Journal of Neuro-Ophthalmology, December 1989, Volume 9, Issue 4

Optokinetic nystagmus. A clinical review.

Although optokinetic nystagmus was described as a clinical phenomenon over 150 years ago, its neurophysiologic mechanism has provoked ongoing controversies and enthusiasm for its clinical application has been sporadic and tepid. In the past 15 years, improvements in clinical and experimental oculography, neuroanatomy, and single unit neuron recordings in alert animals have helped to resolve the neural circuitry of optokinetic nystagmus and to better define its clinical usefulness. The writer reviews the history of the experimental study of optokinetic nystagmus and the clinical circumstances in which this office test may be of particular value.

luumal of Clillieal N<' lIr,,- ol'hthalmolt. s.~ 9( 4): 258- 266. 1989. Optokinetic Nystagmus A Clinical Review Noble J. David, M. D. Although optokinetic nystagmus was described as a clinical phenomenon over 150 years ago, its neurophys­iologic mechanism has provoked ongoing controversies and enthusiasm for its clinical application has been spo­radic and tepid. In the past 15 years, improvements in clinical and experimental oculography, neuroanatomy, and single unit neuron recordings in alert animals have helped to resolve the neural circuitry of optokinetic nystagmus and to better define its clinical usefulness. The writer reviews the history of the experimental study of optokinetic nystagmus and the clinical circumstances in which this office test may be of particular value. Key Words: Optokinetic nystagmus-- Saccades. From the Veterans Administration Medical Center and the Department of Neurology, University of Miami School of Med­icine, Miami, Florida, U. s. A. Address correspondence and reprint requests to Dr. N. J. David at Neurology Service, Veterans Administration Medical Center, 1202 N. W. 16th Street, Miami, FL 33125, U. S. A. This article was presented in honor of J. L. Smith's 60th birth­day. Bascom Palmer Eye Institute N,' uro- Ophthalmology Sym­[ l(, •. ;,., n, .".,,' · · ,, · -, · , · _, · ,, 1. · 01 ir !" l. 1rt tn the' Japan Clinical Oph- 258 © 1989 Raven Press, Ltd., New York After reviewing the available facts about the time- honored neuroophthalmologic phenome­non- optokinetic nystagmus- I deemed the topic appropriate for a symposium honoring Dr. J. L. Smith on the occasion of his 60th birthday. My original goal was to reexamine our understanding of its mechanism and to reassess its diagnostic use­fulness. Nowadays, it seems, the drum or tape is often consigned to a dusty comer of the office, utilized infrequently and without much vigor. My research quickly brought me back to Dr. J. L. Smith's monograph ( 1), published exactly 25 years ago, 1 year after he joined the faculty at the Uni­versity of Miami Department of Ophthalmology. He was enthusiastic then: " The author has become convinced of the usefulness of optokinetic nystag­mus in topical neurologic diagnosis...." Dr. Smith's comments, now a quarter century old, in­spired me to pursue this subject. In addition to the earlier clinical observations and ablative experimental studies in animals, the phenomenon has in the last decade been scruti­nized by the ocular motor physiologists with in­struments that allow a permanent record for com­puterized analysis and characterization of the com­ponent eye movements ( 2). Neurophysiologists have also made use of single neuron unit record­ings in the study of control and production of eye movements ( 3). In both humans and experimental animals, we are acquiring a clearer understanding of optokinetic nystagmus, its variations, its phys­iologic significance, and its usefulness in the ex­amining room. HISTORICAL In 1825, Purkinje ( 4) was impressed with the nystagmoid eye movements of spectators at a cav­alry parade. Later in the century, the legendary Helmholtz ( 5) is said to have noted the nystagmus OPTOKINETIC NYSTAGMUS 259 of passengers on a train watching the passing scenery. The development of an instrument to test the phenomenon, the optokinetic drum, led Barany ( 6) to study patients and note the asymme­try of optokinetic responses in patients with hom­onymous hemianopsia, erroneously ascribing the abnormality to sensory impairment. On the other hand, Ohm ( 7) soon found quite normal optoki­netic nystagmus in both directions in patients with dense and complete homonymous hemianopsia; these observations led to the convention of naming hemianopsia either of the Barany or Ohm type de­pending on whether or not there was an abnormal or normal optokinetic response. In any case, the deficient response was typically seen when targets were taken out of the hemianopic field and to­wards the damaged hemisphere. I review the evi­dence for localization and significance of this asymmetry later. That the optokinetic response occurs involuntar­ily when the patient looks at a succession of targets can easily be proven by doing the test on your colleague. The subject is not aware of eye move­ments nor can she or he easily suppress the re­sponse. That these eye movements also occur as an involuntary response when targets are moved before the eyes of animals, who cannot be in­structed to look, is a well- known fact that has been used to test the visual acuity of animals and that originally led to experiments aimed at clarifying the neurologic circuits involved. In humans, we must await the vagaries of dis­ease to produce the propitious lesions. Students of optokinetic nystagmus were early attracted to the study of experimental animals because they may be precisely lesioned and then tested. Such exper­iments began more than 60 years ago. The work of terBraak ( 8), published in 1936, is regarded as sem­inal. His observations established the following facts. 1. That in all experimental animals, including those who had no foveal vision, optokinetic re­sponse could be induced by movement of the en­tire visual field, such as the stimulation produced by an animal within an illuminated rotating striped drum. 2. Afoveate animals did not respond to the movement of small targets in the visual fields as would cats, dogs, and primates, that is, animals with foveal vision, whose attention could be at­tracted to a succession of moving targets progress­ing horizontally against a stable visual back­ground. 3. terBraak ( 8) distinguished these two types of nystagmus as so- called active nystagmus for the foveal tracking of a succession of small targets, and passive nystagmus to the phenomenon seen when the entire peripheral visual field was moved. This distinction is important in the neurophysiology of optokinetic nystagmus. The " active" type of nystagmus seems to depend very much on cortical vision and is most highly developed in the pri­mates and in humans. It is the type most easily impaired when cortical vision is destroyed by oc­cipital ablation. That optokinetic nystagmus can persist in a decorticate cat or dog, and certainly in the rabbit, is rather difficult for a clinical neurolo­gist to accept. But this " passive" optokinetic nystagmus seems in these animals to be mediated at subcortical level by pathways that do not in­volve cortical vision but which lead directly from the lateral geniculate to the tectal areas and thence to the optomotor centers of the cerebellum and brain stem. II ACTIVEII VERSUS IIPASSIVEII OPTOKINETIC NYSTAGMUS Moreover, there are important distinguishing characteristics of the eye movements, particularly the slow- phase movements, in the two different pathways for the generation of optokinetic move­ments ( 2). The nystagmus produced by the sub­cortical pathway shows a very slow build- up in the velocity of the slow phase of the response, which reaches a maximum and reverses into an lIafter­nystagmus" in the opposite direction when the ro­tation of objects in the peripheral field is stopped. In contrast, the cortical or lI active" nystagmus in­duced by a succession of foveal targets in motion as seen in primates and humans as well as lower animals with foveal vision locks in at full velocity when it begins and is not followed by after­nystagmus. In cats and dogs, the two types of op­tokinetic response are virtually separable in that the " passive" type will persist after the occipital lobes are removed. In primates and humans, it is likely that enough of both systems have been in­corporated into the posterior cerebral hemispheres so that both types, though utilizing separate path­ways for some of their circuitry, are virtually de­stroyed if the occipital lobes are removed. One is inclined to theorize teleologically that, although the afoveate animals, whose experimen­tal prototype is the rabbit, are generally vegetarian grazers whose chief concern is to escape detection and slaughter, their vertebrate cousins, cats and dogs, are primarily carnivores, whose macular in­spection of potential prey moving across the visual field is crucial to survival [ and to " active" optiki- JClin Neuro- ophthalmol, Vol. 9, No, 4, 1989 260 N. J. DAVID netic nystagmus ( OKN)). They must pick out an animal scurrying across the landscape, perhaps one of a herd, and then hold the quarry in clear perspective until it can be overtaken and killed. In primates with highly discriminative cortical vision, the optokinetic function seems to be taken up en­tirely as a cortically mediated activity, providing for a roaming visual search of the environment to assist in feeding and reproductive chores. In this scheme of " active" optokinetic nystagmus pro­voked by foveal vision, it should be remembered that the object of regard is moving across a stable peripheral visual environment, in contrast to the " passive" OKN stimulated by movement of the entire visual environment. Important differences in humans and experi­mental animals must be kept in mind when testing OKN and comparing their responses. Humans can be given verbal instructions and asked to direct visual attention to small moving targets. In all fair­ness, it must also be said that when small targets are moved in the direct line of vision, it is very difficult for humans not to look at them. Animals cannot talk. They must be relied upon to respond instinctively to the moving visual scene, and this often requires stimulation of much or all of the peripheral retina fields as well as central. Experi­mental ablation in the CNS may be freely studied in animals. In humans, we must await the vagaries of disease to produce the proper lesions for study. Notwithstanding the conditions stated above, it is obvious that animals can retain their optokinetic responses after widespread cortical ablation in­cluding bilateral removal of the occipital poles. But the latter structures are essential to the response in primates and particularly in humans. Physiologic researches of the past 15 years are helpful in rec­onciling these differences. OPTOKINETIC- VESTIBULAR INTERACTION Vestibular and visual interrelationships are par­ticularly crucial and have been the subject of excit­ing experimental study in recent years. Opto­kinetic movements driven by rotation or " circularvection" of the entire visual environment ( and thus stimulating the peripheral retina) can be used to obtain the OKN response in fishes and frogs as well as in higher vertebrates and seems more concerned with the orientation of the organ­ism in space, that is, the coordination of the visual environment with the other highly specialized or­gan systems serving orientation. J was fascinated to read of the studies of Waespe JClin Nturo- ophthalmol, Vol. oj. No. i. 191:~; and Henn ( 9) in which single- unit recordings from the vestibular nucleus in alert monkeys have been obtained under controlled experimental con­ditions. The monkey is seated within a striped drum on a chair that will allow either rotation of the monkey, whose head is in a position to stim­ulate the horizontal semicircular canal or whose visual environment with optokinetic ( vertical) striping may be rotated. The direction and speed of rotation of either the monkey's chair or sur­rounding drum may be varied independently. Thus, the visual environment can be removed by darkness or stabilized by rotating the drum and the chair at the same angular velocity, allowing independent stimulation of the labyrinth or visual fields. To summarize these investigators' findings, it can be said that when a neuron in the vestibular nucleus is found whose firing increases in re­sponse to vestibular stimulation caused by rotation in a stable visual environment ( or with the eyes closed) that the same neuron will fire similarly when the visual environment is moved in a direc­tion which simulates ( by opposite motion) angular movement of the head. When the visual and rota­tional stimuli are applied simultaneously, as oc­curs in the normally functioning animal, the re­sponse is further enhanced. When the visual movement and vestibular stimulation are made to be contradictory, the signals tend to cancel and the firing rate falls off. In other words, these investi­gators find that any vestibular neuron that re­sponds to vestibular stimulation by horizontal ro­tation will also correspondingly and appropriately react when the visual universe turns before it ( cir­cular vection) without active labyrinthine stimula­tion. Evidence for this crucial interrelationship be­tween the vestibular function and the optokinetic phenomenon in humans has accumulated over the decades. Ohm ( 10) described asymmetry of the op­tokinetic responses in a patient with vestibular im­balance. Later observers confirmed that peripheral labyrinthine input had the effect of augmenting OKN in the direction of the slow phase ( OKN fast phase and spontaneous vestibular fast phase beat­ing in the same direction). This observation was only true for peripheral vestibular disturbances. Central brainstem lesions usually depressed the optokinetic response. Brandt et al. ( 11) and others studied a patient with acute unilateral labyrinthine disorder and documented the directional preponderance of a nystagmus associated with spontaneous unilateral nystagmus as well as its disappearance as the lab­yrinthine disturbance became quiet and/ or central OPTOKINETIC NYSTAGMUS 261 habituation occurred. Brandt et al. ( 11) concluded that OKN in patients suffering from primary laby­rinthine lesion are not purely visually driven but must be correctly termed " vestibularly biased OKN." EXPERIMENTAL STUDY VERSUS OFFICE OKN Those of us who are office clinicians and who apply the roughshod technique of spinning the drum or moving the tape before our patients' eyes must remember that the experimental literature on OKN in humans is derived from studies of subjects surrounded entirely by a cylindrical drum with black and white stripes similar to the monkey ap­paratus described elsewhere ( 12). This arrange­ment is often coupled with a Barany chair that al­lows rotation of the patient as well as the screen in much the same way as in the study of experimen­tal animals. Illumination, light projection, speed of the drum or chair, and intermittent sinusoidal pat­terns of rotation ( to avoid vestibular adaptation) ­all of these parameters as well as the stimulus size can be well controlled. The subject sitting in such a cylinder and observing the lateral movement of the visual environment is extremely prone to sensa­tion of rotation of his or her own body and with this illusion is very apt to experience the queasi­ness and pallor and sweating that comes with ver­tigo- vertigo produced not by stimulation of the labyrinthine ampullae ( that is, by angular acceler­ation of the head), but by the disparity of dis­charge of the undisturbed organ of balance in con­flict with the visual illusion of rotation. Some of you who have been in this drum have doubtless experienced the vertigo and nausea. But the sensation can also be created in a small movie theater such as in the Smithsonian Museum in Washington, which has steeply sloped seating and a large curved screen that wraps around the view­ing horopter some 120° or more- in other words, filling the visual fields of the spectator. The mu­seum shows a film in which the audience views a cinetape taken from the nose of an airplane whose pilot is constantly performing stunts and aerobat­ics. The twisting and careening environment will in short order have the spectator vertiginous, lurching about in the theater seat, and counter­rolling to compensate for the wild gyrations of the screen. This psychophysiologic observation, like the monkey experiment, demonstrates one does not need labyrinthine excitation to appreciate true vertigo; rather vertigo results from what Brandt and Daroff ( 13) have called the " mismatch" of sen-sory information between the two systems. It does not matter whether the visual or the vestibular in­put provides the inappropriate sensory informa­tion. CLINICAL APPLICATIONS General Comments Once OKN begins in humans, the eyes orient themselves in a direction toward the fast phase ( 2). The speed of the slow phase tends to match the target speed for lower target velocities but falls off rapidly when its limit is reached. The optokinetic component of the fast phase has been shown to have the same speed- amplitude patterns of other refixational saccades and are re­garded as their equivalent. Saccadic velocity is swift and may reach speeds of 7000 / s. Normally, they are capable of resetting the conjugate axes of vision with great speed and accuracy. These move­ments are ultimately generated by neurons within the ipsilateral pontine parareticular formation that fire in high- frequency volleys called " bursts." Si­multaneously, their contralateral brain stem coun­terparts are actively inhibited by " pause" neurons that relax the antagonistic eye muscles. OKN Asymmetry in Hemispheric Lesions We now return to the debate that opened the clinical history of OKN- the study of cerebral dis­ease associated with hemianopic defect and the empiric observation that when targets are taken to the side of the diseased hemisphere the optokinet­ic responses are diminished. Smith, in his monograph in 1963 ( 14), summa­rized his experience with " the positive OKN sign" in homonymous hemianopic defect( s) to wit, " that it was associated with parietal lesions, especially deep ones, but not merely ones causing dense hemianopsia." To explain his findings ( which were entirely with tape- drum " office" testing equipment), he favored the hypothesis proposed by Cord in 1926 ( 15)- that an efferent optomotor tract transversed the deep parietal lobe on its way from the visual centers to subcortical optomotor centers. An alternative explanation- the transcor­tical theory ( 16,26)- held that information travel­ing from the visual centers in the posterior hemi­sphere traveled forward to area eight ( or frontal optomotor center), where the fast phase of nystag­mus was to be initiated. This theory was attractive because the postulated insufficiency of cerebral gaze would be in the direction of the fast phase. J Gin Neuro- ophthalmol. Vol. 9. No. 4, 1989 262 N. ]. DAVID Historically we should mention the several fal­lacies that have delayed our understanding of the phenomenon. The first is that the defect was caused by a sensory ( hemianopic) field loss. This proved to be untrue early in the game when Ohm ( 10) found dense hemianopias without the phe­nomenon and asymmetry was noted in patients who had rather minor visual field defects. The second is that area eight of the frontal cortex generated the saccadic phase of OKN and that damage either to area eight or to the pathways leading to it from the occipital lobe where the per­ception of vision occurred ( the transcortical theory) was responsible for the asymmetry. In truth, the vast majority of large frontal lesions- neoplastic, vascular, and otherwise- have not been observed to show optokinetic asymmetry. Indeed, Smith's ( 1) conclusion was that only in parietal lobe lesions and in large parietal lobe lesions was the asymme­try associated with hemianopsia observed. Another indication that the fast phase of OKN was probably not at fault was that patients with optokinetic asymmetry could produce full sac­cades in the appropriate direction when the laby­rinth was exposed to cold water stimulation. We now believe that the bulk of the fast phase comes from the brainstem neurons that generate sac­cades. The most important single clue to optokinetic asymmetry in cerebral hemianopia probably was a finding that emerged in electrooculographic stud­ies of patients with cerebral lesions. The Clue A hemispherectomized patient underwent total removal of the left cerebral hemisphere, diseased from birth, to control an intractable seizure disor­der. Although his body was underdeveloped on the right side, he could walk and use his right hand and fingers and he also had adequate speech. But one can see an obvious optokinetic deficiency when targets are taken to the left ( re­moved) hemisphere. Now when he is asked to pursue a visual target projected onto the screen before him, he shows on the electronic recording what we can barely and incompletely appreciate with the naked eye- a surprising abnormality in the pursuit function, which is erratic and broken up by " catch- up" saccades when targets are fol­lowed in the direction of his diseased or affected hemisphere. It would appear that his pursuit of a visual target to the left is impaired by the damage to his left hemisphere, th, lt is, that the ipsilateral hemisphere is prim: lrily responsible for horizontal 1elin Nn4To- ophthalmol, 1' 01.9, No. 4, 19B: J pursuit of a moving target. This discovery offered the opportunity to support Cords' hypothesis ( 15) that the ipsilateral parietal lobe sent optomotor in­formation for visual following to the brainstem in this circuit and made unnecessary and unlikely the transcortical theory and participation of the frontal cortex, which others had espoused. In 1979, Baloh et al. ( 16) published a convincing study of two patients with parietal lobe lesions who had asymmetric OKN. Their studies of eye movement recordings revealed quite clearly that foveal tracking in the eyes pursuing a sinusoidally moving target was definitely erratic and disturbed when the eyes were moving toward the damaged hemisphere, an observation in keeping with pre­vious observations of ipsilateral foveal pursuit. Full- field pursuit of a surrounding optokinetic drum was likewise impaired, but voluntary and involuntary saccades ( fast components) were nor­mal. They observed that foveal pursuit was im­paired more than full- field pursuit, indicating the " active" OKN was more affected. They cited fur­ther observations indicating abnormality of the slow phase in their patients. Rotation of both pa­tients within an optokinetic drum in light demon­strated asymmetries of the slow component in con­trast to their response to rotation in dark, thus im­pugning the optokinetic slow- phase contribution of rotary nystagmus. The subjects were also un­able to suppress vestibular nystagmus when rotary movement during visual fixation provoked slow component to the right. They concluded that a pathway running from the deep parietal lobe to the brain stem horizontal gaze center was in­volved, causing the asymmetry by interfering with slow- phase performance. Their observations were employed to support Cords' hypothesis ( 16) and Smith's ( 14) support of it, and to ascribe OKN asymmetry to deficit in the slow ( following) phase. It is only fair to state that optokinetic asymmetry has occasionally been reported in more frontally placed lesions ( 17) and that, although it is gener­ally agreed that OKN fast phase is primarily in the brain stem, one might theorize that the frontal gaze center may be impaired by an anterior hemi­spheric lesion causing at least a temporary asym­metry of responses due to a " deficient saccadic" drive in the contralateral direction. This schema would be consonant with the observation that tar­gets taken toward the damaged hemisphere pro­duce the impaired response, in this case totally unrelated to the hemianopsia. Such asymmetries are apparently subtle and transient. The clinical experiments designed to separate the neural pathway for foveal tracking from that OPTOKINETIC NYSTAGMUS 263 which responds to movement across the periph­eral retina continue but have not yielded a defini­tive result. It is likely in humans that both func­tions utilize to some extent the same pathways, in contrast to the lower animals. It would be remem­bered that the hemispheric lesions in humans that cause this kind of asymmetry are not small and discrete infarcts as a general rule but either very large infarcts or infiltrative tumors that occupy a major portion of the parietal lobe. Indeed Smith ( 1) has always quoted Cogan as believing that in a relatively intact patient with an occipital hemi­anopsia, asymmetry of the optokinetic responses was a better sign of tumor than of vascular infarc­tion. Finally, as fate would have it, in the study of hemispheric lesions in humans, the more expen­sive and elaborate set- up that allows stimulation of the peripheral retina by rotation of the entire visual environment is less apt to reveal a lesion than are smaller targets on tape or drum ( 18). Although the latter machines cannot easily be controlled as to illumination and controlled velocity, they seem to mimic the function of foveal pursuit and stimulate the " active" OKN, which is more sensitive to a parietal lesion. OKN Hysteria Malingering Because OKN is an involuntary response, the automatic cooperation of the subject makes it use­ful in investigating visual function in animals and infants. The same property is also useful in iden­tifying patients with hysterical visual loss or ma­lingering, in one or both eyes; following of the tape and corrective saccades could not occur unless vi­sual function were present. This aspect of the test is best exploited in pa­tients who claim severe visual loss in one or both eyes. The subject is asked to try to see what. is in front of her or him and targets are moved hOrIzon­tally in her or his direct line of vision. Optokinetic jerks reveal that the patient sees more than sh. e or he claims. The patient may at times by consCIOUS effort suppress the response, chiefly by " staring through" the close- up targets to a d. ista~ t po. int be­hind them. But it is difficult to mamtam thIS con­centration. When the subject is placed within one of the rotating drums that fill the entire visual field with moving stripes, suppression of the response is practically impossible. Although a response shows that adequate vision is present to s~~ the targets, one cannot entirely rule out the addItIonal possibility of an organic handicap. OKN in Disease with Loss of Saccadic Function Marked diminution or total loss of the capacity of the eyes to make saccadic ( rapid refixational) movements result in a severe visual handicap that is characteristic of a certain few diseases. One of these is the degeneration known as " pro­gressive supranuclear palsy," a first cousin of Par­kinson's disease, in which the patient develops slow movements and dystonic rigidity of the entire body, trunk, and neck, and gradually loses all vol­untary movement of the eyes, retaining only the ocular cephalic reflexes. The first eye movements to suffer are the saccades and especially in the downward direction, although all directions of gaze are affected ( 19). These patients often com­plain that they cannot see such objects as the ground beneath them, food, or the newspaper on the table before them, although it can be demon­strated that their macular vision is quite good. They become unable to move the eyes to obtain a foveal image and, for that reason, cannot examine the visual universe by moving the eyes from point to point to " regard" the environment. The lesions of this particular disorder are not in the cortex but neurons within the neural axis- in the pons, the Sylvian aqueduct, and the subthalamic areas. As in Parkinson's disease, the substantia nigra is depig­mented. This picture of saccadic paralysis may also be seen in advanced Huntington's chorea and in a variant of the Niemann- Pick neuronal storage dis­ease called " sea blue histiocytosis" ( 20). Examples have been described in the hereditary disorder called " olivopontocerebellar atrophy." A rare indi­vidual is born without the ability to make saccades, a condition that Cogan has called " congenital oc­ulomotor apraxia." The virtue of the optokinetic test in these people is that it shows abnormalities early in the course of the disease when more casual testing of visual ex­cursions may not reveal the diagnosis ( 21). The movies demonstrate the awkward move­ments of the eyes, and the patient's attempt to compensate with head motion. Unfortunately, such movements of the head only lead to contra­versive eye movements through the intact oculo­cephalic reflex. They then must hold the head still until the eyes restitute to primary position. Opto­kinetic testing shows only a limited slow phase tantamount to pursuit in the direction of the target but no corrective saccades ( fast phase). This abnor­mality is found in both horizontal and vertical di­rections. 1Clin Neuro · ophthalmol, Vol. 9, No. 4, 1989 264 N. f. DAVID OKN and Internuclear Ophthalmoplegia Early in the 1960s, Smith showed me phenome­non in several patients with multiple sclerosis whose optokinetic responses showed an interest­ing dissociation. Targets taken to the right, for in­stance, provoke nystagmus in the left eye only, and vice versa. He thought this strange since the classic abduction nystagmus that would be ex­pected in patients with multiple sclerosis showing internuclear ophthalmoplegia would be in the di­rection of gaze--- that is, when patients are taken into right gaze, nystagmus is in the right eye only. The finding was confirmed in several other pa­tients, but its meaning was unclear. It was regu­larly associated with internuclear ophthalmople­gia, and was obvious even when internuclear oph­thalmoplegia ( INO) was present only to a very mild degree. As we studied this optokinetic find­ing further, we began to realize its value in en­hancing the diagnosis of INO. The logical explana­tion ( Fig. 1) came when we were able to examine a patient who had a unilateral INO with underaction of medial rectus on looking to the right, due to a small infarction in the floor of the fourth ventricle. Although the two bundles of the median longitu­dinal fasciculus lie very close together in the pon­tine midline at the floor of the fourth ventricle, occlusion of a small paramedian perforating artery can clearly infarct one of these and spare the other. +- 0 0 0 0 0 0-< \ J\ J\ M " 1WN Q~ QLR l: Jr MLF · · i~ · LESION { A Right partial IND. I Clin Neuro- uphtlullmol, Vol. 9, Nu. 4, 1989 In examining the movies of this patient, it be­came clear that disassociation occurred not when gaze was evoked in the direction of targets but upon corrective saccadic return of the eyes to pick up on the oncoming stimuli. In cine sequences taken from these patients, one can clearly appre­ciate that the abducting eye moves over before the tardy medial rectus action of the adducting eye is brought into play. Another dynamic maneuver in testing the eye movements helped us understand this phenome­non. Lateral gaze is usually tested with slow visual pursuit of an object held in front of the patient. But if one asked the patient with internuclear ophthal­moplegia to refixate rapidly from the primary po­sition of gaze to a position in the lateral midfield 30- 40°, the abducting eye overshoots ( dysmetria) past the target and the adducting eye demon­strates an appreciable lag ( reduced saccadic veloc­ity) in coming over to the target. We call this con­stellation the " ocular dysmetria sign" for INO, in which the eyes are required to make saccadic re­fixation to the oncoming moving targets. The ad­duction lag then becomes much more apparent in this test than in slow pursuit. We then realized that OKN asymmetry was pro­duced by the lag in the adducting eye, with exces­sive abduction of the abducting eye, not in the movement of pursuit ( slow) phase but in the rapid ( saccadic) phase of the test. VI OPTOKINETIC NYSTAGMUS 265 These two tests then, the optokinetic test and the ocular dysmetria test ( 22), are both very useful in magnifying the defect of an often inapparent INO. As a matter of fact, I probably would stick with the ocular dysmetria test if I only had one to do. It will almost always bring out the defect even if it escapes detection in the casual testing of eye movements. OKN in Retraction Nystagmus The OKN tape or drum is also a handy device to assist in the diagnosis of lesions in the region of the cerebral aqueduct of Sylvius. Damage to the gray matter in the region of the posterior commis­sure and quadrigeminal plate results in a variety of abnormal neuroophthalmologic signs: pathologic lid retraction ( Collier's sign), pupillary areflexia, and paralysis of upgaze ( Parinaud's syndrome). But the most exotic manifestation in the so- called Koerber- Salus- Elschnig syndrome is the phenom­enon of retraction nystagmus. This abnormality is seen by viewing the patient from the lateral aspect to appreciate the backward jerking of the eyes with each nystagmoid beat. Al­though the retraction will often be provoked briefly by attempted upgaze or convergence, it is best sustained and observed by lateral inspection during testing of the vertical optokinetic re­sponses, usually best brought out by targets down ( 23). When the patient is viewed from the front the nystagmus includes spasms of convergence with each beat as well as retraction movements. In this remarkable movie, one can see the patient's eyes retracting 2- 3 mm with each beat. The standard explanation is that the elevators and depressors of the eyes are firing synchronously instead of recip­rocally, tugging the globe back into the orbit. This mechanism suggests a defect in reciprocal inhibi­tion of the muscles of the IIIrd and IVth cranial nerves. Although the commonest cause of the syn­drome in the middle- aged and elderly is a stroke in the high basilar distribution, this example was pro­duced by the usual cause in the young- pineal tu­mor. OKN and Congenital Nystagmus From time to time, the ophthalmologist is asked to examine a patient with a sprained neck or head­ache who has been discovered to have horizontal nystagmus, often quite asymmetrical, and aggra­vated by lateral gaze but sometimes present even in the primary position. Those of you who are fas­tidious enough to do optokinetic ( OKN) testing have often been in for a surprise. Instead of beat­ing opposite to the direction of moving targets, the fast phase of nystagmus in these people will be in the same direction as the motion of the tape or drum. Optokinetic reversal has come to be regarded as a clinical sign of specific significance although its physiology is still debated. Reversed OKN is vir­tually pathognomonic for congenital nystagmus. This perverse response was first demonstrated in patients who were known to show the overt famil­ial nystagmus present from birth. Milder examples of congenital nystagmus escape detection in early life and surface later during neurologic evaluation for unrelated complaints. Most patients have a life­long complaint of visual blurring or oscillopsia usually noted in eccentric direction of gaze. The amplitude of the nystagmus is related to the speed of targets. When the eyes of patients with congenital nystagmus are pursuing a visual target, it has been shown that the " null point," that ec­centric attitude of gaze at which the eyes are most quiet, shifts in a direction opposite to that of the visual pursuit ( 24). In other words, the OKN fol­lowing induces an eye position which is, in effect, strenuous lateral gaze that aggravates the fast beat­ing nystagmus- thought by most to be a gaze modulated beating that overrides the OKN phe­nomenon which the examiner is trying to stimu­late. The true nature of the defect in neuronal or­ganization or structure that causes this condition is unknown. Occasional writers have reported acquired neu­rologic disease can cause this reversal, but the con­sensus is that it is pathognomonic for congenital nystagmus ( 25). Studies have revealed that the wave form of congenital nystagmus during OKN stimulation are patterned exactly as those that are seen in gaze- evoked nystagmus in the same indi­vidual. CONCLUSION I hope that you have enjoyed this update on optokinetic nystagmus, an old and often neglected friend, whose acquaintance I made through the good offices of our celebrity, Dr. J. L. Smith. I hope that his enthusiasm is undiminished and that he will join me in urging you to apply the test appropriately in your practice, availing yourselves of its unique diagnostic benefits. This was a pro­pitious moment to congratulate Lawton in his 60th year, half of this time having been spent in the discipline of neuro- ophthalmology. It is because of ' Clin Nellro- ophthalmol, Vol, 9, No. 4, 1989 266 N. J. DAVID my long friendship with him that I have written this article. REFERENCES 1. Smith JL. Optokinetic nystagmus: its use in topical neuro­ophthalmologic diagnosis. Springfield, Illinois: Charles C. Thomas, 1963. 2. Baloh RW, Yee RD, Honrubia V. Clinical abnormalities of optokinetic nystagmus. In: Lennerstrand G, Zee DS, Keller EL, eds. Functional basis of ocular motility disorder. Oxford: Pergamon Press, 1982; 311- 20. 3. Leigh R], Zee DS. The Ileurology of eye movements. Philadel­phia: F. A. Davis Company, 1980: 11- 38. 4. Purkinje JE. Boebachtungen und Versuche zur Physiologie der Sinne. Bd. 2. Neue Beitrage zur Kemltniss des Sehens in subjec­tiver Hinsicht. Berlin, 1825: 60. 5. Helmholtz's treatises on physiological optics ( translated from the 3rd ed.). Southall JPC, ed. New York: Dover Publica­tions, 1962: 247-- 8, 278-- 9. 6. Barany R. Zur Klinik und Theorie des Eisenbahn- nys­tagmus. Arch Augenheilk 1921; 88: 139- 42. 7. Ohm J. Uber optischen Drehnystagmus. Lkin Mbl Augen­heilk 1921; 68: 234- 5. 8. terBraak JWG. Untersuchungen Uber optokinetischen Nystagmus. ( Physio\. Inst., Univ. Leiden.) Arch neerl Phys­io/ 1936; 21: 309- 76. 9. Waespe W, Henn V. Neuronal activity in the vestibular nucleus of the alert monkey during vestibular and optoki­netic stimulation. Exp Brain Res 1977; 27: 523-- 38. 10. Ohm J. Uber die Beziehungen zwischen willkiirlichen, op­tischen und vestibuUiren Augenbewegungen. Z Hals­Nasen- Ohrenheilkd 1932; 32: 234. 11. Brandt TH, Allum JH], Dichgans J. Computer analysis of optokinetic nystagmus in patients with spontaneous nystagmus of peripheral vestibular origin. Acta Otolaryngol ( Stock) 1978; 86: 115- 22. 12. Rahko T. Optokinetic nystagmus. Acta Ophthalmol ISupp/] ( Copenh) 1984; 161: 153-- 8. , Clin Neuro- ophthalmol. Vol. 9, No. 3, 1989 13. Brandt T, Daroff RB. The multisensory physiological and pathological vertigo syndromes. Ann Neurol 1980; 7: 195­203. 14. Smith JL. Optokinetic nystagmus: its use in topical neurooph­thalmologic diagnosis. Springfield, Illinois: Charles C. Thom­as, 1963: 63-- 8. 15. Cords R. Optisch- motorisches Feld und optisch- motorische Bahn. Albrecht von Graefes Arch Ophthalmo/ 1926; 117: 58-- 113. 16. Baloh RW, Yee RD, Honrubia V. Optokinetic nystagmus and parietal lobe lesions. Ann Neurol 1980; 7: 269- 76. 17. Davidoff RA, Atkin A, Anderson Pj, Bender MB. Optoki­netic nystagmus in cerebral disease. Clinical and patholog­ical study. Arch Neurol 1966; 14: 73-- 81. 18. Henn V, Cohen B, Young LR. Visual- vestibular interaction in motion perception and the generation of nystagmus. Neurosci Res Prog Bull 1980; 18: 458-- 651. 19. David N], Mackey EA, Smith JL. Further observations in progressive supranuclear palsy. Neurology 1968; 18: 349- 56. 20. Neville BGR, Lake BD, Stephens R, Sanders MD. A neuro­visceral storage disease with vertical supranuclear ophthal­moplegia, and its relationship to Niemann- Pick disease. A report of nine patients. Brain 1973; 96: 97- 120. 21. Chu Fe. Reingold DB, Cogan DG, Williams AC. The eye movement disorders of progressive supranuclear palsy. Ophthalmology 1979; 86: 422-- 8. 22. Smith JL, David NJ. Internuclear ophthalmoplegia: two new clinical signs. Neurology 1964; 14: 307- 9. 23. David NJ. Nystagmus and other ocular oscillations. In: Mohr JP, ed. Manual of clinical problems in neurology with annotated key references. Boston: Little, Brown and Com­pany, 1984: 80. 24. Dell'Osso LF. Nystagmus and other ocular motor oscilla­tions and intrusions. In: Lessell S, Van Dalen JTW, eds. Neuro- Ophthalmology, vol. III. Amsterdam: Excerpta Medica, 1984: 157. 25. Halmagyi GM, Gretsty MA, Leech J. Reversed optokinetic nystagmus ( OKN): mechanism and clinical significance. Ann Neuro/ 1980; 7: 429- 35. 26. Stenvers HW. Uber die kIinische bedeutung des optischen Nystagmus fur die zerebrale Diagnostik. Schweiz Arch Neu­rol Psychiatr 1925; 14: 279-- 88.