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Investigative Ophthalmology & Visual Science, Vol. 30, No. 1, January 1989Copyright © Association for Research in Vision and Ophthalmology

Adaptation to Telescopic Spectacles:Vestibulo-ocular Reflex Plasticity

Joseph L. Demer, Franklin I. Porter, Jefim Goldberg, Herman A. Jenkins, and Kim Schmidt

The vestibulo-ocular reflex (VOR) is a mechanism for the production of rapid compensatory eyemovements during head movements. To investigate the adaptation of this reflex to spectacle magni-fiers, the effect on the VOR of a brief period of wearing telescopic spectacles during head rotation wasstudied in normal subjects. VOR gain, as measured in darkness, was defined to be the ratio ofcompensatory slow phase eye velocity to head velocity. Initial VOR gain as measured for vertical axissinusoidal head rotation at 0.1 Hz, amplitude 60°/sec, was about 0.7. After 15 min adaptation bysinusoidal rotation during the viewing of a remote video display through X2, X4, or X6 binoculartelescopic spectacles, 47-70% of subjects exhibited significant VOR gain increases of 7-46%. Theseincreases were measured with occlusion of the unmagnified visual field peripheral to the telescopesduring adaptation. There was considerable interindividual variability in adaptation to telescopic spec-tacles. Telescopic spectacle power had little or no effect on the amount of VOR change after adapta-tion, although all telescope powers produced a greater VOR gain change than did adaptation withouttelescopes. Testing of VOR gain at multiple frequencies indicated that adaptation to telescopic spec-tacles by rotation at a single sinusoidal frequency induces VOR gain changes across a broad spectrumof frequencies of head rotation. When the unmagnified peripheral visual field was unobstructed duringadaptation, VOR gain increases were significantly less than when the unmagnified peripheral visualfield was occluded, and were similar to those observed during adaptation without the wearing oftelescopic spectacles at all. VOR gain adaptation was associated with amelioration of symptoms ofoscillopsia and motion discomfort initially experienced by about 20% of subjects wearing telescopicspectacles. Invest Ophthalmol Vis Sri 30:159-170,1989

Retinal image motion of only a few degrees persecond degrades visual acuity,1 and motion of15-25°/sec reduces acuity almost five-fold.2'3 Sincesignificant head movements are ubiquitous, retinalimage slip would constantly degrade visual acuitywere it not for compensatory eye-in-head move-ments.4 Two major inputs induce eye movements tostabilize retinal images. Head acceleration, trans-duced by the vestibular apparatus, produces compen-satory eye movements called the vestibulo-ocular re-flex (VOR). Visually perceived motion is also trackedin cooperation with the VOR to produce visual-ves-tibular interaction (WI) .

The VOR produces eye movements within 12msec of head movement,5 much faster than the 120msec latency of purely visual compensatory move-ments.67 Consequently, the VOR must act in a pre-programmed manner, making compensatory eyemovements before visual feedback is available. The

From the Cullen Eye Institute and Clayton Neurotology Labora-tory, Baylor College of Medicine, Houston, Texas.

Supported by National Institutes of Health grant EY-06394 andthe Clayton Foundation for Research.

Submitted for publication: November 16,1987; accepted August1, 1988.

Reprint requests: Joseph L. Demer, MD, PhD, Jules Stein EyeInstitute, University of California at Los Angeles, 10833 Le ConteAvenue, Los Angeles, CA 90024.

VOR accomplishes this correctly over a wide range ofhead velocities, functioning even in complete dark-ness. The gain of the VOR is defined to be the ratio ofslow phase eye velocity to head velocity.

Ideally, VOR gain would be 1.0 to perfectly stabi-lize retinal images, since this means that a given headvelocity evokes an equal eye velocity in the oppositedirection. In fact, measured VOR gain is usuallysomewhat lower than this,8"10 but in the light theVOR is enhanced by visual-vestibular interaction toincrease the gain to 1.0.10 The visually enhancedVOR is called the visual-vestibulo-ocular reflex(WOR). Although the visual enhancement of VORgain is useful, the visual system has only a limitedcapability to instantaneously influence the gain ofcompensatory eye movements. Because of gradualchanges in the geometry of the orbit and strength ofextra-ocular muscles throughout lifetime, the brainmust recalibrate its normal connections to hold VORgain close to 1.0. The brain apparently uses cumula-tive retinal slip or efference copy of corrective visualpursuit commands, correlated with head movement,to parametrically adjust VOR gain." The long-term adjustment of VOR gain is called VOR gainplasticity.

The plastic nature the VOR has been extensivelystudied in animals made to wear spectacles thatchange the relationship between head movement and

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160 INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / January 1989 Vol. 30

retinal image slip. The wearing of reversing prismspectacles requires a decrease in VOR gain to -1.0 tostabilize images, implying a reversal in the directionof compensatory eye movements. Telescopic specta-cles require that VOR gain increase to equal thepower of the telescopes.10 Plastic adaptation to bothsituations has been demonstrated in numerous spe-cies.8912"15 The phenomenon of VOR gain plasticityis so general and easily demonstrable that it is used asa model of motor learning.16 While all the neuronalcorrelates of VOR gain plasticity are not known, le-sions of the vestibulocerebellum15 and inferior oli-vary nucleus17 have been found to abolish VOR gainplasticity, as has catecholamine depletion producedby infusion of 6-hydroxydopamine.1819

Gonshor and Melvill Jones demonstrated plasticreduction of VOR gain in humans induced by mirrorreversal of vision during head rotation.20 These in-vestigators also demonstrated that wearing of Doveprism reversing spectacles for many days can reducehuman VOR gain by 75%.21 Prism-induced VORgain reductions have been used in the clinical evalua-tion of cerebellar dysfunction in patients,22'23 sincethe wearing of reversing spectacles for only 1 hr dur-ing head rotation decreases VOR gain by a mean of36%.24 Sekine has demonstrated that human VORgain plasticity induced by reversing prisms does notdecline with age even into the seventies.25 The rota-tional magnification of ordinary refractive spectaclelenses has also been found to induce plastic changesin VOR gain.2627

Plastic adaptation of human VOR gain to tele-scopic spectacles has received little attention, despitethe widespread use of these devices as visual aids inthe rehabilitation of the visually handicapped.28

Gauthier and Robinson reported that a single subjectwho wore X2.1 telescopic spectacles for 5 daysachieved a 70% increase in VOR gain.29 Istl-Lentz etal studied the adaptation of eight subjects to thewearing of X2 telescopic spectacles for 5 days, dem-onstrating a 100% VOR gain increase when tested ata frequency of head rotation of 3 Hz, and a 50%increase when tested at 0.5 Hz.30 Aside from prelimi-nary reports from our laboratory,1031 we are notaware of any other detailed reports of human VORgain plasticity with telescopic spectacles.

Upon the initial wearing of telescopic spectacles,subjects invariably experience a mismatch betweenactual VOR gain and the gain demanded by spectaclemagnification.29 Inappropriate VOR gain induces thesensation of an unstable visual world.32 The resultantvisual-vestibular conflict typically causes ataxia, nau-sea and oscillopsia, all of which disappear when VORgain approaches spectacle magnification.10'29'30'32

Thus, human VOR gain adaptation to telescopic

spectacles is an important consideration in their use.The present research was undertaken to investigatethis adaptation in a representative group of normalsubjects as a prelude to a contemplated study of theuse of telescopic spectacles by the visually impaired.

Materials and Methods

This study was approved by the Institutional Re-view Board for Human Research at Baylor College ofMedicine. All participating subjects gave written in-formed consent after the nature of the procedures hadbeen explained fully. A total of 48 normal volunteerswas studied; three of these were unable to completethe protocol due to symptoms of motion sickness andwere excluded from further analysis. Of the subjectscompleting the protocol, 18 were males and 27 werefemales. Ages ranged from 16 to 72 years, with amean of 38 ± 16 (mean ± standard deviation, SD)years. All subjects underwent an eye examination toverify that they were visually normal. Bilateral func-tion of the peripheral vestibular apparatus was veri-fied with cool (30°C) and warm (42°C) water caloricirrigations of each external auditory canal.

Binocular, focusable telescopic spectacles wereemployed. The visual axes were set to converge at aviewing distance of 4 m. Telescopes were nominallyof X2, X4, and X6 powers as specified by their manu-facturers, although actual magnifications differedslightly. The X2 nominal telescopes were of Galileanconfiguration and had a total visual field diameter of16.8°. Galilean telescopes consist of a convex and aconcave lens, and produce an upright image. Usingan optical bench, the actual magnification at a dis-tance of 4 m was found to be X2.1 when focused foran emmetropic eye. The X4 nominal telescopes wereof astronomical configuration and had a total visualfield diameter of 10.3° (nominal 12.5°); measuredmagnification at a distance of 4 m was X4.1. Astro-nomical telescopes contain two convex lenses andordinarily produce an inverted image, but those usedas telescopic spectacles incorporate image erectingprisms. The X6 nominal telescopes were of astro-nomical configuration and had a total visual fielddiameter of 7.5° (nominal 10°); measured magnifi-cation at a distance of 4 m was X6.1. Data were col-lected both with occlusion of the peripheral visualfield outside the telescope eyepieces (occluded config-uration), and without obstruction of this unmagni-fied visual field (nonoccluded configuration).

Subjects were seated in a chair mounted on a verti-cal axis servomotor. Subjects' heads were stabilizedwith a headband against a padded headrest attachedto the chair. A PDP 11/73 minicomputer generatedthe command signal to the servomotor and digitized


No. 1 VOR WITH TELESCOPIC SPECTACLES / Demer er QI 161

the chair velocity signal from a tachometer attachedto the servomotor shaft. In this manner, subjectscould be rotated sinusoidally at various frequencies,or sums of frequencies, and at various amplitudes.

Horizontal and vertical eye position were simulta-neously recorded by bitemporal DC coupled electro-oculography (EOG) using silver-silver chloride elec-trodes. The EOG signal was filtered with a four-pole,low-pass filter having a bandwidth of 0-40 Hz. Thesignal was then digitally sampled at 200 Hz beforebeing stored for subsequent analysis by the minicom-puter. Vertical EOG measurements were analyzedonly qualitatively for the presence of blink artifacts.

Calibration of the horizontal EOG signal wasachieved in a semiautomated manner by measuringthe digitized change in EOG potential for saccades tolighted targets from center to 15° left, and center to15° right, made with the telescopic spectacles rotatedupwards out of the visual axis. An EOG sensitivityfactor was calculated for each set of saccades. Beforeand after each rotational stimulus, two to five calibra-tion sets were performed and the sensitivity factorswere averaged. Calibration factors were required toagree to within 5% of one another for any given VORgain measurement. The experimenter monitoredsubject performance on calibration trials by means ofa rectilinear polygraph display, and excluded trials inwhich target fixation was not maintained or wasgrossly inaccurate due to anticipation of target shift.In order to avoid instability in the corneoretinal po-tential, subjects were allowed several minutes toadapt to altered lighting conditions. Testing was de-layed if systematic changes in EOG sensitivity factorsindicated insufficient adaptation to darkness.

Calculations of VOR gain were automated to avoidbias from human intervention. Eye velocity wascomputed at a resolution of 50 values per second bysmoothing and differentiation of the eye position sig-nal. Slow phase eye velocity was obtained in an itera-tive process by excluding from analysis all velocitysamples exceeding velocity windows related to thestimulus head velocity; these very high and/or oppo-sitely directed velocity samples represent quickphases or saccades. Ordinarily, about 70% of sampledvelocity points were included as slow phases. Eachtrial consisted of four to seven cycles of sinusoidalhead rotation at the single frequency, or at the funda-mental frequency for sum of sines testing. The re-sponse to the first cycle was always discarded since itincluded transient components that are not represen-tative of steady state VOR performance. For eachsingle cycle of head rotation, a sinusoidal curve wasfit to the sampled slow phase eye velocity values usingthe least squares method. For responses to sums ofsines, the amplitudes of each frequency component

were determined using least squares techniques. Theamplitudes of each of the three to six cycles of theresponse were used to compute a mean and standarddeviation for the overall response. Since poor alert-ness33 and muscle artifact tend to decrease the ampli-tude of the VOR response, and since there are noartifacts known to increase amplitude, it was as-sumed that cycles containing particularly low ampli-tude responses were contaminated by poor alertnessor artifacts. For any trial, any sinusoidal cycle havingan amplitude less than 130% of the standard devia-tion below the mean amplitude for that trial was ex-cluded from analysis. This rule will unnecessarily ex-clude only 10% of normally distributed values thatare not contaminated by artifact. The data censoringrule was applied repeatedly to the remaining ampli-tude values until it produced no further data rejec-tion. VOR gain was obtained by dividing eye velocityamplitude values by head velocity amplitude. Thisdata censoring tends to produce slightly higher valuesof gain than does inclusion of all amplitude values,but provides an objective method of removing arti-facts that would ordinarily be discarded manuallyusing poorly defined and arbitrary criteria. The effectof the data censoring rule on the statistical signifi-cance of gain changes after adaptation was evaluatedin 34 subjects tested using X4 telescopic spectacles, aswill be discussed below. Data censoring permitteddemonstration of significant (P < 0.05) gain changesin all of those subjects in whom such changes couldbe demonstrated without such censoring, and in anadditional approximately 10% of subjects in whomthe variability prior to censoring made demonstra-tion of significance impossible.

VOR gain was measured in complete darkness. ForVOR gain measurement using a single frequency ofsinusoidal head rotation, the amplitude was usuallyset to 60°/sec. For VOR gain measurements madesimultaneously at multiple sinusoidal frequencies, acomplicated head velocity stimulus command wasgenerated by the computer using a fundamental fre-quency of 0.025 Hz and four higher, odd-numberedinteger harmonics having no common sums and dif-ferences. The amplitude of each component fre-quency in the sum of sines was 15-20°/sec. This pat-tern of rotation cannot be cognitively predicted bythe subject. Subjects were instructed to look straightahead and to attempt to see anything that might bevisible there. Nothing, of course, was visible in thetotal darkness. This corresponds to an instruction toview earth-fixed targets. Alertness was maintainedusing mental arithmetic and alphabetical listing tasksmonitored by the experimenter via an intercom.

After initial measurements, subjects underwent a15 min period of adaptation training during which



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Fig. 1. Adaptation to tele-scopic spectacles increasesVOR gain as measuredusing single frequency orsum of sines rotations.Points are sampled slowphase VOR eye velocitiesduring single frequency si-nusoidal head rotation at0.1 Hz (top) and sum ofsines head rotation (bot-tom) for a single subject ini-tially (left) and after 15 minadaptation to X2 telescopicspectacles (right). Stimulushead velocity waveforms arenot shown. The smoothcurves represent best sinu-soids or sums of sinusoids fitto the data points by theleast squares method. Gainvalues are given as means± SDs for the six sinusoidalcycles at 0.1 Hz measuredbefore and after adaptation.

they viewed using telescopic spectacles a video moni-tor 4 m away while undergoing sinusoidal rotation.The content of the display consisted of entertainmentprogramming, with an audio channel to maintainsubject alertness. This period of combined visual-ves-tibular experience was designed to train subjects tostabilize gaze against head movement while wearingtelescopic spectacles. The unmagnined visual fieldperipheral to the telescopes was generally occludedduring adaptation, except for one series of experi-ments described below. Various frequencies and ve-locity amplitudes of head rotation were tried in orderto determine the most practical combination for in-ducing short-term VOR gain plasticity. The 0.2 Hzfrequency and 20°/sec amplitude combination wasfound to be the most practical, and this combinationwas employed in the study of most of the subjectpopulation. After the adaptation period, VOR mea-surements were repeated.

Statistical comparisons between groups were madeusing the one-tailed student t-test. Unless stated oth-erwise, a 0.05 level of significance was employed.Linear regression analyses, including computation ofPearson correlation coefficients, were performed on apersonal computer using the SYSTAT statisticalpackage.34

Results

Initial VOR Performance

VOR gain was defined to be the ratio of the ampli-tude of compensatory slow phase eye velocity to head

velocity. Initial VOR gain was measured using sev-eral types of rotational stimuli. Typical eye velocitydata obtained during head rotation in the dark areseen in Figure 1. The upper tracings in this figureillustrate responses to single frequency sinusoidalstimulation. For 34 subjects tested at the frequency of0.1 Hz, amplitude 60°/sec, gain was 0.67 ±0 .11(mean ± SD).

Seven subjects underwent VOR testing using a sumof sines rotational stimulus with a fundamental fre-quency of 0.025 Hz and including the second, fifth,ninth and seventeenth harmonics of the fundamen-tal. The amplitude of each component frequency inthe sum of sines was 15-3O°/sec. The eye velocityresponse to this stimulus is seen in the lower tracingsof Figure 1. These seven subjects were also tested at0.1 and 0.2 Hz, amplitude 60°/sec. Two of these sub-jects were also tested at 0.8 Hz, amplitude 30°/sec.Measurements of VOR gain at multiple frequenciesfor each of these subjects permitted the use of a Bodefrequency response plot to represent VOR perfor-mance, as seen in Figure 2. VOR gains typically in-creased with frequency, and occasionally exceeded1.0 at high frequencies (Fig. 2B). Gain values mea-sured using single frequency sinusoidal rotation dif-fered slightly from those measured using sum of sinesrotation, as illustrated in Figure 2B, which includesboth types of measurements. For single frequencytesting, cycle to cycle variability in the amplitude ofthe VOR response was greater at high frequenciesthan lower ones, although this trend was not evidentin sum of sines data (Fig. 2).


No. 1 VOR WITH TELESCOPIC SPECTACLES / Demer er ol 163

Fig. 2. Telescopic specta-cle adaptation increasesVOR gain across the fre-quency spectrum. VORgain is plotted as a functionof frequency of head rota-tion for two subjects, mea-sured using sum of sines ro-tation. Gains are shown be-fore and after 15 minadaptation to X2 telescopicspectacles, with an ampli-tude of head rotation of20°/sec. (A) Adaptation at0.1 Hz. (B) Adaptation at0.2 Hz. Gain values at 0.1,0.2, and 0.8 Hz (markedwith asterisks) measured forsingle frequency sinusoidalrotation, while remaininggains measured using sumof sines rotation. (C) Adap-tation at 0.4 Hz. (D) Adap-tation at 1.0 Hz.

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Frequency Dependence of VOR Plasticity

At the start of these studies it was not known ifthere existed any dependence of VOR gain plasticityon the single sinusoidal frequency of head rotationused for training adaptation. In order to determinethe effect of adaptation on a broad spectrum of fre-quencies of head rotation, VOR gains were measuredusing a sum of sines rotation in seven subjects beforeand after 15 min adaptation to X2 telescopic specta-cles. During adaptation, subjects viewed a video dis-play through telescopes while rotating at one of var-ious single sinusoidal frequencies from 0.1-1.0 Hz,amplitude 20°/sec. Three of the seven subjects exhib-ited significant VOR gain increases of 0.07-0.18 afteradaptation {P < 0.05); the remaining four exhibited

no consistent gain increases. Gain increases were sim-ilar at all frequencies tested, as illustrated for two ofthe three subjects in Figure 2. Gain increases wereobserved at several frequencies of head rotation dur-ing adaptation (Fig. 2A-D), but were small at an ad-aptation frequency of 1 Hz (Fig. 2). Some subjectsalso underwent additional gain measurements usingsingle frequency sinusoids at various frequencies (Fig.2B). Comparable changes in gain were observed afteradaptation regardless of measurement technique.

After demonstration that adaptation to telescopicspectacles produces a broad band increase in VORgain, testing of VOR gain plasticity could be limitedto a convenient single sinusoidal frequency of headrotation. A test frequency of 0.1 Hz was chosen as acompromise between the time required to acquire



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Fig. 3. There is individual variability in VOR gain changes following 15 min adaptation to telescopic spectacles of various powers. Gainswere measured using head rotations at 0.1 Hz, amplitude 60°/sec. Solid lines indicate subjects whose VOR gains increased after adaptation,while broken lines show decreases or no change. (A) X2 telescopic spectacles. (B) X4 telescopic spectacles. (C) X6 telescopic spectacles.

data on six sinusoidal cycles of rotation, and the in-crease in cycle to cycle gain variability observed athigher frequencies of rotation. All subsequent testingwas then performed at the single sinusoidal frequency0.1 Hz, and all adaptation was performed at the singlesinusoidal frequency 0.2 Hz. The sum of sines rota-tion was not employed during adaptation.

VOR Gain Changes When no Telescopic SpectaclesWere Worn

As a control experiment, six subjects underwentVOR gain measurements at 0.1 Hz, amplitude 60°/sec before and after 15 min adaptation in the mannerdescribed above, except that no telescopic spectacleswere worn, and there was no occlusion of any part ofthe visual field. Subjects were selected from the entiresubject pool for high VOR gain plasticity. InitialVOR gain for this group when tested before adapta-tion to X4 telescopic spectacles was 0.63 ± 0.06(mean ± SD, n = 6 subjects); after adaptation, all sixsubjects exhibited significant (P < 0.05) VOR gainincreases ranging from 14-46%, so that mean VORgain after adaptation was 0.77 ± 0.04. When testedbefore adaptation without wearing of telescopic spec-tacles, initial VOR gain was 0.61 ± 0.06, not signifi-cantly different from the initial value measured ear-lier before adaptation with telescopes. However, evenafter adaptation without telescopic spectacles three ofthe six subjects exhibited significant (P < 0.05) VORgain increases of 5-27%, so that mean VOR gain in-creased to 0.66 ± 0.08. For example, after adaptationwithout telescopic spectacles one subject exhibited anincrease in VOR gain from 0.54 ± 0.11 (mean ± SD,n = 6 cycles) to 0.61 ± 0.04 (n = 5, 12% increase, P> 0.05). After adaptation with telescopic spectacles,the same subject exhibited an increase in VOR gain

from 0.56 ± 0.06 (n = 5) to 0.82 ± 0.02 (n = 5, 46%increase, P < 0.0005). For all subjects tested, themean percentage increase in VOR gain was thus 24%when X4 telescopic spectacles were worn, and 9%when they were not worn.

Effect of Telescope Power

To determine the effect of telescopic spectaclepower on VOR gain plasticity, the conditions of rota-tion during adaptation were held constant at 0.2 Hz,amplitude 20c/sec, and duration 15 min. Subjectswere then tested using telescopic spectacles of X2, X4,and X6 powers. The visual field peripheral to themagnified telescope field was occluded. Data are il-lustrated in Figure 3.

For subjects tested with X2 telescopic spectacles,mean initial VOR gain was 0.71 ± 0.06 (mean± standard error of the mean, SEM, n = 7). MeanVOR gain for the entire group after adaptation in-creased to 0.79 ± 0.07, corresponding to a mean gainincrease of 0.08 ± 0.02 (n = 7). Due to interindivi-dual variability, this pooled mean after adaptationwas not significantly greater for the group than beforeadaptation (P > 0.05). Comparing individual subjectsbefore and after adaptation, five of the seven subjectsexhibited significant (P < 0.05) gain increases of7-17%; the remaining two subjects exhibited insignif-icant increases. The mean percentage gain increasewas 13%. These gain changes are seen in Figure 3A.

For subjects tested with X4 telescopic spectacles,initial VOR gain was 0.67 ± 0.02 (mean ± SEM, n= 34); mean VOR gain after adaptation increased to0.71 ± 0.03, but this difference was not statisticallysignificant because of interindividual variability (P> 0.05). It is more instructive to make intraindivi-


No. 1 VOR WITH TELE5COPIC SPECTACLES / Demer er ol 165

dual comparisons. After adaptation, 16 of 34 subjectsexhibited significant (P < 0.05) VOR gain increasesof 7-46%; of these, the mean increase was 0.08 ± 0.01(n = 24), and the mean percentage gain increase was16%. Ten subjects exhibited gain increases averaging4.1 ± 1.3% (mean ± SEM, range 1-13%) that werenot statistically significant {P > 0.05). Four subjectsexhibited insignificant gain decreases of less than 1%after adaptation. The remaining four subjects exhib-ited larger gain decreases averaging 26.8 ± 14.4%(range 8-39%); three of these decreases were statisti-cally significant (P < 0.05). The gain changes are seenin Figure 3B, where data on representative subjectsonly are shown for clarity; mean gain values shown inthe figure for this subgroup differ slightly from theoverall group means.

The data for the 34 subjects tested with X4 tele-scopic spectacles were also analyzed without the useof the data censoring rule. The initial VOR gain,computed using all six cycles in each sample for eachsubject, was 0.66 ± 0.02 (mean ± SEM, n = 34). TheVOR gain after adaptation increased to 0.68 ± 0.03;because of interindividual variability, this increasewas not statistically significant. However, when in-terindividual comparisons were made, 14 subjectsexhibited statistically significant (P < 0.05) gainincreases of 7-51%, averaging 15.6 ± 3.2% (mean± SEM). Thus, adaptive increases in VOR gain weredemonstrable in most subjects even without use ofthe data censoring algorithm, but this algorithm didserve to improve the consistency of observations.

For subjects tested with X6 telescopic spectacles,initial VOR gain was 0.65 ± 0.04 (mean ± SEM, n= 4). These values include one subject tested using anadaptation stimulus of 0.4 Hz, amplitude 40°/sec.After adaptation, three of four subjects exhibited sig-nificant VOR gain increases {P < 0.05) of 5-38%.The subject tested using the 0.4 Hz adaptation stimu-lus was one of the subjects exhibiting a significantgain increase. For all subjects, VOR gain after adapta-tion increased to 0.74 ± 0.05 (n = 4), but as a result ofinterindividual variation this increase was not signifi-cant compared with the initial gain (P > 0.05). Forsubjects exhibiting the gain increases, the mean in-crease was 0.13 ± 0.06 (n = 3), and the mean percent-age gain increase was 22%. The remaining subjectexhibited a statistically insignificant (P > 0.05) de-crease in gain of 5%. These gain changes are seen inFigure 3C.

Effect of Multiple Periods of Adaptationto Telescopes

Although data on each individual are representedonly once within each subgroup, many of the subjects

repeatedly underwent adaptation to telescopic spec-tacles during participation in the different experi-ments reported here. No cumulative effect of adapta-tion on VOR gain was evident. For individual sub-jects, VOR gains had returned to approximately theirinitial values by the time of repeat testing 1 or moredays later. Repeat gain testing was not performed onthe same day.

Two subjects underwent duplicate testing on dif-ferent days under identical conditions to estimatelong-term repeatability. Subject A had an initial VORgain on the first test day of 0.64 ± 0.02 (mean ± SD, n= 6 cycles); after rotation at 0.2 Hz, amplitude 30°/sec for 15 min while wearing X4 telescopic spectacles,adapted gain was 0.80 ± 0.02 (n = 3, P < 0.0005),representing a 24% gain increase after adaptation. Onrepeat testing 6 months later, initial gain for subject Awas 0.59 ± 0.04 (n = 6); adapted gain was 0.73 ± 0.02(n = 6, P < 0.0005), representing a 23% increase afteradaptation. Subject B had an initial gain of 0.62± 0.02 (n = 5); after adaptation in the same manneras subject A, gain increased to 0.89 ± 0.02 (n = 5, P< 0.0005), representing an increase of 43%. On re-peat testing 4 months later, initial gain for subject Bwas 0.67 ± 0.02 (n = 5); after adaptation, gain in-creased to 0.76 ± 0.02 (n = 4, P < 0.0005), represent-ing an increase of 13%. These results indicate thatplasticity can be repeatedly demonstrated in individ-ual subjects. Repeated testing was not performed onsubjects who had no change or a decrease in gain afteradaptation.

Effect of Subject Age on VOR Gain Adaptation

Since VOR gain adaptation is a form of motorlearning, we tested the hypothesis that this phenome-non is related to subject age. The amount of VORgain change with X4 telescopic spectacles followingthe 15 min adaptation period was studied relative tosubject age using linear regression analysis. It wasnecessary to consider two effects of inattention ondata analysis. Partially attentive subjects were ob-served to exhibit large cycle-to-cycle variability inVOR responses, while less attentive or sleepy subjectsexhibited very low gain responses, with or withoutlarge cycle-to-cycle variability. The data rejection al-gorithm automatically censored up to three of the sixcycles of any subject's VOR response if the amplitudeof those cycles was less than a statistical criterion levelbased upon the mean amplitude of all of the cycles ofthe response. This algorithm was very effective whenmost of the cycles had amplitudes closely distributedaround the mean, with outliers having substantiallylower amplitudes, as is the case for generally alertsubjects. When subjects were only partially attentive,



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Adapted

Non-Occluded Periphery

Fig. 4. Occlusion of unmagnified visual field peripheral to tele-scopic spectacles increases VOR gain plasticity. Gain measured at0.1 Hz, amplitude 60°/sec before and after 15 min adaptation toX4 telescopic spectacles. Plot on the left shows data for adaptationwith occlusion of peripheral visual field, while plot on the rightshows data for adaptation with no occlusion of peripheral visualfield. Values plotted are means for each subject, while listed valuesare for all eight subjects.

however, the cycle-to-cycle variability was so greatthat the statistical criterion for rejection was neversatisfied; subjective evaluation of such recordsshowed that in most such cases, no two cycles hadsimilar amplitudes. When subjects were very poorlyattentive or sleepy, measured response amplitudeswere often uniformly low, so that no cycles satisfiedthe rejection criterion of the data censoring algo-rithm. Consequently, it might be the case that theeight subjects who experienced VOR gain decreasesafter adaptation did so because of inattention andfatigue. To account for this possibility, the relation-ship between VOR gain plasticity and age was exam-ined with and without exclusion of these eight sub-jects.

The relationship between subject age and VORgain plasticity with X4 telescopic spectacles wastested using linear regression analysis. There was con-siderable scatter in a plot (not shown) of the gainchange after adaptation against subject age. When theeight cases were included where VOR gain after adap-tation was less than initial VOR gain, there was aweak inverse relationship between VOR gain changeand age (coefficient for age = -0.002, N = 34, R= 0.370, P = 0.031). As discussed above, one mightassume that cases where VOR gain decreased afteradaptation represent artifacts of subject fatigue andinattention. If such cases are excluded (leaving N= 26 subjects), the relationship between VOR gainchange and age was no longer significant (coefficientfor age -0.001, R = 0.314, P = 0.118). Exclusion ofcases in which adapted VOR gain decreased resultedin a statistically insignificant (P > 0.05) reduction in

the average age of the subject pool tested using X4telescopic spectacles from 40 ± 17 (mean ± SD) yearsto 37 ± 15 years. Since some subjects were tested withX2 telescopic spectacles who were not tested with X4telescopic spectacles, the mean age for the X4 sub-group was slightly but not significantly (P > 0.05)higher than the value for all subjects in the study of 38± 16 years.

Effect of Telescopic Visual Field during Adaptation

When telescopes are mounted in spectacles for useas aids for the visually impaired, only the central vi-sual field is magnified and the periphery is unmagni-fied. To maintain retinal image stability during headmovements in this situation, the gain of compensa-tory eye movements required in central vision isequal to telescope magnification, while the requiredgain for the periphery is 1.0. The effect of the unmag-nified visual field peripheral to the telescope was eval-uated using telescopic spectacles mounted in thenonoccluded configuration. VOR gains were mea-sured before and after a 15 min adaptation period ineight subjects selected for high VOR gain plasticityfrom the subject population. Adaptation to nonoc-cluded telescopic spectacles was performed using theprotocol described above, except that peripheral un-magnified visual field was not occluded during adap-tation.

The effect of peripheral visual field on VOR gainadaptation to X4 telescopic spectacles is summarizedin Figure 4. Initial VOR gain for the subject groupwas 0.65 ± 0.03 (mean ± SEM, n = 8) before adapta-tion with the periphery occluded, and 0.67 ± 0.02before adaptation without peripheral field occlusion.These values do not differ significantly (P > 0.1).After the 15 min adaptation period, each subject ex-hibited a significant (P < 0.05) VOR gain increasewith the periphery occluded, so that VOR gains in-creased by an average of 21% (range 10-46%) to 0.78± 0.03. This is significantly greater than the meangain before adaptation (P < 0.005). Following adap-tation without occlusion of the periphery, only foursubjects exhibited a significant VOR gain increase, sothat VOR gain for all subjects after the adaptationperiod was 0.71 ± 0.02 (n = 8). The mean gain in-crease was 7% (range 0-14%), but the mean gain afteradaptation for the group was not significantly differ-ent from the initial gain (P > 0.05).

Motion Sickness

During adaptation, chair velocities between 20 and40°/sec were employed. Velocity amplitudes ofgreater than 20°/sec frequently produced motionsickness in some subjects, particularly with X4 and


No. 1 VOR WITH TELESCOPIC SPECTACLES / Demer er ol 167

X6 telescopic spectacles. This discomfort consisted ofa visceral discomfort, nausea, headache, diaphoresisand dizziness, and was analyzed qualitatively only.Since motion discomfort made subject cooperationdifficult, and since this discomfort usually reducedVOR gains and increased cycle-to-cycle variability inVOR responses, we chose rotational amplitudes toavoid motion discomfort. In most testing, the ampli-tude of head velocity was set to 20°/sec. Despite this,ten subjects complained of motion discomfort duringchair rotation. Many other subjects were aware ofoscillopsia, a sensation of inappropriate motion ofthe visual world, early in the course of adaptation.This sensation generally resolved before the end ofthe adaptation period. In three subjects, however,motion discomfort was so severe that the subjectsrequested that testing be discontinued. No emesis wasobserved, and these subjects became more comfort-able over a period of about an hour. Seven othersubjects experienced mild or transient motion dis-comfort but were able to complete the rotatory test-ing. One subject, who consistently exhibited markedVOR gain plasticity, also consistently experiencedmotion discomfort both at the start of adaptation totelescopic spectacles, and upon leaving the laboratoryafter completion of the research protocol.

Discussion

The measurements reported here indicate thatVOR gain of normal human subjects may be in-creased by relatively short-term visual-vestibular ex-perience. Previous reports of human VOR gain plas-ticity were for individual subjects or relatively smallgroups of subjects.2627-29'30 We have confirmed thesereports in a large subject population spanning the agerange from 16 to 72 years. In this population, we havedemonstrated that significant VOR gain increasescan be induced in up to 70% of subjects by 15 min ofcombined visual-vestibular experience during wear-ing of telescopic spectacles.

There was considerable interindividual variabilityin the adaptive response of the VOR to telescopicspectacles; under the same experimental conditions,some subjects exhibited no adaptive VOR gain in-crease, while others exhibited VOR gain increases ofup to 46%. Interindividual variability in VOR gainplasticity is also a prominent finding in animal stud-ies.1719 Animal experiments suggest that central cate-cholamine levels are important to VOR gain plastic-ity,1819 making individual variation in neurotrans-mitter levels a possible cause of variation in VORgain plasticity. Lesions of the vestibulocerebeiium,15

inferior olivary nucleus17 and parietal cortex35 arealso known to impair VOR plasticity.

Sekine and colleagues used reversing spectacle ad-aptation to decrease VOR gain in humans, and foundno age-dependence in VOR gain plasticity.25 Withthis type of adaptation, the effect of fatigue would beadditive with the effect of plasticity, since both tendto reduce measured VOR gain. The data presentedhere, which involve plastic increases in VOR gain,demonstrate at most a weak effect of age as a determi-nant of VOR gain plasticity. When considering onlysubjects in whom gain increased after adaptation, thedata suggest no significant correlation between ageand plasticity. This group excluded those subjects inwhom gain decreased after adaptation, where fatiguemay have confounded the responses. However, rela-tively more older than younger subjects were ex-cluded on this basis, and it remains possible that oldersubjects who are more subject to fatigue also havereduced VOR gain plasticity. Nevertheless, VOR gainplasticity was demonstrable in at least one patientover the age of 60 years. It may be concluded that theeffect of age on VOR gain plasticity is at most a smallone. A much larger subject group would be requiredto resolve the issue.

In the present report, frequency spectral analysis ofthe VOR demonstrated that during wearing of tele-scopic spectacles of various powers, adapting headrotation at a single sinusoidal frequency induced sim-ilar plastic VOR gain increases over a wide range oftesting frequencies. Human short-term VOR gainplasticity is thus "broad band," and exhibits no "fre-quency tuning" effect for the frequency of head rota-tion employed during adaptation. Adaptation ofrhesus monkeys to telescopic spectacles over a periodof many hours has been studied by Lisberger andcolleagues.36 In contrast to the findings in the presentreport, these investigators found that the adaptivechange in the VOR gain of monkeys was greatestwhen measured at the frequency used during theadapting head rotation, and that less VOR gainchange occurred at higher or lower frequencies. Simi-lar findings have been reported in cats.37 This discrep-ancy may represent a species difference betweenlower animals and man, or may be the consequenceof studying VOR gain plasticity over different timeperiods. Although a broad band VOR gain increasecan be induced by brief exposure to combined vi-sual-vestibular stimulation, it remains possible thatthe greater change in VOR gain induced by moreprolonged stimulation might produce a larger butfrequency-dependent gain increase at the adaptingfrequency. This issue remains to be resolved.

In this study, VOR gain increases were observedafter a i 5 min adaptation period both without anytelescopic spectacles and during the wearing of tele-scopic spectacles of various powers. It is somewhat



surprising that rotation without telescopic spectaclesproduced any plastic gain increases, although theseincreases were much smaller than when the samesubjects were rotated during the wearing of X4 tele-scopic spectacles. However, normal subjects do nothave a fully compensatory VOR gain of 1.0 on initialtesting at a rotational frequency of 0.1 Hz, sincemeasured values were about 0.7. Although VVORgain measured in light without telescopic spectaclesappears to be exactly compensatory for head move-ment,10 the ocular motor system is neverthelessobliged to employ a visually related command to en-hance VOR gain. The increase in VOR gain follow-ing rotation during unmagnified vision is consistentwith the hypothesis of Miles and Lisberger that effer-ence copy of the pursuit command, rather than reti-nal slip velocity, serves as the driving input for VORgain plasticity." It is unclear why the constant visual-vestibular experience that occurs in daily life does notinduce further increases in VOR gain beyond theaverage value of 0.7 measured at 0.1 Hz. This may bedue to the tendency of VOR gain to increase withfrequency, as illustrated in Figure 2, and previouslyreported by Istl-Lentz and coworkers.30 If physiologicfactors dictate that VOR gain cannot be constantacross the frequency spectrum of head movement,the optimal range of VOR gain would probably beestablished at the higher frequencies, ie, 1 Hz andabove, where visual tracking is least effective. HumanVOR gain adaptation induced by the prolongedwearing of telescopic spectacles during everyday ac-tivities has been reported to produce a greater gainincrease at frequencies of 3 Hz and above.30 TheVOR may thus have a precisely compensatory gain atfrequencies where the limitations of the visual systemmake it most necessary, at the expense of a lower gainat lower frequencies when visual tracking reflexes canmake an effective contribution. It is likely that theincreased pursuit contribution to eye movements re-quired during the wearing of telescopic spectaclesprovides a greater stimulus for an adaptive VOR gainincrease than does unmagnified vision alone.

The VOR gain increases of up to 46% reported hereafter 15 min of combined visual and vestibular expe-rience do not represent an upper limit on humanVOR gain. A longer period of adaptation would pre-sumably induce a larger VOR gain change. Indeed,Gauthier and Robinson have reported a VOR gainincrease of 70% at a measurement frequency of 0.25Hz induced by the wearing of X2.1 telescopic specta-cles continuously for 5 days.29 Istl-Lentz et al havereported complete adaptation of human VOR gainafter 5 days of continuous wearing of X2 telescopicspectacles, but only for gains measured at 3 Hz; in thesame state of adaptation, VOR gains as measured at

0.5 Hz were only 1.29, representing an increase ofonly 50%.30 The upper limit of human VOR gain isnot known.

Significant plastic VOR gain increases were ob-tained using X2, X4, and X6 telescopic spectacles.Regardless of telescope power, approximately47-70% of subjects exhibited VOR gain increases ofapproximately the same magnitude. Since differentsubjects were studied with each telescopic spectaclepower, and since there is considerable interindividualvariation in VOR gain plasticity, it would not be validto make strong statistical inferences about the relativeeffectiveness of spectacles of various powers in in-ducing VOR gain changes. The useful magnified vi-sual field of the telescopic spectacles also decreaseswith increasing magnification, reducing the retinalarea stimulated, and potentially negating some of theeffect of greater magnification. However, the data dosupport the conclusion that each of the telescopicspectacle powers tested can induce significant VORgain changes in roughly the same proportion of sub-jects. Since retinal slip velocity is equal to the productof head velocity and the difference between the idealgain and the actual gain, it may be concluded thatroughly similar VOR gain changes may be associatedwith a very wide range of retinal image slip veloci-ties.38 This could be due to a limitation on the rate ofchange of VOR gain over time as a function of retinalslip velocity, or it implies that retinal slip velocity isnot the driving stimulus for VOR gain plasticity.

When telescopic spectacles are mounted for use asaids for the visually impaired, typically only the cen-tral visual field is magnified and the periphery is un-magnified in order to permit better orientation and toavoid large obstacles.28 This is called the bioptic con-figuration. To maintain retinal image stability duringhead movements in this situation, the gain of com-pensatory eye movements required in central visionis equal to telescope magnification, while the requiredgain for the periphery is 1.0. During head movementretinal slip velocity can never be zero in all parts ofthe retina, for eye movements achieving optimal gainfor central vision will induce retinal slip in the un-magnified periphery. This bioptic configuration cor-responds to the nonoccluded configuration used inthis study and permits evaluation of the relative con-tribution of retinal slip velocity in central vs. periph-eral retina to induction of VOR gain plasticity. Ascompared with a configuration in which the unmag-nified periphery was occluded, VOR gain increasesinduced by the X4 telescopes in the bioptic configura-tion were significantly smaller and were demonstra-ble in fewer subjects. This indicates that the unmag-nified peripheral field inhibits VOR gain plasticity,and may support a role for peripheral retinal slip in


No. 1 VOP> WITH TELESCOPIC SPECTACLES / Demer er ol 169

inducing VOR gain plasticity in humans. However,we report elsewhere that unmagnified peripheral vi-sion also inhibits the immediate modification ofVVOR gain by magnified central vision.39 It remainspossible that the inhibition of VOR gain plasticity byunmagnified peripheral vision is due to a reduction inefference copy of the visual tracking command re-sulting from an inhibition in immediate visual-ves-tibular interaction. Since telescopic spectacles in vi-sual rehabilitation are usually mounted in the biopticconfiguration, this finding suggests that VOR gainplasticity may not occur to a significant extent invisually impaired users of telescopic spectacles.

Rotation during the wearing of telescopic specta-cles was found to be a potent stimulus for motiondiscomfort. Motion discomfort was more frequentwith increasing telescopic spectacle powers and in-creasing amplitudes of head velocity during adapta-tion. Ten subjects noted some symptoms of motiondiscomfort, and three subjects were so symptomaticthat they could not tolerate 15 min rotation at 0.1 Hz,amplitude 20°/sec, while wearing X4 telescopic spec-tacles. In subjects who completed the adaptation pe-riod, the symptoms of motion discomfort abatedduring adaptation, as did oscillopsia. However, sus-ceptibility to motion discomfort varied widely fromsubject to subject, and many subjects had none at all.Further, subjects demonstrating large VOR gainchanges with adaptation were not necessarily im-mune to the symptoms of motion discomfort early inthe course of adaptation, when their VOR gains werelower. At least one subject consistently noted tran-sient motion discomfort each time he put on, or afteradaptation removed, telescopic spectacles. It is likelythat these symptoms are all due to visual-vestibularconflict, since they are reported to disappear whenVOR gain becomes adapted to spectacle magnifica-tion.2932 Indeed, experiments performed in spacehave demonstrated that microgravity reduces the per-formance of the VOR,40 and it is likely that the vi-sual-vestibular conflict generated by this ocularmotor dysmetria is a contributing factor to spacemotion sickness.41 Individual susceptibility to motionsickness induced by visual-vestibular conflict may bea limiting factor in the use of these devices as visualaids for some visually impaired persons.31'42

Key words: telescopic spectacle, adaptation, vestibulo-ocu-lar reflex, plasticity, gain

Acknowledgments

Computer programming was provided by MargaretKallsen, Bradford Daniels and Philip Szeto. Cyndy Coxperformed some of the eye movement testing. GyleeneWilcox provided editorial assistance.

References1. Westheimer G and McK.ee SP: Visual acuity in the presence of

retinal image motion. J Opt Soc Am 65:847, 1975.2. Guedry RE, Lentz JM, and Jell RM: Visual-vestibular interac-

tions: 1. Influence of peripheral vision on suppression of thevestibulo-ocular reflex and visual acuity. Aviat Space EnvironMed 98:270, 1978.

3. Benson AJ and Barnes GR: Vision during angular oscillation:The dynamic interaction of visual and vestibular mechanisms.Aviat Space Environ Med 49:340, 1978.

4. Demer JL, Porter FT, Goldberg J, Jenkins HA, and Schmidt K:The effect of telescopic spectacles on visual acuity during headmotion. In Topical Meeting on Noninvasive Assessment of theVisual System Technical Digest, 87-4. Washington, DC, Opti-cal Society of America, 1987, pp. 104-107.

5. Lanman J, Bizzi E, and Allum J: The coordination of eye andhead movement during smooth pursuit. Brain Res 153:39,1978.

6. Collewijn H: Latency and gain of the rabbit's optokinetic reac-tions to small movements. Brain Res 36:59, 1972.

7. Robinson DA: Control of eye movements. In Handbook ofPhysiology—Section 1: The Nervous System, Vol. II, part 2,Brookhart JM and Mountcastle VB, editors. Bethesda, Ameri-can Physiological Society, 1981, pp. 1275-1320.

8. Miles FA and Eighmy BB: Long-term adaptive changes inprimate vestibuloocular reflex: I. Behavioral observations. JNeurophysiol 43:1406, 1980.

9. Demer JL: The variable gain element of the vestibulo-ocularreflex is common to the optokinetic system of the cat. BrainRes 229:1, 1981.

10. Demer JL, Goldberg J, Jenkins HA, and Porter FI: Vestibulo-ocular reflex during magnified vision: Adaptation to reducevisual-vestibular conflict. Aviat Space Environ Med 58(9,Suppl):A175, 1987.

11. Miles FA and Lisberger SG: Plasticity in the vestibulo-ocularreflex: A new hypothesis. Annu Rev Neurosci 4:273, 1981.

12. Green AE and Wallman J: Rapid change in gain of vestibulo-ocular reflex in chickens. Soc Neurosci Abstr 4:163, 1978.

13. Ito M, Shiida T, Yagi N, and Yamamoto M: The cerebellarmodification of rabbit's horizontal vestibulo-ocular reflex in-duced by head rotation combined with visual stimulation. ProcJapan Acad 50:85, 1974.

14. Michnovicz JJ, Schairer JO, and Bennett MVL: Changes incerebellar activity during adaptive gain control of the vesti-bulo-ocular reflex (VOR) of the goldfish. Soc Neurosci Abstr6:693, 1980.

15. Robinson DA: Adaptive gain control of vestibuloocular reflexby the cerebellum. J Neurophysiol 39:954, 1976.

16. MacKay WA and Murphy JT: Cerebellar modulation of reflexgain. Prog Neurobiol 13:361, 1979.

17. Demer JL and Robinson DA: The effect of reversible lesionsand electrical stimulation of the olivocerebellar system on ves-tibulo-ocular reflex plasticity. J Neurophysiol 47:1084, 1982.

18. Keller EL and Smith MJ: Suppressed visual adaptation of thevestibuloocular reflex in catecholamine-depleted cats. BrainRes 258:323, 1983.

19. McElligott JG and Freedman W: Pharmacological manipula-tion of vestibular plasticity. In Adaptive Processes in Visualand Oculomotor Systems, Keller EL and Zee DS, editors. Ox-ford, Pergamon Press, 1986, pp. 443-450.

20. Gonshor A and Melvill-Jones G: Short-term adaptive changesin the human vestibulo-ocular reflex arc. J Physiol (Lond)251:361, 1976.

21. Gonshor A and Melvill-Jones G: Extreme vestibulo-ocular ad-



aptation induced by prolonged optical reversal of vision. JPhysiol(Lond) 256:381, 1976.

22. Shimizu M, Yagi T, Sekine S, Baba S, Kobayashi Y, andKamio T: Test of vestibulo-ocular reflex using horizontal vi-sion-reversal prisms and visual suppression test. Practica Oto-logicas (Kyoto) 74:1691, 1981.

23. Yagi T, Sekine S, Shimizu M, and Kamio T: New neurotolo-gical test for detecting cerebellar dysfunction—vestibulo-ocu-lar reflex changes with horizontal vision-reversal prisms. AnnOtol Rhinol Laryngol 90:276, 1981.

24. Aoki H, Yagi T, Kobayashi Y, and Kamio T: Effect of VORgain changes on OKN gain control. In The Vestibular System:Neurophysiologic and Clinical Research, Graham MD andKemink JL, editors. New York, Raven Press, 1987, pp.489-491.

25. Sekine S: Age changing effect on the vestibulo-ocular reflex inhumans. Pract Otol (Kyoto) 76:1471, 1983.

26. Collewijn H, Martins AJ, and Steinman RM: Compensatoryeye movements during active and passive head movements:Fast adaptation to changes in visual magnification. J Physiol(Lond) 340:259, 1983.

27. Cannon SC, Leigh RJ, Zee DS, and Abel LA: The effect ofrotational magnification of corrective spectacles on the quan-titative evaluation of the VOR. Acta Otolaryngol (Stockh)100:81, 1985.

28. Jose RT: Treatment options. In Understanding Low Vision,Jose RT, editor. New York, American Foundation for theBlind, 1983, pp. 211-248.

29. Gauthier GM and Robinson DA: Adaptation of the humanvestibuloocular reflex to magnifying lenses. Brain Res 92:331,1975.

30. Istl-Lentz Y, Hyden D, and Schwartz DWF: Response of thehuman vestibuloocular reflex following long-term 2X magni-fied visual input. Exp Brain Res 57:448, 1985.

31. Demer JL, Goldberg J, Porter FI, and Jenkins HA: Sensori-motor adaptation to telescopic spectacles. In Low Vision Prin-ciples and Applications, Woo GC, editor. New York,Springer-Verlag, 1987, pp. 216-231.

32. Estanol B and Lopez-Rios G: Looking with a paralysed eye:

Adaptive plasticity of the vestibulo-ocular reflex. J NeurolNeurosurg Psychiatr 47:799, 1984.

33. Furman JM, O'Leary DP, and Wolfe JW: Changes in the hori-zontal vestibulo-ocular reflex of the rhesus monkey with be-havioral and pharmacological alerting. Brain Res 206:490,1981.

34. Wilkinson L: SYSTAT: The System for Statistics. Evanston,Illinois, SYSTAT, Inc., 1986.

35. Demer JL, Tusa RJ, and Herdman SJ: Unilateral cerebralcortical ablations impair vestibulo-ocular reflex (VOR) gainand plasticity in the cat. Soc Neurosci Abstr 9:868, 1983.

36. Lisberger SG, Miles FA, and Optican LM: Frequency-selectiveadaptation: Evidence for channels in the vestibulo-ocular re-flex? J Neurosci 3:1234, 1983.

37. Godaux E, Halleux J, and Gobert C: Adaptive change of thevestibulo-ocular reflex in the cat: The effects of a long-termfrequency selective procedure. Exp Brain Res 49:28, 1983.

38. Demer JL, Goldberg J, Porter FI, Jenkins HA, and Schmidt K:The effect of telescopic spectacle power on the human vesti-bulo-ocular reflex (VOR) and visual-vestibular interaction.ARVO Abstracts. Invest Ophthalmol Vis Sci 28(Suppl):310,1987.

39. Demer JL, Goldberg J, Porter FI, and Schmidt K: Effect ofperipheral visual field on vestibulo-ocular reflex (VOR) gainplasticity and visual-vestibular interaction. Soc Neurosci Abstr13:392, 1987.

40. Vieville T, Clement G, Lestienne F, and Berthoz A: Adaptivemodifications of the optokinetic and vestibulo-ocular reflexesin microgravity. In Adaptive Processes in Visual and Oculo-motor Systems, Keller EL and Zee DS, editors. Oxford, Perga-mon Press, 1986, pp. 111-120.

41. Watt DGD: The vestibulo-ocular reflex and its possible roles inspace motion sickness. Aviat Space Environ Med 58(9,Suppl):A170, 1987.

42. Demer JL, Porter FI, Goldberg J, Jenkins HA, Schmidt K, andUlrich I: Retrospective analysis of factors predicting functionalsuccess in telescopic spectacle use by low vision patients. InTopical Meeting on Noninvasive Assessment of the VisualSystem, 1988 Technical Digest Series, Vol. 3. Washington,DC, Optical Society of America, 1988, pp. 147-150.


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