Bistable Vision Research Articles

A predictive coding account of bistable perception - a model-based fMRI study.

In bistable vision, subjective perception wavers between two interpretations of a constant ambiguous stimulus. This dissociation between conscious perception and sensory stimulation has motivated various empirical studies on the neural correlates of bistable perception, but the neurocomputational mechanism behind endogenous perceptual transitions has remained elusive. Here, we recurred to a generic Bayesian framework of predictive coding and devised a model that casts endogenous perceptual transitions as a consequence of prediction errors emerging from residual evidence for the suppressed percept. Data simulations revealed close similarities between the model’s predictions and key temporal characteristics of perceptual bistability, indicating that the model was able to reproduce bistable perception. Fitting the predictive coding model to behavioural data from an fMRI-experiment on bistable perception, we found a correlation across participants between the model parameter encoding perceptual stabilization and the behaviourally measured frequency of perceptual transitions, corroborating that the model successfully accounted for participants’ perception. Formal model comparison with established models of bistable perception based on mutual inhibition and adaptation, noise or a combination of adaptation and noise was used for the validation of the predictive coding model against the established models. Most importantly, model-based analyses of the fMRI data revealed that prediction error time-courses derived from the predictive coding model correlated with neural signal time-courses in bilateral inferior frontal gyri and anterior insulae. Voxel-wise model selection indicated a superiority of the predictive coding model over conventional analysis approaches in explaining neural activity in these frontal areas, suggesting that frontal cortex encodes prediction errors that mediate endogenous perceptual transitions in bistable perception. Taken together, our current work provides a theoretical framework that allows for the analysis of behavioural and neural data using a predictive coding perspective on bistable perception. In this, our approach posits a crucial role of prediction error signalling for the resolution of perceptual ambiguities.

Revisiting the Lissajous figure as a tool to study bistable perception

During bistable vision perception spontaneously "switches" between two mutually exclusive percepts despite constant sensory input. The endogenous nature of these perceptual transitions has motivated extensive research aimed at the underlying mechanisms, since spontaneous perceptual transitions of bistable stimuli should in principle allow for a dissociation of processes related to sensory stimulation from those related to conscious perception. However, transitions from one conscious percept to another are often not instantaneous, and participants usually report a considerable amount of mixed or unclear percepts. This feature of bistable vision makes it difficult to isolate transition-related visual processes. Here, we revisited an ambiguous depth-from-motion stimulus which was first introduced to experimental psychology more than 80 years ago. This rotating Lissajous figure might prove useful in complementing other bistable stimuli, since its perceptual transitions only occur at critical stimulus configurations and are virtually instantaneous, thus facilitating the construction of a perceptually equivalent replay condition. We found that three parameters of the Lissajous figure - complexity, line width, and rotational speed - differentially modulated its perceptual dominance durations and transition probabilities, thus providing experimenters with a versatile tool to study the perceptual dynamics of bistable vision.

Frontoparietal Cortex Mediates Perceptual Transitions in Bistable Perception

During bistable vision, perception oscillates between two mutually exclusive percepts despite constant sensory input. Greater BOLD responses in frontoparietal cortex have been shown to be associated with endogenous perceptual transitions compared with "replay" transitions designed to closely match bistability in both perceptual quality and timing. It has remained controversial, however, whether this enhanced activity reflects causal influences of these regions on processing at the sensory level or, alternatively, an effect of stimulus differences that result in, for example, longer durations of perceptual transitions in bistable perception compared with replay conditions. Using a rotating Lissajous figure in an fMRI experiment on 15 human participants, we controlled for potential confounds of differences in transition duration and confirmed previous findings of greater activity in frontoparietal areas for transitions during bistable perception. In addition, we applied dynamic causal modeling to identify the neural model that best explains the observed BOLD signals in terms of effective connectivity. We found that enhanced activity for perceptual transitions is associated with a modulation of top-down connectivity from frontal to visual cortex, thus arguing for a crucial role of frontoparietal cortex in perceptual transitions during bistable perception.

Congruent Auditory Input Can Bias Bistable Vision without Voluntary Attentional Control

Prior research presents conflicting evidence as to whether the ability of congruent auditory information to resolve visual ambiguity is dependent on voluntary attentional selection of congruent stimuli (Van Ee et al., 2009; Alais & Parker, 2006). We used novel speech stimuli to test whether audiovisually congruent visual stimuli were dominant in binocular rivalry even when subjects were not aware which visual stimulus was associated with the auditory stimulus, effectively barring subjects from deliberately selecting the congruent stimulus with attention (verified post-experimentally). The stimuli were derived from prior research demonstrating that speech sounds distort the visual perception of ellipses towards associated mouth shapes: hearing a /wee/ sound causes increased perceived horizontal elongation of a circle, whereas hearing a /woo/ sound produces vertical elongation (Sweeney et al., 2012). In the current study, subjects were presented dichoptically with two animations of ellipses that each continuously elongated horizontally and vertically in alternation. The stimuli presented to each eye differed only in that they (a) were luminance-matched red or green, and (b) alternated counterphase such that, at any time, the horizontal extension of one ellipse was equal to the vertical extension of the other. Simultaneously, repeating voiced syllables /wee/ and /woo/ were played in synchrony with the visual stimuli so that, throughout each trial, there was a shape-sound correspondence with the ellipses presented to only one of the eyes. Subjects were instructed to continuously report which changing ellipse was perceptually dominant throughout the trial, ignoring the auditory stimuli as distracters. Each subject participated in sixteen 32-second trials, counterbalanced for color of congruent stimulus and the eye to which it was presented. Perceptual dominance durations for the audiovisually congruent stimuli were significantly longer than those for the incongruent stimuli. These results demonstrate that phonologically congruent auditory input can bias bistable vision in the absence of voluntary attentional control. Meeting abstract presented at VSS 2013

On the Functional Relevance of Frontal Cortex for Passive and Voluntarily Controlled Bistable Vision

In bistable vision, one constant ambiguous stimulus leads to 2 alternating conscious percepts. This perceptual switching occurs spontaneously but can also be influenced through voluntary control. Neuroimaging studies have reported that frontal regions are activated during spontaneous perceptual switches, leading some researchers to suggest that frontal regions causally induce perceptual switches. But the opposite also seems possible: frontal activations may themselves be caused by spontaneous switches. Classically implicated in attentional processes, these same regions are also candidates for the origins of voluntary control over bistable vision. Here too, it remains unknown whether frontal cortex is actually functionally relevant. It is even possible that spontaneous perceptual switches and voluntarily induced switches are mediated by the same top-down mechanisms. To directly address these issues, we here induced "virtual lesions," with transcranial magnetic stimulation, in frontal, parietal, and 2 lower level visual cortices using an established ambiguous structure-from-motion stimulus. We found that dorsolateral prefrontal cortex was causally relevant for voluntary control over perceptual switches. In contrast, we failed to find any evidence for an active role of frontal cortex in passive bistable vision. Thus, it seems the same pathway used for willed top-down modulation of bistable vision is not used during passive bistable viewing.

Motion discrimination under uncertainty and ambiguity

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.

Early interactions between neuronal adaptation and voluntary control determine perceptual choices in bistable vision

At the onset of bistable stimuli, the brain needs to choose which of the competing perceptual interpretations will first reach awareness. Stimulus manipulations and cognitive control both influence this choice process, but the underlying mechanisms and interactions remain poorly understood. Using intermittent presentation of bistable visual stimuli, we demonstrate that short interruptions cause perceptual reversals upon the next presentation, whereas longer interstimulus intervals stabilize the percept. Top-down voluntary control biases this process but does not override the timing dependencies. Extending a recently introduced low-level neural model, we demonstrate that percept-choice dynamics in bistable vision can be fully understood with interactions in early neural processing stages. Our model includes adaptive neural processing preceding a rivalry resolution stage with cross-inhibition, adaptation, and an interaction of the adaptation levels with a neural baseline. Most importantly, our findings suggest that top-down attentional control over bistable stimuli interacts with low-level mechanisms at early levels of sensory processing before perceptual conflicts are resolved and perceptual choices about bistable stimuli are made.

Surface organization influences bistable vision.

A priority for the visual system is to construct 3-dimensional surfaces from visual primitives. Information is combined across individual cues to form a robust representation of the external world. Here, it is shown that surface completion relying on multiple visual cues influences relative dominance during binocular rivalry. The shape of a surface determined by 1 nonrivalrous visual cue (disparity, structure-from-motion) alters the dominance patterns of a rivalrous region of the image whose shape is defined by another cue (perspective, texture). The findings indicate that contextual information promotes the perception of the member of the rivalrous pair consistent with a smooth surface representation. The results extend the current description of binocular rivalry as a hierarchical process by implying that cue combination affects image selection during bistable viewing.

Role of the Prefrontal Cortex in Attentional Control over Bistable Vision

The primary source of top-down attentional control in object perception is the prefrontal cortex. This region is involved in the maintenance of goal-related information as well as in attentional selection and set shifting. Recent approaches have emphasized the role of top-down processes during elementary visual processes as exemplified in bistable vision where perception oscillates automatically between two mutually exclusive states. The prefrontal cortex might influence this process either by maintaining the dominant pattern while protecting it against the competing representation, or by facilitating perceptual switches between the two competing representations. To address this issue, we investigated reported perceptual reversals in patients with circumscribed lesions of the prefrontal cortex and healthy control participants in three experimental conditions: hold (maintaining the dominant view), speed (inducing as many perceptual switches as possible), and neutral (no intervention). Results indicated that although the patients showed normal switching rates in the neutral condition and were able to control perceptual switches in the hold condition as much as control subjects were, they were less able to facilitate reversals specifically in the speed condition. These results suggest that the prefrontal cortex is necessary to bias the selection of visual representations in accord with current goals, but is less essential for maintaining selected information active that is continuously available in the environment. As for attentional selection, the present results suggest that the prefrontal cortex initiates perceptual reversals by withdrawing top-down support from the dominant representation without (or prior to) boosting the suppressed view.

Role of the Prefrontal Cortex in Attentional Control over Bistable Vision

Abstract The primary source of top-down attentional control in object perception is the prefrontal cortex. This region is involved in the maintenance of goal-related information as well as in attentional selection and set shifting. Recent approaches have emphasized the role of top-down processes during elementary visual processes as exemplified in bistable vision where perception oscillates automatically between two mutually exclusive states. The prefrontal cortex might influence this process either by maintaining the dominant pattern while protecting it against the competing representation, or by facilitating perceptual switches between the two competing representations. To address this issue, we investigated reported perceptual reversals in patients with circumscribed lesions of the prefrontal cortex and healthy control participants in three experimental conditions: hold (maintaining the dominant view), speed (inducing as many perceptual switches as possible), and neutral (no intervention). Results indicated that although the patients showed normal switching rates in the neutral condition and were able to control perceptual switches in the hold condition as much as control subjects were, they were less able to facilitate reversals specifically in the speed condition. These results suggest that the prefrontal cortex is necessary to bias the selection of visual representations in accord with current goals, but is less essential for maintaining selected information active that is continuously available in the environment. As for attentional selection, the present results suggest that the prefrontal cortex initiates perceptual reversals by withdrawing top-down support from the dominant representation without (or prior to) boosting the suppressed view.

Competition in bistable vision is attribute-specific

We employ ambiguous figures and rivalrous stimuli that have multiple ambiguous properties to show that the different attributes of an ambiguous stimulus can undergo independent switching dynamics. This suggests that competition is distributed and attribute-specific, consistent with the known functional segregation of visual processing. Conflicting evidence that binocular rivalry is an early or late visual process may be better understood as evidence for attribute-specific competition occurring at multiple stages of visual processing. Specifically, we show that whether perceptual selection during binocular rivalry is early and eye-based or late and percept-based depends on the particular ambiguous attributes of the rivalrous stimulus.