Enhanced neural synchrony between left auditory and premotor cortex is associated with successful phonetic categorization

Abstract

The cortical dorsal auditory stream has been proposed to mediate mapping between auditory and articulatory-motor representations in speech processing. Whether this sensorimotor integration contributes to speech perception remains an open question. Here, magnetoencephalography was used to examine connectivity between auditory and motor areas while subjects were performing a sensorimotor task involving speech sound identification and overt repetition. Functional connectivity was estimated with inter-areal phase synchrony of electromagnetic oscillations. Structural equation modeling was applied to determine the direction of information flow. Compared to passive listening, engagement in the sensorimotor task enhanced connectivity within 200 ms after sound onset bilaterally between the temporoparietal junction (TPJ) and ventral premotor cortex (vPMC), with the left-hemisphere connection showing directionality from vPMC to TPJ. Passive listening to noisy speech elicited stronger connectivity than clear speech between left auditory cortex (AC) and vPMC at ~100 ms, and between left TPJ and dorsal premotor cortex (dPMC) at ~200 ms. Information flow was estimated from AC to vPMC and from dPMC to TPJ. Connectivity strength among the left AC, vPMC, and TPJ correlated positively with the identification of speech sounds within 150 ms after sound onset, with information flowing from AC to TPJ, from AC to vPMC, and from vPMC to TPJ. Taken together, these findings suggest that sensorimotor integration mediates the categorization of incoming speech sounds through reciprocal auditory-to-motor and motor-to-auditory projections.

Keywords: MEG; dorsal stream; magnetoencephalography; premotor cortex; sensorimotor integration; speech perception.

FIGURE 1

Experimental procedure. Adapted from Alho et al. (2012).

FIGURE 2

Regions-of-interest (ROIs). AC, auditory cortex; TPJ, temporoparietal junction; MC, motor cortex; vPMC, ventral premotor cortex; dPMC, dorsal premotor cortex.

FIGURE 3

Effect of stimulus type and condition on inter-areal phase synchrony. (A) Stronger synchrony in response to noisy compared to intact stimulus type. (B) Stronger synchrony in active compared to passive listening condition. (C) Stimulus type x condition interaction and results from a post hoc t-test showing differences between conditions and stimulus types at the time-frequency point of strongest interaction. The arrows indicate SEM-derived directionality effects based on the pairwise path coefficients. The double arrow denotes undirected interaction. Asterisks indicate significant differences (*p < 0.05, **p < 0.01, ***p < 0.001, uncorrected). Error bars indicate SE.

FIGURE 4

Correlations between inter-areal phase synchrony and syllable identification accuracy. Syllable identification scores plotted against phase synchrony strength (WPLI) at the time-frequency point of strongest correlation. The spearman rank correlation coefficients (r) and corresponding p-values are denoted in each plot. The arrows indicate SEM-derived directionality effects based on the pairwise path coefficients. The double arrow denotes undirected interaction. AC, auditory cortex; TPJ, temporoparietal junction; vPMC, ventral premotor cortex; MC, motor cortex.

FIGURE 5

Comparison between models of effective connectivity. RMSEA was applied to test the goodness-of-fit between all unidirectional SEM models between the three functionally interconnected left-hemisphere areas. The horizontal dashed line denotes the cut-off point with RMSEA < 0.07 considered a good fit (Steiger, 2007). Error bars indicate SE. AC, auditory cortex; TPJ, temporoparietal junction; vPMC, ventral premotor cortex.