)but with relatively preserved
orienting to ipsilateral stimuli (117, 154). Unilateral
lesions in certain cortical regions in animals (56, 153)
and humans (28, 57) induce a similar defect. The
neocortical regions where unilateral lesions induce a
loss of the orienting reflex for contralateral stimuli
are similar to those that induce desynchronization
when stimulated (129). These cortical areas are similar
to those that induce evoked potentials in the mesen-
cephalic reticular-activating system when stimulated
(41) and include the dorsolateral frontal lobe and the
temporoparietal region.
The physiological and behavioral studies just de-
scribed provide evidence that reciprocal relationships
may exist between the mesencephalic reticular for-
mation and certain neocortical areas (Fig. 7). Not only
does the mesencephalic reticular formation influence
the activity of the cortex, but the activity of this
system may in turn be controlled by certain cortical
areas.
Nothing in the previously mentioned or other ex-
periments indicates the existence of a selective effect
on primary thalamic sensory relays that can select
less than a visual, auditory, or somatosensory hemi-
field. The ease with which spatial selectivity has been
demonstrated in the posterior parietal cortex (120)
contrasts with the inability to demonstrate it in pri-
mary sensory cortices such as striate (161) and so-
matosensory (69). If the thalamic gating of primary
sensory inputs were acting as a more sensitive selec-
tion mechanism, investigators should have seen evi-
dence for selective processing in the primary sensory
cortices that receive their only sensory inputs from
the thalamic relay nuclei.
Waszak and Schlag (152) demonstrated that stim-
ulation of the cortex excited the reticular nucleus of
the thalamus. Primary and associative sensory cor-
470 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM V

FIG. 7. Corticoreticular interactions: 1, polysynaptic reticulocortical pathways; 2, sensory trans-

mission; 3, association cortex projections; 4,unimodal projections to reticular nucleus of the thalamus
(NR); 5, sensory convergence to polymodal cortex; 6, supramodal cortex (inferior parietal lobule) and
limbic connections; 7, cortical arousal through mesencephalic reticular formation (MRF) and NR.
STS, superior temporal sulcus; VIS, visual; AUD, auditory; SOM, somatosensory; VPL, ventralis
posterolateralis; MG, medial geniculate; LG, lateral geniculate. [From Watson et al. (156).]

tices (e.g., area 5) send collateral projections to the
reticular nucleus while projecting to the thalamus
(112). When a stimulus is not novel and not biologi-
cally significant, these corticofugal projections to the
reticular nucleus of the thalamus (Fig. 7, pathway 4)
may mediate habituation by selectively influencing
thalamic relay. A study by Yingling and Skinner (165)
supports this capacity for selective control of sensory
input, revealing that stimulation of specific portions
of the reticular nucleus of the thalamus (e.g., lateral
geniculate, medial geniculate, or ventrobasal complex)
abolishes corresponding (visual, auditory, tactile) cor-
tically evoked responses. Jones (74), however, has
shown that dendrites of reticular nucleus neurons
branch extensively and concludes that this anatomical
configuration argues against any selectivity in the
nucleus. There has been no anatomical study trying
to identify a point-to-point anatomical relation of
specific cortical areas to specific portions of the retic-
ular nucleus. Such an analysis would be difficult be-
cause of the problems of present anatomical methods
in identifying terminal degeneration of collaterals
from fibers of passage and of problems in identifying
precisely the limits of the reticular nucleus of the
thalamus that relate to select thalamic nuclei.
In contrast with the unimodal association cortex,
which may project to specific parts of the reticular
nucleus of the thalamus and thereby gate sensory
input in one modality, multimodal convergence areas
may have a more general action on the reticular nu-
cleus.
According to the attentional model presented here,
a generalized arousal response may be mediated by
the mesencephalic reticular-activating system, which
influences the cortex either through a diffuse polysyn-
aptic pathway or by tonic inhibition of the reticular
nucleus of the thalamus. A localized orienting reaction
may be related to cortically mediated inhibition of
specific portions of the reticular nucleus.
INTENTION
Frontal Lobes
Intention refers to the brains preparation to initiate
and organize a movement; loss of this activation may
induce akinesia. Akinesia is the failure to respond to
a meaningful stimulus if the failure cannot be attrib-
uted to weakness (e.g., as induced by motor-unit dys-
function) or to inattention to a stimulus. For example,

monkeys with dorsolateral frontal lobe lesions in the
region of the arcuate sulcus fail to respond to stimuli
presented on the contralateral side (15,81,157). Sim-
ilar defects can be observed in humans (59).
Initially, investigators attributed failure of an ex-
perimental animal to respond to contralateral stimuli
to inattention or neglect (157). However, in most
testing paradigms, affected animals were required to
respond by either orienting to the stimulus or moving
the contralateral limbs to a contralateral stimulus.
Because the animals with frontal lobe lesions were not
weak, it was assumed that they had sensory neglect
when they failed to make the appropriate response. A
different interpretation came from altering the exper-
imental design. Monkeys were trained to use their left
hand to open a left door in response to a right-side
tactile stimulus and their right hand to open a right
door after a left-side tactile stimulus (154). The
trained animals then received a frontal arcuate lesion.
Subsequently, when the trained animals were given a
tactile stimulus on the normal side (ipsilateral to the
lesion) previously sufficient to elicit a response of the
arm in neglected hemispace, they often failed to re-
spond or they responded by opening the door ipsilat-
era1 to the lesion. These results cannot be explained
by postulating any sensory or perceptual abnormality
and are thought to reflect a defect in intention.
Suzuki and Azuma (141) recorded frontal unit ac-
tivity from monkeys trained to make a rapid key
release when a small spot on which they were fixating
dimmed. They found that many neurons in the pre-
frontal and periarcuate area increased their activity
during the gaze period when the monkeys were pre-
paring to release the key. These cells were unaffected
by stimulus parameters; their activity depended on
the behavioral state of the animal. For example, if the
animal was not prepared to release the key and the
release was delayed, the cells showed weak activation.
Furthermore, when a small model of an insect that
induced gaze was presented, activity of the cells did
not increase, which suggested that arousal and selec-
tive attention also could not account for their in-
creased activity. The activity of the neurons therefore
appeared to reflect intentional behavior: their activa-
tion was related to the preparation of the motor sys-
tem to respond to a meaningful stimulus.
Since the work of Ferrier (37), the frontal lobes
have been thought to possess an essential function in
oculomotor control. Robinson and Fuchs (118) stim-
ulated electrically the frontal eye fields and produced
saccades. Bizzi and Schiller (17, 18) studied single
cells in the frontal eye fields and found that most
frontal cells were silent before a spontaneous saccade.
These results suggested that the frontal lobes were
unimportant in the initiation of a saccade. More re-
cently, however, Goldberg and co-workers (21, 47)
obtained a different response when recording from
cells in the frontal eye fields in awake monkeys trained
to perform oculomotor tasks. They found three types
CHAPTER 11: ATTENTION 471
of presaccadic activity: visual, movement, and visual
movement. Forty percent of the cells had visual activ-
ity, and of this 40%,half showed an enhanced response
if the animals were going to make an eye movement
and fixate on the stimulus in the receptive field. If
there was a purposeful saccade without a visual target,
these cells did not discharge. Twenty percent of the
presaccadic neurons discharged before purposeful sac-
cades in total darkness. These movement cells all had
weak or absent visual responses. The remainder of
presaccadic neurons had both visual and movement
activity. When the monkeys could predict what sac-
cade had to be made, 20% of the movement and
visuomovement cells showed anticipatory activity.
That is, the cells responded before the onset of the
signal stimulus. As Bizzi and Schiller (17, 18) found,
spontaneous saccadic activity induced little activity in
these presaccadic neurons. Only purposeful or inten-
tional behavior induced maximal activation of these
cells.
Although the studies of Goldberg and co-workers
(21, 47) suggest that the frontal lobes have a role in
the preparation to make a saccade, the saccade-related
enhanced responses recorded in the frontal eye fields
are similar to those in the superficial layers of superior
colliculus (21, 48, 49). Schiller et al. (128) found that
unilateral frontal lobe lesions induce a decrease in
saccades to contralateral peripheral targets. However,
this function returned with time. Superior collicular
lesions also did not induce permanent saccadic defi-
cits. Combined frontal and superior collicular lesions
were required to induce permanent deficits. These are
parallel systems; one system seems able to function in
the absence of the other.
Several observations suggest that the frontal system
has a more important function in intention than the
collicular system. Unlike the presaccadic neurons in
the frontal lobe, where activity depends on intention,
the movement-related neurons in the intermediate
layers of the colliculus discharge before all saccades.
In addition, animals with frontal lesions have diffi-
culty with visual tasks that require sequencing of
saccades (159).
Guitton et al. (53) observed that patients with fron-
tal lobe lesions had difficulty making saccades away
from flashed stimuli. However, the patients often
looked toward the flashed stimuli before they looked
away, which suggested that the cortical system is
necessary to suppress the stimulus-bound saccade and
to fashion a saccade to the computed location (21).
According to this hypothesis, the frontal eye fields
exert an inhibitory effect on the colliculus. However,
if this inhibitory effect were direct, one would expect
to find cells in the frontal eye field that discharged
tonically and were suppressed during saccades, facili-
tating a release of inhibition. Such cells have not been
found. However, cells with high tonic activity sup-
pressed around saccades have been found in the sub-
stantia nigra pars reticulata that projects to the collic-
472 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM V
ulus with a GABAergic (y-aminobutyric acid) and
presumably inhibitory pathway (64). The frontal eye
fields could control this activity through their projec-
tions to the caudate nucleus, which in turn projects to
the substantia nigra. The results suggest that the
colliculus may be more responsible for the intentive
aspects of the more primitive orienting response to
novel stimuli. The frontal lobes are primarily respon-
sible for making saccades to learned targets, acting
both by providing targeting information directly and
by inhibiting, stimulus-bound collicular activity
through control of the nigral inhibitory system.
Knowledge of the connections of the frontal eye
field is important in understanding its possible con-
tribution in intention to act in response to multimodal
sensory and limbic inputs. This periarcuate region
possesses reciprocal connections with auditory, visual,
and somatesthetic association cortex (25) and has
been identified by evoked-potential studies as an area
of sensory convergence (16).
The periarcuate region also reciprocally connects
with the superior temporal sulcus, another site of
multimodal sensory convergence, and with the intra-
parietal sulcus, an area of somatosensory and visual
convergence. Connections also exist with the prear-
cuate cortex. Subcortically, the periarcuate cortex con-
nects reciprocally with the paralamellar portion of the
dorsomedial nucleus and the adjacent centromedian-
parafascicularis complex (2, 82). The prearcuate cor-
tex projects in a specific way to the intermediate layer
of the superior colliculus. The architecture of the
periarcuate region has a transitional pattern, standing
between that of the agranular motor cortex and the
granular prefrontal cortex. The paralamellar-centro-
median-parafascicularis complex also seems to disrupt
the parallel thalamic relationships of medial thalamus
with granular cortex and lateral thalamus with agran-
ular cortex. Projections to the mesencephalic reticular
core (85) as well as nonreciprocal projections to cau-
date also exist. The periarcuate region also receives
input from the limbic system, mainly from the anterior
cingulate gyrus (6).
In summary, the frontal lobe is connected with the
neocortical unimodal sensory association areas and
sensory convergence areas. These connections may
provide the frontal lobe with information about the
external stimuli that may call the organism to action.
The frontal lobe also is connected to the cingulate
gyrus, a part of the limbic system from which it may
derive motivational information. The frontal lobe con-
nections with the mesencephalic reticular-activating
system may be important in arousal. The frontal lobe
also has connections with the caudate and superior
colliculus and with a thalamic zone that will be dis-
cussed in the next section. The dorsolateral frontal
lobe appears to be an ideal candidate for mediating
the motor response to a stimulus the subject is attend-
ing because it connects with the sensory association
cortex, limbic cortex, reticular formation, basal gan-
glia, and superior colliculus.
Centromedian-Parafascicularis-Frontocortical-
Thalamic Reticular Nucleus System
Contralateral akinesia (an intentional defect) oc-
curs in monkeys after centromedian-parafascicularis
lesions (155), and an akinetic state (e.g., akinetic
mutism) follows bilateral centromedian-parafascicu-
laris lesions in humans (100). The centromedian nu-
cleus receives an input from the precentral cortex.
Proceeding rostrally from the precentral cortex to the
supplementary motor cortex and frontal eye field,
there are fewer projections to the centromedian and
more to the parafascicularis (2). Centromedian-para-
fascicularis also receives input from the globus palli-
dus (97), superior colliculus (84), ventrolateral thala-
mus, and mesencephalic reticular formation (107, 127,
150). The centromedian-parafascicularis complex
projects to the cerebral cortex (75), putamen (77, 97),
caudate (126, 127), and ventrolateral thalamus. The
anterior cingulate gyrus (area 24) interconnects with
the intralaminar nuclei. The anterior cingulate gyrus
also connects with ventral anterior and ventrolateral
thalamus and neostriatum (6, 149).
Centromedian-parafascicularis anatomic connec-
tions with the basal ganglia and premotor cortex sug-
gest that the region may be important in intentional
behavior (156). Low-frequency stimulation of the cen-
tromedian-parafascicularis at 6-12 Hz induces classic
cortical recruiting responses (72). This stimulation
activates the inhibitory reticular nucleus of the thal-
amus through a centromedian-parafascicularis-fron-
tocortical-thalamic reticular nucleus system (164).
Activation of the reticular nucleus of the thalamus
elicits inhibitory postsynaptic potentials in the ven-
trolateral thalamus, which in turn blocks ventrolateral
thalamus transmission to the cortex [Fig. 7, pathways
1, 2; (115)l. Transmission in the ventrolateral thala-
mus has been shown to be inversely proportional to
activity of the reticular nucleus of the thalamus (38).
High-frequency stimulation of the centromedian-
parafascicularis or mesencephalic reticular-activating
system induces inhibition of the reticular nucleus of
the thalamus, EEG desynchronization, and behavioral
arousal (101, 165). This indicates that the thalamic
reticular nucleus can be inhibited by either a mesen-
cephalic reticular-activating system-thalamic reticu-
lar nucleus system or a centromedian-parafascicu-
laris-frontocortical-thalamic reticular nucleus system
and suggests that these systems may independently
mediate some types of behavior.
Anticipation of a response to a meaningful stimulus
inhibits the reticular nucleus of the thalamus and a
negative surface potential over the frontal cortex
(165). This potential occurs if a stimulus has acquired
biological behavioral significance (151). Specifically,
 CHAPTER 11: ATTENTION 473

when a warning stimulus precedes a second stimulus loop, including arcuate gyrus (155), basal ganglia
that requires a motor response, a negative wave, called (146), ventrolateral thalamus (148), and centrome-
the contingent negative variation, appears between dian-parafascicularis (155), have induced a deficit in
the stimuli and is thought to reflect the presence of responding to multimodal sensory stimuli.
motivation, attention, or expectancy. Another nega-
tive potential appears over cortical regions just before Catecholamine Systems
movement and is called a readiness potential.
Skinner and Yingling (137) demonstrated, in a Most of the information relevant to the pharmacol-
conditional tone-shock expectancy paradigm, that ogy of intention comes from studies of animals with
both the frontal negative wave and the inhibition unilateral lesions of dopaminergic pathways originat-
of the reticular nucleus of the thalamus that is nor- ing in the pars compacta of the substantia nigra and
mally elicited by the tone were abolished by block- from the ventral tegmental area just medial to the
ing the centromedian-parafascicularis-frontocortical- substantia nigra. These fibers project to the neostria-
thalamic reticular nucleus system even though orient- tum (the nigrostriatal pathway), to limbic areas of the
ing persisted. Novel stimuli or rapid mesencephalic basal forebrain (nucleus accumbens septi and olfac-
reticular stimulation continued to inhibit the reticular tory tubercle-the mesolimbic pathway), and to the
nucleus of the thalamus. In an operant task involving cerebral cortex (frontal lobes and cingulate gyrus-
alternate bar press to produce reward, the centrome- the mesocortical pathway) (88, 89). These dopami-
dian-parafascicularis-frontocortical-thalamic reticu- nergic fibers course through the lateral hypothalamus.
lar nucleus loop was cooled to a degree sufficient to Bilateral lesions in the lateral hypothalamus in ani-
block cortical recruitment, which induced incorrect mals induce an akinetic state (142), whereas electrical
responses to the previously reinforced bar press (i.e., stimulation in this area reinforces ongoing behavior
perseveration) (138). Further cooling caused the ani- (27, 109). Rats with unilateral lesions of the lateral
mal to stop pressing the bar altogether. These behav- hypothalamus behave similarly to monkeys with dor-
ioral observations demonstrated that an appropriate solateral frontal lesions; they transiently circle toward
response to a meaningful stimulus in an aroused sub- the side of the lesion, but even after they have re-
ject requires an intact centromedian-parafascicularis- covered to the point where spontaneous activity ap-
frontocortical-thalamic reticular nucleus system. In pears symmetrical, they tend to turn toward the dam-
contrast, primitive behavioral orienting elicited by aged side when stimulated and fail to respond to
novel or noxious stimuli depends on an intact mes- sensory stimuli delivered to the contralateral side (96).
encephalic reticular-thalamic reticular nucleus sys- This unilateral neglect in the rat (a unilateral atten-
tem. Responding to basic survival stimuli (e.g., food tional or intentional disturbance or both) can be pro-
when hungry) may also depend on a mesencephalic duced by selectively damaging dopaminergic fibers
reticular-thalamic reticular nucleus system. with the neurotoxin 6-hydroxydopamine (89,95). The
Skinner and Yingling (138) interpreted their data 6-hydroxydopamine lesions in the lateral hypothala-
as supporting a role for the mesencephalic reticular- mus induce unilateral neglect, but kainic acid lesions,
thalamic reticular nucleus system in tonic arousal and which destroy cell bodies but not fibers of passage, do
the centromedian-parafascicularis-frontocortical-tha- not (52). Because of this, the neglect induced by lateral
lamic reticular nucleus system in attention. Find- hypothalamic lesions results from damage to dopa-
ings by Watson et al. (156) support the hypothe- minergic fibers passing through the lateral hypothal-
sized role of the mesencephalic reticular-thalamic re- amus. Damage to the same fibers closer to their site
ticular nucleus system in arousal but also suggest of origin in the mesencephalon causes the same syn-
that the centromedian-parafascicularis-frontocorti- drome (89,94). Brain sites where electrical stimulation
cal-thalamic reticular nucleus system prepares the reinforces ongoing behavior also correspond to por-
aroused organism to respond to a meaningful stimulus. tions of the ascending dopaminergic system (27).
The frontal periarcuate region and the thalamic It is not clear which of the ascending dopaminergic
zone around the ventrolateral, dorsal medial, and in- pathways is most important in mediating this behav-
tralaminar nuclei share some common anatomic fea- ior. Lesions in the mesolimbic system (olfactory tu-
tures. These include reciprocal connections with each bercle or nucleus accumbens) have been reported to
other as well as participation in a complex loop that cause neglect (541,but unilateral lesions of nucleus
extends from periarcuate cortex and centromedian- accumbens do not induce turning behavior in rats,
parafascicularis to caudate, centromedian-parafascic- even when they are given apomorphine (80).Marshall
ularis to putamen, motor cortex to putamen, putamen (94) has shown that the neglect induced in rats by
to globus pallidus, globus pallidus to centromedian- ventral tegmental 6-hydroxydopamine lesions is pro-
parafascicularis and ventrolateral thalamus, and cen- portional to the depletion of striatal dopamine con-
tromedian-parafascicularis and ventrolateral nucleus tent, although less prominent correlations were ob-
completing a loop back to premotor and motor cortex. served between neglect and dopamine depletion in the
Not surprisingly, damage to structures within this olfactory tubercle and nucleus accumbens. Selective
474 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM V
lesions of the mesocortical pathways have not been
accomplished however, rats with unilateral lesions in
the frontal cortex, which receives part of the mesocor-
tical dopaminergic projection, rotate in response to
amphetamines (7, 43).
The results of many pharmacological studies sup-
port the hypothesis that unilateral neglect induced by
substantia nigra or lateral hypothalamic lesions re-
sults from a unilaterally diminished dopaminergic sys-
tem. Animals with unilateral 6-hydroxydopamine or
electrolytic lesions in substantia nigra or lateral hy-
pothalamus, which cause degeneration of ascending
dopaminergic pathways, will turn toward their lesions
when given drugs that increase the release of dopa-
mine from dopaminergic nerve terminals (amphet-
amine, L-dopa), presumably because there are more
such terminals on the undamaged (contralateral) side
(143,145). Stimulation of the ascending dopaminergic
fibers (4) or the striatum (116) induces contralateral
turning. The density of dopamine receptors can be
estimated by taking advantage of the affinity of these
receptors for dopamine-blocking drugs. Using tritiated
spiroperidol, Heikkila et al. (55) showed an increase
in dopamine receptor density in the striatum ipsilat-
era1to a 6-hydroxydopamine lesion of the nigrostriatal
tract. Systemic administration of direct dopamine re-
ceptor agonists, such as apomorphine, induced turning
away from the side of the lesion in these animals (143,
145). This effect has been presumed to result from
receptor hypersensitivity or from increased numbers
of dopamine receptors on the side of the lesion and
can be blocked by prior administration of a dopamine-
blocking drug such as spiroperidol (144).
Additional evidence that dopaminergic systems are
important in turning behavior in rodents comes from
studies of rats without brain lesions. Normal rats have
a spontaneous preference for the direction of turning
that is correlated with asymmetries in striatal dopa-
mine concentrations; normal rats turn away from the
side of greater striatal dopamine concentrations (44).
Amphetamines increase this turning, whereas apo-
morphine may induce turning in the opposite direction
(73). These effects are blocked by dopamine-blocking
drugs such as haloperidol.
Although most studies have used rats, lesions that
probably involve the ascending dopaminergic system
have also induced unilateral neglect in cats (52) and
monkeys (31). In humans, bilateral degeneration of
the nigrostriatal tracts is associated with parkinson-
ism, in which hypokinesia is a major symptom.
Recent studies have revealed that neurons of the
ascending dopaminergic system are under complex
regulation: GABAergic fibers from the striatum pro-
vide feedback inhibition to the dopaminergic neurons
of the pars compacta of the substantia nigra (22).
Other striatonigral projections use the neurotransmit-
ter substance P (40). The terminals of dopaminergic
nigrostriatal neurons contain receptors for dopamine
(79) and GABA (42), each of which can thus poten-
tially affect dopamine release in the striatum. Dopa-
mine autoreceptors also reside on the cell bodies of
dopaminergic neurons in the substantia nigra (79).
Evidence suggests that dopamine is released not only
from dopaminergic axon terminals but also from den-
drites in the pars reticulata of the substantia nigra
(45). Furthermore there are at least two different
classes of dopamine receptors (79), each responsive to
a different range of agonist and antagonist drugs. The
behavioral effect of such drugs will depend on the type
and location of the dopamine receptor most affected.
For example, the dopamine agonist apomorphine
stimulates D2 receptors a t low concentrations. Low
doses of apomorphine may then reduce activity of the
striatonigral dopaminergic system by stimulating D2
autoreceptors on dopaminergic neurons (50). Higher
doses of apomorphine stimulate D, (adenylate cyclase-
associated) receptors, but even higher doses may in-
hibit them (79).
Glowinski et al. (45) demonstrated that the release
of dopamine from axon terminals in the striatum
correlates inversely with the release of dopamine from
dendrites of these same dopaminergic neurons in the
substantia nigra. Furthermore they showed an inverse
relationship between dopamine release in these two
locations on opposite sides of the brain: increased
dopamine release in the right striatum is associated
with decreased dopamine release in the right substan-
tia nigra and the left striatum and increased release
in the left substantia nigra.
Although the mechanisms are not completely un-
derstood, the behavioral and pharmacological data just
summarized indicate that the ascending dopaminergic
system (or a portion of it) is important for some aspect
of attention. Because 6-hydroxydopamine lesions in
the mesencephalon (substantia nigra and ventral teg-
mental area) or lateral hypothalamus induce hypoki-
nesia contralateral to the lesion, and because hypoki-
nesia is a prominent finding in animals with bilateral
lesions of the lateral hypothalamus and in humans
with Parkinsons disease (in which the substantia
nigra degenerates bilaterally), it can be postulated that
ascending dopaminergic pathways, the nigrostriatal
pathway in particular, are important in initiating
movement. The neglect induced by lateral hypothala-
mic or ventral tegmental lesions has been called sen-
sory neglect or inattention, However, when animals
are trained in the crossed response paradigm (turning
to the side opposite a sensory stimulus) and unilateral
neglect is induced, they continue responding to stimuli
delivered to the side opposite their lesion but fail to
turn to the opposite side when stimulated on the
normal side (67). As is the case in monkeys with
frontal arcuate or intralaminar thalamic lesions, this
apparent neglect is in fact a defect in intention to act,
which is due to lesions of the dopaminergic system
(36).
The ascending dopaminergic system has connec-
tions with other structures implicated in attention

and intention. The mesocortical fibers project to areas
in the frontal lobes (20), including the frontal arcuate
region and the anterior cingulate gyrus. Lesions of
these sites induce attentional and intentional disor-
ders (153, 154). Glutaminergic fibers from the cortex
project to the striatum (32). The mesolimbic and
nigrostriatal dopaminergic systems project to the nu-
cleus accumbens and the striatum, respectively, and
these areas in turn probably project through the globus
pallidus to the intralaminar nuclei of the thalamus
(97). The striatum also projects through the globus
pallidus to the ventral anterior and ventrolateral thal-
amus. The intralaminar nuclei also receiye input from
the substantia nigra (63) and have strong projections
to the striatum (51). The neurotransmitters of these
thalamostriatal connections are not known. We pro-
pose that the dopaminergic system, by virtue of its
indirect but strong connection with the motor nuclei
of the thalamus (ventral anterior thalamus, ventrolat-
eral thalamus), has considerable influence on motor
activity and that lesions of this system induce unilat-
eral akinesia.
HEMISPHERIC ASYMMETRIES OF ATTENTION
AND INTENTION
Attention
Many investigators have noted that in humans le-
sions of the right hemisphere induce more frequent
and severe attentional disorders than do lesions of the
left hemisphere (3, 35). Neglect in humans is most
often induced by temporoparietal lesions. This area
may contain structures homologous to the inferior
parietal lobe of monkeys and may contain attentional
effects that are similar to those in monkeys described
by Lynch (91) and Robinson et al. (120). The greater
incidence and severity of neglect from right hemi-
sphere lesions in humans could be explained if parietal
attentional cells or comparator neurons had asym-
metric receptive fields, so that the cells in the left
hemisphere were activated predominantly by novel or
significant stimuli in right hemispace and the cells on
the right side were activated by novel or significant
stimuli in both visual fields or in both sides of hemi-
space. With such an asymmetric distribution of recep-
tive fields, right hemisphere lesions would more often
cause inattention than would left hemisphere lesions
because the intact right can attend to ipsilateral stim-
uli after left hemisphere damage but the left hemi-
sphere cannot attend to ipsilateral stimuli after right-
side damage.
Sokolov (139) proposed that activation of cortical
comparator neurons may give rise to local EEG desyn-
chronization. If activation of comparator neurons in-
duces local desynchronization and the right hemi-
sphere is dominant for attention, the right hemisphere
should desynchronize to stimuli presented in either
CHAPTER 11: ATTENTION 475
field, whereas the left hemisphere should desynchron-
ize only to right-side stimuli.
In investigating Sokolovs suggestion, Heilman and
Van Den Abell(61) found that the EEG recorded from
the right parietal lobe desynchronized equally to right-
or left-side stimuli, whereas the left parietal lobe EEG
desynchronized mainly to right-side stimuli. These
observations support the hypothesis that the right
hemisphere (parietal lobe) dominates these compara-
tor, or attentional, processes. Rosen et al. (125), using
positron emission tomography, and Prohovnik et al.
(1 14), using regional cerebral blood flow, also found
that the right hemisphere is activated by left- and
right-side stimuli. These electrophysiological and iso-
tope studies provide evidence for the special role of
the right hemisphere in attention and help explain
why inattention may often be caused by right hemi-
sphere lesions.
As discussed previously, the temporoparietal region
may also be important in inducing an arousal re-
sponse. Heilman et al. (58) studied patients with right
or left temporoparietal lesions by stimulating the hand
ipsilateral to the lesion and recording galvanic skin
responses. The patients with right-side lesions re-
sponded poorly and those with left-side lesions re-
sponded well (58). We also compared the EEG record-
ings from the undamaged hemisphere of awake pa-
tients with right or left temporoparietal infarctions.
The patients with right-side lesions showed more 8-
and &activity over the undamaged hemisphere than
did the patients with left-side lesions (K. M. Heilman,
R. Gilmore, T. Van Den Abell, and R. T. Watson,
unpublished observations). These studies suggest that
the right hemisphere may have a special role in me-
diating the arousal response as well as in selective
attention.
Intention
In humans, a right parietal lesion sparing the sen-
sory motor cortex or its subcortical projections can be
associated with limb akinesia without other motor
defects (28). The hypokinesia, however, is not always
limited to the contralateral extremities. Although pa-
tients with cerebral lesions confined to a single hem-
isphere have slower reaction times with the hand
contralateral than with the hand ipsilateral to a lesion,
they also have slower reaction times with the ipsilat-
eral hand than normal subjects (13). Lawrence and
Kuypers (87) showed that there is ipsilateral as well
as contralateral motor control of an extremity. How-
ever, the ipsilateral control is limited mainly to the
proximal musculature. Because reaction times are per-
formed by distal musculature, the ipsilateral slowing
found by Benton and Joynt (13) cannot be completely
explained by a motor defect.
DeRenzi and Faglioni (30) and Howes and Boller
(66) used a simple reaction-time task to study patients
with unilateral cerebral lesions. Lesions of either hem-
476 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM V
isphere slowed the reaction times of the hand ipsilat-
era1 to the lesion, but right hemisphere lesions caused
greater slowing than left hemisphere lesions. In the
study by Howes and Boller (66), lesions of the right
hemisphere were not larger than those of the left, so
the hemispheric asymmetry in reaction time could not
be explained by lesion size, as had been previously
postulated.
Warning stimuli may prepare an organism for ac-
tion and thereby reduce reaction times (86). Pribram
and McGuinness (113) used the term activation to
define the physiological readiness to respond to envi-
ronmental stimuli.
Patients with right hemisphere lesions, especially
in the parietal area, have been shown to have reduced
behavioral evidence of activation (66), leading us to
postulate that the right hemisphere may dominate in
mediating the activation process in humans. That is,
the left hemisphere prepares the right extremities for
action and the right prepares both. As a result, in the
presence of nonmotor left hemisphere damage, right-
side limb akinesia is minimal, but left-side akinesia is
severe with right hemisphere lesions. In addition, be-
cause the right hemisphere is more involved than the
left in activating the right extremities, there will be
more ipsilateral hypokinesia with right than with left
hemisphere lesions.
Warning stimuli reduce reaction times (86). If the
right hemisphere dominates the mediation of activa-
tion or intention (physiological readiness to respond),
asymmetries in normal subjects should be discernible.
Heilman and Van Den Abell(60) gave normal subjects
warning stimuli in the right and left visual half-field
followed by stimuli to measure central reaction time.
Warning stimuli projected to the right hemisphere
reduced right-hand reaction times more than warning
stimuli to the left hemisphere reduced left-hand re-
action times. Furthermore warning stimuli projected
to the right hemisphere reduced reaction times of the
right hand even more than warning stimuli projected
directly to the left hemisphere. The results support
the hypothesis that the right hemisphere dominates
activation (60).
SUMMARY AND CONCLUSIONS
This chapter summarizes some advances in under-
standing how the brain mediates attention. Attention
is a complex psychological and physiological construct
that includes arousal, selective attention, and motor
intention. These processes may occur serially or inter-
actively. Physiologically, arousal describes the excit-
ability of the nervous system or portions of the nerv-
ous system. This excitability is not stimulus specific.
Physiologically, selective attention describes excita-
bility changes that are induced by only a subset of
stimuli. Intention refers to the preparation of the
motor systems to interact with the environment.
The physiological basis of attention has been stud-
ied using both ablative and electrophysiological para-
digms. Ablative studies have been used to determine
the areas of the brain critical for attentive function
and the nature of the attentive processes they may
mediate. The electrophysiological approach has cen-
tered on examining the electrical activity of certain
brain structures and learning how manipulation of the
environment changes neural activity.
Moruzzi and Magoun (101) indicated that the retic-
ular formation is critical in arousal. Although the
arousal-activating theory has received criticism, abla-
tive and electrophysiological studies continue to sup-
port the concept. For example, bilateral lesions of the
mesencephalic reticular formation induce coma (the
animals fail to respond to any stimuli) and unilateral
lesions induce a failure to respond to stimuli delivered
on the contralateral side. Stimulation of the mesen-
cephalic reticular formation augments the excitability
of neurons to natural stimuli, desynchronizes electro-
encephalographic slow waves, and obliterates IPSPs.
The mesencephalic reticular formation could affect
sensory processing by two means. No direct connec-
tions from the mesencephalic reticular formation to
the cortex have been demonstrated. Instead, the retic-
ular formation probably projects to the cortex through
relays in the medial thalamus. The mesencephalic
reticular formation may also affect cortical activity by
influencing the thalamic reticular nucleus. This nu-
cleus tonically inhibits thalamic relay nuclei. Stimu-
lation of the mesencephalic reticular formation ap-
pears to inhibit this inhibitory nucleus.
When a stimulus carries biological significance for
an animals behavior, it is treated preferentially by
the animal (selective attention). The first suggestion
that the posterior parietal region cortex may be related
to attentional processes came from observations of
humans and monkeys who had contralateral inatten-
tion from temporoparietal lesions. At electrophysio-
logical levels, selective attention is associated with
selective enhancement of the response of neurons to
an appropriate stimulus. The previously mentioned
investigators have found that certain parietal neurons
enhance their activity when monkeys attend to an
important stimulus. The parietal lobe of human beings
and monkeys not only receives polymodal input from
the association cortex but also receives limbic input,
and the parietal lobes have a close relationship with
the reticular system. These connections provide an
anatomic substrate by which motivation may influ-
ence stimulus processing.
Selective attention, arousal, and habituation are
closely related and interdependent processes that may
be mediated by a cortical limbic reticular-activating
system. Not only is this system important in mediat-
ing selective attention and arousal, but it may also be
important in intention. Intention refers to the prepa-
ration of the brain to initiate a movement. A loss of
intention induces akinesia, failure to respond to a

meaningful stimulus not attributable to either weak-
ness or inattention. Animals with dorsolateral frontal
lobe lesions have contralateral limb akinesia. Electro-
physiologically, the dorsolateral frontal cells appear
to regulate intentional activity because they increase
their activity when the animal is preparing to make a
movement. The dorsolateral frontal lobe has connec-
tions not only with sensory association areas including
the inferior parietal lobe but also with the limbic
cortex, reticular system, and basal ganglia. In addition,
the prefrontal dorsolateral frontal lobe possesses in-
timate connections with motor systems. These con-
nections appear ideally located for initiating and pro-
pa
gramming the motor res onse to an attended stimulus.
In -humans attention 1 and intentional disorders
accompany right more often than left hemisphere
lesions. The results of electroencephalographic and
positron emission tomographic studies support the
postulate that the right hemisphere is dominant for
attention. Unlike the left hemisphere, which attends
primarily to the right side of the body and right
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