Effect of binocular rivalry suppression on the motion aftereffect

EFFECT

OF BINOCULAR RIVALRY SUPPRESSION THE MOTION AFTEREFFECT

ON

STEPHEN W. LEHMKUHLE and ROBERTFox Department of Psychology, Vanderbilt University. Nashville. Tennesser 371-W.U.S.4

(Recriced 17 July 1974; in

rerisedfbm

31 Ocroher 1974)

Abstract-The relative loci within the visual system of the site of the motion aftereffect (MAE) and the site of binocular rivalry suppression was inferred by measuring the magnitude of the MAE when the inducing motion was phenomenally suppressed for > 10 per cent of the inspection period. The MAE magnitude was a function of the duration of physical impingement of the inducing stimulus; the state of suppression exerted no effect. therebv implying that the site of suppression does not occur before the site of the MAE. This result. together with other data. is interpreted to mean that the site of suppression is cortical.

ISTRODUCTION

When naive observers first experience binocular rivalry they are amazed by the fact that suppression renders a strong stimulus Invisible for several seconds. More skeptical observers may suspect the experimenter of abetting the process by physical removal of the stimulus. After reassurance that the suppressed stimulus remains present and impinging upon the retina. the next question that frequently arises is. “Where has the suppressed stimulus gone?” The answer, “It continues to reside in the nervous system,” while undoubtedly correct, is necessarily incomplete. One step toward a more adequate answer about rhe fate of the suppressed stimulus is provided by experiments that measure the sensitivity of the suppressed state to new stimulus information. The results of several experiments have supported two related conclusions: (a) Sensitivity is reduced during suppression. and (b) the reduction m sensitivity applies nonselectively to all categories of stimulation independent of their similarity to the rivalry-inducing stimulus (e.g., Blake and Fox, 1974a; Collyer and Bevan, 1970: Fox and Check. 1966, 1972; Lack, 1973; Wales and Fox, 1970). These characteristics of the suppression state imply that an active inhibitory process at some stage within the visual system prevents the impinging stimulus from reaching the stage of phenomenal awareness, thereby producing rivalry suppression. The stage where inhibition occurs, however, is more difficult to specify. not only because many plausible sites can be envisioned but also because psychophysical methodology is limited in its ability to identify specific stages within the system where significant interaction takes place. The method used in the present experiments allows us to infer the locus of suppression relative to the stages where other visual phenomena are thought to occur. The basic idea is to determine the effect of rivalry suppression on the magnitude of aftereffects produced by prolonged visual stimulation. The magnitude of many aftereffects, such as tilt adaptation and contour displacement (e.g. KGhler and Wallach. 1944). increase up to a limit with the amount of time they are seen. In ideal form. the question is. “Would an aftereffect occur if the inducing stimulus is not seen:‘” The ideal conditions implied by that question cannot be met. however.

for it is not possible to suppress an inducing stimulus for the complete duration of the observation period. Nevertheless. it is possible substantially to reduce the amount of time the stimulus is phenomenally present while leaving unchanged the amount of time the stimulus is physically impinging upon the retina. If suppression precedes the locus of the aftereffect, then the magnitudeofthealiereffectshouldcorrespondto theamount of time the stimulus was phenomenally present, on the assumption that suppression interrupts transmission of the adapting stimulation. If the locus of suppression does not occur before the site of the aftereffect, the magnitude of the aftereffect should correspond to the amount of time the inducing stimulus was physically present. In a recent experiment using this technique, Blake and Fox (1974b) determined the effect of rivalry suppression on two aftereffects produced by adaptation to a grating pattern. The aftereffects were elevation in threshold contrast and shift in spatial frequency. The failure of suppression to alter the magnitude of these two aftereffects was interpreted to mean that the locus of suppression does not occur before the site of these aftereffects. Extending that logic to the present experiments, we measured the effect of suppression on the magnitude of the waterfall illusion (Wohlgemuth, 1911) or, in more contemporary terms, the motion aftereffect. METHOD Apparatus

The basic apparatus was a large haploscope constructed from optic bench components and enclosed in a lightproof housing. The viewing port of the housing was fitted with a biteboard, head rest, and trial frames. each adjustable in three dimensions. The trial frames carried artiikal pupils whose I-mm apertures were located in protruding conical portions so that they could be located as close as possible to the cornea. If corrective lenses were needed by the subject. they were inserted in the trial frames behind the artifical pupils. The pivot points of the major arms of the haploscope were located under the pivot points of the observer’s eyes; the convergence angle of the arms and the distance between pivot points were independently adjustable. Stimulus holders on the haploscope permitted vernier adjustment in I and .I coordinates. At the end of each haploscope arm which were 1m in length. a cathode ray tube (CRT) was mounted in an enclosed housing. The CRT on the right-eye arm contained

the display used for the induction of the motion aftererect. hereafter called the &lAE stimulus. This displa) was a \er[~tally oriented sinusoidal grating with spatial frequent) -_ ‘.4 c deg. mean luminance 1.0 cd m’, and contrast 0.1~. The display was produced by standard methods. .A I-mHz rriangular wave inserred into the vertical asis of the oscilloscope generated a raster; :-axis modulation of the rss[er of the sine wave produced the grating. To introduce controlled linsar motion of the grating. the phase of the :-~.xu signdl wascontinually shifted by continuous rotarion ofa synchroresol\cr; varymg the speed of the motor driving the synchro-resolver varied the velocity of grating movement. The velocity of the pattern used in the experiments was held constant at I deg, sec. To reduce the size of the CRT displa). a field stop, consisting of a 6.5’ x 8.5’ rectangular sheet of translucent Plexiglas, was placed immediately in front of the CRT. The CRT display could be seen through a square I _ aperture in the center of the field stop. The field stop icas evenly transiiluminated by an array of small incandescent lamps. The mean luminance level was 0.6 cd,‘m’. To facilitate fusion, vertical black contours 7.5’ wide separated by 72.5’were located on the left and right Hanks of the aperture. The CRT on the left-eye arm of the haploscope displayed the stimulus for inducing rivalry, hereafter called the suppression stimulus. This stimulus consisted of a horizontally oriented square-wave grating with spatial frequency 3.0 c’ deg. mean luminance Z0cd,‘m2. and contrast 0.74. The contours were phase-shifted 180’ at the rate of 1 Hz. thcrebc producing an apparent up-and-down motion of the display. A field stop identical in all characteristics to the right-eye field stop was located in front of the left-eye CRT. ;\n electronic shutter in the optic path could be dctic-ated to block the suppression stimulus from view. The configuration and parameters of the suppression stimulus and the MAE stimulus were determined through preliminary tvork so as to fuifill two criteria: (1) The MAE stimulus was suppressible for at least 50 per cent of an observation period, and (2) the MAE stimulus was capable of generating a reasonably strong afteretlect. To quantify the magnitude of the aftereffect. the subject reported on the apparent velocity and duration of the aftereffect by moving a throttlelike switch connected to a stripchart recorder. The pen deflection of the recorder provided a graphic record of the subject’s estimate of the aftereffect velocity and duration. For the experimental conditions involving rivalry. the subject continuously reported on the states of dominance and suppression using a lever switch, the output of which was connected to a magnetic tape recorder so that a psrmanent record of the subject’s pattern of rivalry fluctuations wasobtained. For the experimental condition called “rivalry simulation”. which involved intermittent presentation of the M.AE display in a temporal pattern that simulated the course of rivalry suppression, the tape record was us4 10 control the changes in the displays necessary for this condition. During the simulated dominance phases the MAE display was presented while the suppression stimulus was replaced by a homogeneous raster; during simulated suppression phases the suppression stimulus was presented while the MAE display was replaced by a raster. A set of timing and logic units automatically controlled [he events associated with each experimental trial. These events included the initiation and cessation of the MAE display and activation of the shutter that eliminated the suppression stimulus from view. Luminance measurements were made at the beginmng and end of each session with a Pritchard spot photometer. The velocity of the MAE display was monitored via a photocell that counted contour frequency. Subjects

The three subjects were males in their early twenties with well corrected vision. Two subjects, BLK and FMG. were unaware of the theoretical implications of the evperimenl

ESPERI\IE\T

1

The purpose of this experiment was to determine for each of the three subjects the shape of the function bet~vezn duration of inspection and the afteretrrct duration. From this data it would be possible to determine t~vo inspection durations for each subject that occurred on the linear portion of the function, one of which produced an aftereffect duration twice as long as that produced by the other. These values were needed for experiment 2, the main experiment. Nine inspection durations were used. ranging from IO to 90 set in IO-set increments. The order of presentation of durations was quasi-random for each subject. At least 90 set intervened between each observation period. The conditions for observing the aftereffects closely resembled those used in experiment 2. The left-eye and right-eye fields were aligned for fusion. tvith the left-e\e field containing a homogeneous raster in place of the suppression stimulus. The MAE displa) completely dominated the left-eye view. At the end of the inspection period pattern motion stopped. the leftcys view was blocked by the shutter. and the subject immediately began reporting on the course of the aftereffect. Prior to formal data collection the subjects received extensive practice in observing and reporting upon the aftereffects. RSlllIS In Fig. 1. aftereffects are plotted as a function of inspection duration. Consistent with much previous research, the relationship between duration and inspection time is approximately linear up to about 60 sec. at which time saturation begins to occur. Although subjects reported on both the velocity and the duration of the aftereffect, it was apparent that estimates of velocity and duration were quite similar SO it was considered sufficient to use duration alone as a dependent measure.

x

Q A

i i

1

1

f

,

10

20

30

40

INSPECTICN

5-o

/

I

I

a0

70

80

1

ty

DURATION :sec

i

Fig. I. The relationship betueen the durarlon of the motion aftereffect (MAE)and the duration of inspection (one obserbation for each inspection duration\ for each subject.

ss7

E&t of binocular rivalry suppression

T.tble I. .\waged ovrtr observation periods. the table shous the total time the M,AE displa! was visible. the percentage of ttme visible. the mean duratton of dominance phases. and the mean duration of suppression phases for each of the three subjects

Subject

Total Mr\E dominance time (SK)

ESPERIME\T

Per cent MAE dominance

?

The design of this esperiment used four conditions. These were (1) Condition D, where inspection of the MAE display occurred for an inspection duration D in the absence of rivalr!: (2) Condition 30. where inspection of the MAE dtspla? occurred for an inspection duration twice the length of D in the absence of rivalry; (3) Rivalry. in which the MAE display was present for 3D but was phenomenally suppressed for at least 50 per cent of that viewing period; and (4) Rivalry Simulation. in which the MAE display was intermittently presented over the time period 2D following the exact temporal pattern exhibited by the subject during the rivalry condition. If rivalry suppression had no effect upon the duration oE the aftereffect. then no difference would be anticipated between the rivalry condition and the ZD condition. Conversely. if suppression did disrupt the production of the aftereffect. then it is likely that the aftereffect under the rivalry condition would be equal to that obtained either under the rivalry simulation condition or under the D condition. The four conditions were run in the repeated order D, 70. Rivalry. and Rivalry Simulation until five aftere&cts had been obtained under each condition. Based upon the results of experiment 1, the values of D chosen for each subject were: For SWL, D = 30sec: for BLK. D = ‘Osec; for FMG. D = 7Osec. A rest period of 2 min intervened between each trial and a 15. min rest period occurred in the middle of the session. the length of which was approv 2 hr. Refore collecting formal data. the subjects received extensive practice in reporting on rivalry fluctuations. They were instructed to maintain a conservative criterion such that if any portion of the MAE stimulus appeared they were to signal a change in state. All three subjects stated that the rivalry between the fields was generailv clearcut and unitary. characterized bv a minimum oi intermediate states. During the training period considerable attention was devoted to aligning the fields for each subject so that fusion could be easily achieved and maintained. The subjects were instructed to report any instance where there was even a momentary loss of fusion.

The effsctiveness of rivalry suppression in rendering invisible the MAE display for a substantial proportion of the inspection period in the binocular rivalry condition can be assessed from the data in Table I, which shows the average amount of dominance and suppression times exhibited by each of the three subjects. In every case the MAE display was seen for less than 50 per cent of the time.

?Jean dominance phase duration (set)

?&an suppression phase duration (=I

In Fig. 2 the durations of the MAE under the four conditions (D. 20. Rivalry, and Rivalry Simulation) are shown for each of the three subjects. It can be seen that the MAE obtained under the ZD condition and undsr SD

r

2D

R,“ILRY

RI”&RY MIMIC

RWILRY

RlVALRY HlMlC

CONOITION

S-

0

20 CONDITION

CONDITION

Fig. 2. The duration of the MAE for the four conditions oi

experiment Z for each subject. The condition labelled .‘rivalry mimic” on each histogram is the condition referred to as “rivalry simulation” in the text. The confidence intervals represent standard errors for each mean.

the riralry condition are quite similar: the difierenccs between these two conditions do not approach sic&i-

r?SpOn= t0 ;I light increment is impaired during suppreSSiOn (Baran) and Hallden. 19-E: Richards. 1966). cance. The difference bemeen the D and 20 condiiions The interprrtatlon of these dat;l. hoiveier. is made is significant for each of the three obserlsrs. There is complex b> other experiments that h;!tc not found this some tendencv for the rivalry simulation condition to inhibition of the pupillar! contracuoc rcsponje. eb?n >isld a smaller aftereffect than the D condition : this 1s though rather sensitive measurement techniques \vere not surprising since the physical intermittench of the employed (Bradshaw. 1969: Lowe and Ogle, 1966). simulation condition would permit an opportunity for Recent neurophysiolopicsl evidence ior inhibitor) some decay of the aftereffect to occur. interaction in the lateral geniculate oi’ :hs cat (Sanderson. Bishop and Darian-Smith, 1971 : Smger. 1970) has

It is clear from these results that phenomenal suppression exerts no influence upon the magnitude of the motion aftereffect. The conclusion following naturally from that fact must be that suppression does not occur before the site in the visual system where the aftereffect occurs. With respect to the site of the motion aftereffect. several lines of evidence. such as interocular transfer (e.g. Barlow and Brindle:)-, 3963; Scott and Wood. 19z6). induction of the aftereffect using stereoscopic techniques that bypass monocular pathways (e.g.. Anstisand Moulden, 1970: Papert. 1961).and the compatibility of psychophysical data with neurophysiological evidence (e.g. Breltmeyer. 1973; Sekuler and Pantie. 1967: Sutherland, 1961) support the view that the aftereffect arises from the responx of cortical neurons specialized for the detection of motion. From the assumption that the motion aftereffect has a cortical locus. it then follows that the site of suppression is also cortical. Further evidence for the cortical site of suppression comes from the experiment of Blake and Fox (1971b). which showed that suppression eserts no influence on aftereffects associated with adaptation to stationary grating patterns. Since there is considerable evidence. both psychophysical and neurophvsiological, indicating that the site of these aftereffects IS cortical, the necessary conclusion is that the site of rivalry suppression must also be cortical. The identification of suppression with a cortical site is of particular interest because there are grounds for suspecting that the site of suppression could occur at a more peripheral stage in the visual system. One consideration is that the nonselective character of the suppression state would be consistent with the idea that suppression occurs at an early. precortical stage where many different kinds of signals share common pathbvahs. The hypothesis of a precortica! site of suppression must be associated with a model of the rivalr] process that assumes that the site of suppression can be separated from a site or stage where a decision to initiate suppression is made. This decision-making stage would necessarily be at a higher level of the systern where inputs from both eyes can interact and be analyzed. but there is no reason why suppression

would also have to be localized

at that stage. Indeed.

of the evidence for extensive centrlfuga! connections (e.g. studies of the corticogeniculate pathways bq’ Hollgnder, 1974). it is reasonable to suppose that suppression could occur at a separate lower stage in the system. The present evidence does not. of course. make it necessary to abandon the idea that rivalry involves such separate stages, but it does place the constraint that both stages reside at cortical levels. Some evidence for a peripheral site for suppression is provided h\ reports that the pupi!!ar\ contr;Iction in view

led to the suggestion that :his interaction might express itself in binocular rivalry (Blakcmore. !\srscn and Zangwill. 1971). But since the i::hibition is indrpendent ofcortical intluence. as demonstrated bi ablation and by h>Tothcrmia. the analksiz of inputs from both eyes and the decision to im&re suppression uould have to occur in the geniculats There are rcasons. however. for doubting that geniculate neurons possess the characteristics required for performing such an analysis. The failure: of suppression to intluence the courx of either stationar! or moving pattern aftereffects argues against the grn.sica! methods alone. This is so because the small number of psychophysical techniques available for inferentially partitioning the visual system. such as pressure blinding and random element stereograms. al xv?!! as the tech-

nique we have used here. rsquire the assumption of serial processing of information. and the compleslt? of cortical interactions makes that assumption dificult to defend. Thus. the results of this experiment can Supp!!. only a partial answer to the question. -Where has the

suppressed stimulus gone’?

Holliinder H. (19-4) ProJections irom diencephalon in the squirrel monks)

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