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. 2009 Jul 3;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 Doesburg  1 , Jessica J Green, John J McDonald, Lawrence M Ward
Affiliations

Rhythms of consciousness: binocular rivalry reveals large-scale oscillatory network dynamics mediating visual perception

Sam M Doesburg et al. PLoS One. .

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.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1
a,b) The left and right eye stimuli, respectively. c) Schematic representation of the stream of perceptual consciousness wherein discrete moments of perceptual experience coincide with gamma-band synchronization, itself locked to a theta cycle. Periodic gamma-band synchronization is locked to the onset of new conscious percepts and hence to button presses signaling perceptual switching. We imaged these oscillatory cortical networks by comparing gamma synchronization during periodic activations to the intervening period of relative desynchronization. In this figure 0 ms indicates button presses indicating the onset of a new percept. The preceding −600 to −540 ms and −280 to 220 ms analysis windows, as well as the −430 to −370 ms baseline interval, are depicted.
Figure 2
Figure 2. Distribution of durations for perceptual dominance periods.
Data shown here were obtained from the 9 subjects included in the EEG analyses. Black curve indicates prediction of a gamma distribution with scale parameter = 400, shape parameter = 2.1, fitted to durations<4001 ms. Although the chi-squared value is highly significant the distribution fits well. It deviates most markedly for the shortest durations (of which there are more than predicted) and durations from about 1200 ms to 2000 ms (of which there are fewer than predicted).
Figure 3
Figure 3
a) Topography of 35–45 Hz scalp spectral power during the −540 to −600 ms and −220 to −280 ms intervals, relative to the baseline interval, for the (R) right side, (L) left side and (T) top view. b) Periodic bursts of gamma-band scalp activity time-locked to button presses (at 0 ms) indicating perceptual switching. Depicted is gamma-band power averaged across subjects and across the 30 electrodes where gamma activity was most clearly expressed (see Methods). Solid lines denote time-frequency windows used for beamformer source localization; dotted lines denote the baseline.
Figure 4
Figure 4. Surface projected regional gamma-band activations, and inter-regional gamma-band synchronization in the 540–600 ms and 220–280 ms pre-response intervals.
For clarity, separate images are provided for (R) right intrahemispheric, (L) left intrahemispheric and (I) interhemispheric synchronization across cortical regions. Lower brain figures show surface projected anatomical loci for all identified gamma-band activations.
Figure 5
Figure 5
a) Time-course of averaged gamma-band phase synchronization (standardized PLV) between cortical regions identified by beamformer source localization preceding the onset of stable percepts. b) Time-course of averaged intra-regional neural synchronization preceding the onset of stable percepts (standardized amplitude from the analytic signal analysis) at centre frequency identified for inter-regional synchronization (33 Hz).
Figure 6
Figure 6. Theta-modulation of gamma amplitude.
Dotted lines represent the 97.5 (top) and 2.5th (bottom) percentiles and the dark black line indicates the mean of the surrogate distribution for each of the 60 bins of the theta cycle. Jagged red line denotes the mean non-normalized gamma amplitude in each bin. When the gamma amplitude was greater than or less than the surrogate line for two or more successive bins we considered the departure to be significant (p<0.05, two tailed). Left PreCG and right PreCG plots are not shown; they resemble the plot for right DLPFC and show no significant relationship between theta phase and gamma amplitude. Radians on the x-axis are in reference to a cosine wave, which is maximal at 0 radians; one cycle of a 6 Hz cosine wave (thin black line) is superimposed on the graph.
Figure 7
Figure 7. Theta-modulation of gamma-band inter-regional phase locking.
Dotted lines represent the 97.5 (top) and 2.5th (bottom) percentiles and the dark black line indicates the mean of the surrogate distribution for each of the 60 bins of the theta cycle. Jagged red line denotes the non-normalized gamma-band phase locking value in each bin. When phase-locking was greater than or less than the surrogate line for two or more successive bins we considered the departure to be significant (p<0.05, two-tailed). Radians on the x-axis are in reference to a cosine wave, which is maximal at 0 radians; one cycle of a 6 Hz cosine wave (thin black line) is superimposed on the graph.
Figure 8
Figure 8. Two examples of theta-theta phase relationship.
Dotted lines represent the 97.5 (top) and 2.5th (bottom) percentiles and the dark black line indicates the mean of the surrogate distribution for each of the 60 bins of the theta cycle. Jagged red line denotes the mean theta phase of the source indicated on the y-axis in each bin of the theta source indicated on the x-axis. When the mean phase was greater than or less than the surrogate line for two or more successive bins we considered the departure to be significant (p<0.05, two-tailed). Radians on the x-axis are in reference to a cosine wave, which is maximal at 0 radians; one cycle of a 6 Hz cosine wave (thin black line) is superimposed on the graph.
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