Download Chapter Two Ocular Motor System

Chapter Two
Ocular Motor System
2.1
Introduction
The ocular motor system has evolved in parallel with the visual system so that a
number of different classes of eye movement now exist, each with a particular functional
purpose (see table 2.1). Eye movements that were early to evolve keep the eye fixed on
objects of interest. Amongst these eye movements are subsets that are important for
helping to maintain clear vision when the head is moving (vestibular-evoked eye
movements) and when the visual world is moving with respect to the head (optokineticevoked eye movements). With the evolution of the fovea, a requirement for a new
repertoire of eye movements arose. Since visual acuity is greatest when an image is
positioned on the fovea, eye movements that function to rapidly move the eyes towards
objects of interest (saccadic eye movements) and pursue objects of interest (smooth
pursuit eye movements) have evolved. Furthermore, with the evolution of frontally
positioned eyes, eye movements that simultaneously keep the foveae of both eyes on
objects of interest (verging eye movements) evolved.
Table 2.1 Functional classes of human eye movements (adapted from Leigh and Zee 1999).
Class
Main Function
Fixations
Hold the image of a stationary target on the fovea
Vestibular
Stabilize images on the retina during brief head movements
Optokinetic
Stabilize images on the retina during relative movement of
the visual world (such as during sustained head movements)
Smooth Pursuit Hold the image of a moving target on the fovea
Saccades
Rapidly redirect the line of sight towards targets of interest
Vergence
Move the eyes in opposite directions so that images of a
single close target are placed simultaneously on both foveae
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In this chapter, the structure and function of the ocular motor system is reviewed,
with emphasis on saccadic eye movements. The structure and function of the muscle
pulleys is also considered in detail (see Demer 2004 for a comprehensive overview).
2.2
Description of Eye Movements
In the scientific literature, eye movements are usually described as three-
dimensional (3-d) rotations relative to a right-handed head-fixed coordinate system (see
figure 2.1 and appendix). The rotations are composed of three components – torsional,
vertical, and horizontal – with the magnitude of each component depending on the extent
of rotation about each of the three head-fixed base axes (see appendix). Torsional
rotations are those that occur about the naso-occipital x-axis (hx in figure 2.1), with
positive rotations about this axis being clockwise and negative rotations being
counterclockwise according to the right-hand rule (see appendix). Vertical rotations are
those that occur about the inter-aural y-axis (hy in figure 2.1), with positive rotations
being downward and negative rotations being upward. Rotations about the z-axis (hz in
figure 2.1) are known as horizontal rotations, with positive rotations being leftward and
negative rotations being rightward.
hZ
hX
hY
Figure 2.1 Eye movements are described by rotations that have projections onto three head-fixed
base axes. Rotations about the hx axis are torsional rotations. Rotations about the hy axis are
vertical, while those about the hz axis are horizontal rotations. Positive rotations about each of the
axes are indicated by the directions of the grey arrows (adapted from Haslwanter 1995).
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In clinical practice, eye movements are described according to an alternate
nomenclature. Intorsion is torsional rotation of the eye where the upper pole of the iris
moves towards the midline, whereas extorsion is torsional rotation of the eye where the
upper pole of the iris moves away from the midline. Elevation refers to upward rotation of
the eye, whereas depression refers to downward rotation. Abduction is horizontal rotation
of the eye away from the midline, whereas adduction is horizontal rotation of the eye
towards the midline.
2.3
Anatomy of the Ocular Motor System
The ocular motor system consists of the central and peripheral structures
responsible for generating eye movements. A brief review of the anatomy and function of
these structures is given below, along with a detailed review of the anatomy and function
of the recently discovered muscle pulleys.
2.3a
Extra-Ocular Muscles
There are six muscles that move each eye: the four recti (medial, lateral, superior,
and inferior), and the two oblique (superior and inferior) muscles (see figure 2.2). The
recti and superior oblique muscles arise from the annular tendon (or annulus of Zinn),
which is adherent to the optic nerve’s dural sheath and to the periosteum of the optic
canal. The levator palpebrae superioris also originates from the annular tendon; it inserts
into the upper eyelid and functions to elevate it. The recti all insert on the anterior half of
the eyeball. The inferior oblique muscle arises from the inferior wall of the orbit and
inserts on the posterior half of the eyeball. The superior oblique muscle, which also
inserts on the posterior half of the eyeball, is unique in that its tendon passes through an
antero-medially placed fibro-cartilaginous loop, the trochlea, before passing posteriorly to
insert on the eyeball (see figure 2.2).
The main actions and the innervations of the six extra-ocular muscles are listed in
table 2.2. The medial and lateral recti produce eye rotations that are predominantly
horizontal, while the other four muscles produce combinations of vertical and torsional
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eye rotations. The six extra-ocular muscles may be divided into three agonist-antagonist
pairs, where contraction of one muscle in the pair produces the same movement as
relaxation of the other muscle in the pair. The medial and lateral recti make up one pair,
whereas the superior and inferior recti and the superior and inferior oblique muscles make
up the other two pairs.
Figure 2.2 The right orbit, and surrounding structures, viewed from the lateral aspect. The six
extra-ocular muscles are labelled. The lateral rectus and optic nerve have been cut, so that
medially-placed structures are visible (from Williams et al. 1989).
Table 2.2 Main actions and innervations of the extra-ocular muscles (from Kandel et al. 1991).
Muscle
Main Actions
Innervation
Medial Rectus
Adduction
Oculomotor nerve (CN III)
Lateral Rectus
Abduction
Abducens nerve (CN VI)
Superior Rectus
Elevation/Intorsion
Oculomotor nerve (CN III)
Inferior Rectus
Depression/Extorsion Oculomotor nerve (CN III)
Superior Oblique Depression/Intorsion
Trochlear nerve (CN IV)
Inferior Oblique Elevation/Extorsion
Oculomotor nerve (CN III)
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2.3b
Muscle Pulleys
Connective tissue sleeves that surround the rectus muscle tendons, close to the
equator of the eyeball, have been demonstrated histologically (Demer et al. 1995). These
connective tissue structures, which contain collagen, elastin, and smooth muscle, are
attached to one another and to the orbital wall (Demer et al. 1995; Kono et al. 2002a).
Clark et al. (2000) showed, using high-resolution magnetic resonance imaging (MRI),
that these sleeves function as pulleys by keeping the paths of the rectus muscle bellies
fixed in the orbit, while allowing the orientations of the tendons to vary in a manner that
depends on instantaneous eye position (medial rectus data are displayed in figure 2.3).
Muscle Belly
Tendon
Pulley Location
Figure 2.3 The cross-sectional “area centroid” position of the medial rectus muscle belly and
tendon, determined from MRI images, with the eye in different vertical positions. The view is
from the lateral aspect. The data from the top panel are plotted in the bottom panel with
corrections for supero-inferior translation. When the eye is elevated, the tendon (indicated on the
right) is directed upwards, while it is directed downwards when the eye is depressed. To bring
about the observed changes in tendon orientation, the pulley would have to be located within the
area indicated by the dotted rectangle (adapted from Clark et al. 2000).
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The observation that the pulleys change the orientations of the rectus tendons
suggests that the action of each rectus muscle depends on instantaneous eye position. For
example, in the case of the medial rectus, if the subject is looking straight ahead,
contraction of the muscle produces a purely horizontal rotation due to rotation of the
eyeball about the head-fixed z-axis (see figure 2.4a). However, if the eye is elevated, the
muscle pulley alters the pulling direction of the muscle so that the same muscle
contraction produces a rotation that has horizontal and torsional components, due to a
backward tilt in the eye velocity axis (see figure 2.4b).
Figure 2.4 The muscle pulley of the medial rectus keeps the muscle belly fixed in position when
the eye moves from the centre of the ocular motor range (A) to an elevated position (B). However,
the pulley causes the tendon pulling direction to change when the eye is elevated, resulting in a tilt
in the eye velocity axis away from the head-fixed z-axis.
The finding that the pulleys bring about eye position-dependent changes in the
pulling directions of the recti has prompted a number of significant modifications to
theories explaining how eye movement kinematics arise (Raphan 1998; Quaia and
Optican 1998; Smith and Crawford 1998; Thurtell et al. 1999; Misslisch and Tweed
2001). Indeed, the discovery of the muscle pulleys is said to have sparked an “orbital
revolution” (Haslwanter 2002). The influence of the muscle pulleys on the kinematic
properties of saccadic and vestibular-evoked eye movements is considered in detail in the
current project, with the issue being addressed in many of the chapters of this thesis.
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The recti are known to have two histologically distinct layers (Porter et al. 1995):
the inner global layer is continuous from the annular tendon to the insertion of the muscle
tendon on the eyeball, while the outer orbital layer terminates posterior to the scleral
insertion. Demer et al. (2000) re-examined the histology of the recti, reporting that the
orbital layer of each rectus muscle actually inserts on the corresponding muscle pulley.
Kono et al. (2002b) subsequently demonstrated, using high-resolution MRI, that
contraction of each rectus muscle results in posterior displacement of the corresponding
pulley, due to contraction of the orbital layer of the muscle (see figures 2.5 and 2.6).
Relaxation of each rectus muscle results in anterior displacement of the corresponding
pulley, presumably because of decreased opposition to elastic forces imposed by the
pulley suspensory structures (Kono et al. 2002b). The manner in which pulley position
alterations are encoded centrally is yet to be determined.
Figure 2.5 Path of the medial rectus muscle belly and tendon, from a representative subject, with
the eye in four different gaze positions. Supraduction indicates elevation of the eye, while
infraduction indicates depression of the eye. The inflection (arrow) in the muscle path indicates
the approximate location of the muscle pulley. The muscle belly is posterior to the pulley
(leftward on the graph), while the tendon is anterior to the pulley (rightward on the graph). The
pulley position can be seen to alter depending on whether the eye is adducted or abducted.
Contraction of the medial rectus (which leads to adduction) results in posterior displacement of its
pulley, while relaxation of the medial rectus (which occurs during abduction) results in anterior
displacement of its pulley (from Kono et al. 2002b).
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Figure 2.6 The orbital layer of each rectus muscle inserts into the corresponding muscle pulley
(A), so that posterior displacement of the muscle pulley (arrow) is observed when the muscle
contracts (B). The orientation of the eye velocity axis is not altered by retraction of the pulley in
the case illustrated.
2.3c
Ocular Motor Neurons
The motor neurons to the extra-ocular muscles travel in three cranial nerves (CN):
the oculomotor nerve (CN III), the trochlear nerve (CN IV), and the abducens nerve (CN
VI). The oculomotor nerve provides the innervation for the inferior oblique muscle and
for the superior, inferior, and medial recti (see table 2.2). The trochlear nerve innervates
the superior oblique muscle, while the abducens nerve innervates the lateral rectus (see
table 2.2). These nerves each have long intra-cranial courses, since they travel from the
brainstem (in the posterior fossa of the cranial vault) to the orbit. The cell bodies of each
of the motor neurons are located close to the midline in the brainstem, in nuclei with the
same name as the corresponding nerve. Oculomotor neurons originate from the
oculomotor nucleus, which is found in the midbrain at the level of the superior colliculi.
The oculomotor nucleus contains a number of subnuclei, each responsible for innervating
a different muscle (see figure 9-9 in Leigh and Zee 1999). Trochlear neurons originate
from the contralateral trochlear nucleus, found in the midbrain at the level of the inferior
colliculi, while abducens neurons originate from the ipsilateral abducens nucleus, found
in the caudal pons just beneath the floor of the fourth ventricle.
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2.4
Neural Signal to the Extra-Ocular Muscles
For all eye movements, the neural signal travelling to the extra-ocular muscles
conveys both position and velocity information. The final signal is derived from a raw
input that is proportional to the velocity of the resulting eye movement. A position signal
is obtained by integration of the input (velocity) signal. The neural components
responsible for generating the position signal from the input signal have therefore come to
be known as the “neural integrator”. Following the generation of a position signal, it is
combined with the velocity signal to produce the signal that travels to the extra-ocular
muscles to move the eyes. To a first-order approximation, Robinson (1975) described
motor neuron discharge rate R as being related to eye position θ and eye velocity dθ/dt by
R = k (θ − θT ) + r
dθ
dt
where θT is the threshold eye position at which the neuron is recruited into activity, and k
and r are constants.
Both the position and velocity components of the signal are required in order to
compensate for restrictions imposed on eye movements by the orbital contents, such as
forces opposing movements of the eye away from the centre of the ocular motor range
and forces acting to pull the eye back towards the centre when it is positioned
eccentrically. If there is no eye position signal during a period of attempted fixation, for
example, the eye will drift back towards the centre of the ocular motor range due to the
presence of elastic restoring forces acting on the eyeball. The complete or partial loss of
the position component of the signal results from lesions of the integrator (a so-called
“leaky” integrator). During attempted fixation of an eccentric target, loss of the position
component of the signal is clinically evident as centripetal drift of the eye back towards
the centre of the ocular motor range, which is corrected for by saccadic eye movements
back to the target (so-called “gaze-evoked” nystagmus; see sections 3.9 and 8.1).
The means by which the neural integrator produces a position signal from the
velocity signal is a subject of controversy (see chapter 4). The neural integrator and other
central pathways involved in eye movement generation are discussed in greater detail
below, and in chapters 3 and 4.
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2.5
Saccadic Eye Movements
Saccadic eye movements enable humans to rapidly redirect their line of sight
towards objects of interest. Saccades may be identified by their profiles, since they show
a consistent relationship between their peak velocities and amplitudes (Leigh and Zee
1999). Saccades also have stereotyped 3-d kinematic properties, which will be described
and discussed in detail in chapter 4. The central pathways responsible for generating
saccades are considered below.
2.5a
Saccadic Command to the Extra-Ocular Muscles
Recordings from ocular motor neurons during saccadic eye movements have
revealed that the neural command to the extra-ocular muscles is comprised of both phasic
and tonic signals. The initial part of the signal is a high frequency burst of phasic activity,
the pulse, which starts about 8ms prior to the onset of eye rotation (see figure 2.7).
Figure 2.7 The pulse-slide-step of innervation, during a 20° leftward saccade in the monkey
(upper panel), is illustrated (lower panel). The data were recorded from a neuron in the left
abducens nucleus. The slide is denoted by the horizontal bar (from Leigh and Zee 1999).
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The pulse functions to bring about a sudden contraction of the extra-ocular
muscles, so that the eye moves quickly from one target to the next. At the completion of
the eye rotation, there is a new level of tonic innervation to the extra-ocular muscles,
encoded by the step (see figure 2.7). The step signal, which is generated by the neural
integrator (see sections 2.4 and 2.5c), is important for holding the eye in its new position,
since it helps counteract various restoring forces acting on the eyeball. The transition
between the end of the pulse and the beginning of the step has come to be known as the
slide, since it provides a gradual transition between the two signals.
2.5b
Brainstem Circuitry for Saccades
The command signal necessary to produce a saccadic eye movement may arise
from one of a variety of cortical and brainstem structures, including the frontal eye fields,
supplementary eye fields, parietal eye fields, and the rostral poles of the superior colliculi.
These structures control the activity of omnipause neurons, which fire continuously,
except immediately prior to and during saccades. The cell bodies of the omnipause
neurons lie in the nucleus raphe interpositus, which is located in the midline of the pons
between the rootlets of the abducens nerves. Constant stimulation of omnipause neurons
has been shown to result in an inability to generate saccades (Westheimer and Blair 1973),
since omnipause neurons inhibit the brainstem saccadic pulse generator (Strassman et al.
1987; Ohgaki et al. 1989; Nakao et al. 1991).
The neurons comprising the brainstem saccadic pulse generator are located in two
anatomically distinct areas. The pulse generator for horizontal saccades is located in the
caudal pons, in the paramedian pontine reticular formation (PPRF), while the pulse
generator for vertical saccades is located in the rostral midbrain, in the rostral interstitial
nucleus of the medial longitudinal fasciculus (riMLF). The neurons whose cell bodies are
located in these areas are known as excitatory burst neurons (EBNs). Omnipause neurons
are inhibitory neurons that project from the nucleus raphe interpositus to the EBNs. When
the omnipause neurons are inhibited by the cortical or brainstem structure that has given
rise to the saccadic command signal, they stop firing and the EBNs are able to discharge.
The EBNs begin to discharge at high frequency approximately 12ms prior to the onset of
eye rotation. The EBNs are important for producing the pulse signal to the extra-ocular
muscles and their discharge rate is, accordingly, closely correlated with the velocity of the
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eye rotation. The EBNs also send collaterals to the neural integrator, which is responsible
for generating the step component of the signal to the extra-ocular muscles. The pulse
from the EBNs and the step from the neural integrator are combined in the ocular motor
nuclei, to create the final eye movement signal. The firing patterns of the components of
the final common saccadic pathway, and their connections, are summarized in figure 2.8.
Figure 2.8 Schematic diagram showing the brainstem components involved in the generation of
saccades. The omnipause neuron (P), EBN (B), and the ocular motor neuron (OMN) are
illustrated, as are their firing patterns (graphs show spike discharge and discharge rate plotted
against time). Before the onset of a saccade, the omnipause neuron ceases discharging, allowing
the EBN to generate a pulse. The pulse is passed to the neural integrator (NI), which generates a
signal proportional to eye position. The EBN also sends a signal proportional to eye velocity
directly to the ocular motor neuron; this signal is combined with the eye position signal, and the
resulting signal is sent to the eye muscles, producing a saccadic eye movement (E) with the
profile as illustrated in the plot of eye position against time (from Leigh and Zee 1999).
The PPRF is predominantly involved in the generation of horizontal saccades.
EBNs from the PPRF project to abducens motor neurons and internuclear neurons, which
are both located in the ipsilateral abducens nucleus in the pons. The internuclear neurons
decussate and then pass via the contralateral medial longitudinal fasciculus (MLF) to
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synapse on motor neurons in the medial rectus subnucleus of the oculomotor nucleus in
the midbrain. Thus, a pulse signal from the EBNs in the PPRF will result in contraction of
the ipsilateral lateral rectus and contralateral medial rectus muscles, bringing about an
ipsilateral horizontal saccade. Similarly, electrical stimulation of the PPRF results in an
ipsilateral horizontal saccade (Cohen and Komatsuzaki 1972), while a lesion in the PPRF
will result in an inability to generate ipsilateral horizontal saccades (Cohen et al. 1968).
The riMLF is important for the generation of the vertical and torsional
components of saccades (Büttner et al. 1977; Büttner-Ennever and Büttner 1978; King
and Fuchs 1979; Vilis et al. 1989). The EBNs from the riMLF project to motor neurons in
both the oculomotor and trochlear nuclei. Collaterals are also passed to the neural
integrator (see section 2.5c). Since EBNs that are responsible for generating upward and
downward eye movements are located on both sides of the midbrain, a unilateral lesion
will only result in a mild deficit in the ability to generate vertical saccades, while a lesion
that involves both sides will abolish all vertical saccadic eye movements.
2.5c
Neural Integrator
The neural integrator generates the eye position signal from the eye velocity signal.
The neural substrate for the neural integrator was identified by single-unit recording
studies and by studying the effects of lesions on eye movement kinematics. The structures
implicated include the medial vestibular nucleus (MVN), the nucleus prepositus
hypoglossi (NPH), and the interstitial nucleus of Cajal (INC). The flocculus and
paraflocculus of the cerebellum have also been implicated, since their ablation results in a
decrease in the ability to hold steady gaze (Takemori and Cohen 1974; Zee et al. 1981;
Waespe et al. 1983).
The production of the horizontal component of the eye position signal is thought
to occur in the MVN (Miles 1974) and NPH (Lopez-Barneo et al. 1982). The NPH, which
is medial to the MVN in the medulla, receives afferents from and projects to virtually all
of the structures in the brainstem and cerebellum involved in ocular motor function
(Belknap and McCrea 1988; see table 2.3). Cannon and Robinson (1987) confirmed that
both the MVN and the NPH are important for the production of the horizontal eye
position signal. After placing chemical lesions in both areas, they found that any
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subsequent eye movements followed a course that was proportional to the predicted eye
velocity only.
Table 2.3 Major connections of the NPH (adapted from Leigh and Zee 1999).
Inputs
Outputs
Vestibular nuclei:
Vestibular nuclei:
-
-
MVN
MVN
Contralateral NPH
Contralateral NPH
Brainstem reticular formation:
Brainstem reticular formation:
-
medullary reticular formation
-
medullary reticular formation
-
PPRF
-
PPRF
-
riMLF
-
INC
-
INC
Ocular motor nuclei
Ocular motor nuclei
Cerebellum
Cerebellum
Others:
Others:
-
raphe nuclei
-
raphe nuclei
-
nucleus of the optic tract
-
dorsal cap of inferior olive
The INC, a structure in the midbrain reticular formation, is thought to be
important in the production of both the vertical and torsional components of the eye
position signal (King et al. 1980, 1981; Fukushima 1987, 1991; Crawford et al. 1991;
Crawford 1994). It receives neural input from the vestibular nuclei (via the MLF) and the
riMLF. The INC sends output signals to the ocular motor nuclei (Steiger and BüttnerEnnever 1979), the vestibular nuclei, and to the NPH (Cannon and Robinson 1987;
Fukushima 1991). The NPH is also involved in producing the vertical eye position signal
(Baker 1977; Cannon and Robinson 1987).
Since the neural integrator produces an eye position signal from the eye velocity
signal, it performs, in effect, a velocity-position transformation (Tweed and Vilis 1987).
The neural integrator is also known, therefore, as the velocity-position integrator.
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Currently, there are two main hypotheses that attempt to explain how the velocityposition integrator works, based on the implications of modelling studies. Tweed and
Vilis (1987) proposed a “quaternion” integrator model of the velocity-position
transformation, whereas Schnabolk and Raphan (1994) have proposed a “vector”
integrator model. These two models are described and extensively discussed in chapter 4.
2.5d
Cerebellar Influences on Saccades
The cerebellum has a role in determining the metrics of saccadic eye movements,
since total cerebellectomy results in marked saccadic dysmetria (Optican and Robinson
1980). In addition, an inability to hold steady gaze at the end of a saccade (post-saccadic
drift) is observed following cerebellectomy (Optican and Robinson 1980). The role of
several regions of the cerebellum in bringing about normal saccades is considered below
(see Robinson and Fuchs 2001 for a review of the subject).
The dorsal vermis, consisting of lobules VI and VII (see figure 6.1), is thought to
be important in determining saccadic metrics (Selhorst et al. 1976; Optican and Robinson
1980). The dorsal vermis receives inputs from the caudal nucleus reticularis tegmenti
pontis (cNRTP), PPRF, vestibular nuclei, NPH, and inferior olivary nucleus; the major
projection of the dorsal vermis is to the caudal fastigial nucleus (Yamada and Noda 1987).
Pharmacological lesions of the dorsal vermis result in hypometric ipsilateral saccades,
hypermetric contralateral saccades, and gaze deviation away from the side of inactivation
(Sato and Noda 1992). Ablative lesions result in similar abnormalities (Takagi et al.
1998). Bilateral lesions result in hypometria of all horizontal saccades and an increase in
saccadic latency (Barash et al. 1999).
The caudal fastigial nucleus also has a role in determining saccadic metrics
(Optican and Robinson 1980; Vilis and Hore 1981). It receives inputs from the dorsal
vermis, inferior olivary nucleus, and frontal eye fields and superior colliculus (via the
cNRTP); it projects to the omnipause neurons, EBNs, and superior colliculus (Noda et al.
1990). Unilateral pharmacological lesions of the caudal fastigial nucleus result in
hypermetric ipsilateral saccades and hypometric contralateral saccades, whereas bilateral
lesions result in hypermetria of all horizontal saccades (Robinson et al. 1993). Caudal
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fastigial nucleus lesions also result in saccades that are more variable in amplitude when
compared with normal saccades (Robinson et al. 1993).
The flocculus and paraflocculus are important for ensuring that steady gaze is
maintained at the end of a saccadic eye movement, since lesions of these structures result
in post-saccadic drift (Zee et al. 1981). The post-saccadic drift that occurs at the end of
saccadic eye movements in subjects with floccular/parafloccular lesions is thought to be
mainly due to abnormal matching of the pulse and step signals.
2.6
Summary
The ocular motor system has two general functions: to keep the eyes fixed on
targets of interest, and to move the eyes from one target to another. Several classes of eye
movement have evolved so that these functions may be fulfilled in a variety of situations.
Amongst these classes of eye movement are vestibular-evoked eye movements, which
keep the eyes fixed on a target during brief head movements, and saccadic eye
movements, which rapidly move the eyes from one target to another target of interest.
Normal eye movements come about as a result of coordinated contraction and
relaxation of the six extra-ocular muscles, which are innervated by cranial nerves III, IV,
and VI. Both eye position and eye velocity signals must be conveyed in these nerves, to
bring about normal eye movement trajectories and to ensure that the eye remains fixed on
the target of interest following the eye movement. In the case of saccadic eye movements,
the eye velocity signal is generated by the EBNs in the brainstem. The EBNs also send
collaterals to the neural integrator, which generates the eye position signal. The eye
velocity and eye position signals are then combined in the ocular motor nuclei prior to
being relayed to the extra-ocular muscles.
Recent studies of orbital anatomy have demonstrated the presence of muscle
pulleys, which are connective tissue sleeves that surround the rectus tendons near their
insertions on the eyeball. The pulleys change the pulling directions of the tendons in a
manner that depends on the instantaneous eye position. The discovery of these structures
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has prompted a revision of theories attempting to explain how eye movements are
programmed and, hence, how their 3-d kinematic properties arise (see chapter 4). As there
is a comparison between the kinematic properties of saccadic and vestibular-evoked eye
movements in the current project, a description of the anatomy and physiology of the
vestibular system is presented in chapter 3.
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