The completeness of binocular rivalry suppression was measured by recording the fraction of a trial during which targets were perceived as alternating in their entirety, rather than blending together into a composite. It was found that the completeness of rivalry declines with prolonged stimulation. A control condition in which subjects saw the same grating targets, but without rivalry, resulted in no decrement. The phenomenon was spatial-frequency specific. The results suggest that binocular rivalry suppression is mediated by a cooperative mechanism which is susceptible to adaptation

Hollins, Mark

Hudnell, Ken

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Volume 19Number 9 Reports 11177. Fujimoto M and Tomita T: Reconstruction of theslow PHI from the rod potential. INVEST OPMTHAL-MOL Vis SCI 18:1090, 1979.8. Lurie M: Some observations on the c-wave of theelectroretinogram in the intact frog eye. Exp EyeRes 23:197, 1976.9. Lurie M and Marmor MF: Analysis of the responseproperties and light-integrating characteristics ofthe c-wave in the rabbit eye. Exp Eye Res (in press.)10. Lurie M and Marmor MF: Light-integrating capac-ity of the ERG c-wave under different anesthetics.In Proceedings of the XVIth Symposium of the In-ternational Society for Clinical Electrophysiology ofVision, Tazawa Y, editor. Tokyo, 1979, JapaneseJournal of Ophthalmology, pp. 129-133.11. Oakley B II, Flaming DG, and Brown KT: Effects ofthe rod receptor potential upon retinal extracellularpotassium concentration. J Gen Physiol 74:713,1979.Adaptation of the binocular rivalry mecha-nism. MARK HOLLINS AND KEN HUDNELL.The completeness of binocular rivalry suppression wasmeasured by recording the fraction of a trial duringwhich targets were perceived as alternating in their en-tirety, rather than blending together into a composite. Itwas found, that the completeness of rivalry declines withprolonged stimulation. A control condition in which sub-jects saw the same grating targets, but without rivalry,resulted in no decrement. The phenomenon was spatial-frequency specific. The results suggest that binocularrivalry suppression is mediated by a cooperative mecha-nism which is susceptible to adaptation.In a number of perceptual phenomena, thereare alternative ways in which the visual system canprocess information coming from particular re-gions of the field of view. In stereopsis, for exam-ple, a given stimulus element seen by one eye canoften be fused with any of several elements seenby the other eye. Julesz1 has shown that a choiceamong these alternatives is typically made in a"cooperative" way, meaning that the choice madein one spot will influence the making of choices inadjacent regions.The question considered in the present study iswhether binocular rivalry—the perceptual alter-nations which occur when very different stimuliare presented to corresponding regions of the tworetinas—is also a cooperative phenomenon. Whentwo targets rival, there are periods when they al-ternate crisply and in their entirety, while at othermoments portions of both are seen at once.2 Totalsuppression is not simply a coincidence, occurringwhen the small elements comprising a target hap-pen to be suppressed simultaneously, because theamount of perceptual fragmentation is profoundlyinfluenced by changes in the color,3' 4 contrast,5and alignment of target elements,6 even whenthose changes do not selectively favor one targetor the other. This is not in itself evidence of coop-eration, however; uncontrolled factors such as eyemovements might be influenced by stimulusproperties and in turn influence the amount ofrivalry fragmentation.0 We reasoned that if theoften unitary nature of rivalry suppression weredue to an active, cooperative process, then thisprocess might be susceptible to adaptation. Exper-iments reported here show that such adaptationdoes occur.From a distance of just over 1 m, subjects withnormal binocular vision viewed sinusoidal gratingsproduced by standard methods' on oscilloscopescreens. Both eyes viewed the same screen in thefirst set of experiments, whereas separate oscillo-scopes were used for the two eyes in the experi-ment of Fig. 2. Differently oriented Dove prismspositioned close to the two eyes caused the gratingto be vertical in the left eye, horizontal in theright. The stimulus filled a 1° square which wassurrounded by darkness except for bars of diffuselight to aid in fusion. There were four such bars,each paralleling one side of the square, from whichthey were separated by 14 min arc; they were 1° inlength and 9 min arc wide and had a luminance of1 cd/m2.Subjects fixated the approximate center of thegrating, moving their line of sight slightly fromtime to time to minimize the formation of an after-image. A three-position response key allowedthem to report continuously whether they per-ceived the vertical or the horizontal grating, or acomposite of the two. Between trials the gratingswere replaced by a uniform square of the samespace-averaged luminance (1.4 cd/m2), which wasinspected throughout rest periods of less than 5min and for the last 5 min of longer rests.The first experiments began with 5 min of lightadaptation to the uniform square, followed by twobaseline rivalry trials separated by a 100 sec inter-val. After another interval of 100 sec, the rivalryadaptation period began. This consisted of 15 trialsseparated from one another by 20 sec rest periods.Finally, during the recovery period, rivalry wasmeasured at more widely spaced intervals. Alltrials were 100 sec in duration.The results are reported in terms of the numberof seconds per trial which were free of blendingand fragmentation of the targets, i.e., the time forwhich the left eye's target was seen exclusively0146-0404/80/091117+04$00.40/0 © 1980 Assoc. for Res. in Vis. and Ophthal., Inc.1118 Reports Invest. Ophthalmol. Vis. Sci.September 19802 0 -1 0 -00O 3 0oif)~?20oo<DCOA AI 0kA2A#2 A°O• * i<* t OnoAaJ-«~ADAPTA1 O AAOA"•SoAT I O N - ^0AAA Ao oA 41AO«r6MH1oo ° •° . AA A tAKH1 11 0 -0 1000 2000 3000 4000Time from start of adaptation (sec)Fig. 1. Number of seconds of exclusive visibility (complete dominance) within each 100 sectrial is plotted for a baseline period, an adaptation period when the trials occurred in closesuccession, and a subsequent recovery period in which they were more widely spaced. Insome experiments, the spatial frequency of the targets was either 1.54 cy/deg(filled triangles)or 9 cy/deg(filled circles) throughout; unfilled symbols, spatial frequency during adaptation wasdifferent from that used during the pretest and recovery periods: either 1.54 cy/deg duringadaptation and 9 cy/deg during pretest and recovery (circles), or the converse (triangles).Symbols are positioned horizontally at the midpoint of the trials they represent. Each point isthe median of five determinations. The authors served as subjects.plus the time for which the right eye's target wasseen exclusively. Results with 9 cy/deg gratingshaving a contrast [defined as (Lmax ~ Lmin)/(Lmax + Lmin )] of 0.6 are shown by the filled cir-cles in Fig. 1, where the number of seconds ofexclusive visibility4 is plotted for each trial. It canbe seen that the completeness of rivalry declinedsteadily during the adaptation period but returnedapproximately to the baseline level when longerrest periods were given between the trials.We repeated the measurements with a lowerspatial frequency (1.54 cy/deg) and contrast (0.2),conditions which produced an initial level of ex-clusive visibility comparable to that in the firstexperiment. The filled triangles in Fig. 1 showthat the results with these coarse gratings weresimilar to those found at the higher spatial fre-quency. If, however, the spatial frequency waschanged at the end of the adaptation period, therewas an abrupt return of exclusive visibility to itsbaseline level (unfilled symbols). Clearly the de-cline in the completeness of rivalry is spatial-frequency selective.For these measurements, subjects viewed thetargets with the natural pupil. Additional data ob-tained on Subject M. H., with the pupil dilatedand accommodation paralyzed by the installationof 2 drops of 1% cyclopentolate hydrochloride ineach eye, were very similar to those plotted inFig. 1.Because long exposure to gratings can reducetheir apparent contrast,8' 9 we considered the pos-Volume 19Number 9 Reports 1119-100J3T3O•oDCCL50 -—ADAPTAT10NiJJL/a// // y13000 4000 5000Time from start of adaptation (sec)Fig. 2. Amount of exclusive visibility relative to the preadaptation level is plotted for experi-ments in which subjects were exposed to rivalrous stimuli during adaptation (solid symbols)and for experiments in which they received comparable exposure to gratings but did notexperience rivalry (unfilled symbols). The grating was vertical in the left eye and horizontal inthe right. The spatial frequency was 3 cy/deg, and the contrast was 0.4 throughout. In additionto the authors, a naive observer (squares) participated. Each point is the median of fivedeterminations. Before being normalized, the results of this experiment were subjected toMann-Whitney U tests, using an 0.01 level of significance. In the trial begun immediately afteradaptation, the simultaneous condition data were significantly below the successive conditiondata for all three subjects; at 450 sec after adaptation, for two of the subjects; at 1050 sec afteradaptation, for one subject; and by 1850 sec after adaptation, for none of the subjects. Theeffect of rivalry adaptation here is less than in the experiment of Fig. 1, presumably because ofthe longer intertrial intervals employed.sibility that the adaptation effect studied here wassimply a concomitant of changes in perceived con-trast rather than a change in the rivalry mecha-nism itself. This possibility was investigated in anadditional experiment using a naive observer aswell as the authors. The general procedure wassimilar to that in the first set of experiments. Dur-ing the adaptation period, however, the left- andright-eye targets were presented either simulta-neously or successively to the two eyes. In thesimultaneous condition, 100 sec rivalry periods al-ternated with 100 sec rests during which both eyesviewed a uniform square; in the successive condi-tion, 100 sec periods in which the right eye viewedits target while the left eye viewed a uniformsquare alternated with periods of the same lengthduring which the left eye viewed its target whilethe right eye viewed the uniform square. Thus,from the point of view of either eye alone, the two50 min adaptation conditions were closely compa-rable. Only in the simultaneous condition, how-ever, did rivalry occur during the adaptation peri-od. No measurements were made during theadaptation period itself; to do so would have re-quired more vigilance during the simultaneousthan during the successive condition, thus reduc-ing their comparability.The results of this experiment are shown in Fig.2, where, for each subject and condition, theamount of exclusive visibility is plotted relative tothat obtained during the preadaptation trials. Itcan be seen that exclusive visibility was approxi-mately halved as a result of the rivalry adaptationbut showed little or no change after alternatingmonocular exposure to the gratings. Hence rivalryitself can cause exclusive visibility to decline. The1120 Reports Invest. Ophthalmol. Vis. Sci.September 1980pattern of results was the same whether exclusivevisibility for each eye was considered separately or(as in the figures) the two amounts were summed.We conclude that it is possible to adapt themechanism responsible for the frequently ob-served complete suppression or dominance of arivalry target. Our results make it very unlikelythat the increase in fragmentation is due to a cri-terion shift or other attitudinal change on the partof the subject, and they rule out the possibilitythat the drop in the completeness of rivalry resultsprimarily from adaptation to the gratings per se.Although particular patterns of eye movementscould almost certainly influence the course ofrivalry—horizontal saccades might bring a verticalgrating into prominence, for example—an expla-nation based on eye movements is hard to recon-cile with the spatial frequency selectivity of thefatigue effect. The most reasonable interpretationof the data reported here is that binocular rivalrysuppression is a cooperative phenomenon, withthe occurrence of suppression in one region of atarget normally facilitating the occurrence of sup-pression in adjacent regions. The fact that the pro-cess by which this cooperation is effected can berendered temporarily ineffective provides a toolfor dissecting the mechanisms underlying binocu-lar rivalry suppression.We thank Dick King and Paul Shinkman for theircomments on the manuscript.From the Department of Psychology, University ofNorth Carolina, Chapel Hill. This work was supportedby NSF grant BNS77-23050. K. H. is an NIMH trainee,grant 5T32 MH14269-05. Submitted for publicationApril 3, 1980. Reprint requests: Mark Hollins, Depart-ment of Psychology, Davie Hall 013 A, University ofNorth Carolina, Chapel Hill, N. C. 27514.Key words: binocular rivalry, adaptation, perceptualfragmentationREFERENCES1. Julesz B: Foundations of Cyclopean Perception.Chicago, 1971, University of Chicago Press.2. Panum PL: Physiologische Untersuchungen iiber dasSehen mit zwei Augen. Kiel, 1858, SchwersscheBuchhandlung.3. Wade NJ: Monocular and binocular rivalry betweencontours. Perception 4:85, 1975.4. Hollins M and Leung EHL: The influence of color onbinocular rivalry. In Visual Psychophysics and Phys-iology, A Volume Dedicated to Lorrin Riggs, Ar-mington JC, Krauskopf J, and Wooten BR, editors.New York, 1978, Academic Press, Inc., pp. 181-190.5. Hollins M: The effect of contrast on the completenessof binocular rivalry suppression. Perception Psy-chophys 27:550, 1980.6. Whittle P, Bloor DC, and Pocock S: Some experi-ments on fjgural effects in binocular rivalry. Percep-tion Psychophys 4:183, 1968.7. Campbell FW and Green DG: Optical and retinalfactors affecting visual resolution. J Physiol 181:576,1965.8. Blakemore C, Muncey JPJ, and Ridley RM: Percep-tual fading of a stabilized cortical image. Nature233:204, 1971.9. Blakemore C, Muncey JPJ, and Ridley, RM: Stimu-lus specificity in the human visual system. Vision Res13:1915, 1973.Behavioral enhancement of visual responsesof prestriate neurons of the rhesus monkey.DAVID LEE ROBINSON, JOAN S. BAIZER,* ANDBRUCE M. D O W . *Neurons in the superior colliculus, striate cortex, frontaleye fields, and posterior parietal cortex of the monkeyrespond to visual stimuli. Many of these cells dischargemore intensely to a stimulus when it is to be the target fora saccadic eye movement than when fixation is main-tained. We have demonstrated that such enhancement ofthe visual response is also present for cells in prestriatecortex. The prestriate effect is a modulation of the visualresponse and not a concomitant of oculomotor activity. Itis present for eye movements away from as well as intothe visual receptive field and is thus similar to that seenin striate cortex and different from that studied in thesuperior colliculus, frontal eye fields, and posteriorparietal cortex. The visual responses of many prestriatecells habituate with repeated stimulation. When themonkey makes saccadic eye movements to a stimulus thatis eliciting only a habituated response, the enhancementacts as a dishabituation which persists throughout theeye movement trials.Visual stimuli continually excite the retinal re-ceptors. In spite of this sensory bombardment,only a limited number of stimuli evoke a saccadiceye movement. Therefore the visual system musthave mechanisms for selecting salient events.Previous investigations of the visual system of themonkey have attempted to determine the neuralbasis of such selection mechanisms.1"3Neurons in the superior colliculus, frontal eyefields, and posterior parietal cortex respond morevigorously to stimuli in their receptive field if theanimal subsequently makes a saccadic eye move-ment to the stimulus than if fixation is main-tained.1"3 This "enhancement" of the visualresponse is selective; it is present for eye move-ments to the receptive field and is not demon-strable for eye movements to points distant fromthe receptive field. In contrast, the few cells instriate cortex that show enhanced visual responses

Adaptation of the binocular rivalry mechanism

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Adaptation of the binocular rivalry mechanism

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