Neuroscience Letters 360 (2004) 137–140 www.elsevier.

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A fronto-parietal network for chewing of gum: a study on human subjects with functional magnetic resonance imaging
Toshihisa Takadaa,*, Tamaki Miyamotob
a

Department of Oral Functional Science, Graduate School of Dental Medicine, Hokkaido University, Kita-13, Nishi-7, Kita-Ku, Sapporo, 006-8586, Japan b Department of Physiology, Graduate School of Medicine, Hokkaido University, Sapporo, Japan Received 3 December 2003; received in revised form 10 February 2004; accepted 23 February 2004

Abstract The purpose of this study is to investigate human brain activity during mastication using fMRI. Twelve right-handed normal subjects performed two tasks: chewing of gum at their own pace, and imitating the movements of chewing gum. In order to reveal which areas of the brain are more strongly activated while chewing gum, we performed the conjunction analyses of gum chewing minus sham chewing with gum chewing minus rest. The common activity in the orofacial sensorimotor and premotor cortex was subtracted out since it was common to both tasks, but there were some differences in activity in some prefrontal and posterior parietal cortex areas. Our results suggest that a frontoparietal network for mastication exists and may contribute to higher cognitive information processing. q 2004 Elsevier Ireland Ltd. All rights reserved.
Keywords: Functional magnetic resonance imaging; Mastication; Manipulation; Prefrontal cortex; Fronto-parietal network

Can chewing of gum improve brain performance? It is difficult to answer this question. The masticatory movements activate the brain; therefore, it has been generally said that the learning effect is improved or dementia is prevented. Recently, Wilkinson et al. discovered that chewing gum can improve the memory of the person chewing it [14]. They suggest that chewing of gum can improve episodic memory (involving the learning, storage and retrieval of information) and working memory (where information is held ‘on line’). These findings have raised the possibility of a differential involvement of the cortical regions related to human memory in the act of mastication. When humans think about eating, higher-order mental activities must be absolutely essential. For instance, while eating we always have to recognize the features of foods within the mouth and manipulate them adequately during mastication. However, previous neuroimaging studies have not shown that the cortical regions other than primary and nonprimary motor areas were activated during mastication [7]. This result does not reinforce the idea that mastication needs higher-order mental activities. Several neuroimaging findings
* Corresponding author. 9-22, 2-jo, 1-tyoume, Satozuka, Kiyota-Ku, Sapporo, 004-0802, Japan. Tel.: þ81-11-889-5057; fax: þ 81-11-8895057. E-mail address: takada@den.hokudai.ac.jp (T. Takada).

provide the strongest evidence available to date from human studies that the prefrontal cortex plays a role in working memory function [5]. If ‘mastication’ results in increased activity in the prefrontal cortex, this evidence may give a very significant scientific basis to the general idea that ‘mastication’ improves brain performance. However, no one has demonstrated a correlation between the activity in the prefrontal cortex and chewing of gum previously. Moreover, little is known about whether brain activity related to mastication and mere jaw movements are different. In the present experiment, 12 right-handed participants between the ages of 20 and 28 years were tested. Six women and six men participated in this study. None had any history of neurological or psychiatric disorders. Informed consent was obtained from each subject prior to the experiment. The Committee of Medical Ethics, Hokkaido University, approved the protocol of this study. We employed two tasks: (1) a self-paced gum chewing task; (2) a sham chewing task. In the gum chewing task, all subjects were instructed to chew a piece of gum base (Lotte Co., Ltd., Tokyo, Japan) at their own, but constant, pace. During the sham chewing task, the subjects were instructed to mimic chewing movements, but they did not actually have a piece of gum in their mouths. Both task sessions (gum chewing task and sham chewing task) were designed in a block

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T. Takada, T. Miyamoto / Neuroscience Letters 360 (2004) 137–140

manner (four rest and four task blocks, respectively, for 28 and 224 s for a single task session). All subjects participated in both sessions in random order. Each trial began with the rest block, followed by the task block (gum chewing or sham chewing) at a given auditory signal. During the experiment, the room lights were dimmed and the subjects’ eyes were closed. Brain imaging data were acquired on a GE Signa 1.5 T whole-body MRI scanner using a head coil. For functional imaging, we used a gradient-echo echo-planar imaging sequence (GRE-EPI) with the following parameters: FOV 24 £ 24 cm; matrix 64 £ 64; slice thickness 5 mm; slice gap 2.5 mm; TR 4 s; TE 40 ms. The spatial resolution was 3.75 £ 3.75 £ 5 mm. In addition, 12 slices were obtained from a single session. Sessions that showed brain motion exceeding 0.375 mm were repeated to avoid fictional activation due to pixel misalignment. After image construction, fMRI time series data consisting of consecutive EPI images for each slice were analyzed using SPM99 software (Wellcome Department of Cognitive Neurology, London, UK). T1 anatomical images were coregistered to the mean of the functional scans and aligned to the SPM T1 template in the Talairach space. The calculated nonlinear transformation was applied to all functional images for spatial normalization. Finally, the functional images were smoothed with a 6 mm full width at half maximum (FWHM) kernel, Gaussian filter. Contrasts were calculated by fixed-SOA from the protocol as epochs and by convolving them with the hemodynamic response function (HRF) to specify the appropriate design matrix. Condition and subject effects were estimated according to the general liner model at each voxel in brain space. To minimize effects of physiological noise, a high pass filter of 80 s was applied within the design matrix. Moreover, a low pass filter of Gaussian type (4 s) was also used. Specific effects were tested by applying appropriate linear contrasts to the parameter estimates for each condition, resulting in a statistic for each and every voxel, while group data were analyzed using a random effects model. The resulting correlates were transformed into a Z score map. The significant Z value was threshold at z . 3:09 (corresponding to P , 0:001 at each voxel level). Only clusters . 10 activated voxels were reported. Activated brain structures were identified by transforming the MNI coordinate into the brain atlas of Talairach and Tournoux. In this study, we undertook the following comparisons of the main experiment: gum chewing task minus sham chewing task with gum chewing task minus rest. The purpose of this comparison is to reveal which areas of the brain are relatively more strongly activated while chewing gum. We found that the mean ^ SD frequency of the jaw movements during the gum chewing task was 1.15 ^ 0.11 Hz, while the mean frequency was faster than that noted during the sham chewing task (1.24 Hz). The gum chewing task significantly activated the primary sensorimotor cortex extending down into the upper bank of the operculum and insula, the dorsal and ventral premotor

areas (PMA) bilaterally, the supplementary motor area (SMA), the left inferior frontal cortex, the middle frontal gyrus bilaterally, the intraparietal cortex bilaterally and the superior parietal lobe (SPL) bilaterally. However, the SMA, the inferior frontal cortex, and the middle frontal cortex activation did not reach statistical significance (P , 0:05, corrected), although an uncorrected significance level of P , 0:001 was observed. The same areas in the primary sensorimotor areas bilaterally, the dorsal and ventral PMA, and the SMA were also significantly activated during the sham chewing task (P , 0:005, corrected), however in the inferior and middle frontal cortex no increase in activity was observed (P , 0:001, uncorrected). Then, to reveal which areas of the brain were relatively more strongly activated while chewing gum, we performed the conjunction analyses of gum chewing minus sham chewing with gum chewing minus rest. This conjunction analysis was applied by masking, whereby the second subtraction was tested only in pixels that reached significance (P , 0:001) in the first subtraction. This analysis revealed significant activation in the middle frontal cortex bilaterally (x ¼ 50, y ¼ 42, z ¼ 24 in Talairach coordinates with the peak score of Z ¼ 5:78, x ¼ 244, y ¼ 58, z ¼ 14 with Z ¼ 5:62), the left inferior cortex (x ¼ 252, y ¼ 46, z ¼ 214 with Z ¼ 7:34), the inferior parietal lobule (x ¼ 42, y ¼ 266, z ¼ 50 with Z ¼ 3:83, x ¼ 240, y ¼ 268, z ¼ 40 with Z ¼ 3:98) and the right superior parietal lobule (x ¼ 18, y ¼ 280, z ¼ 50 with Z ¼ 4:84) (Fig. 1). Specific activations were obtained in the dorsolateral prefrontal cortex, ventral prefrontal cortex, and parietal cortex during the gum chewing task. In the present study using conjunction analysis, the common activity in the orofacial sensorimotor and premotor cortex was subtracted out since it was common to both tasks. Consequently, we hypothesize that the parieto-frontal network plays an essential role in ‘mastication’. Areas in the middle frontal gyrus and inferior frontal gyrus were activated during the gum chewing task in this study, but were not activated when the subjects merely moved their jaw, tang, and oral mucosa rhythmically (sham chewing task). Therefore, the role of these areas must be involved in whether the gum is actually in the oral cavity. The functional subdivision of the prefrontal cortex has been an issue of much debate recently. A review by Fletcher and Henson [5] more generally states the involvement of the ventrolateral prefrontal area in processes such as updating and maintenance of information. In contrast, processes such as information manipulation activate the dorsolateral prefrontal cortex [4]. Applying these concepts to our data, we would like to argue that prefrontal activation during mastication can be related to the manipulation of somatosensory information and the retention of stimulus related information. Our results may extend recent models on the prefrontal cortex and its contribution to higher cognitive information processing as established in the verbal [2,6],

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Fig. 1. Surface projections of color-coded statistical parametric maps (SPMs) superimposed onto MNI standard brain. Activation revealed by gum chewing minus sham chewing with gum chewing minus rest. Left and right sides represent the left and right hemispheres, respectively. The center represents an overhead view. The threshold is set at P , 0:05, corrected.

visual [3], and visuospatial [11] domain by demonstrating their relevance and applicability for the somatosensory domain related to automaticity such as mastication. However, further studies are needed to investigate the precise role of these prefrontal areas. In particular, studies that manipulate the degree of memory load required are needed. Additionally, an area in the inferior parietal lobule showed activation. This result is consistent with the results reported in a previous study indicating that the activation of the inferior parietal lobule is related to tactile object identification [1]. Furthermore, focal lesions in the inferior parietal lobule are known to produce a selective deficit in shape perception and representation with preserved lower somatosensory functions, spatial abilities, and tactile exploration behavior [9]. In addition, coactivation of the ventral PMA and the inferior parietal lobule was observed. Classically, the ventral sector of the frontal cortex was thought of as an area controlling oro-laryngeal movements. However, a series of recent studies showed that this view only partially describes the function of the ventral PMA [8, 12]. These data suggest that, in addition to the control of oro-laryngeal movements, the ventral PMA is of importance for motor tasks with high motor execution demands [15]. Therefore, we suggest that coactivation of the parietal and the premotor cortex indicates that these areas are part of the cortical network involved in tactile information processing during the mastication. Finally, the SMA was activated during the sham chewing task. The focus of SMA activation was probably located in the pre-SMA [10,13]. However, the SMA showed slight increases in activity (P , 0:001, uncorrected) during the gum chewing task. Our findings may indicate that activity in the cerebral cortex is different between mastication with food and rhythmical jaw movements. However, the contribution of the pre-SMA in mastication requires further research.

In contrast to the present study, a previous neuroimaging study gave negative results for the existence of a frontoparietal network subserving the masticatory movement [7]. We have demonstrated that the coactivation of the prefrontal and the parietal cortex was observed with conjunction analysis. As for these findings, we suggest that our results may extend recent models on the prefrontal cortex and its contribution to higher cognitive information processing. Presumably, the tactile information from the oral cavity, related to a piece of gum, may become a trigger to recollect the ‘mastication’. However, it is unclear what the mechanism underlying oral stereognosis and recognition of the food bolus is, so further investigation is required.

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