5: Examination of the Central Ocular Motor Systems

A. The eyes move at two speeds, fast and slow (Dell'Osso and Daroff, 1999)

1. Physiologic fast eye movements, saccades, include:

   1. All voluntary horizontal and vertical eye movements

   2. The kickback phase of jerk nystagmus, whether pathologic or physiologically induced by caloric or optokinetic stimuli

   3. Rapid eye movements in sleep

2. Pathologic fast eye movements, opsoclonus and ocular flutter, are faster than any saccades that the person can produce by volitional eye movements and are described later.

3. Slow eye movements include:

   1. Smooth pursuit

   2. Vergences (convergence/divergence)

   3. The deviation phase of vestibular and optokinetic nystagmus

B. The five eye movement systems tested by the neurologic examination

Five central systems control voluntary and reflex eye movements. Voluntary selection of a visual target requires saccadic action to move the eyes to the target. After that, fixation, fusion, following, and focusing (vergences and the control of refraction) proceed more or less automatically (Table 5-1).

1. Saccadic system: saccade = to jerk or reign in. Saccadic movement describes eye movements by increments or jerks, like a ratchet (Kennard et al., 1994).

   1. Self-demonstration of saccades:

      1. Look straight ahead. Then, while keeping your head completely still, move your eyes all the way to the right and hold them there.

      2. With your head still, very slowly try to move your eyes as continuously and smoothly as possible all the way from the right to the left. Attend to how your eyes move. Do they move continuously and smoothly or by incremental jerks?

         _______________________________________________

         You will experience your eye movements as jerks, that is, saccades. Try this experiment on other people and observe their saccades.

   2. You cannot move your eyes smoothly voluntarily. All volitional eye movements require saccades.

   3. Frontotegmental corticobulbar pathways are thought to mediate all such saccades (Fig. 5-1).

   4. The supplementary motor area, substantia nigra, superior colliculus, vermis, fastigial nucleus, reticular formation, and vestibular system play roles in saccadic production and accuracy.

   5. To test for saccadic accuracy: Hold up your index fingers about 18 in. apart and ask the patient (Pt) to look at one and then the other. Move the targets around to require the Pt to look at different sites. Saccadic accuracy depends on connections in the dorsal part of the cerebellar vermis and the fastigial nuclei.

2. Fixation (position holding) system

   1. After you choose a visual target and voluntarily saccade onto it, fixation reflexes hold the eyes on the target and promote fusion of both retinal images into one sharp visual image. Breaking away from the chosen target requires generation of another saccade to jerk the eyes away and onto a new visual target. Fixation reflexes tend to keep the eyes on target when the head moves.

   2. Retino-geniculo-occipito-tegmental and retino-occipito-fronto-tegmental pathways mediate fixation and fusion.

3. Smooth pursuit system

   1. Self-demonstration of smooth pursuit:

      1. Keep your head still and facing straight ahead throughout this exercise.

      2. Move your eyes all the way to the right, but this time hold up your finger about 30 cm away, fixate on it, and move it slowly all the way across from right to left. Allow only your eyes to pursue it. If you actually keep your head still and keep your eyes fixed on the moving finger, you will experience smooth rather than saccadic movement.

      3. Practice eliciting smooth pursuit on another person.

   2. The smooth pursuit system keeps the eyes on target when the target moves. Drug intoxication, including alcohol, causes irregular or jerky rather than smooth pursuit of a moving object.

   3. Retino-geniculo-occipito-parieto-frontal-tegmental pathways mediate smooth pursuit.

4. Vergence system

   1. This system converges or diverges the eyes to ensure fusion of the two retinal images and appropriate refraction when the person looks at a near or distant visual target. It also keeps the eyes on target as the target moves toward or away from the person. This system mediates the accommodation reflex.

   2. The vergence system depends on retino-geniculo-occipito-tegmental pathways.

5. The counter-rolling system of the eyes

   1. Self-demonstration of counter-rolling of the eyes:

      1. Hold up your finger at arm's length, directly in front of you. Then, while holding your finger still, fixate on it and move your head horizontally and vertically.

      2. Your eyes will reflexly counter-roll against the direction of head movement to maintain fixation on the chosen visual target.

   2. In the alert Pt, two systems collaborate to hold the eyes on target:

      1. The ocular fixation system.

      2. The proprioceptive system. It arises in the vestibule and neck. It counter-rolls the eyes, an action called the vestibulo-ocular reflex (VOR).

   3. In the comatose Pt who cannot fixate, the examiner (Ex) can move the Pt's head (doll's eye maneuver) to test the counter-rolling reflex (VOR). See VOR in Chapters 9 and 12. Absence of fixation during coma makes counter-rolling depend on the VOR.

6. In summary

   1. If the visual target moves, the smooth pursuit system holds the eyes on target.

   2. If the Pt is conscious and if the head moves, the fixation reflexes and VOR keep the eyes on a target that is still.

   3. If the Pt is unconscious, only the proprioceptive reflexes can act, because the Pt cannot fixate.

7. Now, I haven't just loaded on you five more things to memorize. If you did the exercises, the following mnemonic will work:

   A mnemonic to recall the five eye-movement systems

   1. Hold up your finger and choose to look at it. Your saccadic system will move your eyes onto the target. You have tested the frontotegmental pathways.

   2. Your fixation system will lock the eyes on target until something, a saccade or a reflex, moves them off. You have tested the retino-geniculo-occipitotegmental pathways.

   3. Move your finger right or left or up or down, and the smooth pursuit system will maintain fixation on the target. You have tested the horizontal conjugate movement and the vertical conjugate movement pathways.

   4. Hold your finger still and move your head right or left or up or down, and the counter-rolling system will maintain fixation on the target. You have tested the vestibular and neck proprioceptive and fixation pathways.

   5. Move your finger toward or away from your eyes. The vergence system then angles the eyes to keep them foveated on target and at the same time initiates the accommodation reflex. You have tested the retino-geniculo-occipito-tegmental pathways.

8. The foregoing exercises involved a still head or a still target. If the head and eyes both move toward a target, the counter-rolling by the VOR opposes the head and eye movement and undergoes suppression.

C. The corticopontine pathway for voluntary conjugate horizontal eye movements

1. Different pathways mediate conjugate vertical and horizontal eye movements. The pathway for voluntary conjugate horizontal eye movements begins in the cortex of the posterior-inferior part of the frontal lobe and runs to the pontine tegmentum (Fig. 5-1).

2. This cortical pathway terminates in the paramedian pontine reticular formation (PPRF) near the midline of the pons and responsible for generating horizontal eye movements. This region sends fibers to the ipsilateral abducens nucleus. The abducens nucleus sends fibers via cranial nerve VI to the ipsilateral lateral rectus muscle and, via the medial longitudinal fasciculus (MLF), also sends fibers that cross to the opposite medial rectus subnucleus. The medial rectus subnucleus innervates the medial rectus muscle. Thus, stimulation of the right PPRF or right abducens nucleus will make the eyes deviate conjugately to the right. (Frohman et al., 2001; Fig. 5-1).

3. Effects of interruption of the horizontal gaze pathway

   1. Interruption of the cortical efferent pathway for horizontal movements rostral to its decussation results in deviation of the eyes ipsilateral to the lesion (the eyes "look toward the lesion"), because the opposite pathways are intact and continue to convey tonic innervation.

   2. Interruption caudal to the decussation results in deviation to the side contralateral to the lesion.

4. Effects of interruption of one MLF

   1. After interruption of one MLF, say the right (tip of the arrow in Fig. 5-1), the right eye will not adduct when the Pt attempts to look to the left (Ross and DeMyer, 1966).

   2. In addition to adductor paralysis on left lateral gaze, the Pt's left eye undergoes oscillations, a feature that you cannot deduce from the diagram. Such ocular oscillations are called nystagmus. Hence, a second sign of the MLF syndrome is monocular nystagmus of the abducting eye. At rest the eye has no nystagmus. It occurs only during abduction. The symptoms accompanying the eye movements are diplopia and oscillopsia (oscillating vision).

   3. These two signs, paralysis of the adducting eye and nystagmus of the abducting eye, appear only on gaze to the opposite side of the MLF lesion.

      1. The eyes adduct normally on convergence.

      2. The corticobulbar pathways for convergence and vertical eye movements run directly into the mesencephalon to the LMNs of the III and IV nuclei, rather than looping down into the pons and returning in the MLF.

   4. After a left-sided MLF lesion, what would be the only direction of gaze that would cause diplopia and heterotropia? (To reason out the answer from Fig. 5-1, draw in the pathway from the left cerebral hemisphere with colored pencil) □ looking right/□ looking left/□ looking straight ahead

      ☑looking to the right

   5. Summary of the signs and symptoms of the MLF syndrome

      1. The signs of a unilateral MLF lesion consist of heterotropia and monocular nystagmus. They appear only when the Pt attempts to look away from the side of the interruption of the MLF. Other eye movements, including conjugate vertical gaze and pupillary responses remain normal.

      2. The symptoms of a unilateral MLF lesion may include diplopia and oscillopsia.

      3. During horizontal gaze the Pt cannot □ abduct/□ adduct the eye ipsilateral to the lesion and shows monocular nystagmus of the contralateral, □ abducting/□ adducting eye.

         ☑ adduct; ☑abducting

   6. Describe the signs of a bilateral MLF lesion at the level of the arrow in Fig. 5-1.

      _______________________________________________________

      ______________________________________________

      Monocular nystagmus of the leading (abducting) eye on attempted gaze to either side. Paralysis of adduction of the following (adducting) eye on attempted gaze to either side. The other eye movements and pupillary responses remain.

   7. Would the eyes of a Pt with a bilateral MLF lesion converge during accommodation? □ Yes/□ No. Explain.

      ________________________________________________

      ☑ Yes. The convergence pathways run directly into the midbrain without involving the MLF.

D. Bilateral destruction of the frontal corticotegmental pathway for horizontal gaze (supranuclear paralysis of gaze)

1. If bilateral lesions destroy the pathway to the brainstem from the frontal eye fields, the Pt cannot produce saccades to voluntarily move the eyes to either side, but the vestibular counter-rolling reflexes can still move the eyes to the sides. Some weakness of vertical gaze is present or will develop because the Pt often has a progressive dementia or severe bilateral cerebrovascular disease.

2. After paralysis of voluntary movements, the vestibulo-ocular and fixation reflexes tend to become overly active ("released"). Indeed the full movement of the eyes by reflexes establishes that the LMNs of the ocular motor system are intact and that the cause for the paralysis of eye movements is supranuclear, in the UMNs. The Pt cannot voluntarily break fixation by moving the eyes and must blink or jerk the head to interrupt the afferent arc that maintains the fixation reflex. This condition when seen congenitally in children is called Cogan's syndrome of oculomotor apraxia.

3. The slow deviation phase of calorically induced or optokinetic nystagmus remains but the saccadic kickback fails, because the saccades depend on the integrity of the frontal eye fields.

4. Another form of progressive supranuclear palsy, called the Steele-Richardson-Olszewski syndrome, affects vertical movements first, usually the downward before the upward (Liu et al., 2001; Steele, 1994), and then horizontal movements. The lesion responsible affects the midbrain and basal forebrain structures.

E. Cortical pathway for vertical eye movements

1. Pathways for vertical eye movements arise diffusely from frontal and parietal cortices. Like the convergence pathways, they project directly to the midbrain, without looping down into the pons and reflecting back in the MLF.

2. The cortical pathway for conjugate upward eye movements runs in the tegmentum dorsal to the pathway for downward movements (Bhihdayasiri et al., 2000).

   1. Parinaud's syndrome: Dorsal compression of the midbrain, as from a pineal tumor, mesencephalic hemorrhage or obstructive hydrocephalus, will selectively impair upward vertical movements (Parinaud's syndrome) before affecting downward gaze. Convergence palsy and light-near dissociation of the pupils are commonly present also.

   2. Bell's phenomenon (Sir Charles Bell, 1774–1842)

      1. When most persons attempt to close their eyes, the eyeballs automatically rotate upward and somewhat outward. This associated eyeball movement, called Bell's phenomenon, occurs during voluntary eyelid closure or sleep, but closure of the eyelid by the orbicularis oculi muscle obscures it.

      2. In a Pt with UMN paralysis of voluntary elevation of the eyes, the presence of Bell's phenomenon proves that the midbrain and LMNs for the eye elevation are intact.

      3. The Ex will most easily see Bell's phenomenon if interruption of the facial nerve paralyzes the face, preventing eyelid closure. Idiopathic interruption of the facial nerve is called Bell's palsy (Chapter 7).

3. The cortical pathway for conjugate downward eye movements runs into the midbrain tegmentum dorsomedial to the red nucleus, where a lesion may selectively affect it, sparing vertical and horizontal eye movements (Bhihdayasiri et al., 2000). The lesion interrupts connections with the rostral interstitial nucleus of the MLF (riMLF), the saccadic brainstem center for vertical eye movements (Fig. 5-2), just as the PPRF is a brainstem center for horizontal saccades (see Fig. 5-1).

F. Comparison of the LMN (nuclear), internuclear, and UMN (supranuclear) lesions of the ocular pathways

1. Interruption of LMNs of cranial nerve (CrN) III, IV, or VI paralyzes individual extraocular muscles (EOMs) or sets of muscles. No reflex or voluntary act can activate a muscle affected by LMN paralysis. The Pt suffers diplopia and strabismus.

2. Interruption of internuclear pathways, such as the MLF, paralyzes only movements mediated through that pathway. Other reflexes or voluntary pathways can still activate the ocular muscles. The Pt has diplopia only when that pathway should participate, as in the MLF syndrome.

3. Interruption of supranuclear pathways, the UMNs of the ocular motor system, impairs voluntary conjugate eye movements, not the actions of the individual EOMs. Reflexes can still activate the muscles. The Pt does not have diplopia. We can conclude that ocular movements illustrate the previously announced epigram that UMN lesions paralyze □ movements/□ muscles, whereas LMN lesions paralyze □ movements/□ muscles.

   ☑movements

   ☑muscles

4. In fact, the MLF syndrome helps to emphasize the principle that, when a muscle is paralyzed for only one movement and participates in others, the responsible lesion cannot be at the LMN level.

G. The concept of a head- and eye-centering center

1. Self-demonstration of the head- and eye-centering tendency: You can stare straight ahead, more or less vacantly or vapidly for some period, with no discomfort. Such staring spells, trances, or "tuning out" spells are common, even in infants, and especially in many retarded and learning-disabled children. But if you stare fully to one side, or up or down, discomfort soon demands that you return to the neutral, primary position. To experience the centering demand do this:

   1. Seat yourself comfortably. Pick out a target far to your left, almost behind you. Then turn your head and especially your eyes to the left and keep them there as long as possible, gazing at the target. Blink as necessary but do not break fixation. As you keep the eyes deviated, attend to your own sensations. Time how long you can maintain the deviated position. Now do the experiment.

   2. After some period of increasing discomfort as you keep your head and eyes deviated, a physiologic imperative will demand that you return them to the primary position, sometimes after as little as 30 seconds. You may feel the discomfort as anxiety, vertigo, blurred vision, or even headache. In any event, notice that you felt a considerable relief when you returned to the primary position. Something about the organism wants its eyes and head straight ahead. In fact, many brain-impaired Pts cannot sustain deviation for even 30 seconds, a sign called motor impersistence.

   3. Deviation of the eyes for any reason, voluntary or reflex, triggers a saccade that kicks the eyes back to the primary position, unless overridden by volition, as in the previous experiment. Inhibiting the saccadic kick-back reflex requires some of voluntary effort in the eye deviation experiment as does overcoming visco-elastic forces in the eye socket consequent to deviating the eyes.

2. Many vectors compete to determine the position of the head and eyes at any given instant.

   1. The will or intent of the bearer of the eyes, the emotional state, the survival requirements and advantage-seeking possibilities of the circumstances, and the attractiveness of the visual display.

   2. The position of the head in relation to space, movement, gravity, and the activity of the vestibular system.

   3. The illumination and conditions of vision.

   4. The refractive capability of the eyes and the distance of the visual target.

   5. The demands of binocular fixation and image fusion.

3. Origin of vectors that determine head and eye position: Vectors competing for the control of the head and eyes originate at every level of the neuraxis: posterior frontal cortex (Gaymard et al., 2000), basal motor nuclei, diencephalon, reticular formation, cerebellum, and even the rostral part of the spinal cord. Hence, lesions at any of these levels can more or less influence the movement and position of the head and eyes.

   1. For each head and eye position, vectors act to keep them there and others to move them away. In the aggregate, these opposing vectors result in tonic innervation. The continuous active contraction of the intraocular muscles and EOMs maintains them in a state of oppositional tension that positively determines eye position. The head and eyes seek the null, primary position, not because of the absence of stimulation but because all vectors balance out.

   2. To avoid chaos, some circuitry must integrate and balance these vectors. Although no head- and eye-centering center exists as such in one specific site, the concept of a head- and eye-centering center that balances the right and left vectors and the up and down vectors explains a number of clinical phenomena.

4. A tale of opposing vectors

   1. Normally the right cerebral hemisphere tends to drive the head and eyes to the left, balanced by the left hemisphere trying to drive them to the right. The vectors from the two hemispheres actively oppose and counterbalance each other. Study Figs. 5-3A to 5-3C.

   2. The corollary is that any persistent conjugate deviation of the eyes or head and eyes in any direction means some disorder of the CNS pathways. If only one eye deviates, the lesion affects the LMNs or neuromuscular level.

H. Effect of destructive cerebral lesions on the position of the eyes and head

1. A sudden massive lesion of one cerebral hemisphere, say the right, will interrupt the corticobulbar and corticospinal tracts, causing a complete left hemiplegia. This lesion also nullifies the vector arising in the right hemisphere that should continually strive to turn the eyes and head to the left (Fig. 5-3B).

2. What would you expect the position of the head and eyes to be in the foregoing Pt? □ midline/□ turned to the left/□ turned to the right. Explain.

   _______________________________________________

   _______________________________________________

   ☑ turned to the right. The lesion has eliminated the vector from the right hemisphere that always tries to turn the head and eyes to the left. The vector from the left hemisphere acts unopposed. Therefore, the head and eyes turn to the right, toward the side of the lesion and opposite to the hemiplegic side.

3. The head and eye deviations are most prominent in the acute phase of the lesion (Tijssen et al., 1991). The head- and eye-centering mechanisms reset themselves quickly, but the hemiplegia endures.

I. Effect of irritative lesions on the position of the head and eyes

1. Some cerebral lesions irritate cortical neurons, causing them to fire excessively. Such an irritative lesion initiates epileptic seizures. Electrical stimulation of the cortex has the same effect. Suppose a Pt has a focal epileptic seizure that begins by turning the head and eyes to the right. You would anticipate that the Pt had an epileptogenic focus in the □ right/□ left frontal lobe (Fig. 5-3C).

   ☑ left

2. During the epileptic discharge, the excess of impulses on the left side overcomes the normal vector from the right. After the epileptic cataclysm has subsided, the excessive discharge has metabolically exhausted the neurons in the seizure focus, rendering them temporarily nonfunctional. Immediately after an epileptic seizure caused by a left-sided cerebral lesion, to which side would the head and eyes be turned? □ right/□ left. Explain.

   _________________________________________________

   _________________________________________________

   ☑ left . Because the left eye- and head-turning center is exhausted, the right acts unopposed. The head and eyes turn to the left, opposite to the direction that they turned during the seizure.

J. The rostral midbrain syndrome (Sylvian aqueduct syndrome; pretectal syndrome)

1. Many nuclei and pathways that control the actions of the eyes and pupils surround the rostral part of the Sylvian aqueduct, in the midbrain tectum, pretectum, tegmentum, and periaqueductal gray matter. The actions controlled include upward and downward gaze, vertical ocular alignment, pupillary size, palpebral fissure height, vergences, and the movements mediated by CrN III (Table 5-2).

2. Pure paralysis of upward gaze is known as Parinaud's syndrome

3. Midbrain signs in addition to the Sylvian aqueduct syndrome per se include:

   1. Oculogyric crises

   2. Minimal to severe impairment of consciousness

   3. Hemiparesis or quadriparesis

   4. Decerebrate rigidity

   5. Central neurogenic hyperventilation

   6. Tremor or ataxia

4. The top of the basilar syndrome is caused by infarction in the terminal branches of the basilar artery, the posterior cerebral arteries. These arteries irrigate the midbrain-diencephalic junction and the inferomedial aspect of the temporo-occipital region. Infarction may cause any combination of midbrain, posterior thalamic, or temporo-occipital region signs, including loss of consciousness, depending on the location of the occlusion, the extent of the thrombus, and the collateral flow.

BIBLIOGRAPHY · Central Systems for the Control of Eye Movements

K. The asymmetric tonic neck reflex (ATNR; Magnus-deKleijn reflex): integration of the contralateral visual field, proprioception, touch, the grasp reflex, and voluntary eye movements, or how the infant discovers its own hand

1. Technique to elicit the ATNR

   1. With the infant supine and quiet, gently and slowly turn the infant's head to one side and hold it there for at least 30 seconds. Then turn the infant's head back fully to the opposite side (Fig. 5-4).

   2. Normally the infant extends the arm and leg on the side to which the head is turned and flexes the contralateral extremities. As the head looks to one side, the hand extends into that visual field (Magnus, 1926).

   3. Normal infants 2 to 4 months of age spend much time in the ATNR posture, but they can readily escape from it. During this period, the infant learns to fixate on and to reach for objects and to convert the primitive grasp reflex to volitional grasping of objects.

2. Physiology of the asymmetric tonic neck reflex: The slow head turning stimulates position sense receptors in the neck (fast head turning elicits a counter-rolling vestibular reflex). The afferent pathway runs rostrally into the brainstem reticular formation. Reticulospinal pathways complete the reflex.

3. Interpretation of the ATNR

   1. Because the head and eyes look to the extended hand, the TNR may serve as the forerunner of eye and hand coordination. By sight and proprioception, the infant discovers its own extending hand. If the hand touches an object, the grasp reflex closes the fingers on it. The eyes then learn to direct, via the pyramidal tract, the hand as it explores space and learns to grasp visual targets. The ATNR demonstrates the unity of a visual field, proprioception, touch, and contralateral movement control. The sequence marvelously expresses the law of contralateral cerebral sensorimotor innervation (Chapter 2).

   2. Primitive behaviors such as the ATNR and the grasp reflex disappear as cerebral pathways establish dominance according to the normal developmental timetable. Undue persistence of the ATNR posture, when spontaneously assumed by the infant or induced by an Ex, predicts poor motor development. The more obligatory the ATNR and the longer it persists in infancy, the more abnormal the infant. When strong and persistent, it interferes with sitting and voluntary movement.

4. The ATNR may sometimes reappear in older children or adults who suffer high brainstem or cerebral lesions interrupting corticobulbar and other descending motor pathways: cerebral dominance over the brainstem is lost. Other primitive reflexes also may reappear in aging and dementia (Chapter 11).

5. Summary of the ATNR

   1. When the head of a young infant turns to one side, the ipsilateral extremities tend to □ flex/□ extend, whereas the contralateral extremities tend to □ flex/□ extend.

      ☑ extend; ☑ flex

   2. The foregoing definition is □ operational/□ interpretational. An operational definition states a fact or an agreed upon procedure by which a phenomenon is disclosed.

      ☑ operational

   3. Give an interpretational definition of the TNR.

      ___________________________________________________

      The TNR is a primitive brainstem reflex that promotes the development of normal eye and hand (visuomotor) coordination in infants.

6. What is the prognostic significance of undue persistence of the TNR or any primitive reflex after the first months of life?

   _________________________________________________

   _________________________________________________

   Persistence of the TNR indicates that UMN dominance over the brainstem reflexes is lagging behind the developmental timetable. The infant usually shows permanent deficits in UMN control of movement.

BIBLIOGRAPHY · Asymmetric Tonic Neck Reflex

A. Definition

Nystagmus consists of involuntary, rhythmic oscillations of the eyeballs. Nystagmus can be physiologic or pathologic.

1. Physiologic nystagmus is triggered by:

   1. Spinning (merry-go-round)

   2. Focusing on stripes on a rotating drum (optokinetic nystagmus)

   3. Endpoint gaze

2. Pathologic nystagmus arises most commonly from lesions located in:

   1. The media, retina or optic nerve or optic chiasm that interfere with vision.

   2. Vestibular end organ or nerve.

   3. The brainstem tegmentum and cerebellum (Leigh and Zee, 2006).

3. Diencephalic or cerebral lesions infrequently cause nystagmus. Thalamic lesions or in infants retinal or hypothalamic lesions, such as optic nerve hypoplasia or gliomas, can cause mixed forms of nystagmus. Cerebral lesions may cause a type of gaze paretic nystagmus. Although the clinical findings usually suffice to diagnose the cause of nystagmus, magnetic resonance imaging examination of the brain often is necessary.

B. Symptoms of nystagmus

1. Symptoms may accompany nystagmus:

   1. Oscillopsia: apparent oscillation of objects viewed.

   2. Vertigo: a sensation of movement, generally a feeling of rotation or spinning of self or the environment (Chapter 8).

   3. Nausea: with or without vomiting

   4. Blurred vision

2. The presence of symptoms depends on the rapidity of onset and the duration and site of the lesion. Just as heterotropia of congenital or early origin usually does not cause diplopia, nystagmus of congenital or early origin may not cause symptoms.

C. The signs of nystagmus

If you can describe the Pt's nystagmus well, you need not memorize its endless kinds and causes. Dendrograms (Figs. 5-6 and 5-7) based on the clinical features listed in Table 5-3 will lead to the probable diagnosis. Begin by describing the plane, the type (jerk or pendular), and the direction, if a jerk nystagmus.

1. Note the plane of eye movements (Table 5-3)

   1. Horizontal: eyeball oscillates around the vertical axis.

   2. Vertical: eyeball oscillates around the lateral axis.

   3. Rotatory (torsional): eye oscillates around the anteroposterior (A-P) axis.

   4. Mixed.

      Mnemonic to remember the planes of nystagmus: Name the possible planes of eye movement as related to the three axes of rotation of the eye, the A-P, lateral, and vertical axes.

      1. In horizontal (lateral) nystagmus, the eyeball rotates around the ________ axis.

         vertical

      2. In vertical nystagmus, the eyeball rotates around the __________ axis.

         lateral

      3. In rotary nystagmus (torsions), the eyeball rotates around _____ the axis.

         A-P

   5. Hence, the planes of nystagmus are (order unimportant)

      1. ___________

         horizontal

      2. ___________

         vertical

      3. ___________

         rotatory (torsional)

      4. ___________

         mixed

2. Note the type of nystagmus, pendular or jerk:

   1. Jerk nystagmus has fast and slow components.

   2. Pendular nystagmus resembles a pendulum or metronome. The eyeballs show an equal to-and-fro, metronomic oscillation.

   3. If to equals fro, the Pt has ___________ nystagmus.

      pendular

   4. If to does not equal fro, the Pt has ___________ nystagmus.

      jerk

3. Note the direction of the fast movement of the nystagmus, if the Pt has jerk nystagmus:

   1. The direction of jerk nystagmus means the direction of movement of the fast component.

   2. If the nystagmus jerks to the right side, we say the direction is to the

      _____________________.

      right

   3. If the fast component always jerks in one direction, the nystagmus is unidirectional. If the direction of the jerk changes with the direction of eye movements, the nystagmus is bidirectional. Look for a neutral zone in which the nystagmus changes direction.

   4. Nomenclature note on designating the direction of jerk nystagmus: Custom dictates naming jerk nystagmus by the direction of the fast movement, but the important event is the deviation or slow phase (Leigh and Zee, 2006). The slow movement initiates nystagmus by triggering a saccadic jerk, a kickback reflex. Slow velocity systems include smooth pursuit and optokinetic nystagmus, vergences, and the slow phase of nystagmus induced by vestibular stimulation. Pathologic nystagmus reflects an imbalance in these slow velocity systems that normally should hold the eyes steadily on the visual target (gaze-holding mechanisms).

4. Note the amplitude and rate.

5. Note whether the nystagmus is binocular and symmetrical, monocular, or dissociated. Dissociated nystagmus shows different amplitudes in the two eyes or different directions (Shawkat et al., 2001).

6. Note whether the nystagmus occurs in the primary position or the eccentric positions and the effect of eye movements in the cardinal directions of gaze (Fig. 4-20). Determine whether the nystagmus changes in rate, amplitude, or direction as the eyes fixate in the primary position and move through the various fields of gaze, including convergence. Jerk nystagmus increases when the Pt looks in the direction of the fast phase (Alexander's law), because the volitional and reflex saccades add up.

7. Look for a null point where bidirectional nystagmus is minimal or absent.

8. Test for the effect of changes in head position or posture on nystagmus:

   1. Make quick, rotations of the Pt's head over a short distance and try the Dix-Hallpike maneuver (Chapter 9).

   2. Test for cancellation of the vestibulo-ocular reflex by the eye-to-thumb rotation test. The Pt sits on a revolving stool, extends an arm, holds the thumb vertically, and maintains fixation on the thumb. The Ex rotates the Pt's head, body, and thumb as a unit to the right and left. If eyes break away from the thumb and show nystagmus, the Pt may have a lesion of the cerebellum or central vestibular pathways. Try this simple test yourself.

9. Test for latent nystagmus by covering each eye separately and inspecting the other eye with magnification provided by the ophthalmoscope. By removing fixation, this maneuver releases nystagmus.

10. Look for associated rhythmic movements of the lids, face, jaw, tongue, palate, pharynx, neck, or limbs (palatal and ocular myoclonus).

11. In selected Pts, test for optokinetic nystagmus, the Romberg fall (Chapter 10), past pointing, and caloric irrigation.

12. Consider electronystagmography and radiographic imaging.

D. The laws of nystagmus

These general laws are subject to exceptions but have practical value.

1. Jerk nystagmus

   1. Central and peripheral vestibular lesions may cause jerk nystagmus.

   2. Unidirectional jerk nystagmus is always vestibular in origin.

   3. Acquired bidirectional horizontal nystagmus is almost always central in origin and usually indicates a brainstem lesion or toxic/metabolic state.

   4. Alexander's law: Looking in the direction of the fast phase of a jerk nystagmus increases its amplitude.

   5. Jerk and pendular nystagmus may have a rotatory component.

2. Peripheral versus central origin of nystagmus

   1. The two cardinal features that distinguish peripheral from central vestibular nystagmus are unidirectionality and inhibition of peripheral nystagmus by visual fixation. Fixation has little effect on central nystagmus (Hotson and Baloh, 1998).

   2. Peripheral nystagmus, particularly when vertical has a torsional component, but a pure vertical or pure torsional nystagmus, is always central in origin.

   3. Acquired pendular nystagmus usually is caused by brainstem or cerebellar strokes, neoplasms, or multiple sclerosis.

   4. Positional nystagmus may occur with peripheral vestibular or central lesions.

   5. Acquired peripheral nystagmus is short lasting, and central is long lasting.

3. Nystagmus with posterior fossa/cerebellar disease

   1. Cerebellar lesions or drugs characteristically cause bidirectional gaze-evoked nystagmus, deficient smooth pursuit, impaired saccadic accuracy, and slow initiation of saccades.

   2. Visual suppression of nystagmus is minimal or absent with cerebellar as with any central nystagmus.

   3. Flocculus and paraflocculus lesions cause downbeat nystagmus-deficient smooth pursuit, gaze-evoked nystagmus, and rebound nystagmus.

   4. Upbeat and downbeat nystagmus, especially in the primary position, indicate a posterior fossa lesion (Hirose et al., 1998; Janssen et al., 1998).

   5. Downbeat nystagmus, characterized by slow upward drifts and fast downward phases, may indicate a foramen magnum lesion such as the Chiari malformation (Wagner et al., 2008).

   6. Torsional nystagmus may arise from medullary lesions.

4. Miscellaneous laws

   1. The characteristics of the nystagmus do not differentiate congenital nystagmus without afferent defect from nystagmus with afferent defect.

   2. Gaze-evoked nystagmus may occur with CNS or neuromuscular lesions that cause weakness of eye movements.

   3. Some types of nystagmus stay horizontal on upward gaze: congenital, peripheral vestibular, and periodic alternating.

   4. Cold water irrigation of the horizontal canal of one ear reproduces the effect of an acute vestibular lesion on that side, e.g., fast phase and vertigo to the opposite side, the Romberg fall, and past-pointing to the same side (Chapter 9).

E. Diagnostic dendrograms for specific types of nystagmus

1. Summarize the nystagmus with regard to plane (form), type, and direction (if a jerk type) according to Fig. 5-5.

2. The data from Table 5-3 and Fig. 5-5, when integrated with the history, permits you to enter the dendrograms of Figs. 5-6 and 5-7. Read through the dendrograms for familiarity but do not memorize them. Notice that pendular nystagmus implies an ocular cause or central lesion. Unidirectional jerk nystagmus implies a lesion of the peripheral vestibular system or the immediate central connections.

3. Differentiation of spontaneous peripheral and central vestibular nystagmus (Table 5-4).

4. Differentiation of positional vestibular nystagmus (Table 5-5)

   See Chapter 9 for positional maneuvers and the Romberg test.

F. Some uncommon non-nystagmoid repetitive eye movements

1. Ocular bobbing: A type of eye movement resembling downbeat nystagmus likewise shows a fast downward movement and slow drift back to the primary position, but it differs from nystagmus in being arrhythmic and having a low frequency of 2 to 12 per minute. The lesion, usually vascular (often a hemorrhage), inflammatory, neoplastic, traumatic, or demyelinating, affects the pons, but it also may occur with cerebellar lesions compressing the pons. The Pt is usually comatose and quadriplegic and lacks other spontaneous or induced eye movements.

2. Ocular flutter describes intermittent bursts of lightning-fast eye movements. It may precede or accompany opsoclonus, defined as rapid, chaotic, and more or less continuous non-rhythmic lightning jerks of the eyeballs in various directions ("saccadomania").

   1. Flutter and opsoclonus may be sporadic or associated with neuroblastoma in children or visceral carcinoma in adults.

   2. They belong to types of rapid eye movements without a slow component, whereas nystagmus in general reflects disorders of slow eye-movement systems.

3. Voluntary "nystagmus": Some Pts with Munchausen's syndrome or pseudo-seizures can make rapid shuddering or shimmering ocular movements that resemble nystagmus but consist of back-to-back saccades (Davis, 2000; remember, all voluntary movements are saccadic). Diagnostic features are

   1. The movements are horizontal and equal in excursion.

   2. Sustainable only for short periods, usually less than 15 to 30 seconds, because they require extreme concentration.

   3. Best accomplished with slight convergence.

   4. The Pt frequently blinks and closes the eyes.

   5. Nystagmus stops by having the Pt change the direction of gaze.

G. Electronystagmography

Electronystagmography, as done by neuro-ophthalmologists or ear, nose, and throat specialists, provides a visual quantitative record for the analysis of nystagmus waveforms (Dell'Oss and Daroff, 1999).

BIBLIOGRAPHY · Nystagmus

A. Laws governing the actions of the ocular muscles

1. The law of axial rotation of an eyeball: The six EOMs rotate the eyeball around one of its three axes: A-P, vertical, or horizontal (Fig. 4-1).

2. The law of on-center/off-center pull of the extraocular muscles: The ocular muscles that pull only "on center" have one primary rotary action, whereas those that pull "off center" cause primary, secondary, and tertiary rotations. The line of pull or vector of all EOMs runs medial to the vertical axis, except for the lateral rectus muscle (Fig. 4-17). Corollary: The muscles that pull off center change their actions depending on the position of the eye when the muscle acts (Figs. 4-12 to 4-16).

3. The law of positive tonic oppositional innervation of the intra- and extra-ocular muscles

   1. The intraocular and extraocular muscles of one eye act in oppositional sets that receive equal tonic innervation. (The ciliary muscle ostensibly seems to be an exception, but the elasticity of the lens acts as its opponent.)

   2. Tonic innervation positively holds the eye in position. When the eyes are still, the pull of one muscle balances out the pull of the other.

      1. After paralysis of a muscle, the eye assumes the position, or the pupil assumes the size, dictated by the pull of the intact, tonically innervated, oppositional muscle.

      2. A nuclear, nerve, or neuromuscular lesion paralyzes individual ocular muscles, causing strabismus and diplopia.

      3. Persistent monocular deviation arises peripherally, whereas persistent conjugate (binocular) deviation arises centrally.

B. Laws governing the central control of eye movements

1. The law of conjugate ocular fixation and conjugate movement: The eyes fixate and move conjugately, except during vergences. Corollary: Failure of conjugate fixation and conjugate movement is always abnormal.

2. Hering's law of equal innervation of the corresponding EOMs: The muscles that collaborate to move the two eyes in a given direction receive equal innervation. This law ensures that the two eyes move equally and remain aligned in all directions of gaze, with the retinal images on corresponding sites to avoid blurred vision and diplopia.

3. The law of different pathways for horizontal and vertical conjugate eye movements: The supranuclear pathway for volitional conjugate horizontal eye movements arises in the posterior-inferior frontal cortex and loops down into the pontine tegmentum and back up to the midbrain through the MLF (Fig. 5-1). In direct contrast, the pathways for vertical movements arise more diffusely from the cortex and run directly into the pretectum and midbrain without looping down into the midbrain.

   1. The pathway for conjugate upward eye movements courses into the midbrain dorsal to the pathway for conjugate downward movements.

   2. Corollary: Focal lesions may selectively paralyze horizontal or vertical gaze and may selectively paralyze upward or downward gaze.

4. The law of control of saccades by the frontoparietal tegmental pathway: The frontoparietal ocular motor pathways mediate all saccadic eye movements. Saccadic movements include those that move the eyes voluntarily or restore them to the primary position after deviation by vestibular or optokinetic reflexes and during rapid eye movement of sleep. Corollary: Because fast and slow movements (slow pursuit and vestibular deviation) arise in different pathways, focal lesions may affect the pathways selectively.

5. The law of a positive head- and eye-centering mechanism

   1. Each side of the brain tonically produces vectors that tend to drive the head and eyes to the opposite side. Upward and downward vectors arise bilaterally from the cortex.

   2. Normally, the vectors that try to drive the head and eyes in opposite directions cancel out. The eyes tend to remain in the primary position or, if moved from it, tend to return to the primary position because of active centering vectors (Fig. 5-3).

   3. If the eyes deviate from the primary position for any reason, saccadic kickback tends to restore the eyes to the primary position. Corollary: Any persistent deviation of the eyes horizontally or vertically indicates an unbalanced drive caused by interruption of, or excessive drive from, one of the centering systems.

      1. Destruction of one supranuclear pathway for eye movements results in persistent conjugate deviation of the eyes in the direction dictated by the intact pathway (Fig. 5-3B).

      2. Irritation of one supranuclear pathway for eye movements results in persistent conjugate deviation of the eyes in the same direction dictated by that pathway (Fig. 5-3C).

6. The law of occipito-parietal control of visually mediated reflexes

   1. Visually mediated, clinically testable ocular motor reflexes are fixation, fusion, pursuit, vergences, and optokinetic nystagmus.

   2. All require an intact afferent arc starting with the retina and mediated through the geniculo-occipito-parieto-tegmental and occipito-parietofronto-tegmental pathways.

7. The law of competition between reflex and volitional control of eye movements: Fixation, fusion, following, vergences, and optokinetic nystagmus operate reflexly, but the normal person can override the reflexes by volition. After bilateral interruption of the voluntary pathways, the fixation reflexes may become tenacious or "hyperactive," and then the Pt cannot move the eyes from the target without blinking or moving the head.

8. The counter-rolling law: When the head moves, proprioceptive reflexes, arising in the vestibular system and neck, and fixation reflexes hold the eyes on target by counter-rolling the eyes against the direction of head movement, thus keeping the eyes locked on the visual target. Corollary: Failure of the eyes to counter-roll indicates failure of one or more of these systems. When unconsciousness negates voluntary movements and fixation, failure of the eyes to counter-roll in response to vestibular stimulation by head turning (doll's eye test) or caloric irrigation means interruption of the vestibular system peripherally or in the brainstem tegmentum.

C. Review the five eye systems mnemonic (pages 179–180 and Table 5-1)

D. Table 5-6 outlines the clinical tests for central eye-movement disorders

E. Summaries of the eye examination

1. Five parts of the routine clinical eye examination:

   1. Visual acuity and fields: Snellen, Rosenbaum, and Amsler grids.

   2. Peripheral visual field: confrontation.

   3. Eye movements: test cardinal directions of gaze and the five eye-movement systems (Table 5-1).

   4. Pupils: reaction to light and accommodation.

   5. Ophthalmoscopy.

      1. Anterior segment: external eye to lens.

      2. Posterior segment: vitreous, retina, and optic nerve head.

2. Table 5-7 summarizes the ancillary procedures used to supplement the routine eye examination.

Now we have to unite the individual fragments of the eye examination into a coherent routine. We could easily convince you to practice if you were a tennis player wanting to improve your strokes or an actor. A great actor, preparing to play the role of a physician, would practice hour after hour to capture the exact nuances of professional behavior. Ours, too, is a performing art. If you want to offer a professional performance to your Pts, practice Part V, steps 1 to 5, of the Standard Neurologic Examination (NE). Practice until the steps unite into one beautiful, flowing sequence for testing CrNs II, III, IV, and VI and their central pathways. Then you can say with Blaise Cendrars:

I have deciphered all the confused texts of the wheels and I have assembled the scattered elements of a most violent beauty.

The five steps that you have just rehearsed from the Standard NE constitute a minimum routine examination. Patients with ocular complaints may need more thorough study. Use Table 5-7 as a reference to supplement Part V A of the basic examination.