Functional connectivity of human chewing: an fcMRI study

Abstract

Mastication is one of the most important orofacial functions. The neurobiological mechanisms of masticatory control have been investigated in animal models, but less so in humans. This project used functional connectivity magnetic resonance imaging (fcMRI) to assess the positive temporal correlations among activated brain areas during a gum-chewing task. Twenty-nine healthy young-adults underwent an fcMRI scanning protocol while they chewed gum. Seed-based fcMRI analyses were performed with the motor cortex and cerebellum as regions of interest. Both left and right motor cortices were reciprocally functionally connected and functionally connected with the post-central gyrus, cerebellum, cingulate cortex, and precuneus. The cerebellar seeds showed functional connections with the contralateral cerebellar hemispheres, bilateral sensorimotor cortices, left superior temporal gyrus, and left cingulate cortex. These results are the first to identify functional central networks engaged during mastication.

Figure 1.

Example data from one participant. The horizontal axis for all 3 plots is the number of images in sequential order. Top: BOLD signal sampled from the left motor cortical seed (black) and from the region in the right motor cortex that showed functional connectivity with the left seed (gray). The vertical axis is signal intensity in arbitrary units. The gray square-wave in the plot shows the block design; rest blocks occurred when the square wave is at zero, and chew blocks occurred during the time periods when the square wave is at unity. The reported functional connectivity results are based on temporal correlations unique to the chewing blocks, e.g., images 10-20, 30-40, 50-60…170-180, 190-200. Middle and bottom: Plots of movement parameters for one participant showing translation (middle) and rotational (bottom) movement artifacts.

Figure 2.

Images of the functional connectivity maps for the seeds in the motor cortices. Upper panel: Results for the right motor cortex seed. Three sections are shown in the upper panel: top left, coronal (y = -8); top right, sagittal (x = -16); and bottom left, axial (z = 32). Lower panel: Results for the left motor cortex seed. The 3 sections in the lower panel are: top left, coronal (y = -14); top right, sagittal (x = 4); and bottom left, axial (z = 32). The gray rectangles at the top of the Fig. indicate participant orientations, viz., L, left; R, right; P, posterior; and A, anterior (for axial sections, anterior is toward the top of the page). Color-coded bars display z-scores; results are based on voxel-level, p < 0.001, uncorrected. Key: Anterior cingulate cortex (ACC); cerebellum posterior lobe (Cpl); middle cingulate cortex (MCC); pre-central gyrus (PrG); precuneus (PCun); superior frontal gyrus (SFG); supplementary motor area (SMA). The labels indicate where the peak values occurred; however, several clusters expand into other areas that are not named in the Fig. (see text and Table).

Figure 3.

Images of the connectivity maps for the seeds in the cerebellum. Upper panel: Results for right posterior cerebellar seed. Three sections are shown in the upper panel: top left, coronal (y = -8); top right, sagittal (x = -2); and bottom left, axial (z = 20). Lower panel: Results for left posterior cerebellar seed. The 3 sections in the lower panel are: top left, coronal (y = -50); top right, sagittal (x = 2); and bottom left, axial (z = 65). Brain-section orientations in both panels are the same as those used in Fig. 2. Color-coded bars display z-scores; results are based on voxel-level, p < 0.001, uncorrected. Key: Pre-central gyrus (PrG); precuneus (PCun); Rolandic operculum (ROP); superior temporal gyrus (STG); supplementary motor area (SMA); thalamus (T). The labeled structures indicate where the peak values occurred; however, several clusters expand into other areas that are not named in the Fig. (see text and Table).