Temporal binding, binocular rivalry, and consciousness.

Cognitive functions like perception, memory, language, or consciousness are based on highly parallel and distributed information processing by the brain. One of the major unresolved questions is how information can be integrated and how coherent representational states can be established in the distributed neuronal systems subserving these functions. It has been suggested that this so-called "binding problem" may be solved in the temporal domain. The hypothesis is that synchronization of neuronal discharges can serve for the integration of distributed neurons into cell assemblies and that this process may underlie the selection of perceptually and behaviorally relevant information. As we intend to show here, this temporal binding hypothesis has implications for the search of the neural correlate of consciousness. We review experimental results, mainly obtained in the visual system, which support the notion of temporal binding. In particular, we discuss recent experiments on the neural mechanisms of binocular rivalry which suggest that appropriate synchronization among cortical neurons may be one of the necessary conditions for the buildup of perceptual states and awareness of sensory stimuli.     

The site of binocular rivalry suppression.

Two experiments were performed to localize the site of binocular rivalry suppression in relation to the locus of grating adaptation. In one experiment it was found that phenomenal suppression of a high-contrast adaptation grating presented to one eye had no influence on the strength of the threshold-elevation aftereffect measured interocularly. Evidently information about the adaptation grating arrives at the site of the aftereffect (presumably binocular neurons) even during suppression. In a second experiment 60 s of grating adaptation was found to produce a short-term reduction in the predominance of the adapted eye during binocular rivalry. These findings provide converging lines of evidence that suppression occurs at a site in the human visual system after the locus of grating adaptation and, hence, after the striate cortex.     

Visual awareness due to neuronal activities in subcortical structures: a proposal

It has been shown that visual awareness in the blind hemifield of hemianopic cats that have undergone unilateral ablations of visual cortex can be restored by sectioning the commissure of the superior colliculus or by destroying a portion of the substantia nigra contralateral to the cortical lesion (the Sprague effect). We propose that the visual awareness that is recovered is due to synchronized oscillatory activities in the superior colliculus ipsilateral to the cortical lesion. These oscillatory activities are normally partially suppressed by the inhibitory, GABAergic contralateral nigrotectal projection, and the destruction of the substantia nigra, or the sectioning of the collicular commissure, disinhibits the collicular neurons, causing an increase in the extent of oscillatory activity and/or synchronization between activities at different sites. This increase in the oscillatory and synchronized character is sufficient for the activities to give rise to visual awareness. We argue that in rodents and lower vertebrates, normal visual awareness is partly due to synchronized oscillatory activities in the optic tectum and partly due to similar activities in visual cortex. It is only in carnivores and primates that visual awareness is wholly due to cortical activities. Based on von Baerian recapitulation theory, we propose that, even in humans, there is a period in early infancy when visual awareness is partially due to activities in the superior colliculus, but that this awareness gradually disappears as the nigrotectal projection matures.     

双眼竞争研究现状与展望

双眼竞争是指当双眼所呈现的图像不一致而无法形成单一、稳定的知觉进而造成知觉动态交替变化的现象,其研究已有近200年的历史,至今仍是神经科学、心理学、生理学和临床医学中的研究热点。该文阐述了双眼竞争的概念、常用测量指标;总结了双眼竞争的特点及对双眼竞争的影响因素;讨论了双眼竞争与其他形式的多稳态知觉间的关系。行为实验、脑成像和电生理实验分别揭示了双眼竞争的早期加工模型和晚期加工模型的不足之处,Tong等人综合各方面的实验结果提出了双眼竞争的多层次–混合加工理论模型,这一模型将早期加工和晚期加工模型有机地结合起来,对于研究视觉意识的神经机制具有重要的理论指导意义。在总结已有研究的基础上,该文明确指出了双眼竞争的可应用领域及未来的研究方向     

The temporal course of suppression during binocular rivalry

Orthogonally oriented sinusoidal luminance gratings were dichoptically presented to the observers' left and right eyes. During the subsequent binocular rivalry, a small target was briefly presented (4AFC) to probe the strength of interocular suppression at various temporal latencies. Both stationary and moving rivalrous patterns were investigated. The purpose of experiment 1 was to compare the temporal characteristics of stationary and motion rivalry (0 and 1.2 deg s-1), while that of experiment 2 was to examine rivalry suppression for higher speeds (2 and 4 deg s-1). In all cases, it was found that the strength of suppression remained essentially constant throughout a single phase of binocular rivalry. The results of the investigation also revealed that moving rivalrous patterns lead to greater magnitudes of interocular suppression than static patterns. Despite these differences in the strength of suppression, the results of both experiments show that the temporal characteristics of motion and static rivalry are essentially identical.     

Neural bases of binocular rivalry

During binocular rivalry, conflicting monocular images compete for access to consciousness in a stochastic, dynamical fashion. Recent human neuroimaging and psychophysical studies suggest that rivalry entails competitive interactions at multiple neural sites, including sites that retain eye-selective information. Rivalry greatly suppresses activity in the ventral pathway and attenuates visual adaptation to form and motion; nonetheless, some information about the suppressed stimulus reaches higher brain areas. Although rivalry depends on low-level inhibitory interactions, high-level excitatory influences promoting perceptual grouping and selective attention can extend the local dominance of a stimulus over space and time. Inhibitory and excitatory circuits considered within a hybrid model might account for the paradoxical properties of binocular rivalry and provide insights into the neural bases of visual awareness itself.     

Mountains and valleys: binocular rivalry and the flow of experience

Binocular rivalry provides a useful situation for studying the relation between the temporal flow of conscious experience and the temporal dynamics of neural activity. After proposing a phenomenological framework for understanding temporal aspects of consciousness, we review experimental research on multistable perception and binocular rivalry, singling out various methodological, theoretical, and empirical aspects of this research relevant to studying the flow of experience. We then review an experimental study from our group explicitly concerned with relating the temporal dynamics of rivalrous experience to the temporal dynamics of cortical activity. Drawing attention to the importance of dealing with ongoing activity and its inherent changing nature at both phenomenological and neurodynamical levels, we argue that the notions of recurrence and variability are pertinent to understanding rivalry in particular and the flow of experience in general.     

No representation without awareness in the lateral occipital cortex

Recent research has shown that four small dots presented in the vicinity of, but not adjacent to, a target stimulus can banish that stimulus from conscious awareness. It is thought that the mental representation of the masked stimulus is "erased" by the trailing quartet of dots. Using functional magnetic resonance adaptation, we show that there is no persisting neural representation of the successfully masked stimulus in lateral occipital cortex, a region that has been implicated in the processing of object structure. This finding rules out the alternative interpretation that a lingering neural representation is merely rendered inaccessible to consciousness, as is the fate, for example, of monocular information under conditions of binocular rivalry.     

The subliminal perception of movement and the 'suppression' in binocular rivalry.

An analogy is drawn between the perceptual limitation that characterizes the dichotic listening paradigm and the 'suppression' that occurs in binocular rivalry when different stimuli are presented to the two eyes. An experiment is reported which focuses on the fate of the information residing in a suppressed eye (unattended channel) during binocular rivalry. It is demonstrated that the temporal course of rivalry is sensitive to the presence of a subliminal moving stimulus within the currently suppressed field. The effects are seen to confirm a literal interpretation of Levelt's (1966) thesis which relates changes in the 'stimulus strength' of a rivalling field to subsequent changes in the temporal course of the phenomenon. This interpretation is consistent with the hypothesis that, despite phenomenal suppression, a full analysis is undertaken on the currently non-dominant stimulus. The data are related to models of selective attention, and to the notion that there are parallel visual systems.     

Monocular and binocular rivalry between contours.

The temporal characteristics of binocular and monocular rivalry between orthogonal gratings of the same or complementary colours were investigated. Rivalry was measured in terms of the dominance of either grating or the visibility of composites comprised of parts of both gratings. The total duration for which either grating was dominant was significantly longer in binocular rivalry between gratings of complementary colours. A comparison of binocular and monocular rivalry indicated considerable phenomenal differences between them. Dominance in binocular rivalry corresponds to the visibility of one grating alone; this occurs rarely in monocular rivalry, which is characterized by fluctuations in the distinctiveness of the gratings. The changes in distinctiveness are influenced by colour in a similar manner to that in binocular rivalry, and the frequencies of fluctuations are higher for gratings of complementary colours.     

A common oscillator for perceptual rivalries?

Perceptual rivalry is an oscillation of conscious experience that takes place despite univarying. if ambiguous, sensory input. Much current interest is focused on the controversy over the neural site of binocular rivalry, a variety of perceptual rivalry for which a number of different cortical regions have been implicated. Debate continues over the relative role of higher levels of processing compared with primary visual cortex and the suggestion that different forms of rivalry involve different cortical areas. Here we show that the temporal pattern of disappearance and reappearance in motion-induced blindness (MIB) (Bonneh et al, 2001 Nature 411 798-801) is highly correlated with the pattern of oscillation reported during binocular rivalry in the same individual. This correlation holds over a wide range of inter-individual variation. Temporal similarity in the two phenomena was strikingly confirmed by the effects of the hallucinogen LSD, which produced the same, extraordinary, pattern of increased rhythmicity in both kinds of perceptual oscillation. Furthermore. MIB demonstrates the two properties previously considered characteristic of binocular rivalry. Namely the distribution of dominance periods can be approximated by a gamma distribution and, in line with Levelt's second proposition of binocular rivalry, predominance of one perceptual phase can be increased through a reduction in the predominance time of the opposing phase. We conclude that (i) MIB is a form of perceptual rivalry, and (ii) there may be a common oscillator responsible for timing aspects of all forms of perceptual rivalry.     

Pattern of cortical activity, degree of synchronization, binocular fusion, and binocular rivalry

The synchronization hypothesis is the likely idea for the binding problem in the brain. Here we tested whether the theory is applicable for the occurrence of either binocular fusion or binocular rivalry. We first showed patterns of activated patches in V1 with proceeding from fusion to rivalry on the basis of Hubel and Wiesel's 1979 illustration. We then assumed that the strength of synchrony between the patches in the left-eye and right-eye ocular dominance columns is a crucial determinant for the divergence between fusion and rivalry. By using the strength of fusion between the paired images as a measure of degree of synchrony, we confirm the assumption about interocular vision and the synchronization hypothesis as well.     

A neural theory of binocular rivalry

When the two eyes view discrepant monocular stimuli, stable single vision gives way to alternating periods of monocular dominance; this is the well-known but little understood phenomenon of binocular rivalry. This article develops a neural theory of binocular rivalry that treats the phenomenon as the default outcome when binocular correspondence cannot be established. The theory posits the existence of monocular and binocular neurons arrayed within a functional processing module, with monocular neurons playing a crucial role in signaling the stimulus conditions instigating rivalry and generating inhibitory signals to implement suppression. Suppression is conceived as a local process happening in parallel over the entire cortical representation of the binocular visual field. The strength of inhibition causing suppression is related to the size of the pool of monocular neurons innervated by the suppressed eye, and the duration of a suppression phase is attributed to the strength of excitation generated by the suppressed stimulus. The theory is compared with three other contemporary theories of binocular rivalry. The article closes with a discussion of some of the unresolved problems related to the theory.     

Plaid motion rivalry: correlates with binocular rivalry and positive mood state

Recently Hupé and Rubin (2003, Vision Research 43 531- 548) re-introduced the plaid as a form of perceptual rivalry by using two sets of drifting gratings behind a circular aperture to produce quasi-regular perceptual alternations between a coherent moving plaid of diamond-shaped intersections and the two sets of component 'sliding' gratings. We call this phenomenon plaid motion rivalry (PMR), and have compared its temporal dynamics with those of binocular rivalry in a sample of subjects covering a wide range of perceptual alternation rates. In support of the proposal that all rivalries may be mediated by a common switching mechanism, we found a high correlation between alternation rates induced by PMR and binocular rivalry. In keeping with a link discovered between the phase of rivalry and mood, we also found a link between PMR and an individual's mood state that is consistent with suggestions that each opposing phase of rivalry is associated with one or the other hemisphere, with the 'diamonds' phase of PMR linked with the 'positive' left hemisphere.     

Binocular rivalry and visual awareness

Physiological studies of binocular rivalry have provided important clues to the relationship between neural activity in the brain and visual awareness. However, uncertainty about these insights has been raised by a recent study showing that the events underlying binocular rivalry occur earlier in the visual pathway than was previously thought.     

Does interhemispheric competition mediate motion-induced blindness? A transcranial magnetic stimulation study

Motion-induced blindness (MIB) is a phenomenon, perhaps related to perceptual rivalry, where stationary targets disappear and reappear in a cyclic mode when viewed against a background (mask) of coherent, apparent 3-D motion. Since MIB has recently been shown to share similar temporal properties with binocular rivalry, we probed the appearance-disappearance cycle of MIB using unilateral, single-pulse transcranial magnetic stimulation (TMS)--a manipulation that has previously been shown to influence binocular rivalry. Effects were seen for both hemispheres when the timing of TMS was determined prospectively on the basis of a given subject's appearance-disappearance cycle, so that it occurred on average around 300 ms before the time of perceptual switch. Magnetic stimulation of either hemisphere shortened the time to switch from appearance to disappearance and vice versa. However, TMS of left posterior parietal cortex more selectively shortened the disappearance time of the targets if delivered in phase with the disappearance cycle, but lengthened it if TMS was delivered in the appearance phase after the perceptual switch. Opposite effects were seen in the right hemisphere, although less marked than the left-hemisphere effects. As well as sharing temporal characteristics with binocular rivalry, MIB therefore seems to share a similar underlying mechanism of interhemispheric modulation. Interhemispheric switching may thus provide a common temporal framework for uniting the diverse, multilevel phenomena of perceptual rivalry.     

Conditions required for binocular rivalry suppression

When the two eyes are presented with incompatible stimuli, the two monocular stimuli are seen alternately in a never-ending cycle. It is now widely accepted that the neural processes underlying this phenomenon, binocular rivalry, are distributed across a number of cortical stages. It is not clear, however, where binocular rivalry is initiated. We performed two experiments whose aim was to clarify this issue. In the first experiment, rivalry was induced, and brief test stimuli were delivered to an eye while its inducing stimulus was either dominant or suppressed. Sensitivity to a test stimulus with features similar to those of the suppressed inducing stimulus was reduced only when the test was presented to the eye whose inducing stimulus was suppressed. This indicates that suppression of a monocular channel is a prerequisite for binocular rivalry suppression. The second experiment showed that to induce rivalry, local interocular stimulus incompatibilities were necessary and that conflicting global percepts were not sufficient. These results suggest that low-level visual processes are required for the initiation of binocular rivalry.     

Binocular rivalry and visual awareness: the role of attention

When the right eye and the left eye view dissimilar scenes, the observer does not experience a stable superimposed percept of the images presented to the two eyes, but instead perceives an alternation between the images seen by each eye. A critical question confronting this robust and intriguing phenomenon of binocular rivalry is how the visual system selects the image to be perceived (dominant). The current main-stream literature emphasizes a bottom-up explanation in which the rivalry stimulus with the higher contour strength has the advantage, and becomes dominant in rivalry. Nevertheless, some workers in the past have favored an attention-selection explanation for binocular rivalry. We investigated the role of attention in binocular rivalry by employing novel psychophysical paradigms which capitalized on several established phenomena (e.g. the Cheshire Cat effect, attention cueing, pop-out effect). Our results revealed two major aspects of attention modulation in binocular rivalry. We found that a dominant image is less likely to be suppressed when voluntary attention is directed to it. This suggests the role of voluntary attention in retaining the dominant image in visual awareness. Second, a rivalry stimulus is more likely to become dominant if accompanied by a pop-out cue (in the same eye and proximity). Since a pop-out cue attracts involuntary attention to its location/eye, this result suggests that cue-mediated involuntary attention can promote the ability of a rivalry stimulus to reach visual awareness.     

Conscious behavior explained.

Current neurobiological research on temporal binding in binocular rivalry settings contributes to a better understanding of the neural correlate of perceptual consciousness. This research can easily be integrated into a theory of conscious behavior, but if it is meant to promote a naturalistic theory of perceptual consciousness itself, it is confronted with the notorious explanatory gap argument according to which any statement of psychophysical correlations (and their interpretation) leaves the phenomenal character of, e.g., states of perceptual consciousness open. It is argued that research on temporal binding plays no role in a naturalistic theory of consciousness if the gap argument can be solved on internal philosophical grounds or if it turns out to be unsolvable at the time being. But there may be a way to dissolve or deconstruct it, and the accessibility of this way may well depend on scientific progress, including neurobiological research on the neural correlate of perceptual consciousness.     

On the neural correlates of object recognition awareness: relationship to computational activities and activities mediating perceptual awareness

Based on theoretical considerations of Aurell (1979) and Block (1995), we argue that object recognition awareness is distinct from purely sensory awareness and that the former is mediated by neuronal activities in areas that are separate and distinct from cortical sensory areas. We propose that two of the principal functions of neuronal activities in sensory cortex, which are to provide sensory awareness and to effect the computations that are necessary for object recognition, are dissociated. We provide examples of how this dissociation might be achieved and argue that the components of the neuronal activities which carry the computations do not directly enter the awareness of the subject. The results of these computations are sparse representations (i.e., vector or distributed codes) which are activated by the presentation of particular sensory objects and are essentially engrams for the recognition of objects. These final representations occur in the highest order areas of sensory cortex; in the visual analyzer, the areas include the anterior part of the inferior temporal cortex and the perirhinal cortex. We propose, based on lesion and connectional data, that the two areas in which activities provide recognition awareness are the temporopolar cortex and the medial orbitofrontal cortex. Activities in the temporopolar cortex provide the recognition awareness of objects learned in the remote past (consolidated object recognition), and those in the medial orbitofrontal cortex provide the recognition awareness of objects learned in the recent past. The activation of the sparse representation for a particular sensory object in turn activates neurons in one or both of these regions of cortex, and it is the activities of these neurons that provide the awareness of recognition of the object in question. The neural circuitry involved in the activation of these representations is discussed.