Binocular rivalry provides a valuable means to study how sensory processing gives rise to subjective experiences because it involves a changing percept without any change in the visual stimulus. An important question, however, is whether visual awareness is necessary for binocular rivalry to emerge. To address this question, we presented conflicting random dot motion stimuli in the two eyes at luminance contrasts around perceptual threshold. We asked subjects to report continuously, via button presses, if they noticed any kind of motion in the display (be it coherent or not) and indicate which direction of motion they thought was dominant at any given instant even if they were unaware of any motion in the display. We biased the competition between the two dichoptic stimuli by changing the motion coherence in one eye while keeping it fixed in the other to test if this induced predictable changes in rivalry dynamics. We also probed the strength of the interocular suppression. Our data show that binocular rivalry continues even if subjects claim complete absence of visual motion awareness. This remarkable dissociation between visually guided behavior and visual awareness resembles the dissociation seen in other phenomena, such as blindsight and visual masking. Fluctuations in awareness that did occur were temporally linked to the dominance switches in a manner that is consistent with adaptation reciprocal-inhibition models of binocular rivalry.
It is often assumed that decision making involves neural competition, accumulation of evidence "scores" over time, and commitment to a particular alternative once its scores reach a critical decision threshold first. So far, however, neither the first-to-threshold rule nor the nature of competition (feedforward or feedback inhibition) has been revealed by experiments. Here, we presented two simultaneously flashed targets that reversed their intensity difference during each presentation and instructed human subjects to make a saccade toward the brightest target. All subjects preferentially chose the target that was brightest during the first stimulus phase. Unless this first phase lasted only 40 ms, this primacy effect persisted even if the second, reversed-intensity phase lasted longer. This effect did not result from premature commitment to the initially dominant target, because a strong target imbalance in the opposite direction later drove nearly all responses toward that location. Moreover, there was a nonmonotonic relation between target imbalance and primacy: increasing the target imbalance beyond 40 cd/m(2) caused an attenuation of primacy. These are the hallmarks of hysteresis, predicted by models in which target representations compete through strong feedback. Reaction times were independent of the choice probability. This dissociation suggests that target selection and movement initiation are distinct phenomena.
It is generally believed that percept alternations in binocular rivalry result from the interplay between mutual inhibition and slow adaptation of the competing percepts. This view is supported by growing evidence that dynamic changes in adaptation indeed support percept alternations in binocular rivalry. Empirical evidence for the involvement of mutual inhibition, however, is still scarce. To fill this gap, we presented human subjects with dichoptic random-dot motion stimuli and manipulated the angle between the monocular directions of motion from pure opponent horizontal motion to pure vertical motion in the same direction. We hypothesized that this decrease in motion-direction disparity increases the cross-inhibition gain due to lateral inhibition between neurons in the brain that are coarsely tuned to adjacent directions of visual motion, which predicts the largest changes in dominance at the smallest instead of the largest motion-direction disparities. We found that decreasing the angle between the two monocular directions of motion indeed systematically increased the predominance and mean dominance durations of the motion pattern presented to the ocular dominant eye (as identified by the hole-in-card test). Moreover, this effect was stronger if the contrast of the stimuli was lowered. Simulations showed that these features are indeed hallmark of weighted lateral inhibition between populations of directionally tuned motion-sensitive neurons. Our findings thus suggest dominance and suppression in binocular rivalry arises naturally from this fundamental principle in sensory processing. Interestingly, if the two monocular directions of motion differed <60°, the percept alternations also included transitions to in-between (vertical) motion percepts. We speculate that this behavior might result from positive feedback arising from adapting disinhibitory circuits in the network.
Previous studies have indicated that saccadic eye movements correlate positively with perceptual alternations in binocular rivalry, presumably because the foveal image changes resulting from saccades, rather than the eye movement themselves, cause switches in awareness. Recently, however, we found evidence that retinal image shifts elicit so-called onset rivalry and not percept switches as such. These findings raise the interesting question whether onset rivalry may account for correlations between saccades and percept switches. We therefore studied binocular rivalry when subjects made eye movements across a visual stimulus and compared it with the rivalry in a replay condition in which subjects maintained fixation while the same retinal displacements were reproduced by stimulus displacements on the screen. We used dichoptic random-dot motion stimuli viewed through a stereoscope, and measured eye and eyelid movements with scleral search-coils. Positive correlations between retinal image shifts and perceptual switches were observed for both saccades and stimulus jumps, but only for switches towards the subjects preferred eye at stimulus onset. A similar asymmetry was observed for blink-induced stimulus interruptions. Moreover, for saccades, amplitude appeared crucial as the positive correlation persisted for small stimulus jumps, but not for small saccades (amplitudes < 1°). These findings corroborate our tenet that saccades elicit a form of onset rivalry, and that rivalry is modulated by extra-retinal eye movement signals.
Levelts four propositions (L1-L4), which characterize the relation between changes in "stimulus strength" in the two eyes and percept alternations, are considered benchmark for binocular rivalry models. It was recently demonstrated that adaptation mutual-inhibition models of binocular rivalry capture L4 only in a limited range of input strengths, predicting an increase rather than a decrease in dominance durations with increasing stimulus strength for weak stimuli. This observation challenges the validity of those models, but possibly L4 itself is invalid. So far, L1-L4 have been tested mainly by varying the contrast of static stimuli, but since binocular rivalry breaks down at low contrasts, it has been difficult to study L4. To circumvent this problem, and to test if the recent revision of L2 has more general validity, we studied changes in binocular rivalry evoked by manipulating coherence of oppositely-moving random-dot stimuli in the two eyes, and compared them against the effects of stimulus contrast. Thirteen human observers participated. Both contrast and coherence manipulations in one eye produced robust changes in both eyes; dominance durations of the eye receiving the stronger stimulus increased while those of the other eye decreased, albeit less steeply. This is inconsistent with L2 but supports its revision. When coherence was augmented in both eyes simultaneously, dominance durations first increased at low coherence, and then decreased for further increases in coherence. The same held true for the alternation periods. The initial increase in dominance durations was absent in the contrast experiments, but with coherence manipulations, rivalry could be tested at much lower stimulus strengths. Thus, we found that L4, like L2, is only valid in a limited range of stimulus strengths. Outside that range, the opposite is true. Apparent discrepancies between contrast and coherence experiments could be fully reconciled with adaptation mutual-inhibition models using a simple input transfer-function.
We investigated how interactions between monocular motion parallax and binocular cues to depth vary in human motion areas for wide-field visual motion stimuli (110 × 100°). We used fMRI with an extensive 2 × 3 × 2 factorial blocked design in which we combined two types of self-motion (translational motion and translational + rotational motion), with three categories of motion inflicted by the degree of noise (self-motion, distorted self-motion, and multiple object-motion), and two different view modes of the flow patterns (stereo and synoptic viewing). Interactions between disparity and motion category revealed distinct contributions to self- and object-motion processing in 3D. For cortical areas V6 and CSv, but not the anterior part of MT(+) with bilateral visual responsiveness (MT(+)/b), we found a disparity-dependent effect of rotational flow and noise: When self-motion perception was degraded by adding rotational flow and moderate levels of noise, the BOLD responses were reduced compared with translational self-motion alone, but this reduction was cancelled by adding stereo information which also rescued the subjects self-motion percept. At high noise levels, when the self-motion percept gave way to a swarm of moving objects, the BOLD signal strongly increased compared to self-motion in areas MT(+)/b and V6, but only for stereo in the latter. BOLD response did not increase for either view mode in CSv. These different response patterns indicate different contributions of areas V6, MT(+)/b, and CSv to the processing of self-motion perception and the processing of multiple independent motions.
Recent investigations indicate that retinal motion is not directly available for perception when moving around [Souman JL, et al. (2010) J Vis 10:14], possibly pointing to suppression of retinal speed sensitivity in motion areas. Here, we investigated the distribution of retinocentric and head-centric representations of self-rotation in human lower-tier visual motion areas. Functional MRI responses were measured to a set of visual self-motion stimuli with different levels of simulated gaze and simulated head rotation. A parametric generalized linear model analysis of the blood oxygen level-dependent responses revealed subregions of accessory V3 area, V6(+) area, middle temporal area, and medial superior temporal area that were specifically modulated by the speed of the rotational flow relative to the eye and head. Pursuit signals, which link the two reference frames, were also identified in these areas. To our knowledge, these results are the first demonstration of multiple visual representations of self-motion in these areas. The existence of such adjacent representations points to early transformations of the reference frame for visual self-motion signals and a topography by visual reference frame in lower-order motion-sensitive areas. This suggests that visual decisions for action and perception may take into account retinal and head-centric motion signals according to task requirements.
Recent studies suggest that binocular rivalry at stimulus onset, so called onset rivalry, differs from rivalry during sustained viewing. These observations raise the interesting question whether there is a relation between onset rivalry and rivalry in the presence of eye movements. We therefore studied binocular rivalry when stimuli jumped from one visual hemifield to the other, either through a saccade or through a passive stimulus displacement, and we compared rivalry after such displacements with onset and sustained rivalry. We presented opponent motion, orthogonal gratings and face/house stimuli through a stereoscope. For all three stimulus types we found that subjects showed a strong preference for stimuli in one eye or one hemifield (Experiment 1), and that these subject-specific biases did not persist during sustained viewing (Experiment 2). These results confirm and extend previous findings obtained with gratings. The results from the main experiment (Experiment 3) showed that after a passive stimulus jump, switching probability was low when the preferred eye was dominant before a stimulus jump, but when the non-preferred eye was dominant beforehand, switching probability was comparatively high. The results thus showed that dominance after a stimulus jump was tightly related to eye dominance at stimulus onset. In the saccade condition, however, these subject-specific biases were systematically reduced, indicating that the influence of saccades can be understood from a systematic attenuation of the subjects onset rivalry biases. Taken together, our findings demonstrate a relation between onset rivalry and rivalry after retinal shifts and involvement of extra-retinal signals in binocular rivalry.
Speed and accuracy of visual motion discrimination depend systematically on motion strength. This behavior is traditionally explained by diffusion models that assume accumulation of sensory evidence over time to a decision bound. However, how does the brain decide when sensory evidence is ambiguous, such as in binocular rivalry? Theories on bistable vision propose that such a conflict is resolved through competitive interactions between adapting units encoding the alternative stimulus interpretations. Thus, distinctly different theoretical frameworks have been proposed for deciding under uncertainty and ambiguity; a discrepancy overlooked so far. Here, we studied motion discrimination at stimulus onset under both conditions. In Experiment 1, speed and accuracy were similar when observers viewed noisy, unambiguous motion patterns in which signal dots were either at identical or at different, uncorrelated locations for the two eyes. This result is compatible with a race between two monocular discrimination processes. However, Experiments 2 and 3 showed that reaction times increase under rivalry conditions and that this increase cannot be explained by motion transparency. The data thus reveal competitive rivalry interactions. We discuss a model that can account for the accuracy and latencies observed under both ambiguous and unambiguous conditions, by combining key elements from diffusion and rivalry models.
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