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- Andreas K. Engel, P. Fries, P. Kreiter Konig, M. Brecht & Wolf Singer (1999). Temporal Binding, Binocular Rivalry, and Consciousness. Consciousness and Cognition 8 (2):128-51.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.
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This article summarizes a variety of current as well as previous research in support of a new theory of consciousness. Evidence has been steadily accumulating that information about a stimulus complex is distributed to many neuronal populations dispersed throughout the brain and is represented by the departure from randomness of the temporal pattern of neural discharges within these large ensembles. Zero phase lag synchronization occurs between discharges of neurons in different brain regions and is enhanced by presentation of stimuli. This evidence further suggests that spatiotemporal patterns of coherence, which have been identified by spatial principal component analysis, may encode a multidimensional representation of a present or past event. How such distributed information is integrated into a holistic percept constitutes the binding problem. How a percept defined by a spatial distribution of nonrandomness can be subjectively experienced constitutes the problem of consciousness. Explanations based on a discrete connectionistic network cannot be reconciled with the relevant facts. Evidence is presented herein of invariant features of brain electrical activity found to change reversibly with loss and return of consciousness in a study of 176 patients anesthetized during surgical procedures. A review of relevant research areas, as well as the anesthesia data, leads to a postulation that consciousness is a property of quantumlike processes, within a brain field resonating within a core of structures, which may be the neural substrate of consciousness. This core includes regions of the prefrontal cortex, the frontal cortex, the pre- and paracentral cortex, thalamus, limbic system, and basal ganglia.
& How does neuronal activity bring about the interpretation of visual space in terms of objects or complex perceptual events? If they group, simple visual features can bring about the integration of spikes from neurons responding to different features to within a few milliseconds. Considered as a potential solution to the ‘‘binding problem,’’ it is suggested that neuronal synchronization is the glue for binding together different features of the same object. This idea receives some support from correlated- and periodic-stimulus motion paradigms, both of which suggest that the segregation of a figure from ground is a direct result of the temporal correlation of visual signals. One could say that perception of a highly correlated visual..
Among psychologists and vision scientists,binocular rivalry has enjoyed sustainedinterest for decades dating back to the 19thcentury. In recent years, however, rivalry''saudience has expanded to includeneuroscientists who envision rivalry as a tool for exploring the neural concomitants ofconscious visual awareness and perceptualorganization. For rivalry''s potential to berealized, workers using this tool need toknow details of this fascinating phenomenon,and providing those details is the purpose ofthis article. After placing rivalry in ahistorical context, I summarize major findingsconcerning the spatial characteristics and thetemporal dynamics of rivalry, discuss two majortheoretical accounts of rivalry ( eye vs stimulus rivalry) and speculate on possibleneural concomitants of binocular rivalry.
The neural basis of binocular rivalry has beenthe subject of vigorous debate. Do discrepantmonocular patterns rival for awareness becauseof neural competition among patternrepresentations or monocular channels? In thisarticle, I briefly review psychophysical andneurophysiological evidence pertaining to boththeories and discuss important new neuroimagingdata which reveal that rivalry is fullyresolved in monocular visual cortex. These newfindings strongly suggest that interocularcompetition mediates binocular rivalry and thatV1 plays an important role in the selection ofconscious visual information. They furthersuggest that rivalry is not a unitaryphenomenon. Interocular competition may fullyaccount for binocular rivalry whereas aseparate mechanism involving patterncompetition likely accounts for monocular andstimulus rivalry.
In addressing thescientific study of consciousness, Crick and Koch state, It is probable that at any moment some active neuronal processes in your head correlate with consciousness, while others do not: what is the difference between them? (1998, p. 97). Evidence from electrophysiological and brain-imaging studies of binocular rivalry supports the premise of this statement and answers to some extent, the question posed. I discuss these recent developments and outline the rationale and experimental evidence for the interhemispheric switch hypothesis of perceptual rivalry. According to this model, the perceptual alternations of rivalry reflect hemispheric alternations, suggesting that visual consciousness of rivalling stimuli may be unihemispheric at any one time (Miller et al., 2000). However, in this paper, I suggest that interhemispheric switching could involve alternating unihemispheric attentional selection of neuronal processes for access to visual consciousness. On this view, visual consciousness during rivalry could be bi hemispheric because the processes constitutive of attentional selection may be distinct from those constitutive of visual consciousness. This is a special case of the important distinction between the neuronal correlates and constitution of visual consciousness.
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.
Temporal binding via 40-Hz synchronization of neuronal discharges in sensory cortices has been hypothesized to be a necessary condition for the rapid selection of perceptually relevant information for further processing in working memory. Binocular rivalry experiments have shown that late stage visual processing associated with the recognition of a stimulus object is highly correlated with discharge rates in inferotemporal cortex. The hippocampus is the primary recipient of inferotemporal outputs and is known to be the substrate for the consolidation of working memories to long-term, episodic memories. The prefrontal cortex, on the other hand, is widely thought to mediate working memory processes, per se. This article reviews accumulated evidence for the role of a subcortical matrix in linking frontal and hippocampal systems to select and ''stream'' conscious episodes across time (hundreds of milliseconds to several seconds). ''Streaming'' is hypothesized to be mediated by the selective gating of reentrant flows of information between these cortical systems and the subcortical matrix. The physiological mechanism proposed for this temporally extended form of binding is synchronous oscillations in the slower EEG spectrum (< 8 Hz).
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.
Recent experiments have shown that the amplitudes of cortical gamma band oscillatory activities that occur during anesthesia are often greater than amplitudes of similar activities that occur without anesthesia. This result is apparently at odds with the hypothesis that synchronized oscillatory activities constitute the neural correlate of consciousness. We argue that while synchronization and oscillatory patterning are necessary conditions for consciousness, they are not sufficient. Based on the results of a binocular rivalry study of Fries et al. (1997), we propose that the degrees of oscillatory strength and synchronization of neuronal activities determine the degree of awareness those activities produce. On the other hand, the overal firing rates of neurons in cortical sensory areas are not correlated with the degree of awareness the activities of those neurons produce. The results of the experiment of Fries et al. (1997) appear to conflict with the results of another binocular rivalry experiment, in which monkeys were trained to pull a lever in order to report which stimulus object was being perceived (Leopold & Logothetis, 1996). In the latter experiment, it was demonstrated that the firing rates of neurons in striate cortex did not change during perceptual alterations, while 90% of neurons in inferior and superior temporal cortices changed their firing rate when the perceived image changed. This result led to the conclusion that activities in temporal cortex are correlated with visual awareness, but those in striate cortex are not. We argue that activities in temporal cortex contribute little, if anything, to perceptual awareness, and that their primary function is computational. Thus the correlation between the firing rates of neurons in these areas and the responses of the monkeys is due to the recognition of a particular stimulus object, which in turn is due to the computations made there.
Discussion of Andreas K. Engel , P. Fries , P. Kreiter Konig , M. Brecht & Wolf Singer, Temporal binding, binocular rivalry, and consciousness
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