The coupling between auditory and motor cortices is rate-restricted: Evidence for an intrinsic speech-motor rhythm

Abstract

The relation between perception and action remains a fundamental question for neuroscience. In the context of speech, existing data suggest an interaction between auditory and speech-motor cortices, but the underlying mechanisms remain incompletely characterized. We fill a basic gap in our understanding of the sensorimotor processing of speech by examining the synchronization between auditory and speech-motor regions over different speech rates, a fundamental parameter delimiting successful perception. First, using magnetoencephalography, we measure synchronization between auditory and speech-motor regions while participants listen to syllables at various rates. We show, surprisingly, that auditory-motor synchrony is significant only over a restricted range and is enhanced at ~4.5 Hz, a value compatible with the mean syllable rate across languages. Second, neural modeling reveals that this modulated coupling plausibly emerges as a consequence of the underlying neural architecture. The findings suggest that the temporal patterns of speech emerge as a consequence of the intrinsic rhythms of cortical areas.

Fig. 1. Extracting motor and auditory cortex activity while perceiving speech.

(A) Two examples of the experimental trials. Gray, sound wave; black, its envelope. The upper trial shows a syllable rate of 2.5 Hz, and the lower trial shows a syllable rate of 6.5 Hz. (B) Functional localizations of speech-motor (red) and auditory (blue) regions for three participants. Top row, left hemisphere; bottom row, right hemisphere.

Fig. 2. Activity in auditory cortices synchronizes to the speech envelope across rates.

(A) Increment from baseline of PLV between auditory cortex and the envelope of the sound as a function of frequency. The panels correspond to different syllable rate conditions. Light gray lines, individual subject data; colored line, mean across subjects (red, 2.5 syllables/s; blue, 3.5 syllables/s; green, 4.5 syllables/s; yellow, 5.5 syllables/s; dark gray, 6.5 syllables/s). Vertical line, stimulus rate. (B) Mean PLV around the syllable rate of each condition (syllable rate ±0.5 Hz). Dots, individual participants; black lines, mean across participants; shadowed region, SD.

Fig. 3. Synchronization between auditory and motor cortices is modulated by the heard syllable rate.

(A) Increment from baseline of PLV between auditory and motor cortex activity as a function of frequency. Top left, schematic of analysis. The data panels correspond to the different syllable rate conditions. Light gray lines, individual subject data; colored line, mean across participants (red, 2.5 syllables/s; blue, 3.5 syllables/s; green, 4.5 syllables/s; yellow, 5.5 syllables/s; dark gray, 6.5 syllables/s). Vertical dashed line, stimulus rate. (B) Top: Percent change from baseline of PLV as a function of frequency, averaged across subjects. Straight lines on the top show significant increment from baseline (Wilcoxon signed-rank test, P < 0.03, FDR-corrected). Bottom: Mean PLV around the syllable rate of each condition (syllable rate ±0.5 Hz). Asterisk (*) shows significant difference between conditions (Wilcoxon signed-rank test, P < 0.03, FDR-corrected).

Fig. 4. Correlation between auditory-motor PLV and auditory-speech PLV.

(A) Schematic of analysis. (B) Contralateral motor-auditory PLV as a function of the corresponding auditory-stimulus PLV. Each panel represents a different syllable rate condition (red, 2.5 syllables/s; blue, 3.5 syllables/s; green, 4.5 syllables/s; yellow, 5.5 syllables/s; dark gray, 6.5 syllables/s), and the black line represents the linear fitting of the data. Asterisk (*) shows significant correlation between variables (P < 0.05, FDR-corrected).

Fig. 5. A simple neural model replicates the auditory-motor synchronization pattern.

(A) Schematic illustration of the neural model: Motor cortex modeled through a set of Wilson-Cowan equations representing an inhibitory-excitatory network, and the excitatory population receives the auditory cortex activity as input. (B) Numerical simulations submitted to the same analyses as the experimental data set. Straight lines show significant increment from baseline (Wilcoxon signed-rank test, P < 0.03, FDR-corrected). Asterisk (*) shows significant differences between conditions (Wilcoxon signed-rank test, P < 0.03, FDR-corrected). Colors identify the different conditions (red, 2.5 syllables/s; blue, 3.5 syllables/s; green, 4.5 syllables/s; yellow, 5.5 syllables/s; dark gray, 6.5 syllables/s).