Bistable percepts in the brain: FMRI contrasts monocular pattern rivalry and binocular rivalry

The neural correlates of binocular rivalry have been actively debated in recent years, and are of considerable interest as they may shed light on mechanisms of conscious awareness. In a related phenomenon, monocular rivalry, a composite image is shown to both eyes. The subject experiences perceptual alternations in which the two stimulus components alternate in clarity or salience. The experience is similar to perceptual alternations in binocular rivalry, although the reduction in visibility of the suppressed component is greater for binocular rivalry, especially at higher stimulus contrasts. We used fMRI at 3T to image activity in visual cortex while subjects perceived either monocular or binocular rivalry, or a matched non-rivalrous control condition. The stimulus patterns were left/right oblique gratings with the luminance contrast set at 9%, 18% or 36%. Compared to a blank screen, both binocular and monocular rivalry showed a U-shaped function of activation as a function of stimulus contrast, i.e. higher activity for most areas at 9% and 36%. The sites of cortical activation for monocular rivalry included occipital pole (V1, V2, V3), ventral temporal, and superior parietal cortex. The additional areas for binocular rivalry included lateral occipital regions, as well as inferior parietal cortex close to the temporoparietal junction (TPJ). In particular, higher-tier areas MT+ and V3A were more active for binocular than monocular rivalry for all contrasts. In comparison, activation in V2 and V3 was reduced for binocular compared to monocular rivalry at the higher contrasts that evoked stronger binocular perceptual suppression, indicating that the effects of suppression are not limited to interocular suppression in V1.     

A model for nonlinear stochastic behavior of the pupil

In binocular fusion, pairs of left and right stimuli yielding the same brightness perception constitute an equibrightness curve in a coordinate system whose ordinate and abscissa correspond to the left and right stimulus strengths. A neural network model is presented to elucidate the characteristics of the curve. According to the model, Fechner's paradox is due to the threshold characteristics of the neuron. If the shapes or movements are radically different between the left and right stimuli, the retinal rivalry is caused. That is, only the left stimulus is perceived at one moment and the right stimulus at another moment. The period of left or right eye dominance alternates randomly from time to time. The distribution of the period is approximate to the gamma distribution. In order to account for this fact, a neural network model is proposed, which consists of a pair of neurons receiving inputs with stochastic fluctuations. The computer simulation was carried out with satisfactory results. The model of retinal rivalry is integrated with that of brightness perception.     

Onset rivalry: brief presentation isolates an early independent phase of perceptual competition

When the left and right eyes are simultaneously presented with different images, observers typically report exclusive awareness of only one image. This phenomenon is termed binocular rivalry, reflecting the fact that the dominant image alternates every few seconds in a cycle of perceptual competition that continues indefinitely. Despite the apparent continuity in perceptual switching, we now demonstrate that the initial "onset" period is fundamentally different to all subsequent rivalry epochs. Using brief intermittent presentations, rivalry dominance shows strong biases such that the same target is perceived with each successive stimulus onset. These biases remain consistent within any given location, but vary across the visual field in a distribution that is stable over multiple weeks but highly idiosyncratic across observers. If the presentation exceeds approximately 1sec at any location, however, the very different and much more balanced alternations of sustained binocular rivalry become apparent. These powerful onset biases are observed with brief intermittent presentations at a single location or with continual smooth motion of the targets. Periods of adaptation to one of the rivaling targets induced local switches in dominance to the non-adapted target. However, these effects were generally limited to the spatial site of adaptation and had less influence over each subsequent cycle of the target. We conclude that onset rivalry is independent of sustained rivalry and cannot be explained by local regions of monocular dominance or memory of past perceptual history, but rather reflects low-level, spatially localized factors that are stable over periods of weeks. These findings suggest that brief presentation paradigms are inappropriate for their current use in studies of the mechanisms underlying sustained rivalry. However, brief presentations are ideal for investigating early stages of perceptual competition.     

General validity of Levelt's propositions reveals common computational mechanisms for visual rivalry

The mechanisms underlying conscious visual perception are often studied with either binocular rivalry or perceptual rivalry stimuli. Despite existing research into both types of rivalry, it remains unclear to what extent their underlying mechanisms involve common computational rules. Computational models of binocular rivalry mechanisms are generally tested against Levelt's four propositions, describing the psychophysical relation between stimulus strength and alternation dynamics in binocular rivalry. Here we use a bistable rotating structure-from-motion sphere, a generally studied form of perceptual rivalry, to demonstrate that Levelt's propositions also apply to the alternation dynamics of perceptual rivalry. Importantly, these findings suggest that bistability in structure-from-motion results from active cross-inhibition between neural populations with computational principles similar to those present in binocular rivalry. Thus, although the neural input to the computational mechanism of rivalry may stem from different cortical neurons and different cognitive levels the computational principles just prior to the production of visual awareness appear to be common to the two types of rivalry.     

The spatial origin of a perceptual transition in binocular rivalry

When the left and the right eye are simultaneously presented with incompatible images at overlapping retinal locations, an observer typically reports perceiving only one of the two images at a time. This phenomenon is called binocular rivalry. Perception during binocular rivalry is not stable; one of the images is perceptually dominant for a certain duration (typically in the order of a few seconds) after which perception switches towards the other image. This alternation between perceptual dominance and suppression will continue for as long the images are presented. A characteristic of binocular rivalry is that a perceptual transition from one image to the other generally occurs in a gradual manner: the image that was temporarily suppressed will regain perceptual dominance at isolated locations within the perceived image, after which its visibility spreads throughout the whole image. These gradual transitions from perceptual suppression to perceptual dominance have been labeled as traveling waves of perceptual dominance. In this study we investigate whether stimulus parameters affect the location at which a traveling wave starts. We varied the contrast, spatial frequency or motion speed in one of the rivaling images, while keeping the same parameter constant in the other image. We used a flash-suppression paradigm to force one of the rival images into perceptual suppression. Observers waited until the suppressed image became perceptually dominant again, and indicated the position at which this breakthrough from suppression occurred. Our results show that the starting point of a traveling wave during binocular rivalry is highly dependent on local stimulus parameters. More specifically, a traveling wave most likely started at the location where the contrast of the suppressed image was higher than that of the dominant one, the spatial frequency of the suppressed image was lower than that of the dominant one, and the motion speed of the suppressed image was higher than that of the dominant one. We suggest that a breakthrough from suppression to dominance occurs at the location where salience (the degree to which a stimulus element stands out relative to neighboring elements) of the suppressed image is higher than that of the dominant one. Our results further show that stimulus parameters affecting the temporal dynamics during continuous viewing of rival images described in other studies, also affect the spatial origin of traveling waves during binocular rivalry.     

Color and luminance influence, but can not explain, binocular rivalry onset bias

When an observer is presented with dissimilar images to the right and left eye, the images will alternate every few seconds in a phenomenon known as binocular rivalry. During sustained viewing, the timing of these switches appears to be unpredictable. Recent research has suggested that the initial 'onset' period of rivalry is not random and may be different in its neural mechanism than subsequent dominance periods. It is known that differences in luminance and contrast have a significant influence on the average dominance during sustained rivalry and that perception of luminance can vary between individuals and across the visual field. We therefore investigated whether perception of luminance contrast plays a role in onset rivalry. Observers viewed rival targets of equal brightness for brief presentations in eight locations of the near periphery and reported the color that was first dominant in each location. Results show that minimizing differences in brightness and contrast yields a stronger pattern of onset dominance bias and reveals evidence of monocular dominance. The results suggest that both contrast and monocular dominance play a role in onset dominance, though neither can fully explain the effect.     

Neural field model of binocular rivalry waves

We present a neural field model of binocular rivalry waves in visual cortex. For each eye we consider a one-dimensional network of neurons that respond maximally to a particular feature of the corresponding image such as the orientation of a grating stimulus. Recurrent connections within each one-dimensional network are assumed to be excitatory, whereas connections between the two networks are inhibitory (cross-inhibition). Slow adaptation is incorporated into the model by taking the network connections to exhibit synaptic depression. We derive an analytical expression for the speed of a binocular rivalry wave as a function of various neurophysiological parameters, and show how properties of the wave are consistent with the wave-like propagation of perceptual dominance observed in recent psychophysical experiments. In addition to providing an analytical framework for studying binocular rivalry waves, we show how neural field methods provide insights into the mechanisms underlying the generation of the waves. In particular, we highlight the important role of slow adaptation in providing a “symmetry breaking mechanism” that allows waves to propagate.     

A model of binocular brightness and binaural loudness perception in humans with general applications to nonlinear summation of sensory inputs

A single neural model is proposed to account for how responses of the two eyes and two ears combine to form the perception of binocular brightness and binaural loudness respectively. It involves nonlinear reciprocal feedback inhibition between left and right channels, followed by linear summation between the channels. Local circuit synaptic interactions are an important source of nonlinearity. The model combines inputs in a manner that approximates vector magnitude models in general. This suggests that the model can be applied to a variety of circumstances beyond the visual and auditory data discussed here.     

Neurontropy,an entropy-like measure of neural correlation,in binocular fusion and rivalry

Dynamic random dot stereograms were generated for which the left and right arrays were either identical (100% correlation), or uncorrelated (0% correlation), or the complements of each other (-100% correlation). Any two of these three states of correlation were presented in succession and duration thresholds for detecting the transitions were measured. These thresholds were much longer when the transition went from the uncorrelated state to the correlated state than vice versa. In order to explain the detection thresholds for the various transitions a model based on the notion of an entropy-like measure (to be called neurontropy) has been proposed. It was assumed that in binocular vision both a fusional and a rivalry process operate simultaneously, but in a dual fashion. Thus the correlated state would be regarded the same way by the fusional process as the complemented state by the rivalry process. Transitions from the uncorrelated to the complemented state (and vice versa) were the most difficult to detect, a task which only the rivalry process could accomplish. The long detection thresholds indicate that the rivalry process is less efficient than the fusional process.Address Fill Oct. 1, 1976: Prof. Dr. B. Julesz     

Visible binocular beats from invisible monocular stimuli during binocular rivalry

When two qualitatively different stimuli are presented at the same time, one to each eye, the stimuli can either integrate or compete with each other. When they compete, one of the two stimuli is alternately suppressed, a phenomenon called binocular rivalry [1,2]. When they integrate, observers see some form of the combined stimuli. Many different properties (for example, shape or color) of the two stimuli can induce binocular rivalry. Not all differences result in rivalry, however. Visual 'beats', for example, are the result of integration of high-frequency flicker between the two eyes [3,4], and are thus a binocular fusion phenomenon. It remains in dispute whether binocular fusion and rivalry can co-exist with one another [5-7]. Here, we report that rivalry and beats, two apparently opposing phenomena, can be perceived at the same time within the same spatial location. We hypothesized that the interocular difference in visual attributes that are predominantly processed in the Parvocellular pathway will lead to rivalry, and differences in visual attributes that are predominantly processed in the Magnocellular pathway tend to integrate. Further predictions based on this hypothesis were tested and confirmed.     

The neural transfer characteristic (neurontropy) for binocular stochastic stimulation

Our binocular fusion/rivalry model for the processing of interocular correlations was extended to partial correlations. The results support the concepts of fusion/rivalry inhibition, of catabolism, of adaptation and of the power transforms of correlational information. They also indicate that the neural transfer characteristic for interocular correlation, (also called neurontropy), is highly nonlinear with respect to the degree of mathematical correlation.Address Fill Oct. 1, 1976: Prof. Dr. B. Julesz     

Binocular rivalry requires visual attention

An interocular conflict arises when different images are presented to each eye at the same spatial location. The visual system resolves this conflict through binocular rivalry: observers consciously perceive spontaneous alternations between the two images. Visual attention is generally important for resolving competition between neural representations. However, given the seemingly spontaneous and automatic nature of binocular rivalry, the role of attention in resolving interocular competition remains unclear. Here we test whether visual attention is necessary to?produce rivalry. Using an EEG frequency-tagging method to track cortical representations of the conflicting images, we show that when attention was diverted away, rivalry stopped. The EEG data further suggested that the neural representations of the dichoptic images combined without attention. Thus, attention is necessary for dichoptic images to be engaged in sustained rivalry and may be generally required for resolving conflicting, potentially ambiguous input and giving a single interpretation access to consciousness.     

Stimulus motion propels traveling waves in binocular rivalry

State transitions in the nervous system often take shape as traveling waves, whereby one neural state is replaced by another across space in a wave-like manner. In visual perception, transitions between the two mutually exclusive percepts that alternate when the two eyes view conflicting stimuli (binocular rivalry) may also take shape as traveling waves. The properties of these waves point to a neural substrate of binocular rivalry alternations that have the hallmark signs of lower cortical areas. In a series of experiments, we show a potent interaction between traveling waves in binocular rivalry and stimulus motion. The course of the traveling wave is biased in the motion direction of the suppressed stimulus that gains dominance by means of the wave-like transition. Thus, stimulus motion may propel the traveling wave across the stimulus to the extent that the stimulus motion dictates the traveling wave's direction completely. Using a computational model, we show that a speed-dependent asymmetry in lateral inhibitory connections between retinotopically organized and motion-sensitive neurons can explain our results. We argue that such a change in suppressive connections may play a vital role in the resolution of dynamic occlusion situations.     

A 'sticky' interhemispheric switch in bipolar disorder?

Despite years of research into bipolar disorder (manic depression), its underlying pathophysiology remains elusive. It is widely acknowledged that the disorder is strongly heritable, but the genetics are complex with less than full concordance in monozygotic twins and at least four susceptibility loci identified. We propose that bipolar disorder is the result of a genetic propensity for slow interhemispheric switching mechanisms that become ''stuck'' in one or the other state. Because slow switches are also ''sticky'' when compared with fast switches, the clinical manifestations of bipolar disorder may be explained by hemispheric activation being ''stuck'' on the left (mania) or on the right (depression). Support for this ''sticky'' interhemispheric switching hypothesis stems from our recent observation that the rate of perceptual alternation in binocular rivalry is slow in euthymic subjects with bipolar disorder (n = 18, median = 0.27 Hz) compared with normal controls (n = 49, median = 0.60 Hz, p < 0.0005). We have presented evidence elsewhere that binocular rivalry is itself an interhemispheric switching phenomenon. The rivalry alternation rate (putative interhemispheric switch rate) is robust in a given individual, with a test-retest correlation of more than 0.8, making it suitable for genetic studies. The interhemispheric switch rate may provide a trait-dependent biological marker for bipolar disorder.     

Disrupting parietal function prolongs dominance durations in binocular rivalry

Human brain imaging studies of bistable perceptual phenomena revealed that frontal and parietal areas are activated during perceptual switches between the two conflicting percepts. However, these studies do not provide information about causality, i.e., whether activity reports a consequence or a cause of the perceptual change. Here we used functional magnetic resonance imaging to individually localize four parietal regions involved in perceptual switches during binocular rivalry in 15 subjects and subsequently disturbed their neural processing and that of a control site using 2 Hz repetitive transcranial magnetic stimulation (TMS) during binocular rivalry. We found that TMS over one of the sites, the right intraparietal sulcus (IPS), prolonged the periods of stable percepts. Additionally, the more lateralized the blood oxygen level-dependent signal was in IPS, the more lateralized the TMS effects were. Lateralization varied considerably across subjects, with a right-hemispheric bias. Control replay experiments rule out nonspecific effects of TMS on task performance, reaction times, or eye blinks. Our results thus demonstrate a causal, destabilizing, and individually lateralized effect of normal IPS function on perceptual continuity in rivalry. This is in accord with a role of IPS in perceptual selection, relating its role in rivalrous perception to that in attention.     

A fresh look at the temporal dynamics of binocular rivalry

Human observers viewed dichoptic orthogonal sine-wave gratings and indicated when exclusive visibility occurred in either eye. Contrast was held constant in one eye and was increased or decreased in the other eye for a number of alternation cycles (continuous presentation) or for only the duration of a single period of exclusive visibility (synchronous presentation). The synchronous presentation condition allowed us to identify the differing effects of contrast during the suppressed and during the dominant periods. Mixed phases were recorded as distinct from suppressed and dominant phases, and new classifications of compound-dominant and compound-suppressed phases are defined. The results indicate that binocular rivalry responds to stimulus contrast in two ways. 1) The duty-cycle of dominance and suppression is determined by the relative image contrast between the two eyes, with dominance of the higher contrast image being favored, and 2) the overall rate of alternation is driven by monocular image contrast during the suppressed phase (increased monocular contrast increases the alternation rate) and to a lesser extent by monocular contrast during the dominant phase (increased monocular contrast decreases the rate). A model is developed to reflect these ideas. These results support a reciprocal inhibition oscillator as the underlying mechanism of binocular rivalry.     

Binocular onset rivalry at the time of saccades and stimulus jumps

Recent studies suggest that binocular rivalry at stimulus onset, so called onset rivalry, differs from rivalry during sustained viewing. These observations raise the interesting question whether there is a relation between onset rivalry and rivalry in the presence of eye movements. We therefore studied binocular rivalry when stimuli jumped from one visual hemifield to the other, either through a saccade or through a passive stimulus displacement, and we compared rivalry after such displacements with onset and sustained rivalry. We presented opponent motion, orthogonal gratings and face/house stimuli through a stereoscope. For all three stimulus types we found that subjects showed a strong preference for stimuli in one eye or one hemifield (Experiment 1), and that these subject-specific biases did not persist during sustained viewing (Experiment 2). These results confirm and extend previous findings obtained with gratings. The results from the main experiment (Experiment 3) showed that after a passive stimulus jump, switching probability was low when the preferred eye was dominant before a stimulus jump, but when the non-preferred eye was dominant beforehand, switching probability was comparatively high. The results thus showed that dominance after a stimulus jump was tightly related to eye dominance at stimulus onset. In the saccade condition, however, these subject-specific biases were systematically reduced, indicating that the influence of saccades can be understood from a systematic attenuation of the subjects' onset rivalry biases. Taken together, our findings demonstrate a relation between onset rivalry and rivalry after retinal shifts and involvement of extra-retinal signals in binocular rivalry.     

Perceptual rivalry between illusory and real contours

The interactions between illusory and real contours have been investigated under monocular, binocular and dichoptic conditions. Results show that under all three presentation conditions, periodic alternations, generally called rivalry, occur during the perception of cognitive (or illusory) triangles, while earlier research had failed to find such rivalry (Bradley and Dumais 1975). With line triangles, rivalry is experienced only under dichoptic conditions. A model is proposed to account for the observed phenomena.     

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.     

On the role of attention in binocular rivalry: electrophysiological evidence

During binocular rivalry visual consciousness fluctuates between two dissimilar monocular images. We investigated the role of attention in this phenomenon by comparing event-related potentials (ERPs) when binocular-rivalry stimuli were attended with when they were unattended. Stimuli were dichoptic, orthogonal gratings that yielded binocular rivalry and dioptic, identically oriented gratings that yielded binocular fusion. Events were all possible orthogonal changes in orientation of one or both gratings. We had two attention conditions: In the attend-to-grating condition, participants had to report changes in perceived orientation, focussing their attention on the gratings. In the attend-to-fixation condition participants had to report changes in a central fixation target, taking attention away from the gratings. We found, surprisingly, that attending to rival gratings yielded a smaller ERP component (the N1, from 160-210 ms) than attending to the fixation target. To explain this paradoxical effect of attention, we propose that rivalry occurs in the attend-to-fixation condition (we found an ERP signature of rivalry in the form of a sustained negativity from 210-300 ms) but that the mechanism processing the stimulus changes is more adapted in the attend-to-grating condition than in the attend-to-fixation condition. This is consistent with the theory that adaptation gives rise to changes of visual consciousness during binocular rivalry.