Abstract
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.
Highlights
Consciousness has been envisioned as a dynamic global workspace wherein unified experience is assembled out of relevant constituent elements [1,2]
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, some mechanism must exist to govern the evolution of such a network over time in order to account for the dynamism of experience
The 2220 to 2280 ms and 2540 to 2600 ms intervals were chosen because (i) these were distinct peaks in the recurrent gamma activation relative to the intervening baseline period, (ii) they are consistent with earlier results pertaining to gamma-band neural synchronization time-locked to perceptual switching in binocular rivalry obtained using a similar paradigm [25], and (iii) the 2220 to 2280 ms period corresponds to reaction times expected in a simple perceptual task, suggesting that perceptual switching during this period may have initiated behavioural responses
Summary
Consciousness has been envisioned as a dynamic global workspace wherein unified experience is assembled out of relevant constituent elements [1,2]. This view is consistent with the notion that consciousness is 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 [3] 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 [3,4]. 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 [9] 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 largescale oscillatory dynamics [10,11]
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