Synchronization of neural activity across cortical areas correlates with conscious perception

Abstract

Subliminal stimuli can be deeply processed and activate similar brain areas as consciously perceived stimuli. This raises the question which signatures of neural activity critically differentiate conscious from unconscious processing. Transient synchronization of neural activity has been proposed as a neural correlate of conscious perception. Here we test this proposal by comparing the electrophysiological responses related to the processing of visible and invisible words in a delayed matching to sample task. Both perceived and nonperceived words caused a similar increase of local (gamma) oscillations in the EEG, but only perceived words induced a transient long-distance synchronization of gamma oscillations across widely separated regions of the brain. After this transient period of temporal coordination, the electrographic signatures of conscious and unconscious processes continue to diverge. Only words reported as perceived induced (1) enhanced theta oscillations over frontal regions during the maintenance interval, (2) an increase of the P300 component of the event-related potential, and (3) an increase in power and phase synchrony of gamma oscillations before the anticipated presentation of the test word. We propose that the critical process mediating the access to conscious perception is the early transient global increase of phase synchrony of oscillatory activity in the gamma frequency range.

Figure 1.

Design and behavioral results of experiment. a, Stimulus sequence. The task was to compare a briefly presented word (sample word) with a subsequent word (test word). The sample word visibility was controlled by changing the luminance of the masks. Control conditions were created to assess the brain response to the mask stream. The left timeline shows the duration of each stimulus. The right timeline shows the cumulative time. b, Behavioral performance. The left plot shows stimulus detectability for all conditions, expressed as detectability index (d′), and the middle plot is the success rate. The right plot shows the reaction time for all conditions. Plots indicate mean performance ±1 SD.

Figure 2.

Spectral power and phase synchrony to visible and invisible words. The visible condition (visible − control_visible) and invisible condition (invisible − control_invisible) are shown. The time-frequency plot shows the grand average of all electrodes. The phase-synchrony plot shows the grand average for all of the electrode pairs. The color scale indicates amplitude in SD, calculated over a 500 ms baseline. Zero corresponds to first mask onset. Vertical lines indicate sample- and test-word presentation. a, Time − frequency plot. Two increments of gamma-power emission are visible. The first is only present in the visible condition, and the second is present in both conditions. b, Phase synchrony. There are three statistically significant bursts of synchronous activity. The first and second peaks occur only in the visible condition. No significant differences were found for the last peak.

Figure 3.

ERPs elicited by visible and invisible words. a, Time course of responses to visible and invisible words at different electrodes. The x-axis shows time, and the y-axis shows electrodes; the color scale is expressed in microvolts. Zero represents the first mask onset. Vertical lines indicate sample-word and test-word presentation. Small lines at the top of the graph code for the two time windows corresponding to the voltage scalp maps in b. b, Voltage scalp map for two windows indicated for visible and invisible conditions. The first difference started at 130 ms after sample-word presentation, as a P300a-like component. Then, a P1-like component was observed ∼200 ms after test-word presentation, for both conditions. c, Time course of the signal recorded from left frontal electrode F3.

Figure 4.

Scalp topography of induced gamma power and phase synchrony for the visible and invisible condition. Top row, Visible condition. Bottom row, Invisible condition. The background color indicates induced gamma power averaged in a 50–57 Hz frequency range. Each head represents the average of a 150 ms time window. Time 0 indicates the onset of the sample word. Lines connect pairs of electrodes displaying significant synchronization ( p < 0.000001). Gamma activity does not statistically differ between visible and invisible conditions. In contrast, phase synchrony is stronger in the visible condition during the 40–180 ms time window involving occipito, parieto, and frontal electrodes, with intrahemispheric and interhemispheric connections. In the window between 180 and 330 ms, the pattern of phase synchrony lateralizes over the left hemisphere and restricts to occipito-parietal electrodes.