British Journal of Ophthalmology, 1980, 64, 926-932

Study of congenital nystagmus: optokinetic nystagmusROBERT D. YEE," ROBERT W. BALOH,2 AND VICENTE HONRUBIA3From the 'Department of Ophthalmology, the 2Department of Neurology, and the3Division of Head and Neck Surgery, Department of Surgery, UCLA School of Medicine,Los Angeles, California, USA

SUMMARY A severe defect of optokinetic nystagmus (OKN) was found in 46 patients with congenitalnystagmus. Abnormal patterns of OKN, such as superimposition of pendular oscillations on theoptokinetic slow component and inversion of OKN, were observed. Optokinetic gain (eye move-ment velocity/drum velocity) was decreased compared to that in normal subjects, and optokineticafter-nystagmus, or transient persistence of OKN after cessation of visual stimulation, was absent.These findings suggest that there is a defect in the subcortical optokinetic system in congenitalnystagmus. Optokinetic responses did not clearly differentiate patients who had ocular lesions thatimpair vision, such as ocular albinism and opacities of the ocular media, from patients who did nothave such lesions. Similar abnormal patterns ofOKN were found in both groups of patients, althoughoptokinetic gain tended to be lower in patients with ocular lesions than in those without lesions.

Optokinetic nystagmus (OKN) is a jerk nystagmusthat is usually induced by movement in a large areaof the visual surround during clinical examinationof eye movements. Rotation of patterns, such asvertical stripes that occupy most or all of the visualfield, produces movement of images across theretina. The slow component of OKN tracks themovement of the pattern and tends to stabiliseimages on the retina. During naturally occurringhead movements the visual surround is stationary,and movement of the eyes produces movement ofimages on the retina. The vestibulo-ocular response(VOR) that is induced by the head movementproduces a slow component in the direction oppo-site to that of the head movement and, therefore,decreases movement of images on the retina. How-ever, at low frequencies of rotation (less than 1 Hz)the VOR alone cannot match the velocity of thehead movement and cannot completely stabilise theretinal images. Head movements, by producingmovement of images on the retina, also induce anoptokinetic response. The slow components of theVOR and optokinetic response are in the samedirection and act synergistically to match thevelocity of the head movement and more effectivelystabilise the retinal images improving vision.

Congenital nystagmus is an ocular motor disorderin which instability of fixation is manifested as

Correspondence to Dr R. D. Yee, Jules Stein Eye Institute,Department of Ophthalmology, UCLA School of Medicine,Los Angeles, California 90024, USA.

involuntary oscillations with pendular and complexwave forms.12 Its aetiology is essentially unknown.A clinically useful classification of congenitalnystagmus based on its pathophysiology is notavailable. Previous attempts to construct a classifi-cation have divided patients into those who hadassociated ocular lesions, such as ocular albinismand opacities of the ocular media, and those whodid not have such lesions. It was proposed that poorvision produced by ocular lesions in the first groupled secondarily to instability of fixation, whereasin the second group there was a primary malde-velopment of the ocular motor system. However,there is no difference in nystagmus waveformsbetween these 2 groups of patients to substantiatethis classification.2 Careful clinical examination isthe most effective means of identifying associatedocular lesions. In this study we attempt to determineif OKN differs between patients with associatedocular lesions and those without such lesions.Poorly formed, absent, and inverted OKN havebeen reported in congenital nystagmus.3 However,study of these responses with eye movement record-ings has not been reported in a large number ofpatients.

Patients and methods

PATIENTSForty-six patients with congenital nystagmus werestudied. Each patient received a neuro-ophthalmicexamination to measure visual functions, such as

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visual acuity in the position of gaze with leastnystagmus (null position), and to detect associatedocular lesions that could impair vision, such asocular albinism, chorioretinal scars, and opticatrophy. Twenty-eight patients had no other asso-ciated ocular lesion that could impair vision andwere classified as having motor-defect nystagmus,as described by Cogan.4 Visual acuity ranged from20/25 to 20/60 in this group of patients (average20/40). Eighteen patients with ocular lesions wereclassified as having sensory-defect nystagmus. Theirvisual acuity ranged from 20/40 to 20/400 (average20/100).

EYE MOVEMENT RECORDINGSHorizontal eye movements were recorded monocu-larly with a D-C electro-oculographic system thathad a band width of0-35 Hz (-3 dB). Skin electrodeswere placed at the inner and outer canthi of eacheye. Electrodes were also placed above and belowthe left eye to detect artefacts from eyelid blinks.Patients were seated within a 2-metre diameteroptokinetic drum whose interior consisted of2-5-cm wide, white, vertical stripes that were placedevery 15 degrees against a black background.Patients were instructed to fixate stripes as theypassed in front of them and not to track individualstripes as they traversed their visual fields. The drumwas rotated at constant velocities of 100, 300, and60°/second toward the right and left, and sinusoi-dally at 0-05 Hz and peak velocities of 300 and60°/second. The mean slow component velocity wascalculated for approximately 60 seconds (80 to 120nystagmus cycles) by a laboratory computer afterdigitisation at 200 samples/second. Eye movementswere also recorded during attempted fixation of asmall spot in the primary position and in eccentric,horizontal positions at every 5 degrees to 30 degrees.The effects of eccentric gaze on nystagmus charac-teristics, such as waveform and slow componentvelocity, were compared to eye movements inducedby optokinetic stimulation to verify that the OKNrecorded was not simply the result of eccentricgaze.The gain of the optokinetic response (slow com-

ponent eye velocity/drum velocity) was then calcu-lated. There is difficulty in attempting to measureOKN quantitatively in congenital nystagmus. Thecalculation of gain assumes that the movement ofthe drum is an accurate representation of the move-ment of images on the retina which is the stimulusfor OKN. In congenital nystagmus, however, thespontaneous nystagmus also produces movementof images on the retina. Fortunately the movementof the drum was in one direction and was of constantvelocity, while the smooth movements of the

spontaneous nystagmus were usually in bothdirections and had varying velocity, making detec-tion of an effect of optokinetic stimulation easier.An experimental paradigm could be constructed inwhich retinal images are stabilised during spon-taneous nystagmus by a negative feed-back systemthat detected the nystagmus and moved the drumto match the eye movements. A constant-velocitydrum movement could be added, and an 'open-loop'gain of OKN could be measured. However, in thepresent study without retinal stabilisation thecalculated 'gain' was probably a useful approxima-tion of the function of the optokinetic system andwas a closer approximation to more commonlyused clinical tests of OKN.The optokinetic response in normal subjects is

characterised by a persistence of nystagmus in thedark for several seconds after optokinetic stimula-tion has been stopped (optokinetic after-nystagmus),and by an illusion of self-rotation in the oppositedirection to drum rotation during constant velocityoptokinetic stimulation (circularvection).8-'0 Anattempt was made to induce optokinetic after-nystagmus (OKAN) in 20 patients with motor-defect nystagmus and in 12 patients with sensory-defect nystagmus. After 60 s of drum rotation at aconstant velocity of 60°/s optokinetic stimulationwas terminated by turning off the lights and atransient persistence of OKN was sought. Sixteenpatients with motor-defect nystagmus and 10patients with sensory-defect nystagmus were ques-tioned about circularvection. During 1 minute ofconstant velocity drum rotation at 60°/s patientswere asked if they felt that they were moving, and,if so, in what direction they were rotating. Aftercessation of optokinetic stimulation in the darkthey were asked if the illusion of self-rotationpersisted (post-circularvection).

Results

OKN PATTERNSSeveral patterns of OKN were observed.

Normal. The normal pattern of OKN was a jerknystagmus with the slow component in the directionof drum rotation and the fast component in theopposite direction (Fig. 1). The velocity of the slowcomponent was constant during the nystagmuscycle, resulting in a ramp-like shape of the slowcomponent. Eleven patients with motor-defectnystagmus (39%) ans 7 patients with sensory-defectnystagmus (39%) displayed this normal OKNpattern during stimulation at the several drumvelocities. During optokinetic stimulation the eyesof normal subjects and most patients with congenitalnystagmus deviate in the orbit in the direction of

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A

Fig. 1 Normal pattern ofOKN. A. Nystagmus duringattempted fixation ofastationary target. Top-10°to right. Centre-primaryposition. Bottom-10° to left.Note null position at 100 to left.B. Drum rotating at 60°/s toright. Note ramp-like shape ofslow components. Arrowindicates centre position.C. Drum rotating at 60°/s to left.Arrow indicates centre position.Deflections up are to the right,deflections down are to the left.

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the fast component of OKN, as shown in Fig. 1. Theeyes usually do not deviate more than 15 degreesfrom the midline. The normal pattern of OKN inpatients with congenital nystagmus was not pro-duced by eccentric gaze, as could be seen by com-paring nystagmus in eccentric gaze to OKN. InFig. 1 the null position, or position in which thenystagmus was least in amplitude, was approxi-mately 10 degrees to the left. In most patients thenystagmus has a pendular waveform at the nullposition and a jerk-like waveform in eccentric gazeto either side of the null position. The fast component

or saccade in eccentric gaze is usually in the directionof eccentric gaze. The relatively large amplitude,ramp-like slow component of the normal patternof OKN cannot be explained simply as a result ofeccentric gaze.

Superimposition. The superimposition pattern ofOKN consisted of a high frequency pendularoscillation superimposed on the ramp-like slowcomponent. The slow component was in the direc-tion of drum rotation. A large amplitude fast com-ponent was present in the opposite direction (Fig. 2).In several patients with this OKN pattern the high

Fig. 2 Superimposition patternof OKN. A. Nystagmus duringattempted fixation of a stationarytarget. Top-150 to right.Centre-primary position.Bottom-10° to left. Note smallamplitude, 5 Hz pendularoscillations. B. Drum rotatingat 60°/s to right. Note ramp-likeslow component ofOKN duringintervals in which pendularoscillations are absent. Arrowindicates centre position.C. Drum rotating at 60°/s toleft. Arrow indicates centreposition. Deflections up are tothe right, deflections down areto the left.

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frequency oscillation was absent during part of theslow component ramp, as illustrated in Fig. 2,showing that the pendular oscillation was in factengrafted on a smooth optokinetic response. Thevelocity of the slow component ramp was measuredduring these intervals of absent pendular oscillation.Four patients with motor-defect nystagmus (14%)and 3 patients with sensory-defect nystagmus (17%)had this OKN pattern.

Pseudoinversion and true inversion. The pseudo-inverted pattern of OKN consisted of slow com-ponents in the direction opposite to drum rotationand fast components in the same direction as drumrotation. This pattern simply represented persistenceof the patient's basic nystagmus, that is, the nystag-mus pattern during attempted fixation of a stationarytarget, during optokinetic stimulation rather thantrue inversion of the optokinetic response. Forexample, if the saccade in the basic nystagmuswaveform was towards the left, during drumrotation to the right there might be little effect onthe basic nystagmus, but the saccade towards theleft would give the impression that the optokineticresponse was in the expected direction. Duringdrum rotation to the left the basic nystagmus wouldpersist, but the saccade toward the left would givethe impression that the OKN was inverted. Theclinically observed 'inversion' would be present inonly 1 direction of drum rotation. Two patientswith sensory-defect nystagmus (22%0) had thispattern. No patient with motor-defect nystagmushad this pattern.Some patients showed pseudoinversion of OKN

in both directions of drum rotation. In this patternthe saccade of the basic nystagmus waveform was

Fig. 3 Pseudoinverted patternof OKN. A. Nystagmus duringattempted fixation of a stationarytarget. Top-150 to right.Centre-primary position. Notealteration of cycles withrefoveating saccades to rightand left, and exponentiallyincreasing velocity ofsmootheye movements. B. Drumrotating at 30°/s to right. Notesmall amplitude saccades toright and smooth eye movementswith exponentially increasingvelocity to left. Arrow indicatescentre position. C. Drumrotating at 30°/s to left. Arrowindicates centre position.Deflections up are to the right,deflections down are to the left.

used to track stripe movement at the lower drumvelocities of 10 and 30 degrees/s. In Fig. 3 the basicnystagmus consisted of alternating nystagmuscycles with small saccades to the right and left.Dell'Osso and Daroff' have shown that the saccadein each cycle attempts to refoveate the target.During drum rotation to the right the nystagmuscycle with the saccade to the right predominated.During rotation to the left the cycle with the saccadeto the left predominated. However, close examina-tion of the recorded eye movements showed thatOKN was not actually inverted. The smooth eyemovements of the nystagmus pattern during drumrotation in both directions had exponentiallyincreasing velocities rather than the constantvelocities of the ramp-like slow components of thenormal OKN pattern. These smooth movementsrepresent the smooth movements of the basicnystagmus waveform and not inverted slow com-ponents of OKN. As shown in Fig. 3, this patternof 'pseudoinversion' of OKN was not produced bythe effect of eccentric gaze on the basic nystagmus.Three patients with motor-defect nystagmus (11%)and 2 patients with sensory-defect nystagmus (11%)had this pattern.True inversion ofOKN with reversal of ramp-like

slow components was found in only 2 patients withmotor-defect nystagmus (7%) and in 2 patients withsensory-defect nystagmus (11%), 1 patient withocular albinism, and I patient with oculocutaneousalbinism. In Fig. 4 the slow components of OKNwere ramp-like with constant velocity. A gradualbuild-up of reversal during constant velocity drumrotation was occasionally observed. Therefore mostinstances of 'inversion' of OKN detected by clinical

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Fig. 4 Inverted pattern ofOKN. A. Nystagmus duringattempted fixation ofastationary target. Top-150 toright. Centre-primary position.Bottom-15° to left. Note nullposition at 15° to left. B. Drumrotating at 30°/s to right. Noteslow components are ramp-likeand to the left. Arrow indicatescentre position. C. Drumrotating at 30°/s to left. Noteslow components are to theright. There is gradual build-upofslow component velocity.Arrow indicates centre position.Deflections up are to the right,deflections down are to the left.

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observation alone were found to represent pseudo-inversion rather than true inversion when examinedby eye movement recordings.

OPTOKINETIC GAIN

Gain was not measured in patients with the pseudo-inverted or true inverted pattern of OKN. Twenty-three patients with motor-defect nystagmus (82%)had optokinetic responses in which the OKN gaincould be measured; whereas only 10 patients withsensory-defect nystagmus (56%) had measurableOKN gains. The gains from constant velocity testsand sinusoidal tests are presented in Table 1. Thedata from constant velocity drum rotation to theright are presented. Data from leftward drumrotation were similar. The OKN gain in motor-defect nystagmus was greater than that in sensory-defect nystagmus. For example, during constantvelocity drum rotation at 30°/s the mean OKNgain ± 1 SD for patients with motor-defect nystag-mus was 0-38±0-19, whereas the gain in patientswith sensory-defect nystagmus was 0-22±0-19. The

mean OKN gains for both groups were significantlydifferent from that of normal subjects in our labora-tory, 0-81+0.09.11 The gain in patients with motor-defect nystagnus was significantly greater than thatin patients with sensory-defect nystagmus (P<0-01,Student's t test). The difference between the patientgroups at 60°/s was significant at the 1% level, butthe difference at 10°/s was not significant at the 5%level. During sinusoidal drum rotation (0-05 Hz,30°/s), the mean gains in both patient groups weresignificantly lower than in normal subjects (P<0-01,Student's t test), and were significantly differentfrom each other (P<0-02, Student's t test). Themean gain in motor-defect nystagmus was 0-39±0-14, and in sensory-defect nystagnus was 0-16±0-18. The mean gain in normal subjects in ourlaboratory was 0-75±0-15. The difference betweenthe patient groups at 60°/s was not significant atthe 5% level.The hypothesis that OKN gain was linearly

related to visual acuity was evaluated in all patientsand within each patient group. However, linear

Table I Optokinetic gain1

Constant drum velocity' Peak sinusoidal drunm velocity3

10°/s 30'/s 60'/s 30°/s 60'ls

Normal subjects 0-88±0 074 0-81 ±0-09 0-79±0-13 0-75±0-15 0-71±0-22

Motor-defect nystagmus 0-29±0-13 0-38±0-19 0-35±0-18 0-39±0-14 0-25 ±0-17

Sensory-defect nystagmus 0-20±0-17 0-22±0-19 019±0-19 0-16 ±0-18 0-18±0-12

'Gain = peak eye velocity/peak drum velocity. 2Constant drum rotation to the right. 3Sinusoidal drum rotation at 0-05 Hz. 4Mean gain ±1 SD.

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regression analysis indicated that correlation coeffi-cients of OKN gain and visual acuity were notstatistically significant among all patients (0 577,P>0 05), within the motor-defect group (0 524,P>0 05) or within the sensory-defect group (0-299,P>0.05).

OKAN AND CIRCULARVECTIONNone of the 32 patients tested had OKAN afterconstant velocity optokinetic stimulation in eitherdirection. Some patients had persistence of theirbasic nystagmus with eyes opened in the dark withor without previous optokinetic stimulation. Thisnystagmus was not interpreted as representingOKAN. Eighteen patients with motor-defect nystag-mus (64°') and 7 patients with sensory-defectnystagmus (400o) experienced circularvection (CV).Characteristically, the patients reported an illusionof self-rotation in the direction opposite to thatof drum rotation beginning 5 to 10 seconds afteronset of optokinetic stimulation. CV ended abruptlywhen stimulation was terminated by turning offthe lights. No correlation between OKN gain andCV was found in either patient group.

Discussion

Convincing evidence has been presented that OKNresults from simultaneous stimulation of a subcorti-cal optokinetic system and the pursuit system inmany species. Ter Braak'213 showed that afoveateanimals, such as the rabbit, produced OKN inresponse to movement of large objects (passiveOKN) but did not track small objects of possible'interest' to the animal. Passive OKN persistedafter removal of the cerebral hemispheres in theseanimals and was presumably produced by an en-tirely subcortical ocular motor system. Animalswith a fovea or area centralis, such as the monkeyand dog, had both passive and active OKN. Onlyactive OKN was lost after removal of the cerebralhemispheres or occipital lobes, and presumablyutilised cortical pathways.

Recent studies of OKN in human patients withlocalised lesions affecting the ocular motor sys-tem14-16 suggest that the optokinetic response inman consists of contributions from the smoothpursuit system and a subcortical optokinetic system.The smooth pursuit contribution depends on stimu-lation of the fovea, utilises the retino-geniculo-calcarine sensory pathway and the occipito-mesen-cephalic motor pathway, and produces the rapidbuild-up of slow component velocity of OKNobserved after a step of optokinetic stimulation.The contribution from the subcortical system issimilar to OKN in afoveate animals, such as the

rabbit."7 This contribution depends on stimulationof motion-sensitive cells in the retinal8 20 thatproject via the accessory optic tract to cells in thenucleus of the optic tract.2' There is convincingevidence that motion-sensitive retinal ganglioncells are the input stage of the optokinetic loop inthe rabbit, since their firing rates have been shownto correlate with the velocity of OKN.22 Cellsin the nucleus of the optic tract in turn project tothe vestibular nuclei and cerebellum.23 The opto-kinetic response in afoveate animals is characterisedby a slow, gradual build-up of slow componentvelocity over many seconds and OKAN. In severalpatients with localised lesions of the parietal lobe15and cerebellar flocculi'6 whom we have reported onOKN was characterised by a slow build-up of slowcomponent velocity and preservation of OKAN.Smooth pursuit was severely impaired such that thesubcortical contribution to OKN was 'uncovered'.Ter Braak'4 described a man who was corticallyblind from histopathologically verified infarctionof the occipital lobes, who had no pursuit, but whoshowed the persistence of OKN with a slow build-upand OKAN with rotation of a surrounding opto-kinetic drum in one direction. Presumably theOKN in this patient was produced by the subcorticaloptokinetic system.The pursuit system is probably abnormal in

congenital nystagmus. The function of this systemis difficult to measure, since the smooth movementvelocities of the spontaneous nystagmus are veryhigh (up to 90°/s) and a relatively small velocitycontribution from pursuit is difficult to detect.Pursuit function has been measured in a few patientswith relatively low velocities and has been shown tobe subnormal.224

In normal human subjects OKAN (present inapproximately 70% of subjects in our laboratory)circularvection and postcircularvection in the darkprobably result from stimulation of the subcorticalsystem.8-20 In our patients with congenital nystag-mus slow build-up of OKN, OKAN, and postcircularvection were not observed. In most patientsnystagmus was greatly reduced in amplitude orabsent in the dark with loss of fixation. We wouldexpect that OKAN could be easily observed if itwere present. Although the slow component ofOKN could be obscured by the high velocity smoothmovements of the basic nystagmus in the light, thelow-velocity slow component of OKAN should bedetectable in the dark. The absence of OKAN inour patients was another indication that a normaloptokinetic response was not simply hidden by theintense basic nystagmus. Most of our patients didexperience circularvection during optokinetic stimu-lation, however. Circularvection does not appear to

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correlate with OKN in congenital nystagmus. Asevere defect in the subcortical optokinetic system,therefore, appears to be present. It is unlikely thatthe impaired OKN in congenital nystagmus can beexplained simply by poor visual acuity. Defects ofcentral vision resulting from acquired lesions of themacula in man can be associated with normalOKN.25The abnormalities of OKN in patients with

motor-defect nystagmus were qualitatively similarto but quantitatively different from those in patientswith sensory-defect nystagmus. This suggests thatthe type and location of defect(s) are similar in bothgroups but that the severity is variable. In motor-defect nystagmus we might hypothesise that de-velopmental anomalies are present in the pursuitand subcortical optokinetic systems at birth. Adegree of postnatal development might be requiredin these systems. In sensory-defect nystagmus theabsence of well-formed retinal images or normalconduction through the optic nerves due to bilateralopacities of the ocular media or bilateral opticatrophy could interrupt this postnatal development.Alternatively, in sensory-defect nystagmus 2 distinct,unrelated defects in the visual afferent and ocularmotor systems may be present. The ocular motorlesion would be identical to that in motor-defectnystagmus. Although no basic differences have beenfound between motor-defect nystagmus and sensory-defect nystagmus in nystagmus waveform, frequency,and amplitude,2 or in patterns of OKN, this classifica-tion of congenital nystagmus is still clinically useful.It emphasises the need to search carefully for asso-ciated ocular lesions. The presence of lesions hasimportant implications for the prognosis for usefulvisual function and evaluating clinical indicationsfor prism and surgical therapies. We have foundthat measurement of the patient's best visual acuityin the null position and/or with convergence inwhich the nystagmus amplitude is minimised ishelpful in indicating that associated ocular lesionsare present. Visual acuity is usually less than 20/80in sensory-defect nystagmus and better than 20/60in motor-defect nystagmus despite similar amplitudeof nystagmus. Careful clinical ophthalmic examina-tion, including measurement of visual acuity inthe null position and tests of colour vision, is stillthe best means of detecting associated ocular lesions.

This work was supported by a grant from the National EyeInstitute, NIH Grant 2 ROI EY01853-03.

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