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Mapping Brain Region Activity during Chewing: A Functional Magnetic Resonance Imaging Study
1 Departments of Anatomy and Basic Neuroscience and Correspondence: * corresponding author, onozuka{at}cc.gifu-u.ac.jp
Mastication has been suggested to increase neuronal activities in various regions of the human brain. However, because of technical difficulties, the fine anatomical and physiological regions linked to mastication have not been fully elucidated. Using functional magnetic resonance imaging during cycles of rhythmic gum-chewing and no chewing, we therefore examined the interaction between chewing and brain regional activity in 17 subjects (aged 20-31 years). In all subjects, chewing resulted in a bilateral increase in blood oxygenation level-dependent (BOLD) signals in the sensorimotor cortex, supplementary motor area, insula, thalamus, and cerebellum. In addition, in the first three regions, chewing of moderately hard gum produced stronger BOLD signals than the chewing of hard gum. However, the signal was higher in the cerebellum and not significant in the thalamus, respectively. These results suggest that chewing causes regional increases in brain neuronal activities which are related to biting force.
Key Words: functional magnetic resonance imaging • gum chewing • masticatory system • brain activation • human
Mastication is a coordinated function of the masticatory system that involves the peripheral effector organ, sensory input, and the central nervous system (Kubota et al., 1988; Nakamura and Katakura, 1995). Although the basic motor command for this rhythmic behavior is generated by a neuronal population in the brain stem (Nakamura and Katakura, 1995; Nakata, 1998), the central motor command has been proposed to be induced by a certain neuronal population, which receives rhythmic input activities from the brain stem, integrates the input with other central and peripheral inputs, and sends the command to the cranial motoneurons innervating the jaw, tongue, and facial muscles (Lund and Olsson, 1983; Lund et al., 1984; Rossignol and Dubuc, 1994). In many species, including the cat, rabbit, and monkey, repetitive electrical stimulation of a certain area in the cerebral cortex induces coordinated rhythmic movement of the jaw and tongue (Nakamura and Katakura, 1995). Since this movement is accompanied by secretion of saliva, and the pattern of the movement strongly resembles natural masticatory movement, this area has been called the cortical masticatory area (Nakamura and Katakura, 1995). In recent years, it has been shown that, in humans, gum-chewing not only results in transient increases in energy expenditure and heart rate response (Suzuki et al., 1992), but also increases cerebral blood flow due to changes in internal carotid arterial blood flow (Sesay et al., 2000; Sasaki, 2001). Furthermore, cerebral blood flow imaging during gum-chewing, revealed by positron emission tomography (PET), shows increased blood flow in the bilateral lower frontal and parietal lobes (Watanabe et al., 1992; Momose et al., 1997). However, because of the low spatial and temporal resolution of PET, it is difficult to record actual brain activation during chewing and to identify the fine anatomical regions activated during chewing. To test specific hypotheses about the anatomical and physiological regions involved in processing sensory and motor information in the human brain (Pulvermuller, 1999; Yancey and Phelps, 2001), investigators have used functional magnetic resonance imaging (fMRI), because of its enhanced spatial and temporal resolution (Meisenzahl and Schlosser, 2001), and because it offers the advantage that the actual responses to both chewing and the fine regions linked to chewing can be analyzed. In this study, we used fMRI to evaluate brain activation associated with chewing in intact humans.
Subjects Seventeen subjects (10 males and 7 females, aged 20 to 31 yrs) with normal masticatory function participated in this study, but three of these were excluded from the analysis due to a significant motion artifact. Written informed consent was obtained from each subject after the aims and methodology of the study were explained, and the study received local ethical approval (Committees of Yoro Central Hospital).
Task Paradigm
Image Acquisition For each subject, functional (T2* weighted) images, followed by an anatomical (T1 weighted) image, were acquired by means of a 1.5-T Horizon MRI scanner (General Electric, Milwaukee, WI, USA). The functional images consisted of echo-planar image volumes which were sensitive to BOLD (blood oxygenation level-dependent) contrast in the axial orientation (TE = 44 ms, TR = 4,000 ms). The volume covered the whole brain with a 64 x 64 matrix and 42 slices (voxel size = 3.75 mm x 3.75 mm x 4 mm, slice thickness = 3.8 mm, gap = 0.2 mm). Images with 64 volumes were acquired under each of the two experimental conditions (X and G gum types).
Data Analysis The 64 successive functional images for each subject were normalized to the MNI template, provided by the Montreal Neurological Institute (Lutz et al., 2000), and spatially smoothed with an 8 mm Gaussian kernel on SPM99 software on Matlab (MathWorks, Inc., Natick, MA, USA). Statistical analysis, based on the general linear model approach (Friston et al., 1995), was used. Global changes in the BOLD signal were removed by proportional scaling. The resulting areas of activation were characterized in terms of their peak heights (p < 10-5, uncorrected for multiple comparisons) and spatial extents (> 20 voxels). To determine the increase in the fMRI signal during chewing, we calculated the difference between the signals while chewing and not chewing and expressed it as a percent change in the signal in the absence of chewing. The resultant data were analyzed by ANOVA followed by Scheffé’s post hoc test.
In all subjects, gum-chewing was associated with significant increases in the BOLD signal in various regions of the brain (Figs. 1B, 1C  ). An increase was seen bilaterally in the primary sensorimotor cortex, extending down into the upper bank of the operculum and insula. In addition, increases were seen in the supplementary motor area (extending down into the cingulate gyrus), thalamus, and cerebellum. Fig. 1D shows the chewing-related signal changes in these regions. The locations of the most significant foci of activation for these regions are summarized in the Table , in which the anatomical regions with maximal t values in clusters, with co-ordinates as given in the Talairach and Tournoux (1988) atlas, are shown. In addition, in the cerebellum, chewing of G-type gum resulted in a larger increase in the BOLD signal than the chewing of X-type gum, whereas the converse was true for all other areas, except for the thalamus, in which no difference was seen between the increases due to the chewing of the two gum types.
For further assessment of the effects of gum hardness, the increase in the fMRI signals obtained in each region with the two types of gum was compared. As shown in Fig. 2 , in the case of G-type gum, the increased signal was about 84% of that seen with X-type gum on the left side (F1,26 = 8.44, p < 0.01) and about 92% on the right side (F1,26 = 6.39, p < 0.05) of the sensorimotor cortex, about 80% on the left side of the supplementary motor area (F1,26 = 6.41, p < 0.05), and about 79% on the left side (F1,26 = 10.71, p < 0.01), and about 78% on the right side (F1,26 = 9.28, p < 0.01) of the insula. No significant difference was seen in the thalamus. In the cerebellum, the trend toward a higher signal with G-type gum was significant (F1,26 = 41.15, p < 0.0001, left side; F1,26 = 16.05, p < 0.001, right side).
To the best of our knowledge, this is the first study to use fMRI to investigate the relationship between chewing and regional brain activation. In the present study, the primary sensorimotor cortex was strongly activated by chewing. Penfield and Boldrey (1938) mapped the primary motor cortex in humans by electrically stimulating the exposed scalp during neurosurgery and demonstrated that the masticatory organs are represented on the inferior aspect of the primary motor cortex, close to the lateral fissure. Their mapping is in good agreement with the increased fMRI signal seen in the primary motor cortex during gum-chewing. We also showed relatively large bilateral regions of activation that encompassed the inferolateral primary sensory cortex, in which the masticatory organs are present (Penfield and Boldrey, 1938). Studies in non-human primates have shown that there are many "non-primary" motor areas in the cortex that are associated with voluntary control of movement (Fink et al., 1997). Some of these areas show somatotopic mapping and have direct connections to the primary motor cortex or spinal cord. Fink et al. (1997) used PET to map the location of such areas in humans using voluntary movements of the hand, shoulder, and leg. It is notable that all the non-primary cortical areas associated with chewing identified in the present study [i.e., the supplementary motor area and the insula, also called the masticatory center (Nakata, 1998)] were also identified during hand, shoulder, and leg movements (Fink et al., 1997). Additionally, in the present study, chewing was associated with significant signal increases in the thalamus and cerebellum, typical of those associated with the voluntary control of movement (Passingham, 1993). A significant increase in the fMRI signal (p < 0.05) was seen throughout the striatum, pre-frontal cortex, or parietal cortex, in which blood flow has been shown to be increased by gum-chewing (Momose et al., 1997). However, the peak of the fMRI signal in the striatum could not be isolated due to strong activation of the insula, and the locations of the signal changes in the pre-frontal or parietal cortex were different in each subject. Thus, we cannot rule out the possibility that these signal changes might contain some artifacts or unknown mechanisms. In the cerebellum, chewing of hard gum caused a greater increase in the BOLD signal than did chewing of moderately hard gum. It has been shown that an increase in the masticatory force elevates activities in the masseter muscle (Proschel and Raum, 2001), where sensory information is finally projected to the cerebellum (Kubota et al., 1988). Thus, it is reasonable to say that a greater increase in the signal during chewing of hard gum reflects increased information from the masticatory muscle. The present results, showing lower cortical activation during the chewing of hard gum compared with moderately hard gum, are in good agreement with the findings that mastication of moderately hard food leads to a greater increase in cerebral blood flow than that of soft and/or hard food (Nakata, 1998; Sesay et al., 2000). Taken together with the fact that cerebral activation during mastication of Jello is low (unpublished data), this suggests that chewing with a moderate biting force may be most effective in maintaining neuronal activity within the brain. However, the mechanism underlying chewing-induced regional activation within the brain is unclear at the present time, and further research is required.
This work was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Culture of Japan (12557173, 14370630), Health Sciences Research Grants (H13-21EBM-018) from the Ministry of Health, Labor and Welfare, Japan, and a grant from Lotte Co. Ltd. (Tokyo, Japan). Received for publication June 13, 2002. Revision received August 26, 2002. Accepted for publication September 6, 2002.
Journal of Dental Research, Vol. 81, No. 11,
743-746 (2002) This article has been cited by other articles:
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