Tracking rivalry with neural rhythms: multivariate SSVEPs reveal perception during binocular rivalry.

The contents of awareness can substantially change without any modification to the external world. Such effects are exemplified in binocular rivalry, where a different stimulus is presented to each eye causing instability in perception. This phenomenon has made binocular rivalry a quintessential method for studying consciousness and the necessary neural correlates for awareness. However, to conduct research on binocular rivalry usually requires self-reports of changes in percept, which can produce confounds and exclude states and contexts where self-reports are undesirable or unreliable. Here, we use a novel multivariate spatial filter dubbed 'Rhythmic Entrainment Source Separation' to extract steady state visual evoked potentials from electroencephalography data. We show that this method can be used to quantify the perceptual switch-rate of participants during binocular rivalry and therefore may be valuable in experimental contexts where self-reports are methodologically problematic or impossible, particularly as an adjunct. Our analyses also reveal that 'no-report' conditions may affect the deployment of attention and thereby neural correlates, another important consideration for consciousness research.

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.

Cortical theta phase synchronization involved in mismatch-driven perceptual alternation in binocular rivalry.

When two conflicting images are presented to each eye, a phenomenon called binocular rivalry occurs in which we initially perceive one image, and then our perception switches to the other over time. An enhancement of θ-band phase coherence in visual mismatch oscillatory response (vMOR) is reported to be involved in the facilitation of perceptual alternation when the deviant stimulus is presented unconsciously. In this study, we investigated the modulation effect of θ-band transcranial alternating current stimulation (tACS) on perceptual alternation in binocular rivalry, with a focus on its relationship with the θ-band vMOR. The results showed that tACS had no significant effect on the mean proportion of perceptual alternation. Analyzing the differential effects of the modulation, however, we found a positive correlation between the increase in inter-trial phase coherence of the vMOR and the promotion of perceptual alternation under the unconscious deviant condition. Additionally, our findings indicate that the θ-band phase synchrony between frontal and occipital electrode sides, as measured by the phase lag index, is implicated in perceptual alternation, with an increase (decrease) in connection density observed in participants whose perceptual alternation was increased (decreased) by tACS. These results support the hypothesis that deviant visual stimuli evoke θ-band phase synchrony between the frontal and occipital cortices, thereby enhancing perceptual alternation in binocular rivalry.

Reviving Bistable Perception in Patients With Depression by Decreasing the Overestimation of Prior Precision.

Slower perceptual alternations, a notable perceptual effect observed in psychiatric disorders, can be alleviated by antidepressant therapies that affect serotonin levels in the brain. While these phenomena have been well documented, the underlying neurocognitive mechanisms remain to be elucidated. Our study bridges this gap by employing a computational cognitive approach within a Bayesian predictive coding framework to explore these mechanisms in depression. We fitted a prediction error (PE) model to behavioral data from a binocular rivalry task, uncovering that significantly higher initial prior precision and lower PE led to a slower switch rate in patients with depression. Furthermore, serotonin-targeting antidepressant treatments significantly decreased the prior precision and increased PE, both of which were predictive of improvements in the perceptual alternation rate of depression patients. These findings indicated that the substantially slower perception switch rate in patients with depression was caused by the greater reliance on top-down priors and that serotonin treatment's efficacy was in its recalibration of these priors and enhancement of PE. Our study not only elucidates the cognitive underpinnings of depression, but also suggests computational modeling as a potent tool for integrating cognitive science with clinical psychology, advancing our understanding and treatment of cognitive impairments in depression.

The role of pattern coherence in interocular grouping during binocular rivalry: Insights from individual differences.

Interocular grouping during binocular rivalry occurs when two images presented to each eye combine into a coherent pattern. The experience of interocular grouping is thought to be influenced by both eye-of-origin, which involves excitatory lateral connections among monocular neurons, and pattern coherence, which results from top-down intervention from higher visual areas. However, it remains unclear which factor plays a more significant role in the interocularly-grouped percepts during binocular rivalry. The current study employed an individual difference approach to investigate whether grouping dynamics are mainly determined by eye-of-origin or pattern coherence. We found that participants who perceived interocularly-driven coherent percepts for a longer duration also tended to experience longer periods of monocularly-driven coherent percepts. In contrast, participants who experienced non-coherent piecemeal percepts for an extended duration in conventional rivalry also had longer duration of non-coherent percepts in the interocular coherence setting. This individual differences in experiencing interocular grouping suggest that pattern coherence exerts a stronger influence on grouping dynamics during binocular rivalry compared to eye-of-origin factors.

Perceptual Resolution of Ambiguity: Can Tuned, Divisive Normalization Account for both Interocular Similarity Grouping and Difference Enhancement.

Our visual system usually provides a unique and functional representation of the external world. At times, however, the visual system has more than one compelling interpretation of the same retinal stimulus; in this case, neural populations compete for perceptual dominance to resolve ambiguity. Spatial and temporal context can guide perceptual experience. Recent evidence shows that ambiguous retinal stimuli are sometimes resolved by enhancing either similarity or differences among multiple percepts. Divisive normalization is a canonical neural computation that enables context-dependent sensory processing by attenuating a neuron's response by other neurons. Experiments here show that divisive normalization can account for perceptual representations of either similarity enhancement (so-called grouping) or difference enhancement, offering a unified framework for opposite perceptual outcomes.

Causal role of the frontal eye field in attention-induced ocular dominance plasticity.

Previous research has found that prolonged eye-based attention can bias ocular dominance. If one eye long-termly views a regular movie meanwhile the opposite eye views a backward movie of the same episode, perceptual ocular dominance will shift towards the eye previously viewing the backward movie. Yet it remains unclear whether the role of eye-based attention in this phenomenon is causal or not. To address this issue, the present study relied on both the functional magnetic resonance imaging (fMRI) and transcranial magnetic stimulation (TMS) techniques. We found robust activation of the frontal eye field (FEF) and intraparietal sulcus (IPS) when participants were watching the dichoptic movie while focusing their attention on the regular movie. Interestingly, we found a robust effect of attention-induced ocular dominance shift when the cortical function of vertex or IPS was transiently inhibited by continuous theta burst stimulation (cTBS), yet the effect was significantly attenuated to a negligible extent when cTBS was delivered to FEF. A control experiment verified that the attenuation of ocular dominance shift after inhibitory stimulation of FEF was not due to any impact of the cTBS on the binocular rivalry measurement of ocular dominance. These findings suggest that the fronto-parietal attentional network is involved in controlling eye-based attention in the 'dichoptic-backward-movie' adaptation paradigm, and in this network, FEF plays a crucial causal role in generating the attention-induced ocular dominance shift.

Binocular rivalry under naturalistic geometry: Evidence from worlds simulated in virtual reality.

Binocular rivalry is a fascinating, widely studied visual phenomenon in which perception alternates between two competing images. This experience, however, is generally restricted to laboratory settings where two irreconcilable images are presented separately to the two eyes, an implausible geometry where two objects occupy the same physical location. Such laboratory experiences are in stark contrast to everyday visual behavior, where rivalry is almost never encountered, casting doubt on whether rivalry is relevant to our understanding of everyday binocular vision. To investigate the external validity of binocular rivalry, we manipulated the geometric plausibility of rival images using a naturalistic, cue-rich, 3D-corridor model created in virtual reality. Rival stimuli were presented in geometrically implausible, semi-plausible, or plausible layouts. Participants tracked rivalry fluctuations in each of these three layouts and for both static and moving rival stimuli. Results revealed significant and canonical binocular rivalry alternations regardless of geometrical plausibility and stimulus type. Rivalry occurred for layouts that mirrored the unnatural geometry used in laboratory studies and for layouts that mimicked real-world occlusion geometry. In a complementary 3D modeling analysis, we show that interocular conflict caused by geometrically plausible occlusion is a common outcome in a visual scene containing multiple objects. Together, our findings demonstrate that binocular rivalry can reliably occur for both geometrically implausible interocular conflicts and conflicts caused by a common form of naturalistic occlusion. Thus, key features of binocular rivalry are not simply laboratory artifacts but generalize to conditions that match the geometry of everyday binocular vision.

Effects of hunger and calorie content on visual awareness of food stimuli.

Calorie content and hunger are two fundamental cues acting upon the processing of visually presented food items. However, whether and to which extent they affect visual awareness is still an open question. Here, high- and low-calorie food images administered to hungry or satiated participants were confronted in a breaking-Continuous Flash Suppression paradigm (Experiment 1), measuring the time required to access to visual awareness, and in a Binocular Rivalry paradigm (Experiment 2), quantifying the dominance time in visual awareness. Experiment 1 showed that high-calorie food accessed faster visual awareness, but mostly in satiated participants. Experiment 2 indicated that high-calorie food dominated longer visual awareness, regardless the degree of hunger. We argued that the unconscious advantage (Experiment 1) would represent a default state of the visual system towards highest-energy nutrients, yet the advantage is lost in hunger so to be tuned towards an increased need for any nutritional category. On the other hand, the conscious advantage of high-calorie food (Experiment 2) would represent a conscious perceptual and attentional bias towards highest energy-dense food useful for the actual detection of these stimuli in the environment.

Revisiting the blind mind: Still no evidence for sensory visual imagery in individuals with aphantasia.

The inability to visualise was given the name aphantasia in 2015 by Zeman and colleagues. In 2018 we published research showing that fifteen individuals who self-identified as having aphantasia also demonstrated a lack of sensory visual imagery when undergoing the binocular rivalry imagery paradigm, suggesting more than just a metacognitive difference. Here we update these findings with over fifty participants with aphantasia and show that there is evidence for a lack of sensory imagery in aphantasia. How the binocular rivalry paradigm scores relate to the vividness of visual imagery questionnaire (VVIQ) and how aphantasia can be confirmed is discussed.

Temporal integration by multi-level regularities fosters the emergence of dynamic conscious experience.

The relationship between integration and awareness is central to contemporary theories and research on consciousness. Here, we investigated whether and how information integration over time, by incorporating the underlying regularities, contributes to our awareness of the dynamic world. Using binocular rivalry, we demonstrated that structured visual streams, constituted by shape, motion, or idiom sequences containing perceptual- or semantic-level regularities, predominated over their nonstructured but otherwise matched counterparts in the competition for visual awareness. Despite the apparent resemblance, a substantial dissociation of the observed rivalry advantages emerged between perceptual- and semantic-level regularities. These effects stem from nonconscious and conscious temporal integration processes, respectively, with the former but not the latter being vulnerable to perturbations in the spatiotemporal integration window. These findings corroborate the essential role of structure-guided information integration in visual awareness and highlight a multi-level mechanism where temporal integration by perceptually and semantically defined regularities fosters the emergence of continuous conscious experience.

When mind and body align: examining the role of cross-modal congruency in conscious representations of happy facial expressions.

This study explored how congruency between facial mimicry and observed expressions affects the stability of conscious facial expression representations. Focusing on the congruency effect between proprioceptive/sensorimotor signals and visual stimuli for happy expressions, participants underwent a binocular rivalry task displaying neutral and happy faces. Mimicry was either facilitated with a chopstick or left unrestricted. Key metrics included Initial Percept (bias indicator), Onset Resolution Time (time from onset to Initial Percept), and Cumulative Time (content stabilization measure). Results indicated that mimicry manipulation significantly impacted Cumulative Time for happy faces, highlighting the importance of congruent mimicry in stabilizing conscious awareness of facial expressions. This supports embodied cognition models, showing the integration of proprioceptive information significantly biases conscious visual perception of facial expressions.

Different Mechanisms for Supporting Mental Imagery and Perceptual Representations: Modulation Versus Excitation.

Recent research suggests imagery is functionally equivalent to a weak form of visual perception. Here we report evidence across five independent experiments on adults that perception and imagery are supported by fundamentally different mechanisms: Whereas perceptual representations are largely formed via increases in excitatory activity, imagery representations are largely supported by modulating nonimagined content. We developed two behavioral techniques that allowed us to first put the visual system into a state of adaptation and then probe the additivity of perception and imagery. If imagery drives similar excitatory visual activity to perception, pairing imagery with perceptual adapters should increase the state of adaptation. Whereas pairing weak perception with adapters increased measures of adaptation, pairing imagery reversed their effects. Further experiments demonstrated that these nonadditive effects were due to imagery weakening representations of nonimagined content. Together these data provide empirical evidence that the brain uses categorically different mechanisms to represent imagery and perception.

State-dependent alterations of implicit emotional dominance during binocular rivalry in subthreshold depression.

Binocular rivalry, a visual perception phenomenon where two or more percepts alternate every few seconds when distinct stimuli are presented to the two eyes, has been reported as a biomarker in several psychiatric disorders. It is unclear whether abnormalities of binocular rivalry in depression could occur when emotional rivaling stimuli are used, and if so, whether an emotional binocular rivalry test could provide a trait-dependent or state-dependent biomarker. In the current study, 34 individuals with subthreshold depression and 31 non-depressed individuals performed a binocular rivalry task associated with implicit emotional processing. Participants were required to report their perceived orientations of the rival gratings in the foreground and to neglect emotional face stimuli in the background. The participants were retested after an approximately 4-month time interval. Compared to the non-depressed group, the subthreshold depression group showed significantly longer perceptual dominance durations of the grating with emotional faces as the background (i.e., implicit emotional dominance) at the initial assessment. However, the abnormality was not found at the follow-up assessment. More importantly, we found smaller changes in depressive severity at the follow-up assessment for individuals displaying longer emotional dominance at the initial assessment than for individuals with weaker emotional dominance. The current emotional binocular rivalry test may provide an objective, state-dependent biomarker for distinguishing individuals with subthreshold depression from non-depressed individuals.

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.

Unconscious face processing shows a different lateralisation pattern.

Faces contain rich information and play a pivotal role in human daily social interactions. Previous studies have provided evidence for the left-visual-field-advantage in face perception. The current study investigated lateralisation when face stimuli were unconsciously presented using interocular suppression methods. The results showed that when an unconscious face stimulus was presented in one side of the visual field without other face stimuli, the unconscious face in the right visual field could break through interocular suppression faster than that in the left (Experiments 1 and 2). However, this right visual field processing advantage reversed to the left when a face stimulus either with (Experiment 2) or without (Experiment 3) visual awareness was presented concurrently with or prior to (Experiment 4) the unconscious face stimuli. These results showed that the unconscious face might have a different processing pattern compared with the conscious face. The relationship between this novel behavioural observation and known functional lateralisation of the fusiform face areas is discussed, suggesting a dynamic interaction between the two cortical hemispheres may underlie the formation of visual awareness for faces. The current study expands our understanding of face processing lateralisation and provided evidence on the asymmetric inter-hemisphere interaction patterns in forming visual awareness.

Binocular rivalry in autistic and socially anxious adults.

Background: Social anxiousness is a pervasive symptom in both social anxiety disorder and autism spectrum conditions. Binocular rivalry, which occurs when different images are presented to each eye, has been used to explore how visual and cognitive processing differs across various clinical diagnoses. Previous studies have separately explored whether individuals with autism or anxiety experience binocular rivalry in ways that are different from neurotypical individuals. Methods: We applied rivalry paradigms that are similar to those used in previous studies of autism and general anxiety to individuals experiencing symptoms of social anxiousness at clinical or subclinical levels. We also incorporated rivalrous stimuli featuring neutral and emotional facial valances to explore potential overlap of social processing components in social anxiety and autism. Results: We hypothesized that higher levels of social anxiousness would increase binocular rivalry switch rates and that higher levels of autistic traits would decrease switch rates. However, stimulus condition did not affect switch rates in either diagnostic group, and switch rate was not significantly predictive of dimensional measures of either autism or social anxiety. Discussion: This may suggest a common mechanism for atypical visual cognition styles previously associated with social anxiety and autism. Alternatively, differences in switch rates may only emerge at higher trait levels than reported by the participants in our studies. Furthermore, these findings may be influenced by sex differences in our unique sample.

Different Forms of Plasticity Interact in Adult Humans.

Neuroplasticity is maximal during development and declines in adulthood, especially for sensory cortices. On the other hand, the motor and prefrontal cortices retain plasticity throughout the lifespan. This difference has led to a modular view of plasticity in which different brain regions have their own plasticity mechanisms that do not depend or translate on others. Recent evidence shows that visual and motor plasticity share common neural mechanisms (e.g., GABAergic inhibition), indicating a possible link between these different forms of plasticity, however, the interaction between visual and motor plasticity has never been tested directly. Here, we show that when visual and motor plasticity are elicited at the same time in adult humans, visual plasticity is impaired, while motor plasticity is spared. Moreover, simultaneous activation of working memory and visual plasticity also leads to impairment in visual plasticity. These unilateral interactions between visual, working memory, and motor plasticity demonstrate a clear link between these three forms of plasticity. We conclude that local neuroplasticity in separate systems might be regulated globally, to preserve overall homeostasis in the brain.

Slowed alpha oscillations and percept formation in psychotic psychopathology.

Introduction: Psychosis is in part defined by disturbances in perception. Recent investigations have implicated the speed of alpha oscillations observed in brain electrical activity as reflective of a sampling rate of the visual environment and perception. Although both slowed alpha oscillations and aberrant percept formation are evident in disorders of psychotic psychopathology such as schizophrenia it is unclear whether slow alpha accounts for abnormal visual perception in these disorders. Methods: To examine the role of the speed of alpha oscillations in perception in psychotic psychopathology we gathered resting-state magneto-encephalography data from probands with psychotic psychopathology (i.e., schizophrenia, schizoaffective disorder, and bipolar disorder with a history of psychosis), their biological siblings, and healthy controls. We appraised visual perceptual function without the confound of cognitive ability and effort through the use of a simple binocular rivalry task. Results: We found a slowed pace of alpha oscillations in psychotic psychopathology that was associated with longer percept durations during binocular rivalry, consistent with the assertion that occipital alpha oscillations govern the rate of accumulation of visual information used to generate percepts. Alpha speed varied widely across individuals with psychotic psychopathology and was highly stable across several months indicating that it is likely a trait characteristic of neural function that is relevant to visual perception. Finally, a lower speed of alpha oscillation was associated with a lower IQ and greater disorder symptomatology implying that the effects of the endogenous neural oscillation on visual perception may have wider consequences for everyday functioning. Discussion: Slowed alpha oscillations in individuals with psychotic psychopathology appear to reflect altered neural functions related to percept formation.

Measuring imagery strength in schizophrenia: no evidence of enhanced mental imagery priming.

INTRODUCTION: Recent research shows ambivalent results regarding the relationship between mental imagery and schizophrenia. The role of voluntary visual imagery in schizophrenic hallucinations remains unclear. The aim of the study was to investigate the association between visual imagery, schizophrenia, and the occurrence of schizophrenic hallucinations using an objective visual imagery task. METHODS: The sample consisted of 16 participants with schizophrenia (59.1% female; MAge  = 45.55) and 44 participants without schizophrenia (62.5% female; MAge  = 43.94). Visual imagery was measured using the Vividness of Visual Imagery Questionnaire (VVIQ) as well as the well-validated Binocular Rivalry Task (BRT). Occurrences of hallucinations were assessed using the Launay-Slade Hallucination Scale. RESULTS: Participants with schizophrenia showed more hallucinatory experiences but did not score higher on either the VVIQ or the BRT than participants without schizophrenia. A correlation between the VVIQ and the BRT was found, validating the measurement of visual imagery and enabling the interpretation that visual imagery vividness is not enhanced in people with schizophrenia. CONCLUSION: The association between mental imagery vividness and schizophrenia found in previous studies may be based on other facets of mental imagery than visual imagery.