Journal of Neurology, Neurosurgery, and Psychiatry 1982;45:998-1004

Effects of fixation and optokinetic stimulationon vestibulo-ocular reflex suppressionBR CHAMBERS, MA GRESTY

From the MRC Neuro-Otology Unit, Institute ofNeurology, National Hospital, Queen Square, London

SUMMARY Suppression of the vestibulo-ocular reflex was assessed in normal subjects and patientswith neurological disorders to determine the relative effects on suppression of a single fixationtarget and an optokinetic field. Subjects were rotated sinusoidally in yaw at varying frequencies ofup to 0 5 Hz whilst seated in a Barany chair. A comparison was made between eye movements indarkness, those produced during fixation on a central target mounted to the chair, and eye

movements during fixation on the target plus an "earth-fixed" or "chair-fixed" visual background.Presentation of a background produced only minimal effects on the suppression of the vestibulo-ocular reflex in normal subjects. In patients with impairment of fixation suppression, suppressionof the vestibulo-ocular reflex was not improved after presentation of either form of optokineticfield. The results demonstrate that central fixation is the predominant requirement for suppressionof the vestibulo-ocular reflex. This correlates closely with the ability to pursue. Although theoptokinetic reflex generates following eye movements similar to pursuit, it cannot be used tomediate suppression of the vestibulo-ocular reflex in the absence of an intact pursuit system. Thefindings strengthen the view that the optokinetic reflex evolved to act in synergy with the vestibulo-ocular reflex in generating compensatory eye movements.

The vestibulo-ocular reflex generates eye movementswhich compensate for angular displacement of thehead and maintain the visual axes "on target". If oneobserves a moving target by turning the head, so thatthe target remains stationary relative to the head,then the eye movements generated by the vestibulo-ocular reflex are inappropriate and must besuppressed. This is termed vestibulo-ocular reflexsuppression, and it is usually measured bycomparison of induced nystagmus before and afterpresentation of a central fixation target (fixationsuppression). Barnes, Benson and Prior have shownin normal humans, that when suppression of thevestibulo-ocular reflex and pursuit are compared,similar frequency response curves are obtained, witha fall off in performance at frequencies higher than 1Hz. I This led to the hypothesis that suppression of thevestibulo-ocular reflex depends directly oninformation derived from the smooth pursuit system.This was supported by the clinical observation that inpatients with impaired smooth pursuit, suppressionof the vestibulo-ocular reflex was abnonnal.23

Address for reprint requests: Dr BR Chambers, MRC Neuro-Otology Unit, Institute of Neurology, National Hospital, QueenSquare, London WC1N 3BG, UK

Quantitative analysis "has shown a dissociationbetween pursuit and suppression of the vestibulo-ocular reflex in some patients with neurologicaldisorders.4 This is most likely explained by a selectiveinterruption of visual pathways mediating pursuit orsuppression distal to the lower level of commonfunctional and anatomical organisation.The optokinetic reflex has probably evolved to act

in synergy with the vestibulo-ocular reflex.56 At lowfrequencies of head rotation (< 1Hz), the gain of thevestibulo-ocular reflex is less than unity and theoptokinetic reflex responds to slip of the image of thevisual-world on the retina and helps maintain thevisual axes "on target", as well as providingsubjective information about rotation of the head inspace.7 Because the optokinetic reflex generatesfollowing eye movements similar to those of thepursuit reflex, the question arises as to whether or notthe signals relating to the optokinetic reflex can be.used to suppress the vestibulo-ocular reflex in asimilar way to the pursuit reflex. If that were the case,then the optokinetic reflex would have anantagonistic role with respect to vestibular function,in contrast to the established synergistic relationship.The problem is difficult to resolve in normal subjectsbecause the pursuit and the optokinetic reflex have

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Effects offixation and optokinetic stimulation on vestibulo-ocular reflex suppression

Fig 1 The chair-mounted visual perimeter which when illuminated provided an optokinetic field"sympathetic" to a centralfixation target attached to the perimeter.

similar dynamic characteristics.8 However, in Patients and methodspatients with neurological disorders, it is common to The following investigations were performed on normalfind inpairment of pursuit and fixation suppression, subjects and neurological patients. Throughout all the testswith relatively intact optokinetic nystagmnus. In these described, eye movements and nystagmus were recordedpeople the contribution of the optokinetic reflex to using conventional DC coupled electro-oculography.suppression of the vestibulo-ocular reflex, in the Smooth pursuit in the horizontal plane was measured usingabsence of intact pursuit, may be more readily a moving laser target projected onto a tangent screen twostudied. metres from the subject, by means of a mirror mounted on a

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Chambers, Gresty

Totol darkness Fixation Fixation+ background I I

W~~~~~~~~t Room illumination

Earth-fixed Rbackground II\RScreen illuminan200

/\ A A ~~~~~~~~~~~~~~Scrnillumination _L

Chair-f xedbackground

Fig 2 Raw electro-oculogram records from a normal subject illustrating suppression of vestibularresponses when the subject was presented with afixation target and then background. The upper trace wasobtained when the background was provided by room illumination, and the lower trace when using thechair-mounted visualperimeter. Frequency ofchair oscillation 0 4 Hz. Peak velocity 80 degls.

scanning motor. The target subtended an angle of less thanone degree. Target motion was sinusoidal with a peakdisplacement of 20 degrees and the frequency was variedthrough the range of normal human pursuit (0-1 Hz).Optokinetic nystagmus was elicited using an internallyilluminated motorised striped drum completely enclosingthe subject, which was rotated at velocities ofup to 40 deg/s.Vestibulo-ocular reflex function was studied by measuringresponses to sinusoidal rotation and impulsive angularacceleration and deceleration. Three tests of suppression ofthe vestibulo-ocular reflex were employed to assess fixationsuppression alone and in combination with either an earth-fixed or a chair-fixed optokinetic field. Subjects were seatedand comfortably restrained in a Barany chair driven by a

17- 8 Nm torque motor. A fixation light of the same intensityand colour as the laser pursuit target, and subtending a

similar visual angle, was mounted to the chair in front of thesubject at a distance of one metre. The subject was rotatedsinusoidally in darkness for a few seconds, and thenpresented with the fixation target alone. A few seconds latera stationary (that is earth-fixed) background was presentedby illumination of the room, which provided contrastingvelocity information. The procedure was then repeated withthe subject enclosed within a chair-mounted visualperimeter, such that the entire visual environment movedwith the subject ("sympathetic" field). The perimeter was a

semi-circular striped screen of one metre radius, covered bya roof (fig 1). It was internally illuminated and the subjectcould be presented with a fixation light alone or incombination with the illuminated screen. Frequencies ofoscillation were varied through the lower end of thefrequency response range of the vestibulo-ocular reflex(< 0 5 Hz). When normal subjects were tested the peakvelocity of rotation was increased to a level exceeding thethreshold at which suppression ofthe vestibulo-ocular reflexwas no longer complete, whilst for the patients a peakvelocity of40 degrees/s always exceeded this threshold. Theadvantage of these methods for testing suppression of thevestibulo-ocular reflex was that the conditions could bechanged instantaneously whilst the subject was being

rotated and comparisons were not influenced by minute tominute variation in vestibular peformance which is commonif patients are drowsy or fatigued. In addition observationscould be based on direct inspection of raw electro-oculogram records, eliminating the need for computerassisted quantitative measurements.The protocol described above was performed on 10

normal control subjects and on 20 patients with neurologicaldisorders. The neurological diagnoses included multiplesclerosis, idiopathic cerebellar degeneration, olivoponto-cerebellar degeneration, spinocerebellar degeneration,brain stem glioma, Parkinson's disease and cerebralinfarction (both forebrain and hindbrain). These cases wereselected on the basis of a clinically apparent abnormality ofsuppression of the vestibulo-ocular reflex, using the bedsidetest described by Halmagyi and Gresty.3 The followingcases have been selected because they illustrate some of theabnormalities of pursuit and optokinetic nystagmusencountered in patients with neurological disorders. Eachpatient showed gross abnormalities of optokineticnystagmus in response to.movement of a small hand heldstriped drum but in most cases the responses to full-fieldstimulation illustrated below were considerably improved.Case I Brain stem and cerebellar infarction. A 68-year-oldwoman developed cerebellar ataxia of presumed vascularorigin following general anaesthesia for nephrolithotomy.Neurological signs included a supranuclear palsy of upwardgaze, horizontal gaze nystagmus, central positionalnystagmus, limb incoordination and gait ataxia. Onattempted pursuit there were no recognisable slowfollowing movements and full-field optokinetic stimulationfailed to elicit optokinetic nystagmus (fig 3a, b).Case 2 Brain stem glioma. A 24-year-old man presentedwith a subacute onset of tinnitis, unsteadiness of gait,nausea and vomiting, diplopia and hemisensorydisturbance. On examination there was 1st degreenystagmus to the right, a left 6th nerve palsy, a left lowermotor neuron facial weakness, left sided deafness, and aright sided sensory-motor deficit involving face, arm andleg, with marked right sided ataxia. The deficit was

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- -- Effects offixation and optokinetic stimulation on vestibulo-ocular reflex suppression

(§) Pursuit

2s(@ OKN

I Drum R 30°

t Drum L

(,) Pursuit

[400

OKN

Drum R40t/s Drum L L00/s5 I~~~~~~~~~~~~~~~~~~~~~IJr-~ R

I 4002s

VORS

FL IFL+BG Room

f F~~~~~~~~~'Fig 3 Case 1. Brain stem and cerebellar infarction. (a)attempted pursuit (sinusoidal target motion, frequency 0-2Hz, peak to peak displacement 40 deg). (b) responses tofull-field optokinetic stimulation (constant velocity 30 degls).(c) attempted suppression ofthe vestibulo-ocular reflex whenpresented with fixation target alone and with optokineticfields (frequency 0 4 Hz, peak velocity 40 degls).

progressive and he later developed the "one and a halfsyndrome". A CT scan suggested the presence of a pontineglioma which was subsequently confirmed by biopsy of thelesion. When examined soon after the initial presentation,horizontal pursuit was saccadic in both directions (fig 4a).The optokinetic nystagmus gain was 0 4 with the drumrotating at 40 deg/s, and with the drum moving to the rightthe response was irregular and poorly sustained (fig 4b).Case 3 Idiopathic cerebellar degeneration. A 23-year-old-woman developed a slowly progressive degenerativecondition with oscillopsia, downbeat nystagmus,dysarthria, incoordination and gait ataxia. There was nofamily history. Structural anomalies at the level of thecraniocervical junction were excluded by negativecomputerised tomography and myelography. Attemptedfollowing produced saccadic pursuit movements (fig 5a) andfull-field optokinetic stimulation produced a poor initialresponse followed by a slow buildup of optokineticnystagmus which reached a peak after about 20 seconds (fig5b).Case 4 Right parietal infarction. A 36-year-old womanteacher was admitted after collapsing in the playground ofthe school. She had regained consciousness and was awareof a right frontal headache and left sided weakness. Onexamination there was a mild left hemiparesis andpronounced visual and sensory inattention. She becamedrowsy and a CT scan demonstrated infarction within the

FLVORS

FL-BG[Xrk 4 ~~~~~~~~Room

4fi+ Screen

2s

Fig 4 Case 2. Brain stem glioma. (a) attempted pursuit (0-2Hz, 40 deg). (b) optokinetic nystagmus generated by full-field optokinetic stimulation (40 degls). (c) attemptedsuppression of the vestibulo-ocular reflex when presentedwith fixation target alone and with optokineticfields (0- 4 Hz,40 degls).

territory of the middle cerebral artery with cerebraloedema. A right carotid angiogram and an echocardiographwere normal. When examined later she was fully alert andher motor deficit had recovered although inattentionpersisted. Pursuit movements were broken up in bothdirections but particularly to the right (fig 6a). Optokineticnystagmus induced by drum rotation to the left was normalbut to the right the response was marginally reduced invelocity (fig 6b).

Results

A Normal subjectsRaw electro-oculogram records from a typical controlsubject (fig 2) illustrate the normal responses for thetests of suppression of the vestibulo-ocular reflex.Sinusoidal rotation in total darkness (0 4 Hz, peakvelocity 80 deg/s) induced compensatory eyemovements interspersed with nystagmus quickphases. With fixation the vestibulo-ocular reflex waslargely suppressed but a low amplitude nystagmus(approximately 2 degrees) was still evident.Presentation of room illumination, which providedcontrasting visual information, produced a barelydiscernible change in the nystagmus, which was if

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Chambers, Gresty

Pursuit

! R

400

L

0OKN

tDrum R 400/s

To

Fig 5 Case 3. Idiopathic cerebellardegeneration. (a) attempted pursuit (0O 2 Hz, 40deg). (b) optokinetic nystagmus generated byfull-field optokinetic stimulation (40 degls,constant velocity). Attempted suppression ofthevestibulo-ocular reflex not illustrated.

Pursuit

R

400

-LOKN

( Drum R 25°/s i Duum L 25°/s

VORS

Dark FL FL+BG

I IX Room

I _Screen

Fig 6 Case 4. Right parietal infarction. (a) attemptedpursuit 2 Hz, 40 deg). (b) optokinetic nystagmus generatedby full-field optokinetic stimulation (25 degls). (c) attemptedsuppression of the vestibulo-ocular reflex when presentedwith fixation target alone and with optokineticfields (0-4 Hz,40 degls).

anything slightly better suppressed. Similarly,presentation of a "sympathetic" visual background,moving with the patient, had only a marginal effect onsuppression, but in contrast the effect was adverse.These differences were consistent, but not aspronounced, for the other normal subjects. Althoughdiscernible on raw electro-oculogram records, theeffects were not quantifiable because of the lowamplitude of the nystagmus.

B PatientsThe raw electro-oculogram records obtained fromcase 1 during attempted suppression of the vestibulo-ocular reflex (fig 3c) show that there was no fixationsuppression of vestibular nystagmus, and noimprovement of suppression of the vestibulo-ocularreflex after presentation of either form of optokineticfield. The records from case 2 (fig 4c) demonstratethat the patient had some fixation suppression,however nystagmus of around five degrees inamplitude and modulation of eye position were stillevident. There was no convincing change in thenystagmus after presentation of either optokineticfield. Case 3 was able to centre the eyes whenpresented with a fixation target but unable tosuppress nystagmus with or without illumination ofthe optokinetic fields (not illustrated), even when thefrequency of oscillation was reduced to 0 03 Hz toallow for the time constant 'of the development ofoptokinetic nystagmus. The records of suppression ofthe vestibulo-ocular reflex from case 4 showedprecisely the same results as for case 2 (fig 6c).

Discussion

The results of this study indicate that the optokineticreflex has no significant physiological role in the

0)

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Effects offixation and optokinetic stimulation on vestibulo-ocular reflex suppression

suppression of nystagmus induced by oscillatoryrotational stimuli. In normal subjects, suppression ofthe vestibulo-ocular reflex was slightly enhancedwhen the fixation target was seen to move against a

stationary background. However when the back-ground moved with the target suppression of thevestibulo-ocular reflex was slightly impaired. Theseinfluences were trivial. Guedry et al9 made similarobservations in normal subjects and referred tounpublished work by Benson and Cline. Thedifferences are probably accounted for by an effect onpursuit. It would seem that movement of a targetacross a stationary background permits a moreaccurate assessment of the target's relative velocity;and that this information facilitates the pursuitreflex.'0 The fact that the two forms of optokineticfield had opposite influences in normal subjectsargues against a direct effect on the suppressionmechanism.

In some patients, in whom suppression of thevestibulo-ocular reflex and pursuit were only mildlyimpaired, trivial effects similar to those seen innormals were observed after presentation of theoptokinetic fields. However, in none of the patientswas the velocity threshold at which suppression failedmodified by more than a few degrees/s. This was ofnofunctional benefit in relation to the degree ofimpairment of suppression of the vestibulo-ocularreflex. Many of the patients had some capacity tosuppress. It is probable that amongst these there werecases in whom the mechanism mediating suppressionof the vestibulo-ocular reflex was intact at the level ofthe flocculus (for example case 5). In general thedegree of impairment of fixation suppression was

proportional to the pursuit deficit, and could beattributed to a lack of input into the suppression ofthe vestibulo-ocular reflex mechanism of signalsconcerning relative target motion. In no case was itdemonstrated that optokinetic information gainedaccess to this mechanism.

In humans "passive" optokinetic nystagmus,"induced when the subject stares at the stimulus fieldrather than following a particular feature, is probablyderived from two components. The dominantcomponent has a time constant of the order of200 ms,is dependent on cortical connections and has beenreferred to as a form of "involuntary", pursuit. Incertain disorders this is deficient and optokineticstimulation produces a slowly developing responsewith a time constant of 4 to 5 seconds (for examplecase 3), which is identical to the phylogeneticallyolder form of optokinetic nystagmus seen in loweranimals. 2 With case 3, even when the frequency ofoscillation was reduced sufficiently to allow for thetime constant of the development of this "primitive"form of optokinetic nystagmus, provision of an

optokinetic field did not improve suppression of thevestibulo-ocular reflex. The failure of optokineticstimulation to modify suppression in the presence offull optokinetic nystagmus (in one direction), in apatient with a bilateral deficit of suppression of thevestibulo-ocular reflex (case 4), is the strongestevidence that there is no mechanism by whichoptokinetic related signals may be used forsuppression of the vestibulo-ocular reflex.The results of this study reinforce the view that the

principal function of the optokinetic reflex is to act insynergy with the vestibulo-ocular reflex in generatingcompensatory eye movements during head rotations,since it does not appear to be antagonistic to thevestibulo-ocular reflex. As a corollary, the resultsprovide further evidence that the pursuit. reflex,which is important for suppression of the vestibulo-ocular reflex, and the optokinetic reflexes (passiveform) are physiologically distinct, even though bothare capable of generating smooth eye movements.

Dr. BR Chambers is supported by an AlexanderPiggott Wernher Training Fellowship.

References

'Barnes GR, Benson AJ, Prior ARJ. Visual-vestibularinteraction in the control of eye movement. AviatSpace Environ Med 1978;49:557-64.

2 Dichgans J, Von Reutern GM, Rommelt U. Impairedsuppression of vestibular nystagmus by fixation incerebellar and noncerebellar patients. Arch PsychiatrNervenkr 1978;226: 183-99.

Halmagyi GM, Gresty MA. Clinical signs of visual-vestibular interaction. J Neurol Neurosurg Psychiatry1979;42:934-9.

4 Chambers BR, Gresty, MA. The relationship betweendisordered pursuit and vestibulo-ocular reflexsuppression. J Neurol Neurosurg Psychiatry (in press).

Brandt T, Dichgans J, Koenig E. Differential effects ofcentral versus peripheral vision on egocentric andexocentric motion perception. Exp Brain Res1973;16:476-91.

6 Koenig E, Allum JHJ, Dichgans J. Visual-vestibularinteraction upon nystagmus slow phase velocity inman. Acta Otolaryngol 1978;85:397-410.

Dichgans J, Schmidt CL, Graf W. Visual input improvesthe speedometer function of the vestibular nuclei in thegoldfish. Exp Brain Res 1973;18:319-22.

8 Trinker D, Sieber J, Bartual J. Schwingungsanalyse dervestibulaer, optokinetisch und durch elektrischeReizungausgelosten Augenbewegungen beimMenschen. 1 Mitteilung: Stetige Augenbewegungen:Frequenzgange und Ortskurven. Kybernetik1961;1:21-288.

9 Guedry FE, Lentz JM, Jell RM. Visual-vestibularinteractions: 1. influence of peripheral vision onsuppression of the vestibulo-ocular reflex and visualacuity. Aviat Space Environ Med 1979;50:205-11.

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Hood JD. Observations upon the role of the peripheralretina in the execution of eye movements. ORL1975;37:65-73.

" Rademaker GGJ, Ter Braak JWG. On the centralme;hanisms ofsome optic reactions. Brain 1948;71:48-

Chambers, Gresty

76.12 Yee RD, Baloh RW, Honrubia V, Lau CGY, Jenkins

HA. Slow buildup of optokinetic nystagmus associatedwith downbeat nystagmus. Invest Ophthalmol Vis Sci1979;18:622-9.

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reflex suppression.stimulation on vestibulo-ocular Effects of fixation and optokinetic

B R Chambers and M A Gresty

doi: 10.1136/jnnp.45.11.9981982 45: 998-1004 J Neurol Neurosurg Psychiatry 

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