SECTION IX

Eye–head–neck coordination
Progress in Brain Research, Vol. 143
ISSN 0079-6123
Copyright ß 2004 Published by Elsevier BV.

CHAPTER 35

Current approaches and future directions to

understanding control of head movement

Barry W. Peterson*

Department of Physiology, The Feinberg Medical School, Northwestern University, Chicago, IL 60611, USA

Abstract: This chapter reviews four key issues that must be addressed to advance our knowledge of control of head
movement by the central nervous system (CNS). (1) Researchers must consider how the CNS utilizes the multiple
muscle patterns that can produce the same head movement in carrying out tasks in an optimal way. (2) More attention
must be paid to the dynamics of neck muscle activation that are required to implement head movements and show they
are produced by CNS circuits. (3) Research is required to determine how the multiple pathways that impinge upon neck
motor centers are utilized in a variety of tasks including eye–head gaze shifts, smooth head tracking, head stabilization
and manipulating objects with the head. These pathways include corticospinal, vestibulospinal, reticulospinal (three
subdivisions), fastigiospinal, tectospinal and interstitiospinal tracts. (4) Further analysis is needed to understand how
vestibular signals are modulated during each of the above-mentioned tasks. This ambitious agenda is justified by the
fact that the head–neck motor system is an ideal model for understanding issues of complex motor control.

Introduction weaker than in the arm. The head also participates in

This chapter provides a review of the current state
of work on head-movement control. What follows is
a conceptual look at this system, as illustrated by
diagrams rather than data from the author’s and
others’ laboratories.
An interesting property of the head-movement
control system is that it shares features of both the
eye and arm-movement control systems. Like the eye,
the head is used to control the direction of gaze. It
thus requires mechanisms to keep its orientation
stable in the face of external perturbations. As in the
eye, evolution has solved this problem by provid-
ing strong, short-latency vestibular reflexes, the
vestibulocollic reflexes (VCRs). Muscle-spindle-
driven reflexes, which serve to adjust compliance of
the arm, are also present in the neck (cervococollic
reflexes) but their monosynaptic portion is relatively
*Corresponding author: Tel.: þ 312-503-6216;
Fax: þ 312-503-5101; E-mail: b-peterson2@northwestern.edu
gaze shifts that align the optic axes with an object to
be viewed. Their stereotypic nature makes such gaze
shifts easier to understand than arm movements
whose goals and trajectories are exceedingly diverse.
The presence of both eye- and arm-related control
systems is reflected in the wide variety of pathways
impinging on regions of the cervical spinal cord that
control the neck musculature. These include vestibu-
lospinal, reticulospinal, corticospinal, tectospinal and
fastigiospinal pathways. As described below, motor
commands traversing these pathways are selectively
deployed to accomplish various head-movement
tasks.
This review examines four aspects of head motor
control that shed light on the special properties of
this neuromuscular system. The first two are the
kinematics and dynamics of the head–neck neuro-
muscular system. The author then examines supra-
nuclear commands for voluntary head movements
carried by the various descending pathways that
impinge upon neck motor nuclei. The fourth section

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DOI: 10.1016/S0079-6123(03)43035-5
370

examines neural control strategies for generating eye–

head gaze shifts. A final section will discuss future
directions for research on head-movement control.

Kinematics of the overcomplete head–neck

musculoskeletal system

Various lines of evidence suggest that the head–neck

system is overcomplete in that it has more than the
minimum number of muscles required to control the
motions of its seven joints (Pellionisz, 1988). This
means that there will not be a single unique pattern of
muscle activation associated with every head move-
ment. Rather, a particular movement can be executed
by many different muscle-activation patterns.
Figure 1 illustrates the contrast between kine-
matics of the oculomotor and head-movement
systems. In the oculomotor system, three pairs of
muscles control the three rotational degrees of
freedom of the eye (yaw, pitch and roll). This
corresponds to a situation with three unknowns and
three equations. As a result, one can calculate a single
unique set of activation strengths of each muscle pair
that are required to produce each motion (Robinson,
1982).
Matrix A in Fig. 1 represents the eye movements
that each muscle pair will generate. For instance, the
middle row indicates that activation of the superior/
inferior rectus pair (superior rectus activation
coupled with suppression of inferior rectus) will
produce negligible horizontal rotation, strong
upward rotation (
0.91) and significant torsional
rotation (0.42). Because the matrix is invertible, one
can also compute the pattern of muscle activation
needed to produce a particular motion as represented
in the inverse matrix, B. For instance, the middle row
indicates that a downward pitch motion requires
activation of inferior rectus and inactivation of
superior rectus with a net strength of
0.81 and also
activation of the oblique muscle pair with a strength
of 0.43 to counter the roll motion that the vertical
recti would otherwise produce. There is also a very
weak inactivation of LRMR.
The matrix in Fig. 1C portrays a simplified head/
neck system with three muscles on both the right and
left sides and two joints. Because the muscles do not
align into push/pull pairs as in the eye, each must be
Fig. 1. Kinematic transformation matrices for eye and neck
motor plants. In A and C, rows indicate muscle inputs, and
columns show movement outputs. Values in A, which indicate
the movement produced by each muscle pair, are from
Robinson (1982). B is the inverse of A. Here, rows indicate
movements, and columns show muscles must be activated to
produce them. Movements produced by each muscle in the neck
are still in doubt and thus the matrix elements in C have been
left blank. Muscle abbreviations: LRMR, lateral and medial
rectus; l and r SCM, left and right sternocleidomastoid; l and r
Spi, left and right splenius; l and r Sem, left and right
semispinalis; SOIO, superior and inferior oblique; SRIR,
superior and inferior rectus. Other abbreviations: P, vertical
or pitch eye movement; P1, P2 head pitch about joint 1 and 2,
respectively; R, torsional or roll eye movement; R2, Y2, roll and
pitch of head about joint 2.
considered as acting separately, resulting in six
unknown activation strengths. Two types of joint
are included. One can move only in the pitch
direction, as does the joint between C1 and the skull.
The other can move in all three directions as in the
case of lower cervical joints. This results in four
equations—too few to completely specify the activa-
tion of muscles required to produce a particular
motion. Rather, there are many different solutions
that can all produce the same resultant motion. We
can fill in the matrix elements specifying the motions
each muscle would produce but the 4  6 matrix is
not invertible. Thus, we cannot specify a pattern of
muscle activation that is necessary to produce a given
motion.

Experimental examination of muscle-activation
patterns associated with head movements has
provided examples where multiple activity patterns
were associated with a particular movement and
others where a single pattern was observed. A single
pattern across time and individual subjects was
observed in highly constrained tasks such as
stabilization of the head by the VCR during body
rotation (Keshner et al., 1992; Banovetz et al., 1995;
Uchino, this volume) and generation of isometric
forces with the head (Vasavada et al., 2002). In
contrast, multiple patterns were observed during
tracking of a target with the head (Keshner and
Peterson, 1988; Choi et al., 2000) and when subjects
had to stabilize the head against loads applied with a
weight-pulley system (Keshner et al., 1989). This
suggests that the redundancy inherent in the over-
complete head/neck musculoskeletal system allows
the central nervous system (CNS) to choose different
patterns of muscle activation to execute the same
movement in ways that optimize some aspect of the
movement (see also Sugiuchi et al., this volume).
Obvious distinctions are between rapid, predictive
and fine, visually driven tracking and between force
generation with low and high stiffness. The observed
behavior suggests that different central neural path-
ways are used to drive movements that have such
differing properties. This is an important question to
be addressed in studies recording central neural
activity associated with head movement. Can we
indeed show that different premotor pathways are
active when a movement is made utilizing different
muscle synergies? Also, can we define the way in
which each pattern is optimal and relate it to the task
being performed when the pattern appears? Answers
to these questions will greatly advance our under-
standing of motor systems.
Dynamics of head–neck system and
its neural controllers
Dynamics refers to the way in which amplitude and
timing (phase) of neural or movement signals vary
with frequency of the head movement or of
the stimulus that is eliciting it. Mechanics of the
eye are dominated by viscosity of orbital tissues
and spring-like forces of the extraocular muscles.
371
Correspondingly, extraocular motoneuron (MN)
activity has a burst component related to desired
eye velocity and a tonic component related to eye
position. Mechanics of the head/neck system are
dominated by the inertia of the head and secondarily
by viscoelastic properties of the muscles. Correspond-
ingly, neck muscle activity should be triphasic with
pulses of activity in agonist and antagonist muscles to
accelerate and brake the head at movement onset and
termination with possible tonic activity related to
head deviation. Such signals were in fact reported in
early studies (Zangemeister et al., 1982). The
dynamics of MN and premotoneuron activity,
however, has received relatively little attention in
recent studies of eye–head gaze shifts, which have
emphasized instead the use of common error signals
to drive both the eye and head. This leaves
unanswered questions regarding where in the final
output pathway the appropriate dynamical signals
are generated?
In contrast, studies of head stabilization have paid
a great deal of attention to head/neck dynamics.
Early recordings in the decerebrate cat revealed the
expected second-order behavior with head position
signals at low frequencies and head acceleration
signals at high frequencies (Bilotto et al., 1982).
Angular accelerations of the head activate
regularly and irregularly firing afferents from the
vestibular semicircular canals. It is the latter
that preferentially drive vestibulocollic pathways
(Highstein et al., 1987). Their dynamics include a
pole term that converts angular acceleration to
angular velocity at lower frequencies and a zero term
that converts back to acceleration at higher fre-
quencies above 1 Hz (Fernandez and Goldberg,
1971). These terms form the first part of the VCR
transfer function in Fig. 2.
Wilson et al. (1979) used electrical polarization to
bypass this first afferent-related term allowing them
to observe the further processing of VCR signals in
the CNS. As shown in the transfer function, this
consists of a second pole-zero pair. The second pole
converts the velocity signal produced by the first to
an angular position signal. Again above 1 Hz, the
second zero reverses this effect, yielding an
angular acceleration signal at high frequencies.
Thus, semicircular canal inputs are processed
exactly as required to produce a second-order
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Fig. 2. Dynamics of horizontal head stabilization about a single joint. The symbol s is the LaPlace variable. I, B and K are inertia,
viscosity and stiffness, respectively, of neck. Kc and Kv are constants weighting the action of the CCR and VCR, respectively, on neck
musculature. See text for discussion of time constants (T).
position/acceleration control signal on neck MNs.
Peterson et al. (1985) also observed the dynamics of
responses to rotation of the body about an earth-
fixed head, finding again a second-order signal. This
behavior, which is represented by the cervicocollic
reflex (CCR) transfer function in Fig. 2, likely reflects
the properties of neck muscle spindles.
Measurement of the transfer functions of system
components opened the way for dynamical modeling
of the head stabilization system in cats (Goldberg and
Peterson, 1986) and humans (Peng et al., 1996a,b).
These models have proven remarkably effective
in replicating and explaining the complex dynamic
behavior of the head during horizontal rotations
of the body (Keshner and Peterson, 1995; Keshner
et al., 1995). Several conclusions can be reached
from these models: (1) the VCR is not very effective
in stabilizing horizontal head position in space
at frequencies below 0.5 Hz (gain  0.1); (2) the
VCR and CCR are vital for preventing head
oscillations in the 1–3 Hz range; and (3) a static
vertical VCR appears to be important for stabilizing
the head in an upright posture against the force of
gravity. It is likely that the VCR also plays a role in
stabilizing the head during linear motions of the body
(Lacour and Borel, 1989; Borel and Lacour, 1992;
Borel et al., 1994). This is a topic for future
investigation.
Supranuclear commands for voluntary head
movements
Commands for generating head movements reach
neck MNs from a variety of sources that are shown in
Fig. 3.
Several classes of vestibulospinal neurons project
to neck motor pools. One group includes the
bifurcating position-vestibular-pause (PVP) neurons
that project to both extraocular and neck MNs (Isu
et al., 1988). Their name denotes the fact that they
carry an eye position signal and a vestibular
semicircular canal signal and pause during saccadic
gaze shifts. Perlmutter et al. (1998a) established that
the canal input to these neurons is from a single
canal. Responses of identified bifurcating neurons to
linear head motions have not been studied but it is
likely that they also receive input from otolith
afferents sensitive to linear acceleration as observed
in unidentified PVP neurons (Angelaki et al., 2001).
The likely signal carried by these neurons is a
command for stabilizing eye and head movements
aligned with the coordinate frame of the three
semicircular canals. This would then be distributed
with the proper weights to extraocular and neck MNs
to generate the required motions.
There are also vestibulospinal neurons that project
only to the neck. These typically receive convergent
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Fig. 3. Scheme showing processes involved in generating and controlling eye–head gaze shifts. Commands for saccadic gaze shifts
originate in association areas of frontal and parietal cortex (F-PCx) and activate output systems originating in motor cortex (MCx) and
SC. SC signals reach neck motoneurons (NMn) primarily via reticulospinal neurons (RSN) and oculomotor nuclei (OM) via excitatory
and inhibitory burst neurons (EBN, IBN). Both head and eyes are stabilized in space via pathways originating in semicircular canals
(SCC) and relaying in the vestibular nuclei (VN). The VN are also the relay for smooth pursuit commands relayed via area MST and
cerebellar vermis and flocculus (Cb). The cerebellum also regulates eye and head movements via its fastigial nucleus (FN). Also
included are three mechanisms that regulate gaze shifts: the eye saccade gate implemented by omnipause neurons (OPN); the resettable
neural integrator (RNI) that turns off saccades when the correct goal is reached; and, a head-movement estimator (HME) that cancels
the portion of VN activation due to commanded head movements. HMS are head-movement sensors—possibly muscle spindles. Solid
arrows indicate excitatory connections; open circles, inhibitory connections; open arrows, mixed actions.

input from multiple canals that produce a unique
preferred rotation direction that is likely aligned with
that of the specific motor pools to which they project
(Perlmutter et al., 1998a). It is not known how such
vestibulocollic neurons respond to linear motions.
Observations by Boyle et al. (1996) suggest that this
population may include neurons that receive input
from the cerebellar flocculus and exhibit an eye–head
velocity discharge pattern. They could provide one
pathway for mediating visually guided smooth head
movements.
Finally, neck MNs also receive input from
collateral branches of vestibulospinal neurons pro-
jecting to lower levels of the spinal cord (Perlmutter
et al., 1998b). These long vestibulospinal neurons
exhibit a wide variety of preferred angular rotation
directions including directions that activate semicir-
cular canals on the opposite side. Interestingly, it is
such Type II neurons that appear to receive the
strongest direct input from otolith afferents sensitive
to linear accelerations (Angelaki et al., 2001). The
signals carried by these neurons are likely to mediate
postural-stabilizing responses.
Another major source of input to neck MNs is the
reticulospinal system, which originates from several
groups of neurons in the medial mesencephalic,
pontine and medullary brainstem (Robinson et al.,
1994). The best understood neurons are those that are
located in the paramedian pontine reticular forma-
tion and send their axons to the spinal cord via the
medial reticulospinal tract (mRST). The paramedian
pontine reticular region is the final premotor relay
in the network that controls horizontal gaze shifts.
In addition to mRST neurons, it also contains
excitatory burst neurons (EBNs) that drive horizon-
tal eye movements via projections to abducens MNs
and internuclear neurons (Strassman et al., 1986a,b).
Both mRST and EBN neurons carry a signal related
374
to gaze velocity. They receive strong excitatory inputs
from the superior colliculus (SC), a structure that
specifies the desired metrics of a gaze shift by a spatial
code wherein discharge of neurons in a specific
location on a retinotopic map leads to a saccade
appropriate to foveate a stimulus falling on the
corresponding portion of the retina. Transformation
from the spatial code in the SC to the gaze velocity
code in the reticular formation is thought to involve
weighted projections from SC to the reticular
formation and regulation by cerebellar circuits that
project to the reticular formation via the cerebellar
fastigial nucleus (Optican and Quaia, 2002). (Further
aspects of this system are considered below). Neurons
projecting in the mRST also receive input from
frontal cortex and the vestibular system (Peterson
et al., 1974; Peterson and Abzug, 1975), raising the
possibility that they may participate in voluntary
control of the proximal musculature and postural
reflexes.
Less well understood are the projections to neck
MNs from neurons in the gigantocellular reticular
formation of the medial medulla. These descend
primarily in the ipsilateral and contralateral lateral
reticulospinal tracts (lRSTs) and have both excitatory
and inhibitory actions on neck MNs (Peterson et al.,
1978). The latter pay a key role in the atonia
associated with rapid eye-movement sleep (Terzuolo
et al., 1965). Like mRST neurons, these neurons
receive inputs from frontal cortex, SC, fastigial
nucleus and vestibular and somesthetic afferents
(Peterson and Felpel, 1971; Eccles et al., 1975;
Peterson et al., 1980). This raises the possibility that
they serve a wide variety of functions related to
voluntary head movements, orienting and postural
stabilization. Kitama and colleagues (Kitama et al.,
1995a,b), however, have reported that these functions
may be separated. Neurons that play a key role in
orienting movements produced by the tecto-reticu-
lospinal system (Grantyn and Berthoz, 1985, 1987;
Grantyn et al., 1987, 1992a,b; Grantyn et al., this
volume; Sasaki, this volume) appear to receive
relatively little vestibular input whereas other
neurons in the pontine and medullary reticular
formation respond vigorously to horizontal rotations
and also receive input from the SC. These likely
include the reticulospinal neurons examined by
Bolton et al. (1992), which responded especially
strongly to inputs from otolith organs. This raises the
possibility that the reticulospinal system may contain
separate channels for mediating visually driven
orienting responses, and slow head stabilization and
tracking movements. This suggestion requires further
examination in animals with free heads.
A third reticulospinal projection arises from the
region of central mesencephalic tegmentum corre-
sponding to nucleus subcuneiformis (Robinson et al.,
1994). Some neurons in this region fire prior to
saccades while others discharge later, at the point
when head movement is underway (Waitzman et al.,
1996, 2002). Inactivation of the region results in
hypermetric contralateral saccades (Waitzman et al.,
2000), suggesting that it is involved in the regulation
of gaze-shift amplitude. An intriguing possibility is
that this region plays a role in apportioning the SC
gaze command signal between eye and neck motor
plants.
Corticospinal projections to the neck arise from
several cortical areas including primary motor cortex,
the dorsal and ventral premotor areas and the
supplementary and cingulate motor areas (He et al.,
1993, 1995). In primates, some of these projections
appear to terminate on neck MNs (Dum and Strick,
1996). In the cat, however, the most direct excitatory
cortico-neck MN pathway was disynaptic with a
relay in the pontomedullary reticular formation.
Stimulation of corticospinal fibers below a transected
pyramid gave rise only to disynaptic inhibition
followed by longer latency excitation (Alstermark
et al., 1985, 1992). It is likely that cortico-
reticulospinal connections are stronger than direct
corticospinal connections in primates, as well. They
would allow cortical access to orienting responses
involving synergistic activation of large sets of axial
MNs and to postural adjustments that form a vital
part of many voluntary movements. The latter may
also involve cortico-vestibulospinal pathways. The
special role of the direct pathways remains to be
explored experimentally.
Another descending pathway arises from the
interstitial nucleus of Cajal, which functions as a
controller for vertical gaze position (Fukushima,
1987; see also Fukushima et al., Chapter 37 of this
volume). There are also projections from the SC and
cerebellar fastigial nucleus that appear to terminate
on interneurons within the neck segments of the
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spinal cord (Robinson et al., 1994). These may be the
head-movement analog of projections of these
structures to EBNs that drive eye saccades.
Neuromuscular strategies underlying
eye–head gaze shifts
The most extensive analysis of head movements
concerns their role in eye–head gaze shifts. Figure 4
summarizes key aspects of this behavior.
The lower traces in Fig. 4A indicate the move-
ments of the eyes (in the head) and of the head in
space during an 80 gaze shift. Gaze is the sum of the
other two signals and reflects the point in space
toward which the optic axes of the eyes are directed.
In this example, the eyes and head begin moving at
the same time (gaze shift onset indicated by the first
dotted line) but this can vary (Zangemeister et al.,
1981, 1982; Zangemeister and Stark, 1982). For small
movements, the head is often delayed whereas for
large movements or highly predictable movements,
the head may begin to move before the eyes (Ron
et al., 1993). In this case, the VOR drives the eyes in
the opposite direction, thereby holding gaze stable
until gaze onset.
The gaze shift ends 0.3 s after it began. At this
time, the head is still moving in the direction of the
gaze shift while the eyes are moving in the opposite
direction under the influence of the VOR. In fact, eye
velocity typically reverses direction before the end of
the gaze shift, thereby reflecting an opposing
interaction between gaze drive and the partially
suppressed VOR (Tabak et al., 1996). It was
originally thought that the VOR was normally active
throughout a gaze shift. This would require the
saccadic system to generate a much larger drive in
order to overcome the vestibuloocular eye move-
ments that would oppose the gaze shift (Bizzi et al.,
1976). There is now wide agreement, however, that
the VOR is suppressed during a gaze shift
(Tomlinson and Bahra, 1986a; Ron et al., 1993;
Tabak et al., 1996; Roy and Cullen, 1998). Careful
measurements by Tabak et al. (1996) indicate that the
degree of suppression in the human increases with
amplitude of the gaze shift but is never complete. The
drawing at the top of Fig. 4A is typical, showing
a suppression of 50%. As discussed further below,
there is also evidence that VCRs are suppressed
during active, voluntary head movements (McCrea
et al., 1999; Roy and Cullen, 2001).
Figure 4B illustrates another aspect of eye–head
behavior. Head-movement components of gaze shifts
depend on eye position in the head (Guitton et al.,
1984; Tomlinson and Bahra, 1986b; Guitton and
Volle, 1987; Freedman and Sparks, 1997; Goossens

Fig. 4. Eye–head behavior during gaze saccades. (A) Traces at bottom show trajectories of head in space, eye in head and of their sum
(gaze) during an 80 gaze saccade. Top trace plots VOR gain as measured by Tabak et al. (1996). Vertical lines indicate gaze shift onset,
gaze shift end and head-movement end. (B) Plot of head-movement contribution to gaze shifts as a function of the predicted eye
eccentricity at the end of the gaze shift if the head did not move (the sum of initial eye position in head and the change in gaze), as
analyzed by Stahl (1999). Axes are in degrees.
376
and Van Opstal, 1997; Stahl, 1999; Ceylan et al.,
2000). If a gaze shift can be accomplished by eye
movements alone, leaving the eyes near central
position, the head-movement component will be
minimal. The abscissa on the Fig. 4B graph, which
plots the sum of initial eye position and the gaze shift,
reflects this behavior. If the initial eye position (Ei) is
already in the direction of the gaze shift, Ei þ
G will
be large, and a larger head movement will be planned
than if initial eye position is in the direction opposite
to the gaze shift. The range of allowed eye position
varies between individuals—those with large allowed
ranges are eye movers while those with small ranges
are head movers. The range can also be adjusted to
match cognitive demands of the task. For instance,
when subjects view the world through pinhole glasses,
the range is greatly reduced so that gaze shifts are
largely carried out by moving the head. This allows
the target to remain visible through the pinhole
(Ceylan et al., 2000). The simple form of apportion-
ing gaze shifts can be accomplished by adding an eye
position offset signal to the main reticulospinal
pathway carrying gaze commands to the neck as
shown in Fig. 3, and as observed experimentally
(Grantyn and Berthoz, 1987). It is not clear, however,
how the range is adjusted in accordance with task
demands.
Figure 3 summarizes current knowledge of neural
circuitry involved in generating eye–head gaze shifts.
A major source of commands for such shifts is the
intermediate-to-deep layers of the SC, which receives
inputs from many sources, including gaze centers in
the frontal and parietal cortex (F-PCx). SC discharge
is in the form of a location code where firing of a
particular neuron commands movements to a specific
point on a retinotopic map. Firing intensity varies
somewhat with the motivation of the animal and the
corresponding velocity of the resulting gaze shift, but
this variation is a secondary effect. Output of the
colliculus is thus a gaze displacement command. This
must be converted to a gaze velocity command that
declines to zero as gaze reaches the target. Figure 3
shows conceptually how this can be done. A
resettable neural integrator (RNI) keeps track of
how far gaze has shifted since the saccade began and
its output is subtracted from the SC signal to yield the
desired gaze velocity command. There is evidence
that this process may involve shifting of the locus of
activity on the colliculus during the gaze shift toward
regions that code progressively smaller gaze shifts
(Munoz and Guitton, 1985; Munoz et al., 1991;
Munoz and Wurtz, 1995) but the current models
assign a key role in the process to the cerebellar
vermis (Optican and Quaia, 2002) and its output
pathway via the fastigial nucleus (FN).
The eye-movement component of the gaze shift
passes through a gate representing the inhibitory
action of omnipause neurons (OPN) before reaching
EBNs and inhibitory burst neurons (IBNs). The
presence of this gate explains why activity sometimes
reaches head-movement circuits prior to activation of
EBNs and IBNs. Activity of these bursters then
drives oculomotor neurons (OM). It also charges the
RNI and the eye-position integrator that maintains
eccentric eye positions between gaze shifts (not shown
in Fig. 3). A final action arises from the projection of
IBNs to the vestibular nuclei where they are thought
to inhibit PVP-type vestibuloocular neurons. This
would account for the fact that the pause exhibited by
these neurons is precisely aligned with the time of the
saccadic gaze shift.
The head-movement component of the SC-
controlled gaze shift reaches neck MNs primarily
via reticulospinal neurons (RSNs). As explained
above, there are separate populations of RSNs
responsible for horizontal and vertical head move-
ments located in the mesencephalic, pontine and
medullary tegmentum. The box shown in Fig. 3 is
a composite of these populations. It receives SC-,
motor cortical- and vestibular input, which may be
segregated in different populations of RSNs (Kitama
et al., 1995a). This box also receives an eye-position
signal, which has been observed in medial RSNs of
the pons (Grantyn and Berthoz, 1987; Grantyn et al.,
1992a). As explained above, this signal varies the
activation of RSNs and hence the head-movement
component of gaze shifts depending on the position
of the eyes in the head.
A prominent input to EBNs, IBNs and RSNs
arises from the fastigial nucleus (May et al., 1990;
Robinson et al., 1994). Knowledge of the complex
signals carried by fastigial neurons, and the way in
which they are distributed to different premotoneur-
ons, is currently quite limited. There is a similar lack
of information on the role of pathways from motor
and premotor cortical areas of the frontal lobe

(He et al., 1993, 1995; Dum and Strick, 1996) in
producing head movements. Anatomical and electro-
physiological observations indicate that these path-
ways have powerful actions on RSNs and neck MNs
(Peterson et al., 1974; Alstermark et al., 1985, 1992)
but the signals they carry during behavior have not
been observed. There is also considerable controversy
regarding whether the frontal eye field, a region
traditionally thought to be the primary premotor
cortical center for eye movements, also acts upon the
neck musculature. Given its strong excitatory action
on the SC, it would seem likely that such an action
should exist but some groups have observed it (Tu
and Keating, 2000) while others (Chen and Sparks,
2001) have not.
The vestibular nuclei are an essential component
in organizing and driving stabilizing eye and head
movements that compensate for externally imposed
motions of the head. They do this both via powerful
excitatory and inhibitory projections directly to
extraocular and neck MNs and via projections to
reticular neurons (EBN, IBN, RSN). Also shown is
the direct inhibitory input from Purkinje cells of the
flocculus and nodulus. Little is known about the
latter but the former play a key role in relaying
signals that allow animals to follow small moving
targets (Lisberger et al., 1994). Smooth pursuit eye
movements are mediated by flocculus-receiving
neurons in the vestibular nuclei that exhibit eye–
head, velocity type behavior (Zhang et al., 1995a,b).
Some of these neurons appear to project to the neck,
as well (Boyle et al., 1996), and may be one of the
pathways that contributes to smooth pursuit head
movements. There are also projections to and from
the fastigial nucleus whose roles are poorly under-
stood. One such role may be in organizing postural
adjustments during such behaviors as locomotion.
As in the case of the VOR, there is evidence that
the VCR is suppressed during gaze shifts. Part of this
involves the pause in discharge of PVP neurons that
was discussed. Many of these neurons bifurcate to
project to both eye and neck motor pools (Isu et al.,
1988). Therefore the portion of the VCR due to their
action will be absent during the time of the gaze shift
(but not the entire duration of the head movement).
Several groups have also observed cancellation of the
portion of vestibular input related to a voluntary
head movement in other types of vestibular neurons
377
(Boyle et al., 1996; McCrea et al., 1999; Roy and
Cullen, 2001). These neurons do not cease dischar-
ging as do PVPs. Furthermore, they continue to be
responsive to externally produced head movements.
There is thus selective cancellation of just that
portion of the vestibular signal produced by a
voluntary head movement. This cancellation extends
throughout the duration of the head movement, thus
continuing beyond the end of the gaze shift. In Fig. 3,
this cancellation is mediated by the box labeled ‘head-
movement estimator’ (HME). This mechanism
processes efference copy signals of motor commands
from the SC and motor cortex channels, and head-
movement feedback signals (HMS) to arrive at an
estimate of the vestibular signal that would be
produced by a voluntary head movement. This signal
would then inhibit vestibular neurons. The cancella-
tion appears to be less complete during slow tracking
head movements (K. Cullen, personal communica-
tion), perhaps because the HME does not have access
to signals arriving via the MST-cerebellar pathway.
(MST is the abbreviation for the cortical visual area
which senses image motion.)
Future directions
Compared to the wealth of knowledge available on
oculomotor control, our knowledge of head-move-
ment control is at a very early stage. Significant
progress can be made by studying the head-movement
system using paradigms developed for oculomotor
studies. We need to know how neurons in each of the
sites that project to the neck behave during several
head-movement behaviors. Ideally, neural activity
would be compared across eye–head gaze shifts,
smooth head tracking, head stabilization and reaching
for food with the mouth. Such studies will be much
more valuable if the neurons investigated are identified
(using electrical stimulation) as projecting to the neck,
and perhaps also according to areas of the CNS, which
project to them. This will be a major undertaking since
it involves recordings from several cortical areas, the
SC, three reticular regions [central mesencephalic
reticular formation (CMRF), paramedian pontine
reticular formation (PPRF), gigantocellularis], the
medial, lateral and inferior vestibular nuclei and the
cerebellar fastigial nucleus. It would be valuable to
378

record from several such sites simultaneously in order Acknowledgments

to see how their activity shifts with the animal’s
behavior (see also Kobayashi et al., this volume). The author’s work on head movements is supported
Another approach that can be adopted from our by grant number NS 41288 from the National
oculomotor colleagues is the use of neural systems Institute of Neurological Disorders and Stroke.
models like those used by Galiana and Guitton
(1992). These are indispensable tools in under-
standing the function of neural networks like that Abbreviations
shown in Fig. 3. We will also need models that deal
with the complex kinematics and dynamics of the CCR cervicocollic reflex
head–neck system. Studies reviewed above describe CMRF central mesencephalic reticular formation
the start that has been made in this direction. CNS central nervous system
Hopefully, we will eventually arrive at a neural EBN excitatory burst neuron
network model that incorporates a realistic neck F-PCx frontal and parietal cortex
motor plant and emulates what is known about its HME head-movement estimator
neural control. HMS head-movement feedback signals
Construction of the latter type of model will IBN inhibitory burst neuron
depend upon an experimental approach that is not lRST mRST, lateral and medial reticulospinal
commonly employed in oculomotor studies. This tracts
involves correlation of the activity of neck muscles MN motoneuron
and specific classes of central neurons. Two methods MST cortical visual area sensing image motion
are available. Spike-triggered averaging reveals direct PPRF paramedian pontine reticular formation
actions of the test neuron on different neck motor PVP position-vestibular-pause (neuron)
pools. Correlation of neural and EMG activity RNI resettable neural integrator
reveals the relationship between them and how it RSN reticulospinal neuron
changes across categories of behavior. Since the SC superior colliculus
required analyses can be done off-line after data are VCR vestibulocollic reflex
obtained, they can provide valuable additional VOR vestibuloocular reflex
information about each neuron studied.
This is an ambitious agenda but the author
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