Scientific Understanding of Consciousness
Oscillatory Network Dynamics Mediate Visual Perception
Citation: Doesburg SM, Green JJ, McDonald JJ, Ward LM (2009) Rhythms of Consciousness: Binocular Rivalry Reveals Large-Scale Oscillatory Network Dynamics Mediating Visual Perception. PLoS ONE 4(7): e6142. doi:10.1371/journal.pone.0006142
Rhythms of Consciousness: Binocular Rivalry Reveals Large-Scale Oscillatory Network Dynamics Mediating Visual Perception
Sam M. Doesburg1, Jessica J. Green2, John J. McDonald2, Lawrence M. Ward1,3
1 Psychophysics and Cognitive Neuroscience Laboratory, Department of Psychology, University of British Columbia, Vancouver, British Columbia, Canada, 2 Department of Psychology, Simon Fraser University, Burnaby, British Columbia, Canada, 3 Brain Research Centre, University of British Columbia, Vancouver, British Columbia, Canada
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.
Consciousness has been envisioned as a dynamic global workspace wherein unified experience is assembled out of relevant constituent elements. This view is consistent with the notion that consciousness is chiefly characterized by the qualities of dynamism, selectivity, and integrated subjective experience, attributes explained by the postulation that experience is equivalent to informational integration of relevant neural elements into a large-scale complex. In such a view, the contents of experience would be defined by the activity of the largest and most dominant coalition of functionally integrated neurons at a given moment. Any such process would necessitate continuous and complex rearrangement of neural populations across widespread and diverse cortical regions, a feat that has been attributed to oscillatory dynamics. Low gamma-band (30 Hz to 50 Hz) synchronization between neural groups coding the various features of objects currently populating experience has been proposed as a mechanism for such dynamic functional integration in the brain, and has been suggested to be the biological basis of perceptual experience and feature binding. It has been proposed that synchronization enables transient functional integration between specific neural groups as bursts of action potentials are consistently exchanged during the depolarized phase of the receiving neurons' ongoing membrane potential fluctuations, thereby enhancing communication between populations oscillating in synchrony. Support for this notion can be drawn from findings that mutual influence between neural populations is positively correlated with gamma-band synchronization in both intra-regional and large-scale oscillatory dynamics.
Empirical evidence for the involvement of gamma-band neural synchronization in perceptual binding and awareness flows from diverse lines of research. Results have led to the postulation that the emergence of organized perception corresponds to the reordering of a large-scale representational ensemble by way of oscillatory synchronization in the gamma frequency range. We propose that this mechanism can account for the selective integration of contents into a large-scale neural coalition determining the momentary furnishings of experience. The parameters governing cortical oscillations are also dynamic, allowing for the integration, disintegration, and reconstruction of gamma-oscillatory assemblies in time. Accordingly, we propose that large-scale gamma-band synchronization constitutes an oscillatory substrate for the stream of consciousness.
Cognitive Processes associated with Synchronization of Gamma Rhythms
Cognitive processes closely associated with consciousness, namely attention and working memory, have also been robustly associated with the synchronization of gamma rhythms. Previous research has also revealed that coherent thalamocortical and corticocortical gamma rhythms are associated with mammalian consciousness, as they are characteristic of CNS states associated with experience (wakefulness and REM sleep). Such rhythms also have been proposed to be the neurobiological basis for consciousness, a view supported by the observation that functional decoupling of thalamus and cortex is a cardinal property of general anesthesia.
If gamma rhythms embody an essential feature of the biological basis of consciousness, and if gamma-band synchronization of selective neural populations constructs a large-scale complex defining the contents of consciousness, as we have proposed, then some mechanism must exist to govern the evolution of such a network over time in order to account for the dynamism of experience. Notably, modulation of intra-regional gamma-band (80–150 Hz) synchronization at a frequency in the theta band (4–7 Hz) has been observed using subdural electrodes on human cortex, with gamma envelope amplitude being most pronounced during the trough of the theta cycle. This important result suggests that the construction and degradation of low gamma-band (30–50 Hz) oscillatory neural ensembles might also be governed by theta rhythms.
Locking Gamma-band Synchronization to Theta Oscillations
Locking of low gamma-band synchronization to theta oscillations has been associated with an array of cognitive processes including working memory, attention, and perceptual organization. Transient and periodic desynchronization of gamma rhythms, or phase scattering, has also been observed between periods of synchronization. Similarly, periods of recurrent increased long-range gamma-band phase locking consistent with a theta-frequency modulation are often interposed with periods of baseline level phase locking. We interpret such results as indications that theta-modulated gamma synchronization serves to organize transient functional networks across time.
Specifically, we propose that large-scale ensembles synchronously oscillating in the low gamma frequency range enable transient functional integration of task- and/or percept-specific neural populations, and that theta rhythms govern the temporal dynamics according to which the life cycle of individual gamma-oscillatory ensembles are organized. This interpretation also suggests that only one truly discrete perceptual experience may exist within a single theta cycle, and that the emergence of new perceptual experiences may be time locked to a particular phase of ongoing cortical theta rhythms.
Ascertaining the neural correlates of perceptual consciousness requires separation of brain processes related to experience from those embodying non-conscious stimulus processing, a distinction made possible using binocular rivalry. Binocular rivalry has been employed to study the relationship between neural oscillations and consciousness using flickering, frequency-tagged stimuli to identify neural populations responding to rivaling images. Such studies revealed that when a frequency-tagged image is perceived, increased local and long-range neural synchronization is observed at the flicker frequency of the stimulus, reinforcing the view that consciousness is associated with large-scale synchronously oscillating neural ensembles. Localization of magnetoencephalographic rhythms generated in this fashion reveals widely distributed, localized sources of flicker-entrained neural activity in the cortex.
We propose that the contents of consciousness are defined by which neural populations are integrated into a large-scale gamma-synchronous ensemble at any given time. We further propose that the formation and dissolution of these functional assemblies occurs at a frequency in the theta band, which effectively places temporal constraints on the emergence of new, discrete, perceptual experiences.
A person can have only one discrete experience every theta cycle, effectively implementing a ‘speed limit’ on conscious perception. Large-scale gamma-oscillatory neural assemblies of relevant cortical regions may be synchronized and desynchronized according to a theta cycle that also determines the timing of new perceptual experiences.
Inter-regional gamma-band phase synchronization
We hypothesized that gamma-band phase synchronization would be observed between cortical areas displaying increased gamma-band activation during the 220–280 ms and 540–600 ms pre-response windows. In our view, gamma synchronizations recurring at a theta rate represent the integration of relevant neural populations into large-scale ensembles. This entails functional integration across regions by means of gamma-band phase synchronization. The ongoing rhythm of both intra-regional and inter-regional gamma-band synchronization is consistent with a theta rate of roughly 4–6 Hz.
We found that both the amplitude and the inter-regional synchronization of gamma oscillations in the identified network of cortical regions were coupled to the phases of theta oscillations in those same areas. This confirms that the cortical theta rhythms modulate the periodic assembly and disintegration of gamma-oscillatory neural coalitions time-locked to the onset of new percepts.
Interposed between recurrent gamma-band synchronizations are periods during which gamma rhythms become relatively desynchronized. These intervals likely play an important role in ongoing cortical network dynamics underlying the stream of perceptual consciousness. Transient desynchronization of gamma oscillations has been shown to occur between periods of transient task-relevant synchronization. This process, known as ‘phase scattering’ is understood as a mechanism by which existing task- and/or percept-dependent neural coalitions are terminated.
Electroencephalographic investigation of working memory, a faculty integrally associated with perceptual consciousness, has yielded three additional key findings suggestive of a fronto-parietal network associated with theta-gamma oscillatory mechanisms that may implement a ‘global workspace’ for the retention and manipulation of to-be-remembered material. During the retention interval (1) increased gamma-band activation is observed at frontal and parietal electrodes, (2) coupling of theta-band and gamma-band oscillations is observed at frontal and parietal electrodes, and (3) theta-band and gamma-band synchronization is enhanced between frontal and parietal electrodes. Results such as these are consistent with accumulating evidence that cross-frequency synchronization may be a key mechanism for the organization of dynamic activity in the nervous system.
The results detailed here are consistent with a more general understanding of how mental representations arise from the activity of distributed neural groups. Donald Hebb proposed that memory traces and mental representations were implemented by connectivity within a distributed network of neurons, and that the selective re-ignition of this assembly would be tantamount to recognition and/or recall. This notion is supported by evidence that the perception of a familiar object, even in a degraded form, is also associated with both intra-regional and inter-regional gamma-band synchronization. The Hebbian outlook, coupled with a more modern understanding of functional cortical anatomy, would predict that cortical regions relevant to the representation of a memory would be activated and functionally integrated during recognition and recall. Indeed, it has been shown that recognition of a complex object is associated with gamma-band activation in frontal, parietal and temporal cortex, between which enhanced gamma-band phase synchronization and bidirectional causal interaction are observed.
In light of the present results, this could be viewed as the integration of temporal areas responsible for the processing of complex images into the fronto-parietal gamma-oscillatory network integral to perceptual experience. It is notable that schizophrenia, historically considered to be a disorder of consciousness and characterized by cognitive fragmentation, is associated with abnormal theta and gamma band oscillatory activity during cognitive processing. The essential relationship between theta-gamma mechanisms and consciousness is also highlighted by a possible common neuropharmacological substrate. The bursting of cholinergic projections to cortex from basal forebrain is found only in wakefulness and REM sleep, central nervous system states associated with consciousness, and theta and gamma activity are correlated with bursting in these neurons. Such results demonstrate that gamma-band neural synchronization is a fundamental mechanism for mental representation, and that its disturbance results in alterations of conscious experience.
Implications for free will
Our results may also have implications for the interpretation of what are perhaps some of the most disconcerting findings in human neuroscience. Benjamin Libet used an ingenious experimental paradigm to provide evidence that the conscious intention to initiate a movement was substantially (approximately 300 ms) preceded by the onset of the readiness potential, or RP, a buildup of scalp-recorded electrical activity originating in the motor cortices, taken to indicate the initiation of a behavioural response. Libet considered this to be evidence that unconscious impulses were the true cause of action, and that the conscious experience of intent to move occurred later and was antedated in our experiential model of the world.
Although the experimental paradigm used in the present study was not designed to directly address the temporal relationship between movement and the will to act, our results provide a unique vista on the relation of gamma-band activity and synchronization to consciousness and behaviour. Our data indicate that gamma-band activation of left PreCG, presumably involved in the generation of a behavioural response to a change in consciousness, is uniquely present in the 220–280 ms pre-response period of activation, and is notably absent in the preceding 540–600 ms window. Moreover, left PreCG is integrated into the prefrontal-parietal network by means of inter-regional gamma-band phase synchronization during the same cycle that ITC is activated and integrated into this network. These observations suggest that initiation of behavioural responses signaling the onset of new conscious percepts, at least as indexed by gamma-band activity, precede action and occur at reaction times consistent with those observed in complex perceptual tasks. This is consistent with evidence that gamma-band oscillations in motor cortex are relevant to the initiation and control of movement. This means, contrary to Libet's conclusions, that at least one neural indicator of the timing of conscious experience is compatible with the view that consciousness is relevant to the initiation of volitional action. Initiation of a behavioural response coincides with perception of a new image, indexed by activation and network integration of ITC, indicating that conscious experience is directly related either to the initiation of a behaviour or to the awareness of its initiation. By relating ongoing internal processes to behaviour, rather than attempting to correlate the internal perception of an external event with the timing of behaviour, we have overcome a critical confound of Libet's paradigm. A liberal interpretation of our results would suggest that (1) consciousness, or biological processes directly underpinning consciousness, may indeed control behaviour, and (2) the experience of volition is not antedated. Such interpretations, however, are speculative as our paradigm is not ideal for the evaluation of these hypotheses. It must also be acknowledged that neural activity in other frequency ranges might precede that in the gamma band, and might be more directly related to the initiation of a voluntary response. Thus, our findings simply suggest an intriguing avenue for future research into the chronometry of experience and its implications for free will.
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Return to — Oscillation and Synchronization
Link to — Consciousness Subject Outline
Further discussion — Covington Theory of Consciousness