Journal of Neurology, Neurosurgery, and Psychiatry, 1974, 37, 570-577

Acquired pendular nystagmus with oscillopsia inmultiple sclerosis: a sign of cerebellar nuclei disease

JURGEN C. ASCHOFF,' B. CONRAD, AND H. H. KORNHUBER

From the Department of Neurology, University of Ulm, W. Germany

SYNOPSIS In an unselected series of 644 cases of multiple sclerosis, 25 cases with acquired pendularnystagmus were found. Ten additional cases of pendular nystagmus in multiple sclerosis were

investigated, and four cases from the literature are analysed. Acquired pendular nystagmus is purelysinusoidal in form, ceases with eye closure, is accompanied by oscillopsia, often monocular andvertical in direction, and never accompanied by optokinetic inversion. This is different from con-

genital nystagmus. Acquired pendular nystagmus in multiple sclerosis shows a high correlation withholding tremor of head and arm and with trunk ataxia, and must therefore be viewed as a result oflesions of cerebellar nuclei or their fibre connections with the brain-stem. Supporting evidence isdiscussed. The results fit into a theory of cerebellar function according to which the cerebellar nucleiare involved in the maintenance of positions.

Pendular nystagmus has been defined as oscil-latory eye movements in which fast and slowphases cannot be differentiated. The mostcommon and best known clinical manifestationis congenital pendular nystagmus. Pendularnystagmus and congenital nystagmus are notequivalent, however, because congenital nystag-mus is frequently not pendular, and pendularnystagmus may be acquired. Examples of thelatter are spasmus nutans (Raudnitz, 1897),miners' nystagmus (Ohm, 1954), pendularnystagmus in multiple sclerosis (Uhthoff 1890;Ohm, 1949; Nathanson et al., 1955; Kornhuber,1966), and pendular nystagmus in conjunctionwith palatal myoclonus (Alajouanine et al., 1935;Guillain, 1938; Bender et al., 1952; Nathanson,1956; Chokroverty and Barron, 1969). Relativelyfew cases of acquired pendular nystagmusassociated with multiple sclerosis have beenadequately investigated. For the definition ofvarious kinds of nystagmus including spon-taneous, fixation and gaze nystagmus the readeris referred to Jung and Kornhuber (1964).

In an unselected series of 644 patients withmultiple sclerosis acquired pendular nystagmuswas found in 25 patients. The symptoms of this

Address for reprints: University Hospital, Department of Neurology,SteinhovelstraBe 9, 79 Ulm/Donau, West Germany.

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acquired pendular nystagmus in multiple sclerosiswill be described in an attempt to determine thelocalization of the pathological process under-lying the phenomenon. Preliminary results havebeen published (Kornhuber, 1969; Aschoff et al.,1970). Since the completion of this series in1969, 10 additional cases of acquired pendularnystagmus have been investigated, the results ofwhich fully confirm the conclusion drawn fromthis series of 25 patients.

METHODS

In the course of three years, 644 unselected patientssuffering from multiple sclerosis were investigated, ofwhom 25 exhibited pendular nystagmus. Thirteen ofthese were male and 12 were female, with an averageage of 39 4 years. In 19 patients the illness had anacute onset and showed frequent exacerbations. Inthe remaining six patients the disease followed a morechronic course. Diagnosis of multiple sclerosis wasconfirmed by typical spinal fluid findings, clinicalsymptoms, and disease progress. They all lived withtheir families and required only temporary treatmentin the hospital.Eye movements were recorded by means of AC or

DC electrooculography (electronystagmography) orphoto-electronystagmography. The former methodwas used to record horizontal and vertical eye move-ments (Beckman electrodes) with the eyes both

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Acquired pendular nystagmus with oscillopsia in multiple sclerosis

TABLESUMMARY OF FINDINGS IN 25 PATIENTS WITH MULTIPLE SCLEROSIS SHOWING PENDULAR NYSTAGMUS*

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* Four cases from the literature are summarized at the bottom of the Table.

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Jurgen C. Aschoff, B. Conrad, and H. H. Kornhuber

opened and closed. Recordings were made ofsaccadic and smooth pursuit movements as well asof optokinetic, rotational and postrotational nystag-mus. Recordings were also made over a longerperiod of time of visual fixation, and relaxation withthe eyes closed. For analysis of pendular nystagmus,the direction, inter-eye-phase-relationship, constancyof frequency and amplitudes, influence of fixation,gaze direction, alertness, and rotational accelerationwere evaluated. All 25 patients were investigated atleast twice in the course of several months (up totwo years).

RESULTS

ANALYSIS OF PENDULAR NYSTAGMUS A summaryof the nystagmographic findings, of oscillopsia,scotomata, and visual acuity is given in theTable. Four cases of pendular nystagmus inmultiple sclerosis, which have been fullydescribed in the literature, are included at thebottom of this Table.

Pendular nystagmus during visual fixationreveals a wide range of parameters. It may bemonocular or binocular, and may show a largevariety of directions from linear (horizontal orvertical) through eliptical or circular movementsand even different directions for each eye. Onnystagmographic recordings acquired pendularnystagmus in multiple sclerosis always shows apurely sinusoidal form (Fig. 1). The direction ofthe pendular movements was similar in both

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eyes in 21 patients but different in four patients(cases 4, 5, 7, 9, see Table). Binocular acquiredpendular nystagmus was vertical in six patientsas opposed to horizontal in 15 cases. Both eyesare phase-locked in their oscillating pendularmovements (except for one patient). In thislatter case (no. 10) the pendular nystagmusduring leftward gaze consisted of in-phase move-ments, whereas during gaze to the right thesemovements were 90° out of phase.The average frequency of pendular nystagmus

was 3 9 Hz + 0 05 and was the same for both eyesin a binocular pendular nystagmus. Within thelimits of experimental error, the frequenciesremained constant throughout testing, and wereunaffected by direction of gaze, fixation, andalertness.The amplitude of pendular nystagmus was

usually less than 2° but was as great as 6 to 70 inone patient. In three patients the amplitude wasso small that it could be detected and analysedonly by means of ophthalmoscopic examination.In contrast with the constancy of frequency,there was a marked variability of amplitudesdepending on the direction of gaze (Fig. la), andoffixation (Fig. I b, c). Optokinetic and vestibularstimuli may also affect the amplitude (Table).With the eyes closed, pendular nystagmusinvariably ceases. It might, however, reappearafter a latency of some 10 seconds at the samefrequency but with a much reduced amplitude

FIG. 1. Electronystagmographicrecordings ofpendular nystagmus.(a) Binocular horizontal pendularnystagmus with large amplitudes ongaze to the left. No pendular nystagmuson gaze to the right. Postsaccadicinhibition after saccadic eye movements.(b) Left eye monocular pendularhorizontal nystagmus during fixationwhich disappears when the eyes areclosed. (c) Right eye monocular verticalpendular nystagmus during fixation.Pendular nystagmus ceases after eyeclosure but reappears with smallamplitude after 10-15 seconds.

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Acquir-edpendular nystagmuis with oscillopsia in multiple sclerosis

(Fig. ic). In addition, a postsaccadic inhibitionof pendular nystagmus was observed in mostpatients. After a saccadic eye movement,pendular nystagmus is inhibited for one to twoseconds. This can be shown not only in electro-nystagmographic recordings, but is also observedby patients as a transient inhibition of theiroscillopsia after rapid eye movements (Fig. la).

Seventy per cent of the patients with pendularnystagmus complained of oscillopsia, especiallywhen fatigued or fixating distant objects. Visualacuity was reduced to 20% in nearly all cases,also in three patients (cases 6, 15, 25) the reduc-tion ofvisual acuity was minimal. In three patients(cases 1, 7, 8), with asymmetrical or predomin-antly monocular pendular nystagmus, there was agreater loss of visual acuity in the oscillating eye.Reduction in visual acuity was at least in partdue to the pendular nystagmus because therewere cases without any sign of optic nerve lesion.

Pendular nystagmus can be altered during anacute exacerbation or by a remission of theunderlying disease. In one patient, a previouslyobserved pendular nystagmus ceased after theremission of an acute exacerbation; in anothercase pendular nystagmus was observed todevelop after an acute exacerbation.Gaze nystagmus was present in 23 of the 25

patients, gross dysmetria of horizontal saccadiceye movements in 17 patients. In none of themhas inversion of optokinetic nystagmus beenobserved, as is often seen in congenital pendularnystagmus.

NEUROLOGICAL SYMPTOMS A total of 644patients with multiple sclerosis were examined,25 of whom showed pendular nystagmus. Acomparison between the latter and the 619patients without pendular nystagmus revealedno correlation with duration of illness (average12-7 years for patients with and 11-7 years forpatients without pendular nystagmus), or withage (average 43-5 years for patients with and 44 1years for patients without pendular nystagmus).There was also no significant difference betweenthe two groups as far as frequency and severityof spinal symptoms (spasticity, paresis, auto-nomic dysfunction) are concerned.On the other hand, there was a significant

difference for cerebellar symptoms between thetwo groups. Patients with pendular nystagmus

20 40 6C 80 °Jo 100

cerebellar ataxiaof the upper ortower limb withintention tremor

severe cerebellordisturbance ofpostural equilibrium

trunk ataxia

head tremor INUMBER OF PATIENTS WITH MULTIPLE SCLEROSIS

FIG. 2. Comparison of cerebellar symptoms inpatients with ( ) and without (-)pendular nystagmus.Pendular nystagmus shows a high correlation withsymptoms due to cerebellar lesions.

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2.6 3,0 3.4 3,8 4.2 4,6 50frequency of pendular nystagmus Hz

FIG. 3. Frequencies ofhead tremor versus frequenciesof pendular nystagmus in 13 patients suffering frommultiple sclerosis, and showing head tremor andpenidular nystagmus.

always suffered from severe cerebellar symptomssuch as trunk ataxia, head tremor, intentiontremor, or the cerebellar type of speech dis-turbance. Figure 2 shows the frequency of themain cerebellar symptoms for patients with andwithout pendular nystagmus, as well as opticdisc findings and scotomas. The difference incerebellar symptoms between the two groups is

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highly significant-for instance, trunk ataxia 6%versus 92%, and head tremor 500 versus 72%.The frequency of head tremor shows some

correlation with the frequency of the pendularnystagmus (see Table and Fig. 3). Most often thefrequency of pendular nystagmus is slightlyhigher than the frequency of the head tremor(eight of 13 cases, in the other five patients thefrequencies were virtually identical within0-1 Hz). There was, however, no significantrelationship between the direction of thependular nystagmus and that of the head tremor.Therefore, pendular nystagmus cannot be ex-plained as the vestibular compensation of theeyes for head tremor. The head tremor is evokedby active head holding and disappears in therelaxed supine position.Case 2 with elliptical pendular nystagmus died

of pulmonary embolism. Necropsy showedtypical patchy demyelinizations throughout thespinal cord and in all samples of forebrain,cerebellum and brain-stem.

After completion of the statistical analysis forthe 644 patients, 10 additional cases of acquiredpendular nystagmus in multiple sclerosis wereseen. They completely confirmed our previousfindings in the series ofthe first 25 cases. Acquiredpendular nystagmus can also be present as anisolated symptom. Among the 10 latter cases notincluded in the Table there was a patient whocomplained only of oscillopsia. A monocularhorizontal pendular nystagmus was found, andfrom the patient's history the diagnosis ofmultiple sclerosis in full remission (except for thependular nystagmus) was established. Acquiredpendular nystagmus with oscillopsia can thusremain as an isolated symptom in multiplesclerosis in the remission phase.

DISCUSSION

Acquired pendular nystagmus has been found inapproximately 400 of our patients with multiplesclerosis, which represents a higher proportionthan previously presumed in the literature,although Uhthoff in 1890 observed pendularnystagmus in conjunction with multiple sclerosisin seven out of 100 investigated patients. Adetailed description of pendular nystagmus inmultiple sclerosis is available in only three casesby Nathanson et al. (1955), one case by Ohm

(1949), and one case by Kornhuber (1966).Bender (1965) in his work on oscillopsia addition-ally has described acquired pendular nystagmuswith vertical, horizontal, and rotatory directionsas the course of oscillopsia whereby lesions of thebrain-stem have been predominantly describedas the underlying disease. Other forms ofabnormal eye movements such as ocular dys-metria, ocular myoclonus, or spasmus nutansshould not be confused with pendular nystagmus.

Diagnostic differentiation between acquiredpendular nystagmus in multiple sclerosis andcongenital pendular nystagmus can be made asfollows: congenital pendular nystagmus isseldom purely sinusoidal; it lacks a verticalcomponent with the rare exception of the auto-somal dominant inherited pendular nystagmus(Dichgans and Kornhuber, 1964) and theamplitude and direction of the nystagmus arebilaterally similar. Acquired pendular nystagmusin multiple sclerosis, in contrast, frequentlyexhibits vertical components, and usually thereare dissimilarities of direction and amplitude.Inversion of optokinetic nystagmus-typical formany cases of congenital nystagmus-neverappears in acquired pendular nystagmus. Finally,oscillopsia and neurological symptoms excepthead tremor are not found in patients withcongenital nystagmus. Acquired pendular nystag-mus in multiple sclerosis resembles more closelythe acquired form of pendular nystagmus ofminers than congenital nystagmus, with theexception of the rare autosomal-dominantlyinherited form which shows several similaritiesto the acquired pendular nystagmus in multiplesclerosis such as vertical components, headtremor, and lack of optokinetic inversion(Dichgans and Kornhuber, 1964).The highly significant correlation between

cerebellar symptoms and pendular nystagmusfound in our patients indicates that pendularnystagmus is a cerebellar symptom. Of the twomain structures within the cerebellum (cortexand nuclei) the cerebellar cortex will not elicitpendular nystagmus either by stimulation (Cohenet al., 1965) or by lesions (Kornhuber, 1968;Aschoff and Cohen, 1972). Therefore, thecerebellar nuclei or their fibre connections withthe brain-stem are obviously the structures thelesions of which may cause pendular nystagmus.For this conclusion there is supporting evidence

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from four sources: (1) from the analogy withpostural tremor, (2) from our necropsy case, (3)from electrical stimulation experiments of thecerebellar nuclei in man, and (4) from the fewcases of pendular nystagmus in patients withpalatal myoclonus due to vascular lesions citedin the literature.

ANALOGY OF PENDULAR NYSTAGMUS AND POS-TURAL TREMOR Acquired pendular nystagmusin multiple sclerosis is present only duringfixation and ceases with eye closure. Thuspendular nystagmus can be interpreted as aholding tremor of the eyes similar to the holdingtremor of the head or of the limbs produced bylesions of the cerebellar nuclei or of their fibreconnections with the brain-stem and thalamus.Kornhuber (1971, 1973) has viewed the main-tenance ofposition as a function of the cerebellarnuclei. He pointed out that the cerebellar nucleiare analogous in function as well as in anatomicalconnections with the vestibular nuclei, thefunction of which is certainly to hold a position.The difference between the cerebellar andvestibular nuclei is that the vestibular nuclei holdthe position of the whole body with respect togravity while the cerebellar nuclei hold theposition of parts of the body with respect tocerebral commands.

NECROPSY FINDINGS IN CASE 2 Widespreaddemyelination in many parts of the nervoussystem is common in multiple sclerosis, andnecropsies, therefore, are not particularly helpfulin localizing those nervous structures whosedestruction leads to pendular nystagmus. How-ever, it is remarkable that, in the necropsy of ourseries, there were extensive lesions in the cere-bellum. Lesions in the cerebellum do not belongto the common localizations of plaques inmultiple sclerosis. Lumsden (1970) reported thatonly 6% of the plaques are localized in thecerebellum.

OSCILLATING EYE MOVEMENTS DURING ELECTRICALSTIMULATION OF CEREBELLAR NUCLEI IN MANThe only report of a pendular nystagmus beingelicited by electrical stimulation comes fromNashold et al. (1969). They observed oscillatingeye movements in man after electrical stimulation

of the medial cerebellar nuclei. The fact thatother authors investigating the destruction ofcerebellar nuclei (Ferrier and Turner, 1894;Sachs and Finscher, 1927; Botterell and Fulton,1938b; Carrea and Mettler, 1947; Krayenbuhland Siegfried, 1969; Guglielmino and Strata,1971) or the destruction of cerebellar peduncles(Ferrier and Turner, 1894; Ferraro and Barrera,1936; Walker and Botterell, 1937; Botterell andFulton, 1938a) did not especially mentionpendular nystagmus is no contradiction to thepositive findings, because these authors did notpay particular attention to changes in eye move-ments nor to different kinds of nystagmus.

PENDULAR NYSTAGMUS AND PALATAL MYOCLONUSAFTER VASCULAR LESIONS Pendular nystagmusclosely resembling pendular nystagmus in mul-tiple sclerosis has been described in patients withpalatal myoclonus (Bender et al., 1952; Nathan-son, 1956; Chokroverty and Barron, 1969).Necropsies performed on these patients showedin all cases lesions in the dentate nucleus or thebrachium conjunctivum, and in addition in theinferior olive (Alajouanine et al., 1935; Guillain,1938; Bender et al., 1952; Nathanson, 1956). Theinferior olive appears to have no effect on theoculomotor system (Wilson and Magoun, 1945).Therefore only the lesions within the dentatenucleus or the brachium conjunctivum canaccount for the pendular nystagmus.

Anatomically, there are known to be connec-tions between the dentate nucleus and theoculomotor nuclei (Carpenter and Strominger,1964), and between the fastigial nucleus and thepontine gaze centre for horizontal eye move-ments (Walberg et al., 1962). Another projectionis known from the dentate and interpositusnuclei onto the supranuclear gaze centre forvertical and rotatory eye movements (Mehleret al., 1958). For a summary of these projectionsbetween cerebellar nuclei and supranuclear gazecentres relevant for eye movements see Aschoff(1973).

Lesions within the cerebellar nuclei or theirefferent projections to the supranuclear centresfor horizontal or vertical eye movements, there-fore, interact with the holding function of thesecentres. Depending on which of the cerebellarnuclei is affected by the lesion, a vertical,horizontal, or elliptical pendular nystagmus is

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produced. The direct connection from deep cere-bellar to oculomotor nuclei may be responsiblefor some asymmetry of pendular nystagmusbetween the two eyes. Oscillopsia, finally, is theimmediate consequence of oscillatory eyemovements.

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