The corollary discharge in humans is related to synchronous neural oscillations

Abstract

How do animals distinguish between sensations coming from external sources and those resulting from their own actions? A corollary discharge system has evolved that involves the transmission of a copy of motor commands to sensory cortex, where the expected sensation is generated. Through this mechanism, sensations are tagged as coming from self, and responsiveness to them is minimized. The present study investigated whether neural phase synchrony between motor command and auditory cortical areas is related to the suppression of the auditory cortical response. We recorded electrocorticograms from the human brain during a vocalizing/listening task. Neural phase synchrony between Broca's area and auditory cortex in the gamma band (35 to ∼50 Hz) in the 50-msec time window preceding speech onset was greater during vocalizing than during listening to a playback of the same spoken sounds. Because prespeech neural synchrony was correlated (r = -.83, p = .006), with the subsequent suppression of the auditory cortical response to the spoken sound, we hypothesize that phase synchrony in the gamma band between Broca's area and auditory cortex is the neural instantiation of the transmission of a copy of motor commands. We suggest that neural phase synchrony of gamma frequencies may contribute to transmission of corollary discharges in humans.

Figure 1

Phase locking value (PLV) between Broca’s area and auditory cortex. (A) Intracranial electrode contact placements of patient A are shown and the neuroelectric signals of two circled electrode contacts (i.e., A12 circled in yellow and G8 circled in red) were used to calculate PLVs for both of vocalizing and listening conditions. Electrode contacts A12 and G8 are located in Broca’s area and auditory cortex, respectively. (B) electrocorticogram data were epoched to onsets of participant-generated speech sounds. The averaged event-related potential of electrode contact A12 is shown (listening condition is in blue trace and vocalizing condition is in red trace). (C) As in (B), for electrode contact G8 and N100 suppression in vocalizing condition (red trace) is observed. (D) In vocalizing condition, PLVs between electrode contacts A12 and G8 from −300 ms to 300 ms in gamma frequencies, ranging from 25 Hz to 50 Hz are shown. PLV ranges from 0 (no phase synchrony) to 1 (perfect phase synchrony). (E) As in (D), for listening condition. (F) The difference plot of Figures 1D and 1E (i.e., PLVs of vocalizing condition minus PLVs of listening condition) shows enhancement of PLVs in warm colors and suppression of PLVs in cold colors during Vocalizing compared to Listening.

Figure 2

Percentage changes of significant differences of phase locking values (PLVs) between vocalizing and listening conditions. PLV represents the phase synchrony between Broca’s area and auditory cortex at the given frequency and time point. This figure shows the percent changes in the significant differences of PLVs between Vocalizing and Listening with Listening as the baseline ({[PLV_Vocalizing−PLV_Listening]_significant / PLV_Listening} × 100%, see details in “METHODS”). Since it is based on significant differences of PLVs between two conditions, red regions would represent significant enhanced changes of PLVs from the baseline, blue regions would represent significant suppressed changes of PLVs from the baseline, and green regions would represent non-significant changes of PLVs between two conditions.

Figure 3

Relationship between N100 suppression and averaged percent change of significant differences of PLVs. Intracranial electrode placements of patients A, B, and C are shown, in (A), (B) and (C), respectively. The neuroelectric signals of circled electrode contacts (i.e., Broca’s area circled in blue and auditory cortex circled in yellow) were used for calculating phase locking values (PLVs) and the averaged percent change of significant differences of PLVs (see details in “METHODS”). The averaged event-related potentials to speech onset of green-rectangle-selected electrodes are shown in bottom-left corner of (A), (B), and (C) (magenta trace is Vocalizing and blue trace is Listening). (D) The averaged percent change of significant differences of PLVs is on the x-axis and N100 suppression is shown on the y-axis (see details in “METHODS”). Two-tailed Pearson’s correlation coefficients (r) and ANCOVA results are shown in the upper-right corner. A two-tailed Pearson’s correlation coefficient (r) between the yellow-circled N100 suppression and its corresponding averaged percentage change of significant differences of PLVs was calculated (i.e., the hollow circles and the dashed line; r = −0.825, p = 0.006). Additionally, a mixed model analysis of covariance (ANCOVA) was applied to those hollow-circled values (F_(1,5) = 9.058, p = 0.03). The other two-tailed Pearson’s r between the best N100 suppression (from the green-rectangle-selected electrode) and the grand mean of averaged percentage changes of significant differences of PLVs was computed (i.e., the solid circles and line; r = −0.998, p = 0.044).