JOURNAL OF THE OPTICAL SOCIETY OF AMERICA

Visual Disinhibition with Binocular and Interocular PresentationsDANIEL N. ROBINSON

Electronics Research Laboratories, Columbia University, New York, New York 10027(Received 12 May 1967)

Subjects were given combinations of two and three brief concentric flashes of equal luminance underbackward masking conditions. Intervals between the first (TF) and second (CF) flashes were 10, 20, 50, 75,100, and 200 msec. When third flashes (DF) were present, they were separated from CF by the same inter-vals. Two modes of presentation were employed: binocular presentations in which all flashes were pre-sented to both eyes and interocular presentations in which TF and CF were presented to the left eye andDF to the right. With binocular view, the backward masking of CF by DF resulted in the disinhibition ofTF, otherwise masked by CF under two-flash conditions. Disinhibition was not obtained under interocularpresentations. A major conclusion is that recurrent influences within the human retina are not preservedmore centrally (retrochiasmally) in the visual system.INDEx HEADINGS: Vision; Detection.

THE importance of neural mechanisms in deter-Tmining visual perception was not fully appre-ciated until Crawford's research on backward masking'although retroactive inhibitory effects had been prom-inent in the vision literature for some time. 2

4 Craw-ford's finding, that sensitivity is reduced by subsequentstimulation, has been confirmed with various visualstimulus arrangements by many investigators'8 andits analog in other sensory systems has been estab-lished.9 -'0 Backward masking has interesting featuresin common with metacontrast."1 Backward masking isproduced by following a test field (TF) with a moreenergetic concentric conditioning field (CF). Typically,CF is either larger, more intense, longer in duration,or some combination of these with respect to TF. Inmetacontrast, TF and CF are spatially displaced andmay be temporally concurrent or sequential. Whilebackward masking has usually been treated as athreshold increment effect and metacontrast as a varia-tion in apparent brightness, both terms have often beenused interchangeably and the effects are treated togetherin literature surveys.'2 Moreover, each is assumed tooccur in part as a result of underlying neural mech-anisms functionally similar to those found in Limrulusand as described by Hartline, Ratliff, and their col-laborators." 3"4 Interconnections in the lateral eye ofLimnulus are such that the response of a given unit isinfluenced not only by stimulation but also by activity

B. H. Crawford, Proc. Roy. Soc. (London) B134, 283 (1947).2 A. Broca and D. Sulzer, J. Physiol. (Paris) 4, 632 (1902).3H. Pieron, Ann. Psychol. 26, 1 (1925).4G. Fry, Am. J. Physiol. 108, 701 (1934).' H. D. Baker, J. Opt. Soc. Am. 43, 798 (1953).6 R. Boynton, W. R. Bush, and J. Enoch, J. Opt. Soc. Am. 44,

55 (1954).7 W. S. Battersby and- I. Wagman, Am. J. Physiol. 203, 359

(1962).8 W. R. Bush, J. Opt. Soc. Am. 45, 1047 (1955).9J. M. Pickett, J. Acoust. Soc. Am. 31, 1613 (1959).

E. Schmid, J. Exptl. Psychol. 61, 400 (1961).l1 M. Alpern, J. Opt. Soc. Am. 43, 648 (1953).12 D. Raab, Psychol. Bull. 60, 118 (1963)."H. K. Hartline and F. Ratliff, J. Gen. Physiol. 41, 1049

(1958).14 F. Ratliff, W. H. Miller, and H. K. Hartline, Ann. N. Y.

Acad. Sci. 74, 210 (1958).

in neighboring units. In addition, the system has beenidentified as a recurrent one" in that inhibition of aninhibitor will result in disinhibition. Fry'0 proposed thatthis type of recurrent influence is not present in humanvision (based upon simultaneous brightness contrasteffects). Alpern and David,'7 however, report suchdisinhibition from brightness-matching studies involv-ing spatially displaced light patches; i.e., metacontrastconditions. Robinson,'8 using brief, concentric circularpatches found disinhibition in human vision underbackward-masking conditions. By delivering transientstimuli to concentric retinal regions he was able toassess aspects of the system response often concealedby "steady state" judgements of apparent brightness."9Robinson measured TF detection in the presence andabsence of a third (disinhibiting) flash (DF), presented20 msec after CF and with twice the area and twicethe luminance of CF. It was found that TF detectionwas significantly improved; i.e., "disinhibition" oc-curred, in the DF-present condition. The limitationsof this study, however, precluded statements concern-ing the locus of the disinhibition and the temporal rangeover which it operates. Since the three concentricflashes were of discriminably different luminances, theresulting detection rates were inextricably tied to con-tour and boundary perceptual effects.2 0

The present experiment, therefore, is an extension ofthe earlier and attempts to isolate more clearly theprocesses involved in the disinhibition effect. In thepresent study, (1) data obtained with binocular pre-sentations are compared with those obtained inter-ocularly, thus permitting comparisons between retinaland more central (retrochiasmal) influences, (2) allflashes are of photometrically matched luminance suchthat boundary recognition complications are reducedif not completely eliminated, and (3) the ranges and

"s F. Ratliff, H. K. Hartline, and W. H. Miller, J. Opt. Soc.Am. 53, 110 (1963).

1G G. Fry, Am. J. Optom. 25, 162 (1948).17 M. Alpern and H. David, J. Gen. Physiol. 43, 109 (1959)."D. Robinson, Science 154, 157 (1966)."On this point, see particularly S. H. Bartley and T. M.

Nelson, J. Psychol. 55, 121 (1963).20 G. Fry and S. H. Bartley, J. Exptl. Psychol. 19, 351 (1936).

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February1968 DISINHIBITION WITH BINOCULAR PRESENTATIONS

combinations of TF-CF and CF-DF intervals areincreased to permit assessments of the temporal limitsof the disinhibition effect.

METHOD

Apparatus: A modified Scientific Prototype three-channel tachistoscope with associated timers and powersupplies was used to present stimuli. Each field of thetachistoscope was limited by circular apertures ofdifferent diameters, such that circular patches of 23',46', and 92', visual angle were exhibited by the threefields. Opal diffusing glass was placed between theargon mercury-vapor discharge lamps and the aperturesin order to make the luminance uniform in each field.A foveal fixation field was provided by lighting thethird channel with a continuous dim red-tinted tung-sten filament bulb which illuminated the largestaperture. Under binocular viewing conditions, all threefields were visible to both eyes and the subject wasinstructed to maintain constant fixation of the dim-redpatch. Neutral density filters were inserted such thatthe luminance of each patch irrespective of sizewas maintained at 5 mL and the luminance of thefixation patch was 0.5 mL. Under these conditionsKodak 0.6 neutral density filters were placed just infront of the subject's view. With interocular presen-tations, these neutral density filters were replaced byplane polarizers. These and other polarizers that wereplaced in the filter compartments in front of the subjectwere arranged so that fields one and two were visibleto the left eye and field three was visible to the right eye.The fixation lamp was positioned in the third field at apoint beyond the polarizer in that field and, therefore,the fixation patch was visible to both eyes. The 0.6 logneutral filters were necessary to keep luminances equalunder the two conditions of presentation. Insertion ofthe polarizers reduced luminance by 0.6 log relative tobinocular (unpolarized) presentations. To compensate,neutral filters were inserted during the binocular pre-sentations. Each stimulus was 5 msec; the fixationpatch was present for all of each experimental session.

PROCEDURE

Each subject was dark adapted long enough for thefixation patch to become readily visible (from 3 to 5min) and was informed that flashes of differing sizeswould be presented either singly or in combination of2 or 3. He was instructed to refer to the smallest flashas "one," the intermediate-size flash as "two" and thelargest flash as "three". The subject was informed thaton any given trial any one or combination of flashesmight be presented. Practice at identifying each flashwith its appropriate designation (one, two, or three)was provided until no errors were made in detectingeach flash and identifying it properly on all of 10presentations. Following practice, the subject was ex-posed to 36 combinations of intervals separating TF

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FIG. 1. Percent of 1st (Test) flashes seen by each subject withbinocular presentations as a function of the interval between thetest flash (TF) and the second (conditioning) flash (CF). Theparameter is CF-DF (third or disinhibiting) flash intervals. Theopen circle (o) = 10 msec, the x = 20 msec, closed circle (.)= 50msec, triangle (A) =75 msec, square () =100 msec, and circlewith x (0) = 200 msec. The dotted curve is based upon TF-CFtrials, i.e., no third flash occurred. Each point is the outcome of20 trials.

(23' visual angle) from CF (46' visual angle) and CFfrom DF (92' visual angle). These 36 combinationsresulted from six TF-CF intervals (10, 20, 50, 75, 100,and 200 msec) paired with each of six CF-DF intervalshaving these same durations. For TF-CF only, nothird flash presented there were 20 trials at each of thesix intervals and 20 control trials on which only one ofthe two flashes was presented. There were 20 trials ateach of the 36 TF-CF-DF combinations under bothbinocular and interocular viewing. Interspersed amongthe 720 trials under each viewing condition, were 20control trials. The total number of trials for eachsubject was, therefore, 1620:

TF-CF only

TF-CFTF-CF-DF (binocular)

120 trials, 20 with eachof TF-CF intervals

20 control trials20 trials with each of 36

combinations

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DANIEL N. ROBINSON

100

50

10 20 50 75 100TF-CF INTERVAL (MSEC)

FIG. 2. Percent of 1st (Test) flashes seen by each subject withinterocular presentations as a function of the interval betweenthe test flash (TF) and the second (conditioning) flash (CF).The parameter is CF-DF (third or disinhibiting) flash intervals.The open circle (o)=10 msec, the x=20 msec, closed circle(*)=50 msec, triangle (A)=75 msec, square (E))=100 msec,and circle with x (X)=200 msec. The dotted curve is basedupon TF-CF trials, i.e., no third flash occurred. Each point isthe outcome of 20 trials.

TF-CF-DF (interocular) 20 trials with each of 36combinations

TF-CF-DF (binocular) 20 control trialsTF-CF-DF (interocular) 20 control trials.

Combinations of intervals were assigned randomly andshifts from binocular to interocular presentations wereinitiated after each block of 50 trials. Subjects weregiven approximately 100 trials per session for 16 sessions,each session lasting from 45 min to 1 h.

SUBJECTS

Three subjects were used in the experiment. All threewere given all TF-CF trials and all binocular TF-CF-

10 20 50 75 100 200TF-CF INTERVAL (msec)

FIG. 3. Surmmary of individual data plotted in Fig. 1. Eachpoint is based upon 60 trials with binocular presentations (20trials for each of three subjects). The parameter is again theinterval between second and third (CF-DF) flashes. The dottedcurve is TF-CF trials. Code is the same as in Figs. 1 and 2.

DF trials. One subject was unable to maintain fixationduring interocular presentations: consequently, she waseliminated from that phase of the research. The datareported below, therefore, were obtained from threesubjects with binocular presentations and two withinterocular presentations.

RESULTS

On the 60 control trials, two of the subjects made noerrors and one subject made two errors. Figure 1presents the results from the three subjects givenbinocular presentations and Fig. 2 shows the resultsfrom the two subjects given interocular presentations.Percent TF seen is plotted at the six TF-CF intervalsfor each interval of CF-DF (second flash-third flash).In each graph, the dotted line represents TF detectionswhen no third flash was given. Figures 3 and 4 sum-marize the individual results given in Figs. 1 and 2.Under binocular viewing, TF detection is significantlybetter at CF-DF intervals of 10 and 20 msec than underconditions lacking a DF. Furthermore, disinhibition isseen to weaken as a function of the CF-DF interval.With interocular presentations, this trend is reversed.The greater the temporal separation between CF andDF, the higher the rate of detection of TF. Thisreversal of trend is summarized in Fig. 5 in which"percent TF seen" is plotted as a function of theCF-DF interval with TF-CF as a parameter. Thisreversal under the two viewing conditions is not revealedin the effects of DF upon CF. With both binocular andinterocular presentations, the percent of CF detectedincreases as a function of the CF-DF interval as shownin Fig. 6.

The statistical reliability of these results was deter-mined by Sign-Test2" comparisons between TF detec-tion under three-flash conditions at each value of CF-DF and TF detection under two-flash conditions. Thesecomparisons were made for both binocular and inter-ocular presentations. With binocular presentations, TF

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FIG. 4. Summary of individual data plotted in Fig. 2. Eachpoint is based upon 40 trials (20 trials for each subject at eachCF-DF interval), with interocular presentations.

21 The Sign Test allows computation of the significance ofdirectional differences in pairs of observations. Thus, if a and bare compared N times, the Sign Test statistic specifies the prob-ability that a will be greater than b on any number of occasionsup to N.

256 Vol. 58

Februaryl968 DISINHIBITION WITH BINOCULAR PRESENTATIONS

is detected significantly (p 70.01) more frequently witha third flash presented 10 or 20 msec after CF than itis on TF-CF trials. With interocular presentations,this significance obtains at CE-DF intervals of 75and 200 msec. At 10 and 20 msec, TF detection issignificantly poorer with third flashes present than withonly TF and CF.

DISCUSSION

The occurrence of disinhibition under binocularviewing appears to support the view of the humanretina as a recurrent network allowing inhibition andfacilitation effects among neighboring units.'51 7 In thepresent experiments, interocular backward maskingwas readily obtained but disinhibition failed to occur;i.e., while the third flash successfully masked a pre-ceding secondflash to the other eye, it did not reducethe backward-masking effect of the second upon thefirst. Instead, systematic increases of the detection ofboth the first and second flashes occurred as the thirdwas separated by greater intervals. Interestingly, forone subject, TF detection appears to be enhanced withinterocular presentations at the longest intervals be-tween CF and DF. Thus, there remains the possibilityof facilitation at more central loci in the visual system.

Recent models intended to describe interactive pro-cesses in vision, audition, and touch2 2 assume refractoryfields concentric with regions of excitation. To accountfor backward masking, metacontrast, Mach bands,etc., such models require (a) that refractory surrounds

200 0 20 5o 75 00SNTERVAL BETWEEN 2nd AND 3rd FLASHES EMSECI

FIG. 5. First-flash detection as a function of the interval betweenthe second (CF) and third (DF) flashes with binocular (3 subjects)(left) and interocular (2 subjects) (right) presentations. Theparameter is the 1st (TF) to 2nd (CF) flash interval. Withbinocular presentations, increases of CF-DF result in decreasedTF detection. With interocular presentations, increases of CF-DFresult in increased TF detection.

22 G. v. Bk&sy, J. Opt. Soc. Am. 50, 1060 (1960).

100 200 10 20 50 75 loo

INTERVAL BETWEEN 2n AND 3d FLASHES (I.-c)

FiG. 6. Percent 2nd (conditioning) (CF) flashes seen as afunction of the CF-DF (3rd flash) interval with TF-CF intervalsas parameters (same code as for Fig. 1). Binocular functions (left)are from three subjects and interocular (right) from two subjects,each given 20 presentations at each value of TF-CF and for eachCF-DF. Interocular backward masking is apparent but weakerthan binocular backward masking.

are larger than the associated core of excitation and (b)that multiple inhibitory influences are additive. Thepresent results do not support these assumptions.Rather, the particular interaction (inhibition orfacilitation) appears to depend upon concurrent activityin the system. In pilot phases of the present research,subjects were shown first and third flashes in the absenceof a second. Under these conditions, the third maskedthe first. At the same intervals, but with a secondinserted, the first was detected. Effects of such a kindare not entirely consistent with models which imposemore rigid functions upon the sensory systems. Theeffects of stimulation are not determined solely by theposition of the stimulated regions relative to neighboringones but by the state of both the stimulated and theneighboring regions at the time of stimulation.

SUMMARY

Test-flash detection was compared under (a) two-flash and three-flash conditions and (b) binocular andinterocular presentations. It was found that, withbinocular presentations a third flash which masked apreceding second would disinhibit a first flash, other-wise masked by the second. This disinhibitorv effectdid not occur with interocular presentations in whichthe first and second flashes were presented to one eyeand the third flash to the other.

ACKNOWLEDGMENT

The author acknowledges the assistance of DonaldO'Neill in gathering and summarizing the data andassisting generally in the conduct of the research.

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