Dynamics Of Binocular Rivalry Research Articles

Pupillometry indexes ocular dominance plasticity

Short-term monocular deprivation in normally sighted adult humans produces a transient shift of ocular dominance, boosting the deprived eye. This effect has been documented with both perceptual tests and through physiological recordings, but no previous study simultaneously measured physiological responses and the perceptual effects of deprivation. Here we propose an integrated experimental paradigm that combines binocular rivalry with pupillometry, to introduce an objective physiological index of ocular dominance plasticity, acquired concurrently with perceptual testing. Ten participants reported the perceptual dynamics of binocular rivalry, while we measured pupil diameter. Stimuli were a white and a black disk, each presented monocularly. Rivalry dynamics and pupil-size traces were compared before and after 2 h of monocular deprivation, achieved by applying a translucent patch over the dominant eye. Consistent with prior research, we observed that monocular deprivation boosts the deprived-eye signal and consequently increases ocular dominance. In line with previous studies, we also observed subtle but systematic modulations of pupil size that tracked alternations between exclusive dominance phases of the black or white disk. Following monocular deprivation, the amplitude of these pupil-size modulations increased, which is consistent with the post-deprivation boost of the deprived eye and the increase of ocular dominance. This provides evidence that deprivation impacts the effective strength of monocular visual stimuli, coherently affecting perceptual reports and the automatic and unconscious regulation of pupil diameter. Our results show that a combined paradigm of binocular rivalry and pupillometry gives new insights into the physiological mechanisms underlying deprivation effects.

An Accumulating Neural Signal Underlying Binocular Rivalry Dynamics.

During binocular rivalry, conflicting images are presented one to each eye and perception alternates stochastically between them. Despite stable percepts between alternations, modeling suggests that neural signals representing the two images change gradually, and that the duration of stable percepts are determined by the time required for these signals to reach a threshold that triggers an alternation. However, direct physiological evidence for such signals has been lacking. Here, we identify a neural signal in the human visual cortex that shows these predicted properties. We measured steady-state visual evoked potentials (SSVEPs) in 84 human participants (62 females, 22 males) who were presented with orthogonal gratings, one to each eye, flickering at different frequencies. Participants indicated their percept while EEG data were collected. The time courses of the SSVEP amplitudes at the two frequencies were then compared across different percept durations, within participants. For all durations, the amplitude of signals corresponding to the suppressed stimulus increased and the amplitude corresponding to the dominant stimulus decreased throughout the percept. Critically, longer percepts were characterized by more gradual increases in the suppressed signal and more gradual decreases of the dominant signal. Changes in signals were similar and rapid at the end of all percepts, presumably reflecting perceptual transitions. These features of the SSVEP time courses are well predicted by a model in which perceptual transitions are produced by the accumulation of noisy signals. Identification of this signal underlying binocular rivalry should allow strong tests of neural models of rivalry, bistable perception, and neural suppression.SIGNIFICANCE STATEMENT During binocular rivalry, two conflicting images are presented to the two eyes and perception alternates between them, with switches occurring at seemingly random times. Rivalry is an important and longstanding model system in neuroscience, used for understanding neural suppression, intrinsic neural dynamics, and even the neural correlates of consciousness. All models of rivalry propose that it depends on gradually changing neural activity that on reaching some threshold triggers the perceptual switches. This manuscript reports the first physiological measurement of neural signals with that set of properties in human participants. The signals, measured with EEG in human observers, closely match the predictions of recent models of rivalry, and should pave the way for much future work.

Integration and suppression interact in binocular vision.

Contingent on stereo compatibility, two images presented dichoptically can lead to either binocular integration, thus generating stable stereopsis, or interocular suppression that induces binocular rivalry with bistable perception that alternates between the two images. The relationship between binocular integration and interocular suppression concerns how our brain processes binocular inputs to form unified visual awareness but remains unclear. Here, a series of psychophysical experiments were conducted to address this question, revealing that these collaborative and competitive binocular interactions are interconnected and would mediate one another according to their strength. Specifically, Experiments 1a and 1b showed that the presence of binocular rivalry inhibited peripheral stereopsis, significantly elevating the stereo threshold, with higher elevation resulting from increasing rivalry contrast. Experiments 2a and 2b showed that existing stereopsis with increasing binocular disparity balanced the dynamics of peripheral binocular rivalry, rendering more equivalent eye dominance. Based on these interactions, we suggest that binocular integration and interocular suppression may mediate one another through an overlapping mechanism for regulating eye dominance, with strong stereo percepts tending to reduce eye dominance and strong rivalry tending to increase eye dominance.

Measuring the reliability of binocular rivalry.

Binocular rivalry is a widely used tool in sensory and cognitive neuroscience to investigate different aspects of vision and cognition. The dynamics of binocular rivalry (e.g., duration of perceptual dominance phases and mixed percept proportions) differ across individuals; based on rivalry dynamics, it is also possible to calculate an index of ocular dominance (by comparing the perceptual dominance of the images in the two eyes). In this study, we investigated the reliability of binocular rivalry dynamics using different methods for dichoptic stimulation and different rivalry stimuli. For the three main indices we defined (ocular dominance, phase durations and mixed percept proportions), we found a high test-retest reliability across sessions. Moreover, the test-retest reliability of the ocular dominance index was predictable from its internal consistency, supporting its stability over time. Phase durations and mixed percept proportions, in contrast, had worse test-retest reliability than expected based on internal consistency, indicating that these parameters are susceptible to state-dependent changes. Our results support the use of the ocular dominance index and binocular rivalry in the measurement of sensory eye dominance and its plasticity, but advise caution when investigating the association between phase durations or mixed percepts and stable characteristics like psychological traits or disorders.

InFoRM (Indicate-Follow-Replay-Me): Rivalry generates individual, validated introspection maps and generates new insights in binocular rivalry dynamics

InFoRM (Indicate-Follow-Replay-Me): Rivalry generates individual, validated introspection maps and generates new insights in binocular rivalry dynamics

Visual cortex cTBS increases mixed percept duration while a-tDCS has no effect on binocular rivalry.

Neuromodulation of the primary visual cortex using anodal transcranial direct current stimulation (a-tDCS) can alter visual perception and enhance neuroplasticity. However, the mechanisms that underpin these effects are currently unknown. When applied to the motor cortex, a-tDCS reduces the concentration of the inhibitory neurotransmitter gamma aminobutyric acid (GABA), an effect that has been linked to increased neuroplasticity. The aim of this study was to assess whether a-tDCS also reduces GABA-mediated inhibition when applied to the human visual cortex. Changes in visual cortex inhibition were measured using the mixed percept duration in binocular rivalry. Binocular rivalry mixed percept duration has recently been advocated as a direct and sensitive measure of visual cortex inhibition whereby GABA agonists decrease mixed percept durations and agonists of the excitatory neurotransmitter acetylcholine (ACH) increase them. Our hypothesis was that visual cortex a-tDCS would increase mixed percept duration by reducing GABA-mediated inhibition and increasing cortical excitation. In addition, we measured the effect of continuous theta-burst transcranial magnetic stimulation (cTBS) of the visual cortex on binocular rivalry dynamics. When applied to the motor or visual cortex, cTBS increases GABA concentration and we therefore hypothesized that visual cortex cTBS would decrease the mixed percept duration. Binocular rivalry dynamics were recorded before and after active and sham a-tDCS (N = 15) or cTBS (N = 15). Contrary to our hypotheses, a-tDCS had no effect, whereas cTBS increased mixed percepts during rivalry. These results suggest that the neurochemical mechanisms of a-tDCS may differ between the motor and visual cortices.

Brief period of monocular deprivation drives changes in audiovisual temporal perception

The human brain retains a striking degree of plasticity into adulthood. Recent studies have demonstrated that a short period of altered visual experience (via monocular deprivation) can change the dynamics of binocular rivalry in favor of the deprived eye, a compensatory action thought to be mediated by an upregulation of cortical gain control mechanisms. Here, we sought to better understand the impact of monocular deprivation on multisensory abilities, specifically examining audiovisual temporal perception. Using an audiovisual simultaneity judgment task, we discovered that 90 minutes of monocular deprivation produced opposing effects on the temporal binding window depending on the eye used in the task. Thus, in those who performed the task with their deprived eye there was a narrowing of the temporal binding window, whereas in those performing the task with their nondeprived eye there was a widening of the temporal binding window. The effect was short lived, being observed only in the first 10 minutes of postdeprivation testing. These findings indicate that changes in visual experience in the adult can rapidly impact multisensory perceptual processes, a finding that has important clinical implications for those patients with adult-onset visual deprivation and for therapies founded on monocular deprivation.

Binocular rivalry from luminance and contrast

Binocular rivalry is the phenomenon that when two incompatible images are simultaneously presented, one to each eye, the two images compete with each other to be the dominant percept. Studying the underlying neural mechanisms of binocular rivalry is useful for understanding the mechanisms of interocular inhibition. Levelt’s Propositions, a set of four propositions that were originally published over fifty years ago, are not only useful for characterizing the perceptual dynamics of binocular rivalry, but can also provide a metric for assessing the common or differential neural mechanisms of binocular rivalry when diverse stimulus types are used. In the present study, we conducted a series of psychophysics experiments, where we compared the rivalry dynamics of two quite different types of stimuli. Orthogonal gratings, a classic type of rivalry stimulus, were contrasted with luminance patches, a type of rivalry stimulus that is relatively less studied. Our results showed that, similar to the orthogonal gratings, the alternate percepts in luminance-only rivalry were described by the modified Levelt’s Propositions, despite the clearly slower alternation rates for luminance patches. However, unlike the mixed percepts observed during transitions between oriented gratings, fusion percepts during luminance rivalry were common, could be lustrous, and obeyed the same Propositions, suggesting a regime of tri-stability. Overall, both types of rivalry are consistent with recent models that posit separate binocular and monocular channels embedded within neural circuits that also accomplish contrast normalization. Finally, luminance rivalry is discussed in the contexts of binocular summation and suppression, as well as Fechner’s paradox.

Using psychophysical performance to predict short-term ocular dominance plasticity in human adults.

Binocular rivalry has become an important index of visual performance, both to measure ocular dominance or its plasticity, and to index bistable perception. We investigated its interindividual variability across 50 normal adults and found that the duration of dominance phases in rivalry is linked with the duration of dominance phases in another bistable phenomenon (structure from motion). Surprisingly, it also correlates with the strength of center–surround interactions (indexed by the tilt illusion), suggesting a common mechanism supporting both competitive interactions: center–surround and rivalry.In a subset of 34 participants, we further investigated the variability of short-term ocular dominance plasticity, measured with binocular rivalry before and after 2 hours of monocular deprivation. We found that ocular dominance shifts in favor of the deprived eye and that a large portion of ocular dominance variability after deprivation can be predicted from the dynamics of binocular rivalry before deprivation. The single best predictor is the proportion of mixed percepts (phases without dominance of either eye) before deprivation, which is positively related to ocular dominance unbalance after deprivation. Another predictor is the duration of dominance phases, which interacts with mixed percepts to explain nearly 50% of variance in ocular dominance unbalance after deprivation. A similar predictive power is achieved by substituting binocular rivalry dominance phase durations with tilt illusion magnitude, or structure from motion phase durations. Thus, we speculate that ocular dominance plasticity is modulated by two types of signals, estimated from psychophysical performance before deprivation, namely, interocular inhibition (promoting binocular fusion, hence mixed percepts) and inhibition for perceptual competition (promoting longer dominance phases and stronger center–surround interactions).

Binocular rivalry dynamics associated with high levels of self-reported autistic traits suggest an imbalance of cortical excitation and inhibition

An imbalance in cortical excitation and inhibition (E/I) may underlie both social and non-social symptoms of autism spectrum conditions (ASC). Recent work suggests that an E/I imbalance may underlie some of the sensory differences that are characteristic of ASCs such as anomalous perception. Binocular rivalry dynamics are thought to reflect the balance of E/I in the brain and could serve as a behavioural biomarker for ASC. Previous studies of clinical ASC populations have found a slower rate of binocular rivalry transitions; increased duration of the mixed percept and reduced perceptual suppression. There are some mixed reports of altered rivalry dynamics in the neurotypical population with high self-reported levels of autistic traits. Therefore, we used simple grating stimuli to measure binocular rivalry dynamics in a sample of seventy-nine adults aged 18–55 years. We additionally measured the level of autistic traits with the AQ-10 and used CAPS as a measure of anomalous perception. Bayesian correlations showed that those with higher AQ scores had a slower rate of perceptual switching and a longer mixed percept duration. Significant regression models with CAPS and AQ score revealed that AQ score was a significant predictor of switch rate and mixed percept duration, whereas CAPS was not. We also report that CAPS significantly predicted perceptual suppression, whereas AQ score did not. Overall, our findings suggest that in a non-clinical population, autistic traits are a predictor of binocular rivalry dynamics and the cortical E/I imbalance thought to underlie symptoms of ASC may extend to the broader phenotype.

Age-dependency in binocular rivalry is reflected by exclusive percepts, not mixed percepts

Some aspects of decision-making are known to decline with normal aging. One of the known perceptual decision-making processes which is vastly studied is binocular rivalry. It is well-established that the older the person, the slower the perceptual dynamics. However, the underlying neurobiological cause is unknown. So, to understand how age affects visual decision-making, we investigated age-related changes in perception during binocular rivalry. In binocular rivalry, the image presented to one eye competes for perceptual dominance with the image presented to the other eye. Perception during binocular rivalry consists of alternations between exclusive percepts. However, frequently, mixed percepts with combinations of the two monocular images occur. The mixed percepts reflect a transition from the percept of one eye to the other but frequently the transitions do not complete the full cycle and the previous exclusive percept becomes dominant again. The transitional idiosyncrasy of mixed percepts has not been studied systematically in different age groups. Previously, we have found evidence for adaptation and noise, and not inhibition, as underlying neural factors that are related to age-dependent perceptual decisions. Based on those conclusions, we predict that mixed percepts/inhibitory interactions should not change with aging. Therefore, in an old and a young age group, we studied binocular rivalry dynamics considering both exclusive and mixed percepts by using two paradigms: percept-choice and percept-switch. We found a decrease in perceptual alternation Probability for older adults, although the rate of mixed percepts did not differ significantly compared to younger adults. Interestingly, the mixed percepts play a very similar transitional idiosyncrasy in our different age groups. Further analyses suggest that differences in synaptic depression, gain modulation at the input level, and/or slower execution of motor commands are not the determining factors to explain these findings. We then argue that changes in perceptual decisions at an older age are the result of changes in neural adaptation and noise.

Altered Visual Plasticity in Morbidly Obese Subjects.

SummaryGrowing evidence indicates a close link between energy metabolism and neural plasticity as obesity is associated with alterations of cognitive functions, memory, and hippocampal neurogenesis. However, it is still unknown whether obesity can affect low-level sensory plasticity. Here we investigated this issue by probing early visual plasticity induced by short-term (2 h) monocular deprivation in a group of adult volunteers with a wide range of Body Mass Index (BMI), from normal weight to morbid obesity. We found that the effect of monocular deprivation decreased with increasing BMI, and morbidly obese subjects (BMI>40) failed to show the homeostatic plasticity effect seen in normal-weight participants. In addition, morbidly obese subjects exhibited altered binocular rivalry dynamics compared with normal-weight observers. These results show for the first time that the impact of obesity observed at the neural and cognitive level extends to basic sensory processing and plasticity.

Lateralized occipitotemporal tDCS modulates dynamics of binocular rivalry between faces and words

Lateralized occipitotemporal tDCS modulates dynamics of binocular rivalry between faces and words

GABAergic Inhibition Gates Perceptual Awareness During Binocular Rivalry.

Binocular rivalry is a classic experimental tool to probe the neural machinery of perceptual awareness. During rivalry, perception alternates between the two eyes, and the ebb and flow of perception is modeled to rely on the strength of inhibitory interactions between competitive neuronal populations in visual cortex. As a result, rivalry has been suggested as a noninvasive perceptual marker of inhibitory signaling in visual cortex, and its putative disturbance in psychiatric conditions, including autism. Yet, direct evidence causally implicating inhibitory signaling in the dynamics of binocular rivalry is currently lacking. We previously found that people with higher GABA levels in visual cortex, measured using magnetic resonance spectroscopy, have stronger perceptual suppression during rivalry. Here, we present direct causal tests of the impact of GABAergic inhibition on rivalry dynamics, and the contribution of specific GABA receptors to these dynamics. In a crossover pharmacological design with male and female adult participants, we found that drugs that modulate the two dominant GABA receptor types in the brain, GABAA (clobazam) and GABAB (arbaclofen), increase perceptual suppression during rivalry relative to a placebo. Crucially, these results could not be explained by changes in reaction times or response criteria, as determined through rivalry simulation trials, suggesting a direct and specific influence of GABA on perceptual suppression. A full replication study of the GABAB modulator reinforces these findings. These results provide causal evidence for a link between the strength of inhibition in the brain and perceptual suppression during rivalry and have implications for psychiatric conditions including autism.SIGNIFICANCE STATEMENT How does the brain accomplish perceptual gating? Here we use a direct and causal pharmacological manipulation to present insight into the neural machinery of a classic illusion of perceptual awareness: binocular rivalry. We show that drugs that increase GABAergic inhibition in the brain, clobazam (GABAA modulator) and arbaclofen (GABAB modulator), increase perceptual suppression during rivalry relative to a placebo. These results present the first causal link between GABAergic inhibition and binocular rivalry in humans, complementing classic models of binocular rivalry, and have implications for our understanding of psychiatric conditions, such as autism, where binocular rivalry is posited as a behavioral marker of disruptions in inhibitory signaling in the brain.

Slower Binocular Rivalry in the Autistic Brain.

Autism has traditionally been regarded as a disorder of the social brain. Recent reports of differences in visual perception have challenged this notion, but little evidence for altered visual processing in the autistic brain exists. We have previously observed slower behaviorally reported rates of a basic visual phenomenon, binocular rivalry, in autism [1, 2]. During rivalry, two images-one presented to each eye-vie for awareness, alternating back and forth in perception. This competition is modeled to rely, in part, on the balance of excitation and inhibition in visual cortex [3-8], which may be altered in autism [2, 9-14]. Yet direct neural evidence for this potential marker of excitation/inhibition (E/I) balance in autism is lacking. Here, we report a striking alteration in the neural dynamics of binocular rivalry in individuals with autism. Participants viewed true and simulated frequency-tagged binocular rivalry displays while steady-state visually evoked potentials (SSVEPs) were measured over occipital cortex using electroencephalography (EEG). First, we replicate our prior behavioral findings of slower rivalry and reduced perceptual suppression in individuals with autism compared with controls. Second, we provide direct neural evidence for slower rivalry in autism compared with controls, which strongly predicted individuals' behavioral switch rates. Finally, using neural data alone, we were able to predict autism symptom severity (ADOS) and correctly classify individuals' diagnostic status (autistic versus control; 87% accuracy). These findings clearly implicate atypical visual processing in the neurobiology of autism. Down the road, this paradigm may serve as a non-verbal marker of autism for developmental and cross-species research.

Individual differences in continuous flash suppression: Potency and linkages to binocular rivalry dynamics

Binocular rivalry (BR) and continuous flash suppression (CFS) are compelling psychophysical phenomena involving interocular suppression. Using an individual differences approach we assessed whether interocular suppression induced by CFS is predictable in potency from characteristics of BR that are plausibly governed by interocular inhibition. We found large individual differences in BR dynamics and, in addition, in the strength of CFS as gauged by the incidence and durations of breakthroughs in CFS during an extended viewing periods. CFS’s potency waned with repeated trials, but stable individual differences persisted despite these mean shifts. We also discovered large individual differences in the strength of the post-CFS shift in BR dominance produced by interocular suppression. While CFS breakthroughs were significantly negatively correlated with shifts in BR dominance after CFS, there were no significant associations between individual differences in alternation rate during pre-CFS binocular rivalry and either breakthroughs during CFS or post-CFS dominance shifts. Bayesian hypothesis tests and highest posterior density intervals confirmed the weak association between these two forms of interocular suppression. Thus, our findings suggest that the substantial individual differences in BR dynamics and CFS effectiveness are modestly related but not entirely mediated by one common neural substrate.

Altering brain dynamics with transcranial random noise stimulation

Random noise can enhance the detectability of weak signals in nonlinear systems, a phenomenon known as stochastic resonance (SR). This concept is not only applicable to single threshold systems but can also be applied to dynamical systems with multiple attractor states, such as observed during the phenomenon of binocular rivalry. Binocular rivalry can be characterized by marginally stable attractor states between which the brain switches in a spontaneous, stochastic manner. Here we used a computational model to predict the effect of noise on perceptual dominance durations. Subsequently we compared the model prediction to a series of experiments where we measured binocular rivalry dynamics when noise (zero-mean Gaussian random noise) was added either to the visual stimulus (Exp. 1) or directly to the visual cortex (Exp. 2) by applying transcranial Random Noise Stimulation (tRNS 1 mA, 100–640 Hz zero -mean Gaussian random noise). We found that adding noise significantly reduced the mixed percept duration (Exp. 1 and Exp. 2). Our results are the first to demonstrate that both central and peripheral noise can influence state-switching dynamics of binocular rivalry under specific conditions (e.g. low visual contrast stimuli), in line with a SR-mechanism.

Altered Visual Plasticity in Morbidly Obese Subjects

Growing evidence indicates a close link between energy metabolism and neural plasticity as obesity is associated with alterations of cognitive functions, memory and hippocampal neurogenesis. However, it is still unknown whether obesity can affect low-level sensory plasticity. Here we investigated this issue by probing early visual plasticity induced by short-term (2h) monocular deprivation in a group of adult volunteers with a wide range of Body Mass Index (BMI), from normal-weight to morbid obesity. We found that the effect of monocular deprivation decreased with increasing BMI, with morbidly obese subjects (BMI>40) failed to show the homeostatic plasticity effect seen in normal-weight participants. In addition, morbidly obese subjects exhibited altered binocular rivalry dynamics compared with normal-weight observers. These results show for the first time that the impact of obesity observed at the neural and cognitive level extends to basic sensory processing and plasticity.

Direct Neural Read-Out of Binocular Rivalry Dynamics in Autism using EEG

Direct Neural Read-Out of Binocular Rivalry Dynamics in Autism using EEG

Causal Push-and-Pull Modulation of Binocular Rivalry Dynamics using GABAergic Drugs

Causal Push-and-Pull Modulation of Binocular Rivalry Dynamics using GABAergic Drugs