Dynamic causal modeling analysis reveals the modulation of motor cortex and integration in superior temporal gyrus during multisensory speech perception

Abstract

The processing of speech information from various sensory modalities is crucial for human communication. Both left posterior superior temporal gyrus (pSTG) and motor cortex importantly involve in the multisensory speech perception. However, the dynamic integration of primary sensory regions to pSTG and the motor cortex remain unclear. Here, we implemented a behavioral experiment of classical McGurk effect paradigm and acquired the task functional magnetic resonance imaging (fMRI) data during synchronized audiovisual syllabic perception from 63 normal adults. We conducted dynamic causal modeling (DCM) analysis to explore the cross-modal interactions among the left pSTG, left precentral gyrus (PrG), left middle superior temporal gyrus (mSTG), and left fusiform gyrus (FuG). Bayesian model selection favored a winning model that included modulations of connections to PrG (mSTG → PrG, FuG → PrG), from PrG (PrG → mSTG, PrG → FuG), and to pSTG (mSTG → pSTG, FuG → pSTG). Moreover, the coupling strength of the above connections correlated with behavioral McGurk susceptibility. In addition, significant differences were found in the coupling strength of these connections between strong and weak McGurk perceivers. Strong perceivers modulated less inhibitory visual influence, allowed less excitatory auditory information flowing into PrG, but integrated more audiovisual information in pSTG. Taken together, our findings show that the PrG and pSTG interact dynamically with primary cortices during audiovisual speech, and support the motor cortex plays a specifically functional role in modulating the gain and salience between auditory and visual modalities.

Supplementary information: The online version contains supplementary material available at 10.1007/s11571-023-09945-z.

Keywords: Dynamic causal modeling; McGurk effect; Motor cortex; Multisensory information processing; Superior temporal gyrus.

Fig. 1

Behavioral and fMRI experimental paradigm. A In behavioral task, all participants were instructed to observe the lip movements and listen carefully, and then report what syllable they percept. B In the fMRI task, all participants were allowed to do the same actions with that in the behavioral task excluding reporting. SOA, stimulus onset asynchrony

Fig. 2

A Brain regions with significant task-dependent activation in the group-level statistic (n = 63; one-sample t-test, P < 0.05, FDR-corrected). Brain map was generated with BrainNet Viewer version 1.61 (http://www.nitrc.org/projects/bnv/); B ROIs. The anatomy map (n = 63) was employed to determine node peak selection, in which four peaks were showed in red. We only explored regions from the left hemisphere. The anatomy map was visualized with the MRIcron version 4 (https://www.nitrc.org/projects/mricron). MNI, Montreal Neurological Institute; FuG, fusiform gyrus; pSTG, posterior superior temporal gyrus; mSTG, mid-superior temporal gyrus; PrG, precentral gyrus

Fig. 3

A Results of the family level inference in all participants. The best family of models were the DCMs with bidirectional endogenous connections among the four ROIs (Family 1, family exceedance probability = 80.56%). B Results from the BMA within family. RFX BMS favored the model with modulatory influences on the connections from PrG to FuG, FuG to PrG, PrG to mSTG, mSTG to PrG, mSTG to pSTG, FuG to pSTG (Model 13, model exceedance probability = 34.92%). (C) Overview of the winning model (Model 13). FuG, fusiform gyrus; pSTG, posterior superior temporal gyrus; mSTG, mid-superior temporal gyrus; PrG, precentral gyrus

Fig. 4

Winning model with averaged coupling strength (A- and B- matrix) for excitatory (red) and inhibitory (green) connections (*P < 0.05, **P < 0.01, ***P < 0.001, uncorrected). Coupling strength differences between strong and weak perceivers are illustrated using bar plots (solid star: P < 0.05, FDR-corrected). FuG, fusiform gyrus; pSTG, posterior superior temporal gyrus; mSTG, mid-superior temporal gyrus; PrG, precentral gyrus