Single units and conscious vision.

Figures that can be seen in more than one way are invaluable tools for the study of the neural basis of visual awareness, because such stimuli permit the dissociation of the neural responses that underlie what we perceive at any given time from those forming the sensory representation of a visual pattern. To study the former type of responses, monkeys were subjected to binocular rivalry, and the response of neurons in a number of different visual areas was studied while the animals reported their alternating percepts by pulling levers. Perception-related modulations of neural activity were found to occur to different extents in different cortical visual areas. The cells that were affected by suppression were almost exclusively binocular, and their proportion was found to increase in the higher processing stages of the visual system. The strongest correlations between neural activity and perception were observed in the visual areas of the temporal lobe. A strikingly large number of neurons in the early visual areas remained active during the perceptual suppression of the stimulus, a finding suggesting that conscious visual perception might be mediated by only a subset of the cells exhibiting stimulus selective responses. These physiological findings, together with a number of recent psychophysical studies, offer a new explanation of the phenomenon of binocular rivalry. Indeed, rivalry has long been considered to be closely linked with binocular fusion and stereopsis, and the sequences of dominance and suppression have been viewed as the result of competition between the two monocular channels. The physiological data presented here are incompatible with this interpretation. Rather than reflecting interocular competition, the rivalry is most probably between the two different central neural representations generated by the dichoptically presented stimuli. The mechanisms of rivalry are probably the same as, or very similar to, those underlying multistable perception in general, and further physiological studies might reveal much about the neural mechanisms of our perceptual organization.     

Fusion and rivalry are dependent on the perceptual meaning of visual stimuli

We view the world with two eyes and yet are typically only aware of a single, coherent image. Arguably the simplest explanation for this is that the visual system unites the two monocular stimuli into a common stream that eventually leads to a single coherent sensation. However, this notion is inconsistent with the well-known phenomenon of rivalry; when physically different stimuli project to the same retinal location, the ensuing perception alternates between the two monocular views in space and time. Although fundamental for understanding the principles of binocular vision and visual awareness, the mechanisms under-lying binocular rivalry remain controversial. Specifically, there is uncertainty about what determines whether monocular images undergo fusion or rivalry. By taking advantage of the perceptual phenomenon of color contrast, we show that physically identical monocular stimuli tend to rival-not fuse-when they signify different objects at the same location in visual space. Conversely, when physically different monocular stimuli are likely to represent the same object at the same location in space, fusion is more likely to result. The data suggest that what competes for visual awareness in the two eyes is not the physical similarity between images but the similarity in their perceptual/empirical meaning.     

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.     

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.     

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.     

Independent binocular rivalry processes for motion and form

During binocular rivalry, conflicting monocular images undergo alternating suppression. This study explores rivalry suppression by probing visual sensitivity during rivalry with various probe stimuli. When two faces engage in rivalry, sensitivity to face probes is reduced 4-fold during suppression. Rivaling global motions also rivaled very deeply when probed with a global motion. However, in a surprising finding, sensitivity to face probes is completely unimpaired during global motion rivalry, and motion sensitivity is unimpaired during face rivalry. This suggests that rivalry suppression is localized to the neurons representing the image conflict, which means that probes of a different kind suffer no suppression. Sensibly, this would leave visual processes not involved in rivalry free to function normally.     

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.     

Dichoptic plaids may rival, but their motions can integrate

When the eyes view incompatible images, binocular rivalry usually results: image constituents in corresponding parts of the monocular visual fields are not perceived simultaneously. We asked naive undergraduates to view dichoptic, dioptic, and monoptic plaids. The dichoptic images evoked strong binocular rivalry when contrast was high, especially if the component gratings were set in motion. Nevertheless, the subjects' visual systems integrated the motion information across the two eyes, producing a unitary motion percept that did not reflect the image in either eye alone. By manipulating the relative spatial scale of the gratings, we affected how well the motion cohered: the results were remarkably similar between dichoptic and traditional dioptic plaids. By manipulating the relative speed of the gratings, we systematically affected the perceived direction of motion of the plaids; these results were also remarkably similar for dichoptic and dioptic plaids. Thus, the motion analysis of dichoptic and dioptic plaids is proceeding according to very similar rules, even though the dichoptic images are incompatible and evoke binocular rivalry.     

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.     

Interhemispheric switching mediates perceptual rivalry

BACKGROUND: Binocular rivalry refers to the alternating perceptual states that occur when the images seen by the two eyes are too different to be fused into a single percept. Logothetis and colleagues have challenged suggestions that this phenomenon occurs early in the visual pathway. They have shown that, in alert monkeys, neurons in the primary visual cortex continue to respond to their preferred stimulus despite the monkey reporting its absence. Moreover, they found that neural activity higher in the visual pathway is highly correlated with the monkey's reported percept. These and other findings suggest that the neural substrate of binocular rivalry must involve high levels, perhaps the same levels involved in reversible figure alternations. RESULTS: We present evidence that activation or disruption of a single hemisphere in human subjects affects the perceptual alternations of binocular rivalry. Unilateral caloric vestibular stimulation changed the ratio of time spent in each competing perceptual state. Transcranial magnetic stimulation applied to one hemisphere disrupted normal perceptual alternations when the stimulation was timed to occur at one phase of the perceptual switch, but not at the other. Furthermore, activation of a single hemisphere by caloric stimulation affected the perceptual alternations of a reversible figure, the Necker cube. CONCLUSIONS: Our findings suggest that interhemispheric switching mediates perceptual rivalry. Thus, competition for awareness in both binocular rivalry and reversible figures occurs between, rather than within, each hemisphere. This interhemispheric switch hypothesis has implications for understanding the neural mechanisms of conscious experience and also has clinical relevance as the rate of both types of perceptual rivalry is slow in bipolar disorder (manic depression).     

The dynamic model of binocular rivalry

Binocular rivalry is an interesting phenomenon observed in the human vision. It occurs when the right and left eyes are given different stimuli (pictures). This paper describes a mathematical model which explains the mechanism of binocular rivalry. Our basic assumption is that binocular rivalry is elicited by the mutual inhibition between the right and left visual neuron systems. The mutual inhibition between two neurons is first discussed in detail, where a special emphasis is put on a fatigue effect of neurons, and then its results are applied to a simulation model of binocular rivalry.     

Female competition for availability of males in insects: the Nezara viridula (Linnaeus, 1758) model

Multimodal communication in solitary stinkbugs enables them to meet, mate and copulate. Many plant‐dwelling species exchange information during the calling phase of mating behavior using substrate‐borne vibratory signals. A female‐biased gender ratio induces rivalry and competition for a sexual partner. Female competition for males, first described among Heteroptera in three stinkbug species, revealed species specific differences and opened the question of plasticity in individually emitted temporal and frequency signal characteristics during calling and rival alternation. To address this question and gain an insight into the mechanisms underlying stinkbug female rivalry, we compared the characteristics of alternated signals in the southern green stinkbug Nezara viridula (Linnaeus, 1758) (Hemiptera: Pentatomidae). Compared to male rivalry, female rivalry is more complex, lasts longer and runs through successive phases by a combination of different song types. The male pheromone triggers alternation between females, producing song pulses that occasionally overlap each other. One female initiates the rivalry by changing individual pulses into pulse trains of three different types. The competing female alternates with pulses of changed temporal characteristics at lower levels of rivalry and by varying the frequency characteristics of pulse trains at higher levels. During female rivalry, the male either stops responding or occasionally emits calling and courtship signals in response to the female that has produced signals of steady temporal characteristics. Female rivalry shows complex and species specific patterns of information exchange at different levels with a broad‐range variation of temporal and frequency characteristics of, until now, unidentified vibratory emissions.     

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.     

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.     

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.     

The role of temporally coarse form processing during binocular rivalry

Presenting the eyes with spatially mismatched images causes a phenomenon known as binocular rivalry-a fluctuation of awareness whereby each eye's image alternately determines perception. Binocular rivalry is used to study interocular conflict resolution and the formation of conscious awareness from retinal images. Although the spatial determinants of rivalry have been well-characterized, the temporal determinants are still largely unstudied. We confirm a previous observation that conflicting images do not need to be presented continuously or simultaneously to elicit binocular rivalry. This process has a temporal limit of about 350 ms, which is an order of magnitude larger than the visual system's temporal resolution. We characterize this temporal limit of binocular rivalry by showing that it is independent of low-level information such as interocular timing differences, contrast-reversals, stimulus energy, and eye-of-origin information. This suggests the temporal factors maintaining rivalry relate more to higher-level form information, than to low-level visual information. Systematically comparing the role of form and motion-the processing of which may be assigned to ventral and dorsal visual pathways, respectively-reveals that this temporal limit is determined by form conflict rather than motion conflict. Together, our findings demonstrate that binocular conflict resolution depends on temporally coarse form-based processing, possibly originating in the ventral visual pathway.     

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.     

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.     

Long-term speeding in perceptual switches mediated by attention-dependent plasticity in cortical visual processing

Binocular rivalry has been extensively studied to understand the mechanisms that control switches in visual awareness and much has been revealed about the contributions of stimulus and cognitive factors. Because visual processes are fundamentally adaptive, however, it is also important to understand how experience alters the dynamics of perceptual switches. When observers viewed binocular rivalry repeatedly over many days, the rate of perceptual switches increased as much as 3-fold. This long-term rivalry speeding exhibited a pattern of image-feature specificity that ruled out primary contributions from strategic and nonsensory factors and implicated neural plasticity occurring in both low- and high-level visual processes in the ventral stream. Furthermore, the speeding occurred only when the rivaling patterns were voluntarily attended, suggesting that the underlying neural plasticity selectively engages when stimuli are behaviorally relevant. Long-term rivalry speeding may thus reflect broader mechanisms that facilitate quick assessments of signals that contain multiple behaviorally relevant interpretations.     

Perceptual grouping of biological motion promotes binocular rivalry

Investigation of perceptual rivalry between conflicting stimuli presented one to each eye can further understanding of the neural underpinnings of conscious visual perception. During rivalry, visual awareness fluctuates between perceptions of the two stimuli. Here, we demonstrate that high-level perceptual grouping can promote rivalry between stimulus pairs that would otherwise be perceived as nonrivalrous. Perceptual grouping was generated with point-light walker stimuli that simulate human motion, visible only as lights placed on the joints. Although such walking figures are unrecognizable when stationary, recognition judgments as complex as gender and identity can accurately be made from animated displays, demonstrating the efficiency with which our visual system can group dynamic local signals into a globally coherent walking figure. We find that point-light walker stimuli presented one to each eye and in different colors and configurations results in strong rivalry. However, rivalry is minimal when the two walkers are split between the eyes or both presented to one eye. This pattern of results suggests that processing animated walker figures promotes rivalry between signals from the two eyes rather than between higher-level representations of the walkers. This leads us to hypothesize that awareness during binocular rivalry involves the integrated activity of high-level perceptual mechanisms in conjunction with lower-level ocular suppression modulated via cortical feedback.