Adaptive center-surround interactions in human vision revealed during binocular rivalry

We used binocular rivalry as a psychophysical probe to explore center-surround interactions in orientation, motion and color processing. Addition of the surround matching one of the rival targets dramatically altered rivalry dynamics. For all visual sub-modalities tested, predominance of the high-contrast rival target matched to the surround was greatly reduced-a result that disappeared at low contrast. At low contrast, addition of the surround boosted dominance of orientation and motion targets matched to the surround. This contrast-dependent modulation of center-surround interactions seems to be a general property of the visual system and may reflect an adaptive balance between surround suppression and spatial summation.     

Perceptual dominance during binocular rivalry is prolonged by a dynamic surround

We examined whether dynamic stimulation that surrounds a rival target influences perceptual alternations during binocular rivalry. We presented a rival target surrounded by dynamic random-dot patterns to both eyes, and measured dominance durations for each eye’s rival target. We found that rival target dominance durations were longer when surrounds were dynamic than when they were static or absent. Additionally, prolonged dominance durations were more apparent when the dynamic surround was alternately presented between the two eyes than when it was presented simultaneously to both eyes. These results indicate that dynamic stimulation that surrounds a rival target plays a role in maintaining the current perceptual state, and causes less perceptual alternations during binocular rivalry. Our findings suggest that dynamic signals on the retina may suppress rivalry, and thus provide useful information for stabilizing perceptions in daily life.     

Eye rivalry and object rivalry in the intact and split-brain

Both the eye of origin and the images themselves have been found to rival during binocular rivalry. We presented traditional binocular rivalry stimuli (face to one eye, house to the other) and Diaz-Caneja stimuli (half of each image to each eye) centrally to both a split-brain participant and a control group. With traditional rivalry stimuli both the split-brain participant and age-matched controls perceived more coherent percepts (synchronised across the hemifields) than non-synchrony, but our split-brain participant perceived more non-synchrony than our controls. For rival stimuli in the Diaz-Caneja presentation condition, object rivalry gave way to eye rivalry with all participants reporting more non-synchrony than coherent percepts. We have shown that splitting the stimuli across the hemifields between the eyes leads to greater eye than object rivalry, but that when traditional rival stimuli are split as the result of the severed corpus callosum, traditional rivalry persists but to a lesser extent than in the intact brain. These results suggest that communication between the early visual areas is not essential for synchrony in traditional rivalry stimuli, and that other routes for interhemispheric interactions such as subcortical connections may mediate rivalry in a traditional binocular rivalry condition.     

Center-surround interactions in visual motion processing during binocular rivalry

When each eye is confronted with a dissimilar stimulus, the percept will generally alternate between the two. This phenomenon is known as binocular rivalry. Although binocular rivalry occurs at locations where targets overlap spatially, the area surrounding rivalrous targets can modulate their dominance. Here we show that during binocular rivalry of oppositely moving gratings, a surrounding grating moving in the same direction as one of the two leads to increased dominance of the opposite direction of motion in the center. This increased dominance of the opposite direction in the center was observed irrespective of the eye to which the surround was presented. Inspection of the results for different conditions reveals that the preference for the opposite direction of motion cannot be explained by a single mechanism operating beyond binocular fusion. We therefore suggest that this phenomenon is the outcome of center-surround interactions at multiple levels along the pathway of visual motion processing.     

Effect of transient versus sustained activation on interocular suppression

Switches in perceptual dominance resulting from either binocular rivalry or flash suppression likely involve some mechanism of interocular suppression, although it is unclear from past research whether different mechanisms are involved in the two cases. Using monocular, centrally fixated sinusoidal gratings surrounded by contiguous annuli of rivalrous gratings, suppression of the entire central grating was possible using either technique. However, the magnitude of the suppression was unaffected by the presence of an ipsilateral surround for flash suppression, yet, for binocular rivalry, suppression no longer occurred when the surrounds were fusible. Nevertheless, computational modeling demonstrates that the differences between the techniques may be attributable to the sustained versus transient stimulation of the contralateral surround, with the magnitude of the suppression proportional to the activation of the contralateral surround. Consistent with this, suppression extends over a greater distance at the onset of the contralateral surround than during sustained rivalry. Therefore, it is likely that perceptual dominance in both binocular rivalry and flash suppression is based on the same mechanism of interocular suppression.     

Strength and coherence of binocular rivalry depends on shared stimulus complexity

Presenting incompatible images to the eyes results in alternations of conscious perception, a phenomenon known as binocular rivalry. We examined rivalry using either simple stimuli (oriented gratings) or coherent visual objects (faces, houses etc). Two rivalry characteristics were measured: Depth of rivalry suppression and coherence of alternations. Rivalry between coherent visual objects exhibits deep suppression and coherent rivalry, whereas rivalry between gratings exhibits shallow suppression and piecemeal rivalry. Interestingly, rivalry between a simple and a complex stimulus displays the same characteristics (shallow and piecemeal) as rivalry between two simple stimuli. Thus, complex stimuli fail to rival globally unless the fellow stimulus is also global. We also conducted a face adaptation experiment. Adaptation to rivaling faces improved subsequent face discrimination (as expected), but adaptation to a rivaling face/grating pair did not. To explain this, we suggest rivalry must be an early and local process (at least initially), instigated by the failure of binocular fusion, which can then become globally organized by feedback from higher-level areas when both rivalry stimuli are global, so that rivalry tends to oscillate coherently. These globally assembled images then flow through object processing areas, with the dominant image gaining in relative strength in a form of 'biased competition', therefore accounting for the deeper suppression of global images. In contrast, when only one eye receives a global image, local piecemeal suppression from the fellow eye overrides the organizing effects of global feedback to prevent coherent image formation. This indicates the primacy of local over global processes in rivalry.     

The influence of chromatic context on binocular color rivalry: perception and neural representation

The predominance of rivalrous targets is affected by surrounding context when stimuli rival in orientation, motion or color. This study investigated the influence of chromatic context on binocular color rivalry. The predominance of rivalrous chromatic targets was measured in various surrounding contexts. The first experiment showed that a chromatic surround's influence was stronger when the surround was uniform or a grating with luminance contrast (chromatic/black grating) compared to an equiluminant grating (chromatic/white). The second experiment revealed virtually no effect of the orientation of the surrounding chromatic context, using chromatically rivalrous vertical gratings. These results are consistent with a chromatic representation of the context by a non-oriented, chromatically selective and spatially antagonistic receptive field. Neither a double-opponent receptive field nor a receptive field without spatial antagonism accounts for the influence of context on binocular color rivalry.     

Visual grouping on binocular rivalry in a split-brain observer

We studied the effects of visual grouping on binocular rivalry in the left and right hemispheres of a split-brain observer, JW. In Experiments 1 and 2, we compared responses to traditional rivalry stimuli (e.g., a red vertical grating presented to the left eye and a green horizontal grating presented to the right eye) with responses to Diaz-Caneja stimuli (i.e., half of each grating was presented to one eye and the other half to the other eye). As found for intact-brain observers, JW reported episodes of exclusive visibility of coherent stimuli (e.g., of a red vertical grating alternating with a green horizontal grating) with Diaz-Caneja stimuli that were fewer and briefer than with traditional stimuli. This occurred in both hemispheres, demonstrating that during binocular rivalry, contours from one eye can be grouped with those of the opposite eye to create a coherent percept, even in the isolated hemispheres of the split-brain observer. In Experiment 3, we studied the tendency of rivalry in adjacent patches to synchronize. When both patches were in one of JW's hemifields, rivalry synchronized for similarly oriented stimuli, the same as happened for intact-brain observers. When the patches were in JW's opposite hemifields, there was no synchronizing of rivalry, unlike what happened for intact-brain observers. This suggests that rivalry processed in JW's two hemispheres is independent. We conclude that rivalry is processed fully within each hemisphere.     

Independent binocular integration for form and colour

Although different features of an object are processed in anatomically distinct regions of the cerebral cortex, they often appear bound together in perception. Here, using binocular rivalry, we reveal that the awareness of form can occur independently from the awareness of colour. First, we report that, if both eyes briefly view a grating stimulus prior to the presentation of the same grating in one eye and an orthogonal grating in the other, subjects tend to report perceptual dominance of the non-primed grating. The primer was most effective when it was similar in orientation, spatial frequency and spatial phase to one of the rival images. Next, we showed that the process underlying the binocular integration of chromatic information was selectively influenced by the colour of a previously presented stimulus. We then combined these paradigms by using a primer that had the same colour as one rival stimulus, but the same form as the other stimulus. In this situation, we found that rival stimuli differing in form and colour can sometimes achieve states of dominance in which the chromatic information from one eye's image combines with the form of the other eye's image temporarily creating a binocular impression that corresponds with neither monocular component. Finally, we demonstrated that during continuous viewing of rival stimuli differing in form and colour, chromatic integration could occur independently of form rivalry. Paradoxically, however, we found that changes to the form of the stimulus had more of an influence on chromatic integration than on form rivalry. Together these phenomena show that the neural processes involved in integrating information from the two eyes can operate selectively on different stimulus features.     

Exogenous attention and endogenous attention influence initial dominance in binocular rivalry

We investigated the influence of exogenous and endogenous attention on initial selection in binocular rivalry. Experiment 1 used superimposed +/-45 degrees gratings viewed dioptically for 3s, followed by a brief contrast increment in one of the gratings to direct exogenous attention to that grating. After a brief blank period, dichoptic stimuli were presented for various durations (100-700 ms). Exogenous attention strongly influenced which stimulus was initially dominant in binocular rivalry, replicating an earlier report (Mitchell, Stoner, & Reynolds. (2004). Object-based attention determines dominance in binocular rivalry. Nature, 429, 410-413). In Experiment 2, endogenous attention was manipulated by having participants track one of two oblique gratings both of which independently and continuously changed their orientations and spatial frequencies during a 5s period. The initially dominant grating was most often the one whose orientation matched the grating correctly tracked using endogenous attention. In Experiment 3, we measured the strength of both exogenous and endogenous attention by varying the contrast of one of two rival gratings when attention was previously directed to that grating. The contrast of the attended grating had to be reduced by an amount in the neighborhood of 0.3 log-units, to counteract attention's boost to initial dominance. Evidently both exogenous and endogenous attention can influence initial dominance of binocular rivalry, effectively boosting the stimulus strength of the attended rival stimulus.     

The motion-induced position shift depends on the visual awareness of motion

Visual motion signals distort the perceived positions of briefly presented stimuli; a briefly-flashed, stationary stimulus appears spatially displaced in the direction of a nearby motion. The present study examined the role of the visual awareness of motion in the motion-induced position shift by using exclusive dominance and suppression of binocular rivalry. Observers dichoptically viewed a flickering radial checkerboard and two sinusoidal gratings that drifted vertically in opposite directions. When observers viewed exclusively either the checkerboard or motion stimulus, two horizontal lines were flashed, one for each side of the rivalry stimulus. During the exclusive dominance of the grating motion, the lines appeared to shift in the directions of the nearby motions. The position shift was identical to that during non-rivalry, monocular viewing of the motion stimulus. However, when the grating motions were completely suppressed, no position shift was observed. These results demonstrate that the motion-induced position shift depends on the visual awareness of motion.     

Center-surround inhibition and facilitation as a function of size and contrast at multiple levels of visual motion processing

Visual context often plays a crucial role in visual processing. In the domain of visual motion processing, the response to a stimulus presented to a neuron's classical receptive field can be modulated by presenting stimuli to its surround. The nature of these center-surround interactions is often inhibitory; the neural response decreases when the same direction of motion is presented to center and surround. Here we use binocular rivalry as a tool to study center-surround interactions. We show that magnitude of surround suppression varies as a function of luminance contrast and surround width. Increasing the size of surround motion increased surround suppression at high contrast. Furthermore, large, high-contrast surrounds facilitated opposite-direction motion in the center. For stimuli presented at low contrast, surround suppression peaked at a smaller surround width. In addition, we provide evidence that surround inhibition occurs at multiple levels of visual processing: Surround inhibition in motion processing is likely to originate from both monocular and binocular processing stages.     

Increasing depth of binocular rivalry suppression along two visual pathways

Binocular rivalry refers to the alternating perception that occurs when the two eyes are presented with incompatible stimuli: one monocular image is seen exclusively for several seconds before disappearing as the other image comes into view. The unseen stimulus is physically present but is not perceived because the sensory signals it elicits are suppressed. The neural site of this binocular rivalry suppression is a source of continuing controversy. We psychophysically tested human subjects, using test probes designed to selectively activate the visual system at a variety of processing stages. The results, which apply to both form and motion judgements, show that the sensitivity loss during suppression increases as the subject's task becomes more sophisticated. We conclude that binocular rivalry suppression is present at a number of stages along two visual cortical pathways, and that suppression deepens as the visual signal progresses along these pathways.     

A binocular rivalry study of motion perception in the human brain

The relationship between brain activity and conscious visual experience is central to our understanding of the neural mechanisms underlying perception. Binocular rivalry, where monocular stimuli compete for perceptual dominance, has been previously used to dissociate the constant stimulus from the varying percept. We report here fMRI results from humans experiencing binocular rivalry under a dichoptic stimulation paradigm that consisted of two drifting random dot patterns with different motion coherence. Each pattern had also a different color, which both enhanced rivalry and was used for reporting which of the two patterns was visible at each time. As the perception of the subjects alternated between coherent motion and motion noise, we examined the effect that these alternations had on the strength of the MR signal throughout the brain. Our results demonstrate that motion perception is able to modulate the activity of several of the visual areas which are known to be involved in motion processing. More specifically, in addition to area V5 which showed the strongest modulation, a higher activity during the perception of motion than during the perception of noise was also clearly observed in areas V3A and LOC, and less so in area V3. In previous studies, these areas had been selectively activated by motion stimuli but whether their activity reflects motion perception or not remained unclear; here we show that they are involved in motion perception as well. The present findings therefore suggest a lack of a clear distinction between 'processing' versus 'perceptual' areas in the brain, but rather that the areas involved in the processing of a specific visual attribute are also part of the neuronal network that is collectively responsible for its perceptual representation.     

Shifting eye balance using monocularly directed attention in normal vision

In binocular vision, even without conscious awareness of eye of origin, attention can be selectively biased toward one eye by presenting a visual stimulus uniquely to that eye. Monocularly directed visual cues can bias perceptual dominance, as shown by studies using discrete measures of percept changes in continuous-flash suppression. Here, we use binocular rivalry to determine whether eye-based visual cues can modulate eye balance using continuous percept reporting. Using a dual-task versus single-task paradigm, we investigated whether the attentional load of these cues differentially modulates eye balance. Furthermore, both color-based and motion-based cue stimuli, non-overlaid and peripheral to the rivalry grating stimuli, were used to determine whether shifts in eye balance were stimulus specific. Aligned to cue stimulus onset, time series of percept reports were constructed and averaged across trials and participants. Specifically, for the monocular attention conditions, we found a significant shift in eye balance toward the cued eye and a significant difference in the time taken to switch from the dominating percept, regardless of whether the attention stimuli is color based or motion based. Although we did not find a significant main effect of attentional load, we found a significant interaction effect between the attentionally cued eye and attentional load on the shift in eye balance, indicating an influence of monocular attention on the shift in eye balance.     

Attending to auditory signals slows visual alternations in binocular rivalry

A previous study has shown that diverting attention from binocular rivalry to a visual distractor task results in a slowing of rivalry alternation rate between simple orthogonal orientations. Here, we investigate whether the slowing of visual perceptual alternations will occur when attention is diverted to an auditory distractor task, and we extend the investigation by testing this for two kinds of binocular rivalry stimuli and for the Necker cube. Our results show that doing the auditory attention task does indeed slow visual perceptual alternations, that the slowing effect is a graded function of attentional load, and that the attentional slowing effect is less pronounced for grating rivalry than for house/face rivalry and for the Necker cube. These results are explained in terms of supramodal attentional resources modulating a high-level interpretative process in perceptual ambiguity, together with a role for feedback to early visual processes in the case of binocular rivalry.     

Both monocular and binocular signals contribute to motion rivalry

There is an ongoing debate on whether binocular rivalry involves competition among monocular cells or binocular cells. We investigated this issue psychophysically with two specially designed test stimuli. One test stimulus contained monocular motion signals but greatly reduced binocular motion signals, while the other contained binocular motion signals but no monocular motion signals. For comparison, we also employed a normal rivalrous control containing both monocular and binocular motion signals, and a non-rivalrous flicker-noise control with neither monocular nor binocular motion signals. We found that binocular rivalry for the two test stimuli was significantly reduced compared with the normal rivalrous control, but not completely eliminated compared with the non-rivalrous control. Therefore, both monocular and binocular motion signals appear to contribute to motion rivalry, suggesting that motion rivalry must involve competition among both monocular and binocular cells.     

Stimulus flicker alters interocular grouping during binocular rivalry

When the two eyes are presented with sufficiently different stimuli, the stimuli will engage in binocular rivalry. During binocular rivalry, a subject's perceptual state alternates between awareness of the stimulus presented to the right eye and that presented to the left eye. There are instances in which competition is not eye-based, but instead takes place between stimulus features, as is the case in flicker and switch rivalry (F&S). Here we investigate another such instance, interocular grouping, using a Diaz-Caneja type stimulus in conjunction with synchronous stimulus flicker. Our results indicate that stimulus flicker increases the total duration of interocularly bound percepts, and that this effect occurs for a range of temporal flicker frequencies. Furthermore, the use of contrast-inversion flicker causes a decrease of total dominance duration of the interocularly bound percepts. We argue that different flickering regimes can be used to differentially stimulate lower and higher levels of visual processing involved in binocular rivalry. We propose that the amount of interocularly combined pattern-completed percept can be regarded as a measure of the level at which binocular rivalry is resolved.     

Temporal frequency and contrast tagging bias the type of competition in interocular switch rivalry

The nature of competition underlying perceptual alternations in binocular rivalry remains controversial. Interocular swapping of rivalrous stimuli can result in either slow irregular perceptual alternations that bridge multiple interocular switches or fast regular alternations that are time locked to the stimulus exchanges. We labeled either the inputs to the eyes or the individual rivalrous stimuli using temporal frequency and contrast tagging. Tagging of eye-of-origin signals enhanced the fast regular perceptual alternations associated with eye rivalry, while stimulus tagging shifted perception towards slow irregular alternations characteristic of stimulus rivalry. Thus, the type of competition in binocular rivalry can be biased based on additional cues in the visual inputs. The results are consistent with a model in which the brain combines information across multiple visual features to resolve ambiguities in visual inputs.     

Binocular rivalry suppression disrupts recovery from motion adaptation.

The motion aftereffect (MAE) lasts longer when the test period does not immediately follow adaptation, a phenomenon called storage. Does storage of the MAE occur if the test target is present but rendered phenomenally invisible owing to the presence of a rival target presented to the other eye during the storage period? Our experiment addressed this question. Following adaptation to a drifting grating, an intervening period preceded testing with a stationary grating. During this period, the adapted eye either viewed the test target immediately or was occluded, and the unadapted eye either viewed a high-contrast rival target or was occluded. Thus four conditions were employed. The duration of the residual MAE was found to be longer for the rivalry condition (grating and rival target viewed) than for the normal MAE condition (grating viewed), and comparable to that in the stored MAE condition (both eyes occluded). Thus, the MAE is stored when the test target is rendered invisible due to binocular rivalry, indicating that a suppressed target is ineffective at promoting decay of the MAE. So while suppression does not prevent information about the adapting grating from reaching the site of generation of the MAE (Lehmkuhle & Fox, 1975), it can prevent information about the test target from reaching the site of the stored MAE. Current models attribute the MAE to reduced responsiveness of direction-selective cortical neurons (Sutherland, 1961; Barlow & Hill, 1963). Thus, storage should reflect a differential return of these adapted cells to preadapted response levels, dependent on postadaptation stimulation.(ABSTRACT TRUNCATED AT 250 WORDS)