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8.1 Introduction
Normal visual perception requires the proper functioning of ocular motor systems that control the position and movement of the eyes to focus the
image of the object-of-interest (i.e., the visual target) on corresponding areas of the retinas of the two eyes. For example, in addition to producing
adjustments in pupil size and lens refraction, accommodation involves the convergence of the two eyes to direct onto the foveae the images of near
objects. Eye movements are also controlled to direct the eyes towards a visual target and to follow the movements of the visual target. Such eye
movements are controlled by gaze systems. They coordinate the movement of the two eyes to ensure that the images on the two retinas fall on
corresponding areas of the binocular field. When this fails, diplopia (double vision) results.
Figure 8.1
The extraocular muscles of the right eye and their actions. Antagonistic actions pull the
eye in opposite directions whereas synergistic actions pull the eye in the same
direction.
For each eye, six muscles work together to control eye position and movement. Two extraocular muscles, the medial rectus and lateral rectus, work
together to control horizontal eye movements (Figure 8.1, left).
Contraction of the medial rectus pulls the eye towards the nose (adduction or medial movement).
Contraction of the lateral rectus pulls the eye away from the nose (abduction or lateral movement).
The actions of these two muscles are antagonistic: one muscle must relax while the other contracts to execute horizontal eye movements. Four other
extraocular muscles working together control vertical eye movements and eye rotation around the mid-orbital axis (Figure 8.1, right). Contraction of the
To direct the eye upward or downward, two muscles contract synergistically as the two antagonist muscles relax. For example, to elevate the eye while
looking straight ahead, the superior rectus and inferior oblique contract together as the inferior rectus and superior oblique relax. The superior rectus
and inferior oblique muscles working together pull the eye upward without rotating the eye. To depress the eye while looking straight ahead, the inferior
rectus and superior oblique contract together as the superior rectus and inferior oblique relax. The inferior rectus and superior oblique working together
pull the eye downward without rotating the eye.
Three cranial motor nuclei provide efferent control of the extraocular muscles. Activation of the motor neurons produces contraction of the innervated
muscle.
Figure 8.2
The axons of the abducens interneurons decussate and travel in the
medial longitudinal fasciculus to the contralateral oculomotor nucleus to
excite the motor neurons controlling the medial rectus of the eye
contralateral to the abducens nucleus.
The motor neurons controlling synergist and antagonist muscles must coordinate their activities to produce the desired eye movements. Within the
abducens nucleus are abducens interneurons, which send their axons into the contralateral medial longitudinal fasciculus (MLF). They ascend in
the MLF to end on oculomotor neurons controlling the medial rectus (Figure 8.2). The abducens interneurons coordinate the activity of the ipsilateral
lateral rectus with that of the contralateral medial rectus. For example, excitation of the motor neurons in the left abducens nucleus will result in
contraction of the left lateral rectus and abduction of the left eye (i.e., movement of the left eye towards the left). Excitation of the interneurons in the
left abducens nucleus will excite neurons in the right oculomotor nucleus that innervate the right medial rectus. Contraction of the right medial results in
adduction of the right eye (i.e., movement of the right eye towards the left). Consequently, both the right and left eyes will be directed towards the left
when the left abducens nucleus is excited.
Interconnections between the trochlear nucleus and oculomotor nuclear complex coordinate their activity to allow the upward and downward
movement of the eyes. These interconnecting axons appear to travel along with the fibers of the tectospinal tract (that is, they do not travel in the
medial longitudinal fasciculus).
Table I
Classification of Eye Movements
Eye Movement Type Function
Gaze Stabilization
Vestibulo-ocular
Initiated by vestibular mechanisms during brief/rapid head movement
Optokinetic (vestigial in humans) Initiate by visual mechanisms during slow head movement
Gaze Shifting
Vergence
Adjusts for different viewing distance
Smooth Pursuit Follows moving visual target
Saccade Directs eyes toward visual target
Vestibulo-ocular reflexes produce eye movements that compensate for head movements detected by the vestibular system. You have learned in earlier
chapters how the vestibular system detects head movements and initiates the vestibulo-ocular responses.
B. Optokinetic Nystagmus
Notice that optokinetic nystagmus is a visual-ocular response - driven by visual stimuli moving across the visual field. Vestibular nystagmus is a
vestibulo-ocular response - driven by a vestibular stimulus (i.e., accelerating head movement). In humans, the smooth pursuit system predominates
in producing eye movements that track moving visual targets. As the optokinetic system is vestigial in humans, it will not be covered in this lecture.
8.4 Gaze Shifting: Eye Movements to Focus the Image on the Fovea
Three gaze shifting systems function during foveation: smooth pursuit, which directs the eyes to follow a moving visual target; saccade, which directs
the eyes toward a visual target; and vergence, which alters the angle between the two eyes to adjust for changes in distance from the visual target.
We have covered the neural control of convergence during accommodation in the previous lecture.
A. Voluntary Saccades
Voluntary or guided saccades are eye movements initiated to bring an object-of-interest into view or initiated under direction (e.g., to the command
“eyes left”). Saccades consist of short, rapid, jerky (ballistic) movements of predetermined trajectory that direct the eyes toward some visual target.
are involved in initiating voluntary saccades that locate and focus on a particular object-of-interest.
are located posteriorly in the middle frontal gyrus.
compute the direction and amplitude of the saccade.
send their axons in the internal capsule, crus cerebri and corticotectal tract to the midbrain where they decussate and end in the superior
colliculus.
Figure 8.3
The voluntary saccades circuit. The frontal eye field
generates the command signals that initiate eye
movement in a contralateral direction (i.e., to the right in
this figure). The signal is sent to the superior colliculus
and caudate nucleus. The superior colliculus, in turn,
sends control signals to the gaze centers in the midbrain
and pons reticular formation. The posterior parietal
cortex, part of the dorsal visual stream, determines
whether the visual target has been achieved and sends
corrective signals to the frontal eye field and superior
colliculus when the visual target has not come into view.
The basal ganglion structures, the caudate and
substantia nigra, help regulate the action of the superior
colliculus.
The superior colliculus can initiate and control saccades independent of input from the frontal eye field. However, the motor control signals initiated
by the frontal eye field and the superior colliculus differ in function.
Normally the frontal eye field initiates voluntary and memory-guided saccades,
whereas the superior colliculus initiates reflex orienting saccades.
However, when the frontal eye field is damaged, the superior colliculus will compensate for the loss following a short period of dysfunction. For
example, damage to the right frontal eye field produces a transient inability to look voluntarily to the left side.
Because voluntary saccades are not, in general, initiated by visual stimuli, afferent visual control occurs only after the fact. That is, the visual system
(i.e., the posterior parietal visual association cortex6 in Figure 8.3) is used to determine whether the saccade was successful in bringing the desired
object into view. Consequently, the saccades consists of a series of short, fast eye movement, followed by a check by the visual system as to whether
the desired visual target is in view, which may be followed by another series of brief eye movements to locate the visual target. The repeated sequence
of brief, rapid eye movements and image check until the visual target is in view characterizes saccades.
B. Smooth Pursuit
Smooth pursuit (tracking) is an eye movement elicited by a moving visual target that the eyes follow voluntarily or under direction (e.g., the request to
"watch the moving pen"). Pursuit movements are described to be voluntary, smooth, continuous, conjugate eye movements with velocity and trajectory
determined by the moving visual target. By tracking the movement of the visual target, the eyes maintain a focused image of the target on the fovea.
Notice that a visual stimulus (the moving visual target) is required to initiate this eye movement.
Temporal eye field neurons in the non-human primate (parts of Brodmann's areas 39 or MST- medial superior temporal gyrus & 37 or MT- middle
temporal gyrus.
are believed to be involved in the initiation and guidance of smooth pursuit eye movements7(Figure 8.4)
compute the direction and velocity of the moving visual target.8
correspond to neurons in superior temporal-inferior parietal areas in humans. That is, damage to the temporal-parietal areas in humans produce
symptoms similar to those produced by damage to MT and MST in non-human primates.
send their axons to the dorsolateral pontine nucleus (DLPN).
appear to initiate the smooth pursuit - at the request of the temporal eye field neurons
also send their axons to the dorsolateral pontine nucleus
computes the direction and speed of eye movement (pursuit) necessary to match the direction and velocity of the moving visual target
axons decussate and end in the contralateral cerebellum9
The cerebellum
send axons to the abducens, trochlear and oculomotor nuclei via the medial longitudinal fasciculus
control smooth pursuit eye movements - for the temporal eye field
Consequently, the vestibular nuclei help coordinate the activities of antagonist muscles involved in eye movements during smooth pursuit and
vestibule-ocular reflexes.10
Note that there are two decussations (double crossings) involved in the horizontal smooth pursuit pathway (i.e., the DLPN axons and the axons of the
vestibular nuclei providing excitatory input to the abducens nucleus). Consequently, the command signals generated by the MST and MT cortical
neurons result in an execution of smooth pursuit eye movement in a direction ipsilateral to these cortical neurons. Normally, a command generated by
the left MST and MT cortical neurons results in both eyes tracking the movement of an object moving to the left.
Figure 8.4
The smooth pursuit pathway. The temporal eye
field sends signals to the dorsolateral pontine
nuclei indicating the direction and velocity of
movement of the visual target. The dorsolateral
pontine nuclei determines the direction and
velocity of eye movement necessary to tract the
visual target and sends that information on to
cranial nerve nuclei by way of the cerebellum
and vestibular nuclei. That is, this pathway
engages the vestibulo-ocular circuit to control
smooth pursuit eye movements. The frontal eye
field appears to initiate, but not direct, the eye
movement "at the request" of the temporal eye
field.
Damage to the lower motor neurons that innervate an extraocular muscle results in a flaccid paralysis of the muscle, whereas damage to upper motor
neurons produce deficits only in selective types of movements (e.g., smooth pursuit).
Damage to an extraocular muscle’s motor neurons results in a paralysis of the muscle that is often manifested as a strabismus (a misalignment of the
two eyes). At rest (while attempting to look straight ahead), the denervated eye is deviated from its normal position by the unopposed action of the
muscle that is its antagonist. The strabismus may result in double vision (diplopia) because the image falling on the retina of each eye will be from non-
corresponding areas in the binocular visual fields. When the patient closes one eye, the double image is replaced by a single image.
Damage to the oculomotor nerve. As we have already covered this topic in the previous lecture, a brief summary of the effect of oculomotor nerve
lesion on eye movements will be presented.
All of the extraocular muscles, except the lateral rectus and superior oblique, will be denervated and paralyzed and the patient will be unable to
elevate or adduct the eye ipsilateral to the oculomotor nerve damaged.
The innervation of the superior palpebrae muscle and the ciliary ganglion (postganglionic parasympathetic innervation of the iris sphincter and
ciliary muscles) will also be lost. Consequently, there will be ptosis, dilated pupil and lateral strabismus in the denervated eye.
Figure 8.5
Observe the patient's response to the commands
of the control buttons.
Symbols: The arrow indicates the direction of the
Rig ht Le ft eye movement. The plus symbol represents the
position of the eye that has not deviated from mid
PLAY PLAY PLAY position.
LOOK RIGHT LOOK S TRAIGHT LOOK LEFT
c 2000 UTHS CH
at rest, the eye is deviated down and laterally (is depressed and abducted) - a lateral strabismus - because the lateral rectus is unopposed.
on an attempted gaze to the right, the left medial rectus will not contract to adduct the left eye (i.e., it will not move the eye toward the nose,
medially).
Consequently, at rest and during an attempted right lateral gaze, the lateral strabismus will result in a diplopia. On attempting to adduct the eye (i.e.,
look right or during convergence), the left lateral rectus relaxes and the left eye deviates to the midline, but not past it.
Damage to the trochlear nerve. When the trochlear nerve is damaged, the symptoms are mild. The downward and lateral movement of the eye may be
weakened and may cause diplopia when reading or descending stairs. A patient may present with his head tilted because the damaged eye is extorted
(i.e., rotated with top of the eye tilted away from the nose) and slightly elevated because of the paralysis of the superior oblique muscle. Tilting the
head away from the affected eye brings the visual axis of the partially paralyzed eye into alignment with the visual axis of the normal eye.
Figure 8.6
Observe the patient's response to the
commands of the control buttons. Symbols: The
arrow indicates the direction of the eye
Rig ht Le ft movement. The plus symbol represents the eye
that has not deviated from mid position.
PLAY PLAY PLAY
LOOK RIGHT LOOK S TRAIGHT LOOK LEFT
c 2000 UTHS CH
is not sensory
involves only one eye
may involve an extraocular muscle or its lower motor neurons
lateral rectus OR
abducens nerve
left side (i.e., the symptoms are ipsilesional)
Electrophysiological tests indicate that the left lateral rectus is responsive (i.e., normal). You conclude that the left abducens nerve has been damaged.
Damage to the abducens nerve. The lateral rectus will be denervated and paralyzed and the patient will be unable to abduct the eye. For example, if
the left abducens nerve is damaged, the left eye will not abduct fully (move away from the nose, towards the left, laterally). While attempting to look
straight ahead, the left eye will be deviated medially towards the nose (medial or nasal strabismus) due to the unopposed action of the medial rectus
of the left eye. On attempting to gaze left, the left eye may deviate to the midpoint, but not past it, because the medial rectus of the left eye is relaxed.
The patient may complain of double or blurred vision (diplopia) when looking towards the ipsilesional side (i.e., left) or when looking straight ahead.
Damage of upper motor neurons does not result in a flaccid paralysis. However, the muscle will not be activated into the response normally controlled
by the upper motor neuron (e.g., voluntary saccades controlled by the frontal eye field). However, the muscle will perform reflex responses (e.g.,
convergence during accommodation or nystagmus during head rotation) and responses controlled by other intact ocular motor circuits.
Figure 8.7
Observe the patient's response to the
commands of the control buttons. Symbols:
The arrow indicates the direction of the eye
Rig ht Le ft movement. The plus symbol represents the
position of the eye that has not deviated from
PLAY PLAY PLAY mid position.
LOOK RIGHT LOOK S TRAIGHT LOOK LEFT
c 2000 UTHS CH
Neural imaging tests indicate a small infarct (i.e., a lacunar stroke) in the region of the left facial colliculus. You conclude that the damaged area
includes the left abducens nucleus.
Damage to the abducens nucleus. The result is an abnormality of conjugate horizontal eye movements called lateral gaze paralysis. With the eyes at
rest, there is a medial strabismus in the eye ipsilateral to the damage (indicating abducens motor neuron damage). During an attempted lateral gaze,
both eyes cannot be moved beyond the midline in an ipsilesional direction (i.e., toward the damage side). As the left abducens interneurons send
axons to the right oculomotor neurons innervating the medial rectus of the right eye (Figure 8.2), the failure to perform a lateral gaze to the left
suggests an abducens nucleus lesion. An attempted lateral gaze in a contralesional direction (away from the damaged side) is successful. Note that as
the lower motor neurons (i.e., the abducens motor neurons), as well as a motor control center (i.e., the abducens interneurons), are damaged, both
reflex and voluntary eye movements in the horizontal plane are affected.
An example of the effect of damage to the medial longitudinal fasciculus is presented in the Appendix.
Figure 8.8
Observe the patient's response to the commands of
the control buttons. Notice at the "look straight"
command, this patient exhibits a "left gaze preference"
when the eyes are at rest. Symbols: The arrow
Rig ht Le ft indicates the direction of the eye movement. The plus
symbol represents the position of the eye that has not
PLAY PLAY PLAY
deviated from mid position.
LOOK RIGHT LOOK S TRAIGHT LOOK LEFT
c 2000 UTHS CH
are directed to the left at rest (i.e., exhibits a left gaze preference)
have full mobility when looking up and down and to his left
cannot move together toward the right (i.e., both eyes stop at mid position).
is not sensory
involves a right hemiplegia (i.e., he can't move his right body or face)
involves Broca's aphasia (i.e., his speech is non-fluent)
involves failure of both eyes to perform a lateral gaze to the right
Neural imaging tests indicate infarction of branches of the medial cerebral artery supplying the lateral surface of the left frontal cortex.
Damage to the voluntary saccades circuit. Damage to the frontal cortical eye field and the midbrain (superior colliculus) effect voluntary and reflex
saccades, particularly those in the horizontal plane. Immediately following unilateral damage of the frontal cortical eye field, there is an inability to
voluntarily initiate a horizontal eye movement in a direction contralateral to (away from) the side of the lesion. That is, immediately following a right
frontal lobe lesion, both eyes cannot be moved voluntarily to the left beyond the midline. However, both eyes will move to the left beyond the midline to
vestibular stimulation. Both eyes can also be directed to the side ipsilateral to the lesion and may tend to deviate toward the lesion when the eyes are
at rest. The deficits disappear with time if the damage is localized to the frontal cortical eye field and does not involve the superior colliculus.
Figure 8.9
Observe the patient's response to the commands
of the control buttons. Notice at the "look straight"
command, the patient's eyes tend to wander when
at rest. Also notice at the "look left" command, the
patient's eyes tend to move in a jerky, step-like
Rig ht Le ft manner. Symbols: The arrow indicates the
direction of the eye movement. The plus symbol
PLAY PLAY PLAY
represents the position of the eye that has not
LOOK RIGHT LOOK S TRAIGHT LOOK LEFT deviated from mid position.
c 2000 UTHS CH
is not sensory
involves Wernieck's aphasia (i.e., impaired comprehension and inability to repeat)
involves failure of smooth pursuit to the left
Neural imaging tests indicate infarction of branches of the left medial cerebral artery supplying the caudal superior temporal gyrus and inferior parietal
gyrus.
Damage to the smooth pursuit circuit: Damage to the temporal eye field causes deficits in the ability to fixate on objects and to track them. Attempts to
fixate on a target will be undermined by severe instability and wandering of the eyes. Tracking movements are jerky rather than smooth when
attempting to follow an object moving in a direction toward (ipsilateral to) the side of the lesion. Note that the smooth pursuit circuit includes a double
crossing and the temporal eye field controls ipsilateral eye movements (i.e., right cortex controls smooth pursuit to the right). When the temporal eye
field is damaged, the two eyes may follow a visual target in an ipsilesional direction; but does so using the voluntary saccades circuit. That is, if the
frontal cortical eye fields are intact, the eyes may be moved voluntarily (guided saccade) toward an object of interest ipsilateral to the impairment.
However, in this case, the movements will be jerky unlike the eye movements in smooth pursuit. Tracking of visual targets contralateral to the lesion
will be smooth.
8.10 Summary
This chapter reviews the ways in which voluntary eye movements are initiated by cerebral cortical activity and involve more ocular motor control
structures than the simple ocular reflexes. The cortical areas initiate eye movements and work through brainstem ocular motor centers to produce a
response, i.e., there are no direct connections between the cerebral cortex and the extraocular motor nuclei. The smooth pursuit system utilizes a
pontine nucleus, the cerebellum, and the vestibulo-ocular reflex pathway to execute eye movements to tract visual targets. The voluntary saccades
system is similar to other voluntary motor systems in engaging areas in the frontal cortex to initiate the response and in influencing the motor neurons
indirectly through lower motor control structures (i.e., the vertical and horizontal gaze centers). The gaze centers function to coordinate and control the
activity of motor neurons to insure that the extraocular muscles act synergistically to produce conjugate saccades.
Question 1 A B C D E
A. Vestibular nystagmus
B. Optokinetic nystagmus
C. Saccades
D. Smooth pursuit
E. Accommodation
Question 2 A B C D E
A 57-year old male with a past history of high blood pressure awakens with a terrible headache. His eyes tend to drift
about and when he is asked to track a pen moving to his left, both eyes move in short, jerky steps. In contrast, both eyes
move smoothly when his eyes track a pen moving to his right. Given the patient's history, a radiological study is
scheduled to determine whether a stroke had occurred. The study determines the area of infarction to include which of
the following?
Example A1
Symptoms. A patient visits his primary care physician at the urging of his wife. She noticed that his left eye lid was drooping slightly and that his face appeared flushed. She was concerned he might have suffered a stroke. On examination, it was noted that his le
Figure 8.A1
Observe the patient's eyes under low illumination.
Also observe the reaction of the patient's eyes to
Rig ht Le ft light directed in the left or right eye.
PLAY RES ET PLAY
Lig ht rig ht e ye Lig ht le ft e ye
c 2000 UTHS CH
not sensory
an autonomic motor dysfunction
Pathway(s) affected: You conclude that structures in the following motor pathway have been affected is
Sympathetic Innervation of the Eye. Horner's syndrome is a constellation of symptoms that includes miosis, pseudoptosis and enopthalmosis (sunken eyeball). It is characteristic of damage to the sympathetic innervation of the face provided by the superior cervic
Example A2
Symptoms. A 35 year-old female complains that she has double vision when she attempts to look to the right. When looking straight ahead, both her eyes assume normal positions (Figure 8.A.2). She is able to look up and down and to the left with both eyes. Ho
Figure 8.A2
Observe the patient's response to the commands
of the control buttons. Symbols: The arrow
indicates the direction of the eye movement. The
Rig ht Le ft plus symbol represents the position of the eye that
has not deviated from mid position.
PLAY PLAY PLAY
LOOK RIGHT LOOK S TRAIGHT LOOK LEFT
c 2000 UTHS CH
is not sensory
does not present with a strabismus when the eyes are at rest position
involves the left eye only when attempting a lateral gaze to the right
is not lateral gaze paralysis because the left eye can be abducted when looking left
is not paralysis of the left medial rectus because the left eye can be adducted during convergence and does not exhibit lateral strabismus at rest.
do not involve lower motor neurons or muscles (i.e., the left eye can adduct during convergence)
involve upper motor neurons (i.e., conjugate lateral eye movements)
Neural imaging tests indicate demyelination of the medial longitudinal fasciculus on the left side.
Damage to the medial longitudinal fasciculus. The medial longitudinal fasciculus (MLF) is a fiber tract that contains, in part, axons of the vestibular nuclei and of the contralateral abducens interneurons. Lesions in the MLF results in an abnormality of conjugate ho
Figure 8.A3
The left medial longitudinal
fasciculus has been damaged
and cannot carry excitatory
signals from the right
abducens interneurons to the
left oculomotor neurons
controlling the left medial
rectus.
Recall the left MLF carries the axons of the right abducens interneurons to the left oculomotor neurons, which control the medial rectus of the left eye (Figure 8.A.3). Also recall that contraction of the medial rectus of the left eye directs the left eye nasally (i.e., con
Both eyes are adducted on convergence as the axons from the supraoculomotor area to the oculomotor neurons controlling the medial rectus muscles of the two eyes are not affected by MLF lesions.
Table II
Classification of Eye Movement & Their Neural Control Structures
Eye
Function Afferent Input* & Motor Control Structures
Movement
Cerebellum
Follows
Smooth (watches) a Lateral Pursuit: Medial Vestibular nucleus
Pursuit moving visual
target
VIm Lateral Rectus of One Eye
KEY: VII - Abducens Interneuron; VIm - Abducens Motor Neurons; III - oculomotor Motor Neurons; IV - Trochlear Motor Neurons
[1] Note that each oculomotor nerve controls the extraocular muscles of its ipsilateral eye, i.e., the right nerve controls the superior and inferior oblique and superior and
inferior rectus of the right eye.
[2] For the curious, the vertical gaze center is located in the rostral interstitial nucleus of the medial longitudinal fasciculus and, according to some, also in the interstitial
nucleus of Cajal.
[3] This is all you need to know about the role of the basal ganglion for ocular motor tasks.
[6] Recall the posterior parietal cortex is part of the dorsal visual stream that determines the "where" of the visual scene (i.e., the location and movement of the visual
target).
[7]Please note this is in disagreement with Nolte, pg. 521, Figure 21-15, which identifies the extrastriate cortex as the course o the cortical neurons controlling smooth
pursuit.
[8]Recall from the lectures on the visual system that these cortical areas, MST and MT, are part of the visual sensory circuit involved with detecting the "where" of a
visual stimulus.
[9]For the curious, the DLPN axons end in the flocculus, paraflocculus & vermis of the cerebellum.
[10] the paramedian pontine reticular formation and abducens interneurons coordinate the activities of antagonistic muscles involved in horizontal eye movements
during saccades.