Vision Research 40 (2000) 3089–3098

The influence of repetitive eye movements on vergenceperformance

Weihong Yuan a,*, John L. Semmlow a,b

a Department of Biomedical Engineering, Rutgers Uni6ersity, PO Box 909, Piscataway, NJ 08855-0909, USAb Department of Surgery (Bioengineering), Robert Wood Johnson Medical School–UMDNJ, New Brunswick, NJ 08901, USA

Received 21 September 1999; received in revised form 20 February 2000

Abstract

We measured the peak velocity of convergence eye movement responses in four normal subjects before and after a large numberof either repetitive vergence or repetitive saccadic eye movements. A 20% decrease in the mean value of peak velocity wasobserved in vergence responses after 100 repetitive step vergence eye movements. However, 100 cycles of slow sinusoidal vergencetracking did not induce any notable change in vergence dynamics. Five hundred repetitive saccadic eye movements also causedan approximately 20% decrease in peak velocity. The reduction in peak velocity was related to the number of repetitions for bothvergence and saccadic fatiguing stimuli. The frequency of occurrence of double-vergences was also used as an index to monitorthe influence of repetitive eye movements on convergence performance. Results showed that repetitive step convergencemovements could double, or even triple, the frequency of the occurrence of double-vergence responses, while slow sinusoidalvergence tracking or repetitive saccades had no influence on the frequency of response doubles. © 2000 Published by ElsevierScience Ltd.

Keywords: Vergence; Saccade; Dynamics; Fatigue; Repetitive eye movement; Frequency of occurrence; Double-vergence response

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1. Introduction

Fatigue is an important, yet insufficiently under-stood, aspect in vision research and oculomotor con-trol. For many biological systems, fatigue manifests asan aftereffect following a heavy task load. Althoughvisuomotor fatigue is a common phenomenon, it is noteasy to define the load (the cause of fatigue) or the‘aftereffect’ (the fatigue itself), in a simple, precise anduncontroversial manner. For the visuomotor system,the load/task could be reading a book, watching avideo, or counting cells through a microscope. Theaftereffect might include alterations in the visual sen-sory system, central nervous system, or oculomotorbehavior. In addition to these various factors, mentalalertness or other subjective or psychological factorscould further complicate the problem.

For the past several decades, the influence of fatigueon saccade and vergence eye movements has been of

major interest in oculomotor control. However, manyfundamental questions regarding the extent to whichthe system can be fatigued, which part in the system isfatigued, or even whether or not the system can befatigued, still remain controversial. To study the influ-ence of fatigue on saccades, Bahill and Stark (1975a)had their subjects perform a large number of saccadiceye movements and found that saccadic performancechanged significantly once the subjects fatigued, includ-ing an increase in occurrence of double or overlappingsaccade and glissades (Bahill & Stark, 1975a; Bahill,Ciuffreda, Kenyon, & Stark, 1977). Schmidt, Abel,Dell’Osso, and Daroff (1979) studied intra- and inter-subject variability using the saccadic main sequence andfound no evidence of short-term muscle fatigue. Al-though one of their subjects did show a decrease inpeak velocity in the last five saccades of a 15-trialsequence, the group average values showed no consis-tent change in peak velocities over various amplitudes.They believed that ‘mental fatigue’, i.e. decreased alert-ness, was responsible for the decrease of peak velocityin saccadic responses. Fuchs and Binder (1983) also

* Corresponding author. Fax: +1-732-4453753.E-mail address: whyuan@biomed.rutgers.edu (W. Yuan).

0042-6989/00/$ - see front matter © 2000 Published by Elsevier Science Ltd.PII: S 0 0 4 2 -6989 (00 )00162 -0

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studied the fatigue resistance of extraocular muscle.After two strenuous saccade experiments (1860 trials,31 min in each of the experiments), their subjectsshowed a 10% decrease in peak velocity. This modestdecrement was attributed to a lack of attention andmotivation, again, so-called ‘mental fatigue’. Theyconcluded that the extraocular muscles could not befatigued in normal usage. Saito (1992) studied thefatigue characteristics of eyeball mobility, (includingmuscle and CNS control over the muscle). Despitecomplaints of fatigue from subjects, the author con-cluded that temporal and spatial characteristics ofsaccades were not significantly affected by fatigue. Ina recent study of saccadic performance in monkey,Straube, Fuchs, Usher, and Robinson (1997) foundthat after 5000 repetitive trials, saccade movementswere slower, but only by a small amount.

While the influence of fatigue on the saccadic sys-tem is still far from resolved, even less is knownabout the influence of fatigue on the vergence system.Schor and Tsuetaki (1987) found the adaptability ofthe convergence system was reduced after repetitiveramp tracking exercises. They found that thisaftereffect also affected the mutual interactions be-tween accommodation and vergence. They pro-posed a central site for this fatigue, where ‘tonic ver-gence is controlled.... and (where) perhaps disparityvergence is controlled’. They did not look foralterations in the dynamic characteristics ofdisparity vergence. Owens and Wolf-Kelly (1987)found that the vergence tonus (i.e. tonic vergence)changed due to extensive near work and theybelieved this might be an explanation for some as-pects of visual fatigue. Tonic vergence (also referredto as dark vergence) is the resting position of twoeyes when there is no disparity vergence and accom-modative stimulus. Tonic vergence shifted inward af-ter an intense reading task and the subjective ratingsof visual fatigue ‘were significantly correlated withchanges in dark vergence’ (Owens & Wolf-Kelly,1987). Tyrrell and Leibiwitz (1990) studied the rela-tion between vergence effort and visual fatigue thatwas defined in terms of a subjective criterion. Theyfound that dark (tonic) vergence was significantly cor-related with four of six subjective symptoms of visualfatigue.

Erkelens (1987) studied ocular disparity vergenceresponses to disparity stimuli with different ampli-tudes and wave shapes. He found that the vergencesystem gradually ceased responding to large, sustaineddisparities. He also found differences in behavior dur-ing the late vergence response due to a small numberof repeating stimuli; e.g. two successive steps, or aseries of pulses. However, the changes observed inErkelens’ study were due to short-term adaptation or

motor learning, not fatigue effects induced by a largenumber of repetitive responses.

From the brief review above, we note several prob-lems in previous studies of vergence fatigue. First,some vergence fatigue studies were based, at leastpartially, on subjective estimation (Owens & Wolf-Kelly, 1987; Tyrrell & Leibiwitz, 1990) which isdifficult to define and often has large variability. Forexample, the use of ‘back/neck pain’ (Tyrrell & Leibi-witz, 1990) as a general index to quantify visual fa-tigue is questionable. In addition, it has been foundthat the characteristics of physiological fatigue maybe ‘independent of subjective complaint of visual fa-tigue’ (Saito, 1992). Second, most studies were limitedto monitoring changes in tonic vergence (Schor &Tsuetaki, 1987; Owens & Wolf-Kelly, 1987; Tyrrell &Leibiwitz, 1990). Tonic vergence is also readilymodified by extended periods of near work (i.e. prismadaptation) which would confound any fatigue ef-fects. Peak velocity, main sequence, and other dy-namic indices have not been measured in fatiguestudies of vergence performance as has been done insaccades (Bahill et al., 1977; Schmidt et al., 1979;Fuchs & Binder, 1983). Third, in some studies(Owens & Wolf-Kelly, 1987; Tyrrell & Leibiwitz,1990; Heuer, Hollendiek, Kroger & Romer, 1989), thevisual work load used to produce fatigue in either thesaccadic or vergence systems was not clearly defined.For example, ‘one hour of near work’ (Owens &Wolf-Kelly, 1987) would have involved vergence, sac-cade, and other types of eye movement. Since noneof these were quantitatively counted, it was difficultto tell how much effort was actually required fromthe various oculomotor control systems. The abovelimitations also make it difficult to identify potentialsites where the fatigue occurs.

To address the limitations cited above, the taskload should be better defined, and behavioral fea-tures, particularly dynamic characteristics, should bemeasured. The load in this study was either pure ver-gence or pure saccadic eye movements, and istermed ‘fatiguing-vergence’ or ‘fatiguing-saccade’, re-spectively. Both types of fatiguing stimuli were pre-sented for a fixed number of repetitions at a constantamplitude. Evaluation of subject fatigue was based onresponse dynamics, including the peak velocity, mainsequence ratio (peak velocity divided by maximumamplitude), and the occurrence of double-vergencemovements.

The major goal of this study is to investigatewhether either repetitive saccadic or vergence eyemovements can influence subsequent vergence perfor-mance. The use of both vergence and saccades toinduce fatigue may allow us to isolate the oculomotorcontrol components that are modified by fatigue.

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2. Method

2.1. Subjects

Four human subjects, two males and two females,participated in the project. All of the subjects hadnormal binocular vision. Subject JS has been participat-ing in oculomotor control experiments for many yearsand has substantial knowledge of oculomotor behaviorand the goal of the research. The other subjects, LA,YD, and MB, had periods of training and were awareof the general goals of the experiments, but had noknowledge of the specific objective of any given experi-ment. UMDNJ and Rutgers University IRB boardshave approved the experiments, and written consentforms were obtained after the experimental methodswere explained to subjects.

2.2. Stimulus presentation, data collection, andcalibration

Vergence stimuli in this research included 4° stepconvergence stimulus and 4° sinusoidal vergence stim-uli. For the vergence stimulus, two oscilloscopes (P31phosphor and a bandwidth of 20 MHz) were arrangedas a haploscopic configuration to produce a stereo pairof vertical luminous lines against an otherwise com-pletely dark background. The stimulus on each oscillo-scope was a vertical line with a height of 5° and a widthof 0.15°. In the experiment, these target images werereflected by a pair of partially reflecting mirrors placed45° angle relative to the straight ahead direction. Thesubjects were required to keep these two lines fused inevery 2-s trial during the experiment. The movementsof the vertical stimulus lines were controlled by aPC-486 microcomputer. Since the stimulus did notmove in depth relative to the subject, this stimuluspresentation eliminated depth information that other-wise could induce vergence interaction from the accom-modation or proximal system. The stimulus forfatiguing-saccades was a symmetrical pair of physicaltargets, viewed directly through the partially reflectingmirrors. These targets were placed 10° apart at thesame distance (50 cm) as the vergence stimulus andthere was no depth difference between these two targetpositions.

Eye movements were recorded using a Skalar in-frared eye movement monitor (Model 6500). The moni-tor used two arrays of photo-detectors to measure thehorizontal position of each eye. The eye movementmonitor system had a published bandwidth of 200 Hz,a resolution of 1.5 min of arc, and a linear range of925° (3%). Measurement accuracy was estimated atapproximately 6 minarc based on an evaluation ofrepeated measurements and noise level. The eye move-ment signal was low-pass filtered at a cut-off frequency

of 50 Hz, and the signal was sampled at a frequency of200 Hz. To minimize head movement artifacts and toavoid possible influences from the vestibular system, adental impression bite bar was used to stabilize thehead. Each trial was 2-s long with a step change ofstimulus in convergent direction at the beginning. Theeye movement was not recorded as the target jumpedback in divergent direction at the end of each trial.Only convergence step responses were recorded foranalysis. Responses to other stimuli were not recordedalthough these responses were monitored during theexperiment to insure compliance.

Calibration was carried out by recording the eyemovement monitor output at two known eye positions:one immediately before and the other at the end of eachexperimental response trial. During the off-line analy-sis, each response was constructed by the computerfrom a calibration curve based on these two points. Onselected trials, a three-point calibration was performedprior to each response to evaluate linearity under exper-imental conditions. This calibration procedure showedthat the average nonlinearity was 3% of the total move-ment with a maximum of 5%. The two eye movementresponses were separately calibrated, and after calibra-tion, the individual eye movements were subtracted toproduce the overall vergence response. The velocitieswere computed using the two-point central differencedifferentiation algorithm (Bahill, Kallman & Lieber-man, 1982). In this algorithm, the velocity at a givenpoint is obtained by dividing the position differencebetween the two points on either side by the timedifference between these two points.

2.3. Experimental protocol

Five experiments were done in this research, witheach preformed on a different day. Each experimenthad three consecutive phases: a control phase; a fatigu-ing phase; and a fatigue evaluation phase.

The task in the first phase, the control phase, was thesame for all five experiments. In this phase, 50 repeti-tive 4° convergence step stimuli were presented to thesubjects. These 50 step convergence responses weremeasured and analyzed as baseline data for conver-gence performance. In preliminary experiments, the dy-namic characteristics of the first 10 responses werecompared with the last 10 responses in the 50 responsesmeasured in first phase. The peak velocity, maximumamplitude, main sequence ratio, and number of occur-rence of response doubles in these two groups of datadid not show any notable differences.

The task in the second phase, the fatiguing phase,was modified in different experiments with regard tostimulus type and/or number of repetitive movements.As shown in Table 1, the task in the fatiguing phase ofthe first experiment was 100 repetitive 4° step conver-

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gence movements, which required approximately 6–7min. These 100 convergence step responses were as-sumed to induce the fatigue effect. In the fatiguingphase of the second experiment, the task was to followvergence stimulus moving smoothly as a sinusoidalwaveform with an amplitude of 4° and a frequency of0.25 Hz. This also required approximately 7 min. Thetasks in the second phase of the three other experimentswere similar. They were all 10° voluntary saccademovements, but the number of movements requiredwas different: either 100, 250, or 500 saccades in thethree saccade-fatiguing experiments, respectively. Thesetasks required approximately 2.5, 6, and 12 min,respectively.

The task in the third phase, the fatigue evaluationphase, was the same as in the first phase for all fiveexperiments: 50 repetitive 4° step convergence move-ments. These responses were recorded to evaluate theeffect of the fatiguing movements. The initial 50 andthe final 50 vergence step responses in each experimentwere analyzed to compare the difference in dynamicsbetween normal responses and responses generated fol-lowing fatiguing movements. Since the only protocoldifference between the various experiments was in thesecond phase among various experiments, we will referto an experiment by its fatiguing phase task. Again,only the convergence step responses in the first phaseand the third phase in each experiment were recordedfor analysis. Responses in the second phase were notrecorded with the only exception being the first experi-ment where the fatiguing task was 100 vergence stimuli.Those responses not being recorded were monitoredduring the experiment to insure compliance.

2.4. Data analysis

Data analysis was done using the MATLAB andAXUM software packages, while statistical analysisused the SAS software package.

Since an increase in double responses has been foundin association with repetition-induced fatigue of thesaccadic system (Bahill et al., 1977), we expect that thefrequency of occurrence of double-vergence responsesmight also be associated with vergence fatigue. Ver-

gence doubles are analogous to the double responsesobserved in the saccade system (Bahill & Stark, 1975a).Double-vergence responses were first described by Al-varez, Semmlow, and Yuan (1998). They contain twoclosely-spaced, high-velocity initial components in re-sponse to a single vergence step stimulus. Time plots ofa typical double-vergence response from each of thefour subjects are shown in Fig. 1 (note the two peaks inthe velocity curves). Alvarez et al. (1998) showed thatthe contribution of the first component in a doubleresponse could vary over a very wide range, but wasalways less than 80% of the vergence amplitude. To beclassified as a response double, the velocity profile hadto show two distinct peaks, separated by 160 to 400 ms,with the minimum value being the normal vergenceresponse latency (Rashbass & Westheimer, 1961; Cum-ming & Judge, 1986). In addition, the estimated finalposition in the first component should be less than 80%of stimulus amplitude, and the peak velocity of thesubsequent movement should be larger than 50% of thepeak velocity of the first initial component as found byAlvarez et al. (1998).

In addition to the frequency of occurrence of double-vergence responses, peak velocity and maximum ampli-tude were analyzed for possible modifications byrepetition-induced fatigue. Bahill and Stark (1975b)introduced the ‘main sequence ratio’, which was con-structed by dividing peak velocity by response ampli-tude, to provide quantitative description of thefirst-order dynamics in the response. This ratioquantifies the first-order dynamics of a response. Peakvelocity is easy to determine from the velocity curves;however, maximum amplitude is sometimes difficult tomeasure, especially in responses where the final positionwas approached by a slow compensatory movementthat followed the initial rising transient. To accuratelymeasure the amplitude of the initial rising transient ofthe response, we used an extrapolation procedure basedon the phase plane trajectory of the response as alsodescribed previously (Semmlow, Hung, Horng, & Ciuf-freda, 1994; Alvarez et al., 1998). The measurement ofpeak velocity, maximum amplitude, and main sequenceratio were made only on non-double convergenceresponses.

Table 1Design of experiment

Second phase (fatiguing phase)First phase (control phase) Third phase (fatigue evaluation phase)Experiment

1 50 repetitive 4° step convergences50 repetitive 4° step convergences 100 repetitive 4° step convergences100 cycles periodic 4° sinusoidal vergence50 repetitive 4° step convergences 50 repetitive 4° step convergences2

50 repetitive 4° step convergences3 100 repetitive 10° saccades 50 repetitive 4° step convergences50 repetitive 4° step convergences 250 repetitive 10° saccades 50 repetitive 4° step convergences4

50 repetitive 4° step convergences500 repetitive 10° saccades50 repetitive 4° step convergences5

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Fig. 1. Typical vergence time plots showing double-vergence responses to a 4° step stimulus for subjects JS, LA, YD, and MB. The solid linerepresents position and the dashed line represents velocity. There are two peaks in the velocity curves. In plots A and B, these two peaks are quitedistinct while in plots C and D, these two peaks are more closely spaced and overlap.

Table 2Main sequence ratio comparisona

Main sequence ratio. fatigued byMain sequence ratio control Main sequence ratio, fatigued by 500 SaccadesSubject100 step vergences

JS 6.4191.106.6691.13 6.3291.15LA 3.9290.73 3.8590.71 3.6690.69YD 4.4190.73 4.5090.81 4.1990.73

4.6190.774.8690.62 4.6590.71MB

a No statistical significance between columns (ANOVA P\0.05). Variability given as standard deviation.

3. Results

3.1. Main sequence ratio

Table 2 shows the main sequence ratio of vergenceresponses in two of the experiments for our four sub-jects. A repeated measures ANOVA was applied to themain sequence values of Table 2 and no statisticallysignificant difference was found (P\0.05) in main se-quence ratio between the control responses and re-sponses fatigued by either 100 step vergences or 500saccadic responses.

3.2. Peak 6elocity

Although the main sequence ratios were similar forvergence responses in the normal (control) and fatiguedphases, the mean peak velocities of the vergence re-sponses following the fatiguing phase were usually lessthan the corresponding control phase. Fig. 2 demon-strates the quantitative comparison of mean peak veloc-

ity in the normal vergence response, vergence responsesfatigued by 100 repetitive 4° step vergences, and ver-gence responses fatigued by 500 repetitive 10° saccades.As shown in this figure, all four subjects had a similardecrease in mean peak velocity, about 20% lower thannormal, after being fatigued by 100 repetitive stepvergence responses. Coincidentally, 500 repetitive sac-cades also caused approximately the same decrease invergence performance with regard to mean peak veloc-ity. Applying the repeated measures ANOVA to peakvelocity data in the three conditions (control phase,fatigue evaluation phase after 100 vergence, and fatigueevaluation phase after 500 saccade) showed that theywere significantly different (PB0.0006). The SNK (Stu-dent–Newman–Keuls Test) multiple comparisonshowed that the control phase was significantly differ-ent (PB0.05) from both fatiguing evaluation phases,although the two fatigue evaluation phases (saccadeinduced and vergence induced) were not significantlydifferent from each other. As expected, the reduction inpeak velocity and the absence of a change in main

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Fig. 2. Comparison of mean peak velocities in normal vergence responses, vergence responses after repetitive vergence, and vergence response afterrepetitive saccades shown as bar graphs with error bars representing standard deviation. For all four subjects, mean peak velocity was highest fornormal vergence. Mean peak velocity of vergence responses after 100 repetitive vergence movements was almost identical to that of vergenceresponses after 500 repetitive saccades: approximately 20% lower than normal vergence.

Fig. 3. Time evolution of peak velocity in the first experiment where 100 convergence step stimuli were used as fatiguing task in its second phase.The peak velocities of responses in all three phases (control phase, fatiguing phase, and fatiguing evaluation phase) are plotted against trialnumber. There is a clear decrease in peak velocity after the subject performs large amount of vergence movements. (A). Subject MB. (B) SubjectYD.

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Fig. 4. (A) Comparison of mean peak velocity where tracking 100 cycles of periodic sinusoidal vergence movements was the fatiguing task. Theerror bar represents standard deviation. No difference with regard to mean peak velocity is observed in vergence responses after trackingsinusoidal vergence stimuli. (B) Comparison of mean peak velocity in the three experiments where repetitive saccades were used as fatiguing task.One hundred saccades did not show any noticeable change in mean peak velocity, while 250 saccades and 500 saccades caused different amountof reduction, 10 and 20%, respectively, in the subsequent vergence responses.

sequence ratio result in a lower amplitude and reducedaccuracy of the initial transient portion in fatiguedresponses (to avoid redundancy, amplitude data was notpresented). The accurate final position was alwaysachieved by a slow movement during the latter portionof the response.

Fig. 3 shows the time evolution of the change of peakvelocity in vergence responses in the first experimentwhere 100 step vergence stimuli were used as the fatiguingtask. The peak velocity of each individual response isplotted for all three phases as a function of trial number.The time course plot appears to level out after 150responses, suggesting that this number of vergence re-sponses produce a maximal change in vergence peakvelocity. Fig. 4A shows comparisons of mean peakvelocity when the vergence system was fatigued by 100cycles of periodic sinusoidal vergence movements. Nosignificant difference in peak velocity is observed betweenthe control and fatigued condition.

Fig. 4B compares the mean peak velocity values innormal vergence and vergence fatigued by either 100, 250or 500 repetitive saccades. Vergence peak velocity is littleaffected by 100 repetitive saccades. Two hundred andfifty repetitive saccades induced an intermediate decreasein peak velocity, approximately 10%, compared to con-trol vergence. Five hundred repetitive saccades caused a20% decrease in peak velocity compared with normalvergence. Fig. 4B shows no clear indication that 500saccades produce a maximal decrease in vergence peak

velocity and it is possible that a larger number offatiguing saccades would produce a greater decrease.This influence of additional fatiguing saccades will re-quire strongly motivated and well trained subjects, andwill be the subject of future studies.

3.3. Frequency of occurrence of double 6ergence

In addition to the changes in peak velocity, we alsoobserved changes in the frequency of occurrence ofdouble-vergences after vergence induced fatigue. Dou-ble-vergences such as shown in Fig. 1 were observed inour experiments and showed similar dynamics character-istics to those reported by Alvarez et al. (1998). As shownin Fig. 5, the frequency of occurrence of double-vergenceis small in normal vergence responses. During the initial50 vergence responses, the percentage of double re-sponses was approximately 8, 6, 4, and 4% for subjectJS, LA, YD, and MB respectively. After 100 repetitivefatiguing vergence, the frequency of occurrence of dou-ble-vergence responses was significantly increased (PB0.015, t-test). For subjects JS and LA, the frequency ofoccurrence of double-vergence responses in the fatigueevaluation stage increased to around 20 and 22%, respec-tively, while for the other two subjects, YD and MB, asmaller, but still substantial, increase was seen from 4%each to 10 and 12%, respectively. However, for vergenceresponses following repetitive saccadic eye movements,the frequency of occurrence of double-vergences did not

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show any significant change (P\0.8, t-test) in any ofour four subjects as shown in Fig. 5.

4. Discussion

In this research, we fatigued the vergence systemusing various tasks in order to determine the generalcharacteristics of fatigue effects and possibly distinguishwhich part in the vergence system was responsible forthe performance alteration.

Fig. 2 shows an approximately 20% decrease in ver-gence peak velocity produced by only 100 vergencefatiguing stimuli. Using repetitive saccades (Fuchs &Binder, 1983) could reduce saccadic peak velocity by10%, but only after 1830 repetitions. They attributedthis decrease to a lack of attention, not fatigue, sincethey found the subjects were able to increase peakresponse velocity if they were kept alert. Similarly,Epelboim et al. (1997) were able to demonstrate funda-mental changes in saccadic dynamics simply by addinga manual task to the oculomotor task. Finally, Erkelens’(1987) study showed that the vergence system exhibitssubstantial changes in behavior following relative shortperiods of sustained disparity and that this short-termadaptation was ‘selective for a limiting range of dispar-ity around the adapting disparity stimulus.’ Erkelens(1987) found this ‘adaptation is erased during a short

period after each blink’, which suggests an attentionfactor is responsible for the behavioral changes.

Taken together, these studies indicate that higherlevel function can modify the lower level motor controlsignal and offer a possible explanation for the vergence-induced vergence fatigue. However, we believe that thevergence-induced decrease of vergence peak velocity inour study was not due to the lack of attention. Ourrepetitions were relatively short (100 vergences lastingless than 8 min) and we frequently reminded the subjectto stay alert. To test if alertness level was a significantfactor, we compared the peak velocities in the fatiguedresponses before and after the subjects were verballyreminded to stay alert. No significant change was ob-served in peak velocity for either the vergence- orsaccadic-fatigued responses. In addition, the presenta-tion of 100 cycles of sinusoidal vergence stimulation,which required approximately the same amount of timeand effort as the fatiguing vergence step stimuli, did notinduce a noticeable change in peak velocity.

The 20% decrease of vergence peak velocity after 100repetitive step vergence movements could be due toeither muscle fatigue and/or fatigue of vergence neuralcontrol process. However, the only structures in thevergence system that can be influenced by saccadicmovements are the eye muscles and possibly the finalcommon pathway. Using saccadic eye movement as thefatiguing task required a larger number of repetitions in

Fig. 5. Comparison of the frequency of occurrence of double-vergence responses occurred in the control phase and fatigue evaluation phases (thereare fifty responses in each of these phases). For all four subjects, the frequency of occurrence of double-vergence responses following fatiguingvergence stimuli increased dramatically compared to that of normal vergence responses. However, the frequency of vergence doubles afterrepetitive saccades did not show any consistent change.

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order to generate the same decrease in peak velocity asvergence step movements: 500 saccades were required toproduce approximately the same decrease (20%) invergence velocity as 100 vergence movements. Fatigueeffects were substantially reduced when the number ofsaccadic repetitions decreased, and was effectively absentfor 100 repetitions. Since we expect that 100 repetitive 10°saccades would present a heavier load than 100, 4° stepvergences for both the ocular muscles and the finalcommon pathway, we argue that the reduction in peakvelocity after 100 repetitive step vergences is due to thefatigue of vergence neuronal components and not thosemechanisms that reduce velocity following fatiguingsaccades.

The results showed increased frequency of occurrenceof double-vergences after repetitive vergence eye move-ments while repetitive saccadic eye movements did notinduce any consistent change in the frequency of occur-rence of double-vergence. Previous studies (Alvarez et al.,1998) have shown that vergence double-responses occurwhen the amplitude of the initial component is less thanapproximately 80% of required to reach the final posi-tion. These studies also showed that the double responseswere generated by internal circuitry that monitored theamplitude of the initial pulse signal and called for thegeneration of a second pulse if the first pulse was toosmall (Alvarez, Semmlow, Yuan, & Munoz, 2000). Thus,the increase in frequency of occurrence of double-ver-gence responses also suggests that repetitive vergence eyemovements induce fatigue in the neural processes thatproduce the pulse command signal and this fatigueresults in a decreased pulse amplitude. In these cases,another second pulse signal is generated in order to reachthe desired final position, giving rise to double-vergencemovements. Therefore, we believe that the fatigue effectcaused by the repetitive step vergence comes from themodification of brainstem neural processes rather thanthe modification of neuromusculature efficiency.

The relative decrease in vergence peak velocity (ap-proximately 20%) following 500 repetitive saccades isgreater than the decrease found in saccadic peak veloc-ities recorded by Fuchs and Binder (1983) who showedonly a 10% decrease after 1830 saccadic trials. Clearly thevergence system is more sensitive to reductions in neuro-musculature efficiency induced by repetitive use. Thedifference in ‘fatigueability’ between the vergence andsaccadic system may be due to the differences in theunderlying neuronal control signals of the two systems.The neuronal control signal for a saccade can be de-scribed as a pulse-step waveform (Robinson, 1964; Fuchs& Luschei, 1970). For large saccades, there is consider-able evidence that the saccadic system controls move-ment amplitude by modifying pulse width, not pulseheight (Enderle & Wolfe, 1987, 1988), including evidencefrom model simulation and parametric sensitivity analy-sis (Hsu, Bahill, & Stark, 1976) and Fourier analysis

(Harris, Wallman, & Scudder, 1990). However, thevergence system uses a different strategy for controllingresponse amplitude. In a recent model-based analysis,Yuan, Semmlow, Alvarez, and Munoz (1999) found thatpulse width was a very stable parameter with only smallrandom deviations over a range of response amplitudesfrom 2 to 12°, while pulse height was highly correlatedwith the vergence stimulus amplitude in this range. Inaddition, the vergence pulse/step ratio, which representsthe relative contribution of pulse and step control signalto the overall response, is approximately 1.2�4 (Yuanet al., 1999), much less than that used in saccade control(9.5 for a 5° saccade as estimated in Hsu et al.’s (1976)work).

The difference in control strategy might explain thedifference of the effort required in order to induce fatigueeffects in the saccadic and vergence systems. The largesaccade pulse control signal, even though not fullysaturated in medium amplitude saccades, may be betterable to compensate for reduced efficiency in the finalcommon pathway. Therefore, the external performanceof the saccadic system would not be as easily modifiedby repetitive saccadic movement. In the vergence system,which is modulated by variations in pulse height, anyreduction in the efficiency of the neuromusculaturewould be directly reflected in response velocity.

5. Conclusion

This investigation has shown that fatigue caused by alarge number of saccadic eye movements reduced meanpeak velocity in subsequent vergence responses. Thisfatigue effect is believed to be due to the changes inoculomotor neuro-musculature. Repetitive vergence eyemovements decreased peak velocity, but also increasedthe frequency of occurrence of double-vergence re-sponses. These two effects were attributed to fatigue inthe vergence neurons that generate the pulse signal.Repetitive slow vergence movement (the tracking ofsinusoidal vergence) induced no change in subsequentvergence responses suggesting that attention was notresponsible for the fatigue effects.

Acknowledgements

This work was supported, in part, by a grant from theNational Science Foundation IBN-9511655.

References

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