A monocular contribution to stimulus rivalry

Abstract

When corresponding areas of the two eyes view dissimilar images, stable perception gives way to visual competition wherein perceptual awareness alternates between those images. Moreover, a given image can remain visually dominant for several seconds at a time even when the competing images are swapped between the eyes multiple times each second. This perceptual stability across eye swaps has led to the widespread belief that this unique form of visual competition, dubbed stimulus rivalry, is governed by eye-independent neural processes at a purely binocular stage of cortical processing. We tested this idea by investigating the influence of stimulus rivalry on the buildup of the threshold elevation aftereffect, a form of contrast adaptation thought to transpire at early cortical stages that include eye-specific neural activity. Weaker threshold elevation aftereffects were observed when the adapting image was engaged in stimulus rivalry than when it was not, indicating diminished buildup of adaptation during stimulus-rivalry suppression. We then confirmed that this reduction occurred, in part, at eye-specific neural stages by showing that suppression of an image at a given moment specifically diminished adaptation associated with the eye viewing the image at that moment. Considered together, these results imply that eye-specific neural events at early cortical processing stages contribute to stimulus rivalry. We have developed a computational model of stimulus rivalry that successfully implements this idea.

Keywords: ambiguous stimuli; binocular rivalry; bistable perception; flicker-and-swap rivalry.

Fig. 1.

Experiment 1. Effect of stimulus-rivalry suppression on formation of the TEAE. (A) Schematic of colored rival gratings (Left) and achromatic test grating (Right). The test grating matched one of the rival gratings in orientation and spatial frequency but covered only one-half of the stimulus area, either left or right. The observer’s responses (left vs. right) following each test presentation guided an adaptive procedure to an estimate of the observer’s contrast detection threshold. (B) Stimulus-rivalry presentation sequence. (C) Detection thresholds following stimulus rivalry (yellow) were compared with thresholds following exposure to two other display sequences, both constructed by omitting part of the stimulus-rivalry sequence. In the One Orientation condition (blue), exposure to the adapting orientation matches that produced in the Stimulus Rivalry condition, but in the One Eye condition (orange), exposure to the adapting orientation is reduced relative to stimulus rivalry. LE, left eye; RE, right eye. (D) TEAE (y axis) in the Stimulus Rivalry (SR) condition is significantly weaker than that in the One Orientation (OO) condition but matches the TEAE in the One Eye (OE) condition. Both results indicate that stimulus-rivalry suppression attenuates contrast adaptation.

Fig. 2.

Experiment 2. Effect of stimulus-rivalry suppression on adaptation of monocular neurons. (A) During ordinary stimulus rivalry, perceptual dominance is distributed approximately equally across the two eyes (Upper), precluding differential accumulation of monocular adaptation in the processing streams of the left and right eyes. A designated eye can be made to receive the dominant image for a larger proportion of the time by online adjustment of the eye-exchange cycle in response to perceptual reports (Lower), thus allowing the possibility of differential accumulation of monocular adaptation. (B) During ordinary stimulus rivalry (Top row), the eye-exchange cycle was symmetrical, but during biased stimulus rivalry (Middle and Bottom rows), each period of the exchange cycle consisted of a short interval viewing one eye/orientation combination and a long interval viewing the opposite eye/orientation combination. By selecting whether the strategy illustrated in the Middle row or in the Bottom row was used, it was possible to force the dominant stimulus to be imaged within a designated eye for a relatively large proportion of the total viewing duration of stimulus rivalry. (C) Extended periods of stimulus rivalry were followed by binocular rivalry between the same two rival images. Because binocular-rivalry dominance durations are influenced by monocular adaptation, they can reveal buildup of differential monocular adaptation during biased stimulus rivalry.

Fig. 3.

Results of experiment 2. Perceptual dominance of the eye that received the dominant image for a larger proportion of the time during stimulus rivalry (SR) was reduced during subsequent binocular rivalry (BR), both in overall ratio (A) and in individual durations (B), indicating that monocular adaptation associated with this eye was elevated, compared with the eye that mostly received the suppressed image during stimulus rivalry. (C) This difference in predominance between the two eyes wore off over the course of binocular-rivalry viewing, consistent with an adaptation-based account. (D) Ocular imbalance in binocular-rivalry dominance correlated on an observer-to-observer basis with the magnitude of the imposed imbalance in ocular dominance during stimulus rivalry.

Fig. 4.

Accommodating the present findings in models of stimulus rivalry. (A) This schematic shows an existing stimulus-rivalry model developed by Wilson (3). The first stage (black) is a standard binocular-rivalry model with orientation-tuned monocular populations (striped circles) that interact via mutual inhibition (connecting lines with dots at the ends), and to that is added a second stage consisting of binocular, eye-independent populations (blue), again connected via mutual inhibition. In this hybrid model, inhibition at the monocular stage is silenced during stimulus rivalry, leaving only competition at the eye-independent stage. This exclusion of between-eye inhibition explains stimulus rivalry’s apparent immunity to eye swaps but does not fit well with the present evidence that stimulus rivalry modulates monocular neurons. (B) Starting from the same binocular-rivalry model, we extended it with within-eye cross-orientation inhibition (purple) and between-eye iso-orientation inhibition (orange). This model variant still explains stimulus rivalry, and it is consistent with our findings because it does not exclude competition at a monocular stage. Eqs. 1–3 in Methods define the components and interactions comprising this model, and those can be summarized as follows. Activity levels in the orientation-tuned populations are indicated by variable names E_{orientation,eye} (e.g., E_45,L for the population sensitive to right-tilted gratings presented to the left eye). Each of these populations receives three kinds of inhibition, indicated by I_{orientation,eye} (e.g., I_−45,L for inhibition arising from the population sensitive to left-tilted gratings presented to the left eye), corresponding to this figure’s black, purple, and orange lines. Each of these populations furthermore exhibits self-adaptation, indicated by H_{orientation,eye}. (C) Model of B exhibits stimulus rivalry’s characteristic periods of stimulus dominance that span several eye swaps, showing that relocation of competition to a binocular stage is not necessary to explain stimulus rivalry. a.u., arbitary units.