Neural signature of the conscious processing of auditory regularities

Abstract

Can conscious processing be inferred from neurophysiological measurements? Some models stipulate that the active maintenance of perceptual representations across time requires consciousness. Capitalizing on this assumption, we designed an auditory paradigm that evaluates cerebral responses to violations of temporal regularities that are either local in time or global across several seconds. Local violations led to an early response in auditory cortex, independent of attention or the presence of a concurrent visual task, whereas global violations led to a late and spatially distributed response that was only present when subjects were attentive and aware of the violations. We could detect the global effect in individual subjects using functional MRI and both scalp and intracerebral event-related potentials. Recordings from 8 noncommunicating patients with disorders of consciousness confirmed that only conscious individuals presented a global effect. Taken together these observations suggest that the presence of the global effect is a signature of conscious processing, although it can be absent in conscious subjects who are not aware of the global auditory regularities. This simple electrophysiological marker could thus serve as a useful clinical tool.

Fig. 1.

Experimental design. (A) On each trial 5 complex sounds of 50-ms-duration each were presented with a fixed stimulus onset asynchrony of 150 ms between sounds. Four different types of series of sounds were used, the first 2 were prepared using the same 5 sounds (AAAAA or BBBBB), and the second 2 series of sounds were either AAAAB or BBBBA. (B) Each block started with 20–30 frequent series of sounds to establish the global regularity before delivering the first infrequent global deviant stimulus.

Fig. 2.

Local and global ERP effects in the active counting task. Averaged voltage scalpmaps of the local and global subtractions (deviant minus standard) are plotted (top) from 100 to 484 ms after the onset of the fifth sound. Corresponding thresholded t tests scalpmaps (red) are shown for each condition. ERPs of 3 representative electrodes are shown (bottom box) for the 4 elementary conditions (local/global X standard/deviant).

Fig. 3.

Brain dynamics of local and global effects. (A) Brain fMRI activations are shown for the local (top left) and the global (top right) effects in Talairach's space (horizontal and sagittal slices). For each anatomical view, 1 intracerebral electrode is displayed (yellow disk). (B) Averaged LFPs (top) and LFPs power (bottom) are plotted against time for local standard (green) and local deviant (red) trials (left pair), and for global standard (green) and global deviant (red) trials (two right pairs). (C) Source activity averaged across the Broadman area including the corresponding intracerebral electrode (BrainStorm software, Matlab) is plotted against time.

Fig. 4.

Local and global effects in individual subjects. (Left) Each horizontal line summarizes an individual subject t test statistics (left for the local effect; right for the global effect). Individual statistics are plotted for 10 subjects from each of the Counting (top), Mind-wandering (middle) and Visual interference (bottom) groups. (Right) For each group, we computed a mean individual statistical index by defining linear bins of individual t test statistical significance (0 for P > 0.05; 1 for P < 0.05; 2 for P < 0.01; 3 for P < 0.005; 4 for P < 0.001; 5 for P < 0.0005; and 6 for P < 0.0001).

Fig. 5.

Local and global effects in noncommunicating patients. Individual statistics are plotted for the 8 noncommunicating patients VS or MCS patients. (Left) Each horizontal line summarizes an individual subject statistics. (Right) Averaged high-density ERPs of the local (top) and global (bottom) effects of patient MCS 1. Voltage scalp topographies are shown for the MMN ≈200 ms (top left), for the local effect vertex-positivity ≈300 ms (top right), and for the global effect (bottom).