Rhythms of Consciousness: Binocular Rivalry Reveals Large-Scale Oscillatory Network Dynamics Mediating Visual Perception

Consciousness has been proposed to emerge from functionally integrated large-scale ensembles of gamma-synchronous neural populations that form and dissolve at a frequency in the theta band. We propose that discrete moments of perceptual experience are implemented by transient gamma-band synchronization of relevant cortical regions, and that disintegration and reintegration of these assemblies is time-locked to ongoing theta oscillations. In support of this hypothesis we provide evidence that (1) perceptual switching during binocular rivalry is time-locked to gamma-band synchronizations which recur at a theta rate, indicating that the onset of new conscious percepts coincides with the emergence of a new gamma-synchronous assembly that is locked to an ongoing theta rhythm; (2) localization of the generators of these gamma rhythms reveals recurrent prefrontal and parietal sources; (3) theta modulation of gamma-band synchronization is observed between and within the activated brain regions. These results suggest that ongoing theta-modulated-gamma mechanisms periodically reintegrate a large-scale prefrontal-parietal network critical for perceptual experience. Moreover, activation and network inclusion of inferior temporal cortex and motor cortex uniquely occurs on the cycle immediately preceding responses signaling perceptual switching. This suggests that the essential prefrontal-parietal oscillatory network is expanded to include additional cortical regions relevant to tasks and perceptions furnishing consciousness at that moment, in this case image processing and response initiation, and that these activations occur within a time frame consistent with the notion that conscious processes directly affect behaviour.     

A Neural Network Approach to fMRI Binocular Visual Rivalry Task Analysis

The purpose of this study was to investigate whether artificial neural networks (ANN) are able to decode participants’ conscious experience perception from brain activity alone, using complex and ecological stimuli. To reach the aim we conducted pattern recognition data analysis on fMRI data acquired during the execution of a binocular visual rivalry paradigm (BR). Twelve healthy participants were submitted to fMRI during the execution of a binocular non-rivalry (BNR) and a BR paradigm in which two classes of stimuli (faces and houses) were presented. During the binocular rivalry paradigm, behavioral responses related to the switching between consciously perceived stimuli were also collected. First, we used the BNR paradigm as a functional localizer to identify the brain areas involved the processing of the stimuli. Second, we trained the ANN on the BNR fMRI data restricted to these regions of interest. Third, we applied the trained ANN to the BR data as a ‘brain reading’ tool to discriminate the pattern of neural activity between the two stimuli. Fourth, we verified the consistency of the ANN outputs with the collected behavioral indicators of which stimulus was consciously perceived by the participants. Our main results showed that the trained ANN was able to generalize across the two different tasks (i.e. BNR and BR) and to identify with high accuracy the cognitive state of the participants (i.e. which stimulus was consciously perceived) during the BR condition. The behavioral response, employed as control parameter, was compared with the network output and a statistically significant percentage of correspondences (p-value <0.05) were obtained for all subjects. In conclusion the present study provides a method based on multivariate pattern analysis to investigate the neural basis of visual consciousness during the BR phenomenon when behavioral indicators lack or are inconsistent, like in disorders of consciousness or sedated patients.     

A Spiking Neuron Model for Binocular Rivalry

We present a biologically plausible model of binocular rivalry consisting of a network of Hodgkin-Huxley type neurons. Our model accounts for the experimentally and psychophysically observed phenomena: (1) it reproduces the distribution of dominance durations seen in both humans and primates, (2) it exhibits a lack of correlation between lengths of successive dominance durations, (3) variation of stimulus strength to one eye influences only the mean dominance duration of the contralateral eye, not the mean dominance duration of the ipsilateral eye, (4) increasing both stimuli strengths in parallel decreases the mean dominance durations. We have also derived a reduced population rate model from our spiking model from which explicit expressions for the dependence of the dominance durations on input strengths are analytically calculated. We also use this reduced model to derive an expression for the distribution of dominance durations seen within an individual.     

How to Create and Use Binocular Rivalry

Each of our eyes normally sees a slightly different image of the world around us. The brain can combine these two images into a single coherent representation. However, when the eyes are presented with images that are sufficiently different from each other, an interesting thing happens: Rather than fusing the two images into a combined conscious percept, what transpires is a pattern of perceptual alternations where one image dominates awareness while the other is suppressed; dominance alternates between the two images, typically every few seconds. This perceptual phenomenon is known as binocular rivalry. Binocular rivalry is considered useful for studying perceptual selection and awareness in both human and animal models, because unchanging visual input to each eye leads to alternations in visual awareness and perception. To create a binocular rivalry stimulus, all that is necessary is to present each eye with a different image at the same perceived location. There are several ways of doing this, but newcomers to the field are often unsure which method would best suit their specific needs. The purpose of this article is to describe a number of inexpensive and straightforward ways to create and use binocular rivalry. We detail methods that do not require expensive specialized equipment and describe each method''s advantages and disadvantages. The methods described include the use of red-blue goggles, mirror stereoscopes and prism goggles.     

A Model of Binocular Rivalry and Cross-orientation Suppression

Binocular rivalry and cross-orientation suppression are well-studied forms of competition in visual cortex, but models of these two types of competition are in tension with one another. Binocular rivalry occurs during the presentation of dichoptic grating stimuli, where two orthogonal gratings presented separately to the two eyes evoke strong alternations in perceptual dominance. Cross-orientation suppression occurs during the presentation of plaid stimuli, where the responses to a component grating presented to both eyes is weakened by the presence of a superimposed orthogonal grating. Conventional models of rivalry that rely on strong competition between orientation-selective neurons incorrectly predict rivalry between the components of plaids. Lowering the inhibitory weights in such models reduces rivalry for plaids, but also reduces it for dichoptic gratings. Using an exhaustive grid search, we show that this problem cannot be solved simply by adjusting the parameters of the model. Instead, we propose a robust class of models that rely on ocular opponency neurons, previously proposed as a mechanism for efficient stereo coding, to yield rivalry only for dichoptic gratings, not for plaids. This class of models reconciles models of binocular rivalry with the divisive normalization framework that has been used to explain cross-orientation. Our model makes novel predictions that we confirmed with psychophysical tests.     

Image-Based Grouping during Binocular Rivalry Is Dictated by Eye-Of-Origin

Prolonged viewing of dichoptically presented images with different content results in perceptual alternations known as binocular rivalry. This phenomenon is thought to be the result of competition at a local level, where local rivalry zones interact to give rise to a single, global dominant percept. Certain perceived combinations that result from this local competition are known to last longer than others, which is referred to as grouping during binocular rivalry. In recent years, the phenomenon has been suggested to be the result of competition at both eye- and image-based processing levels, although the exact contribution from each level remains elusive. Here we use a paradigm designed specifically to quantify the contribution of eye- and image-based processing to grouping during rivalry. In this paradigm we used sine-wave gratings as well as upright and inverted faces, with and without binocular disparity-based occlusion. These stimuli and conditions were used because they are known to result in processing at different stages throughout the visual processing hierarchy. Specifically, more complex images were included in order to maximize the potential contribution of image-based grouping. In spite of this, our results show that increasing image complexity did not lead to an increase in the contribution of image-based processing to grouping during rivalry. In fact, the results show that grouping was primarily affected by the eye-of-origin of the image parts, irrespective of stimulus type. We suggest that image content affects grouping during binocular rivalry at low-level processing stages, where it is intertwined with eye-of-origin information.     

Touch Interacts with Vision during Binocular Rivalry with a Tight Orientation Tuning

Multisensory integration is a common feature of the mammalian brain that allows it to deal more efficiently with the ambiguity of sensory input by combining complementary signals from several sensory sources. Growing evidence suggests that multisensory interactions can occur as early as primary sensory cortices. Here we present incompatible visual signals (orthogonal gratings) to each eye to create visual competition between monocular inputs in primary visual cortex where binocular combination would normally take place. The incompatibility prevents binocular fusion and triggers an ambiguous perceptual response in which the two images are perceived one at a time in an irregular alternation. One key function of multisensory integration is to minimize perceptual ambiguity by exploiting cross-sensory congruence. We show that a haptic signal matching one of the visual alternatives helps disambiguate visual perception during binocular rivalry by both prolonging the dominance period of the congruent visual stimulus and by shortening its suppression period. Importantly, this interaction is strictly tuned for orientation, with a mismatch as small as 7.5° between visual and haptic orientations sufficient to annul the interaction. These results indicate important conclusions: first, that vision and touch interact at early levels of visual processing where interocular conflicts are first detected and orientation tunings are narrow, and second, that haptic input can influence visual signals outside of visual awareness, bringing a stimulus made invisible by binocular rivalry suppression back to awareness sooner than would occur without congruent haptic input.     

Influence of Contrast and Coherence on the Temporal Dynamics of Binocular Motion Rivalry

Levelt’s 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.     

Naturalistic Stimulus Structure Determines the Integration of Audiovisual Looming Signals in Binocular Rivalry

Rapid integration of biologically relevant information is crucial for the survival of an organism. Most prominently, humans should be biased to attend and respond to looming stimuli that signal approaching danger (e.g. predator) and hence require rapid action. This psychophysics study used binocular rivalry to investigate the perceptual advantage of looming (relative to receding) visual signals (i.e. looming bias) and how this bias can be influenced by concurrent auditory looming/receding stimuli and the statistical structure of the auditory and visual signals.Subjects were dichoptically presented with looming/receding visual stimuli that were paired with looming or receding sounds. The visual signals conformed to two different statistical structures: (1) a ‘simple’ random-dot kinematogram showing a starfield and (2) a “naturalistic” visual Shepard stimulus. Likewise, the looming/receding sound was (1) a simple amplitude- and frequency-modulated (AM-FM) tone or (2) a complex Shepard tone. Our results show that the perceptual looming bias (i.e. the increase in dominance times for looming versus receding percepts) is amplified by looming sounds, yet reduced and even converted into a receding bias by receding sounds. Moreover, the influence of looming/receding sounds on the visual looming bias depends on the statistical structure of both the visual and auditory signals. It is enhanced when audiovisual signals are Shepard stimuli.In conclusion, visual perception prioritizes processing of biologically significant looming stimuli especially when paired with looming auditory signals. Critically, these audiovisual interactions are amplified for statistically complex signals that are more naturalistic and known to engage neural processing at multiple levels of the cortical hierarchy.     

Separating Fusion from Rivalry

Visual fusion is the process in which differing but compatible binocular information is transformed into a unified percept. Even though this is at the basis of binocular vision, the underlying neural processes are, as yet, poorly understood. In our study we therefore aimed to investigate neural correlates of visual fusion. To this end, we presented binocularly compatible, fusible (BF), and incompatible, rivaling (BR) stimuli, as well as an intermediate stimulus type containing both binocularly fusible and monocular, incompatible elements (BFR). Comparing BFR stimuli with BF and BR stimuli, respectively, we were able to disentangle brain responses associated with either visual fusion or rivalry. By means of functional magnetic resonance imaging, we measured brain responses to these stimulus classes in the visual cortex, and investigated them in detail at various retinal eccentricities. Compared with BF stimuli, the response to BFR stimuli was elevated in visual cortical areas V1 and V2, but not in V3 and V4 – implying that the response to monocular stimulus features decreased from V1 to V4. Compared to BR stimuli, the response to BFR stimuli decreased with increasing eccentricity, specifically within V3 and V4. Taken together, it seems that although the processing of exclusively monocular information decreases from V1 to V4, the processing of binocularly fused information increases from earlier to later visual areas. Our findings suggest the presence of an inhibitory neural mechanism which, depending on the presence of fusion, acts differently on the processing of monocular information.     

Influence of Retinal Image Shifts and Extra-Retinal Eye Movement Signals on Binocular Rivalry Alternations

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.     

Binaral Rivalry in the Presence of Visual Perceptual and Semantic Influences

When two different odorants are presented simultaneously to the two nostrils, we experience alternations in olfactory percepts, a phenomenon called binaral rivalry. Little is known about the nature of such alternations. Here we investigate this issue by subjecting unstable and stable olfactory percepts to the influences of visual perceptual or semantic cues as participants engage in simultaneous samplings of either two different odorants (binaral) or a single odorant and water (mononaral), one to each nostril. We show that alternations of olfactory percepts in the binaral setting persist in the presence of visual perceptual and semantic modulations. We also show that perceptual cues have a stronger effect than semantic cues in the binaral case, whereas their effects are comparable in the mononaral setting. Our findings provide evidence that an inherent, stimulus-driven process underlies binaral rivalry despite its general susceptibility to top-down influences.