Speech networks at rest and in action: interactions between functional brain networks controlling speech production

Abstract

Speech production is one of the most complex human behaviors. Although brain activation during speaking has been well investigated, our understanding of interactions between the brain regions and neural networks remains scarce. We combined seed-based interregional correlation analysis with graph theoretical analysis of functional MRI data during the resting state and sentence production in healthy subjects to investigate the interface and topology of functional networks originating from the key brain regions controlling speech, i.e., the laryngeal/orofacial motor cortex, inferior frontal and superior temporal gyri, supplementary motor area, cingulate cortex, putamen, and thalamus. During both resting and speaking, the interactions between these networks were bilaterally distributed and centered on the sensorimotor brain regions. However, speech production preferentially recruited the inferior parietal lobule (IPL) and cerebellum into the large-scale network, suggesting the importance of these regions in facilitation of the transition from the resting state to speaking. Furthermore, the cerebellum (lobule VI) was the most prominent region showing functional influences on speech-network integration and segregation. Although networks were bilaterally distributed, interregional connectivity during speaking was stronger in the left vs. right hemisphere, which may have underlined a more homogeneous overlap between the examined networks in the left hemisphere. Among these, the laryngeal motor cortex (LMC) established a core network that fully overlapped with all other speech-related networks, determining the extent of network interactions. Our data demonstrate complex interactions of large-scale brain networks controlling speech production and point to the critical role of the LMC, IPL, and cerebellum in the formation of speech production network.

Keywords: graph theoretical analysis; hemispheric lateralization; large-scale networks; resting state; speech production.

Fig. 1.

Brain activation during speech production and the seed regions. A group statistical parametric map of brain activation during speech production is shown on inflated cortical surfaces and series of coronal slices in the AFNI standard Talairach-Tournoux space. Black spheres indicate the location of 14 seed regions of interest. The corresponding location coordinates are given in Table 1. Color bar indicates t-values.

Fig. 2.

Organization of brain networks controlling speech production. A: bilateral shared network during speech production showing connectivity from the left hemisphere seed regions (I) and from the right hemisphere seed regions (II). B: distinct connectivity from individual seed networks, not overlapping with any other network during speech production showing connectivity from the left hemisphere seed regions (I) and from the right hemisphere seed regions (II). Brain connectivity is presented on inflated brain surfaces to depict cortical connectivity and on axial and sagittal brain slices to depict subcortical and cerebellar connectivity in the AFNI standard Talairach-Tournoux space. Color bar in A shows a percent overlap between individual seed networks. Color bar in B shows the color-coded connectivity from 7 seed regions. M1, primary motor cortex (area 4p); IFG, inferior frontal gyrus; SMA, supplementary motor area; STG, superior temporal gyrus; CC, cingulate cortex; Put, putamen; TH, thalamus.

Fig. 3.

Organization of resting-state brain networks associated with speech production. A: bilateral shared network during the resting state showing connectivity from the left hemisphere seed regions (I) and from the right hemisphere seed regions (II). B: distinct connectivity from individual seed networks, not overlapping with any other network during the resting state showing connectivity from the left hemisphere seed regions (I) and from the right hemisphere seed regions (II). Brain connectivity is presented on inflated brain surfaces to depict cortical connectivity and on axial and sagittal brain slices to depict subcortical and cerebellar connectivity in the AFNI standard Talairach-Tournoux space. Color bar in A shows a percent overlap between individual seed networks. Color bar in B shows the color-coded connectivity from 7 seed regions.

Fig. 4.

Distinct connectivity of individual seed networks during speech production (A) and the resting state (B). Block diagrams show distinct connections, not overlapping with any other network connections of individual seed networks during speech production and the resting state in the left and right hemispheres. SPN, speech-production network; RSN, resting-state network; ITG, inferior temporal gyrus; SMG, supramarginal gyrus; AG, angular gyrus.

Fig. 5.

Graph-theoretical characteristics of speech-controlling brain regions. A: brain views show the relative positions of the examined regions (graph nodes). The color of the spheres represents nodal strength [normalized to the range (0,1) and scaled with respect to the 14 depicted regions]. The bar charts depict the nodal values of normalized local efficiency (B), normalized clustering coefficient (C), normalized betweenness centrality (D), and nodal strength averaged across subjects in RSN (blue) and SPN (red) (E). Asterisks indicate statistically significant differences between RSN and SPN at a family-wise error (FWE)-corrected P ≤ 0.05. Cbl, cerebellum.

Fig. 6.

Functional network lateralization. Laterality indices of shared RSN and shared SPN (A) and graph theoretical measures (B). Negative values indicate right hemispheric lateralization; positive values indicate left hemispheric lateralization. Asterisk denotes significant difference.