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J Dent Res 83(10):762-766, 2004
© 2004 International and American Associations for Dental Research

RESEARCH REPORT
Clinical

Chewing-side Preference is Involved in Differential Cortical Activation Patterns during Tongue Movements after Bilateral Gum-chewing: a Functional Magnetic Resonance Imaging Study

H. Shinagawa1,5,*, T. Ono1, E. Honda2,6, T. Sasaki2, M. Taira3, A. Iriki4, T. Kuroda1, and K. Ohyama1

1 Maxillofacial Orthognathics, 2 Oral/Maxillofacial Radiology, and 3 Cognitive Neurobiology, Graduate School, Tokyo Medical and Dental University, 5-45 Yushima 1-chome, Bunkyo-Ku, Tokyo 113-8549, Japan; 4 Department of Physiology, Nihon University, School of Medicine, Tokyo 113-8610, Japan; 5 Tokyo Metropolitan Institute of Gerontology, Tokyo 173-0015; and 6 Department of Oral/Maxillofacial Radiology, The University of Tokushima, Tokushima 770-8503, Japan;

* corresponding author, h-shinagawa.mort{at}tmd.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Contralateral dominance in the activation of the primary sensorimotor cortex (S1/M1) during tongue movements (TMs) has been shown to be associated with a chewing-side preference (CSP). However, little is known about its interaction with chewing-related cortical activation. Functional magnetic resonance imaging was performed before and after gum-chewing in six subjects who exhibited a left CSP to determine the relationship between the CSP and activation patterns in the S1/M1 during TMs. Before the subjects chewed the gum, activation foci were found in the bilateral S1/M1. In the left hemisphere, both signal intensity and the area of activation significantly increased during TMs within 10 min after subjects chewed gum. Moreover, this augmented activation significantly decreased within 20 min during tongue protrusion and leftward movement. In the right hemisphere, there were no marked changes during TMs. These results suggest that bilateral gum-chewing enhances activation of the S1/M1 ipsilateral to the CSP during TMs.

KEY WORDS: tongue movement • chewing-side preference • cortical activation • gum-chewing • functional magnetic resonance imaging


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Recent functional neuroimaging studies have revealed that mastication activates several cerebral regions, with the greatest activation in the primary sensorimotor cortex (S1/M1) in both hemispheres, without any significant difference between hemispheres (Momose et al., 1997; Onozuka et al., 2002, 2003; Tamura et al., 2003). This lack of hemispheric dominance in the activation pattern has been attributed to the plausible symmetrical contraction of masticatory muscles during chewing and/or cortico-cortical projections between S1 and M1 (Zarzecki et al., 1978; Tamura et al., 2003). Mastication may not be performed symmetrically: Most subjects appear to chew predominantly on one side of the dentition or the other during chewing, which is referred to as the chewing-side preference (CSP; Pond et al., 1986; Mioche et al., 2002). During chewing, the jaws and tongue show cyclic movement that has a close functional connection, not only spatially but also temporally (Palmer et al., 1997; Mioche et al., 2002; Hiiemae and Palmer, 2003). Indeed, in a functional magnetic resonance imaging (fMRI) study, it has been shown that the blood-oxygenation-level-dependent (BOLD) signal was significantly increased in the S1/M1 contralateral to the CSP during TMs (Shinagawa et al., 2003). Unfortunately, the relevance of the CSP to masticatory-related activation in the S1/M1 has not yet been studied.

It has been shown that there are no significant differences in regional cerebral blood flow in the S1/M1 before and after gum-chewing (Momose et al., 1997). In contrast, it was demonstrated that the cortical temperature increased during and after gum-chewing (Funakoshi et al., 1989). This discrepancy regarding the short-term effect of mastication may be clarified by a technique that has better spatial resolution, such as fMRI. However, previous fMRI studies on mastication have had several drawbacks, such as a lack of stabilization of the head to allow for natural head motion during jaw movement, and contamination by physical/electrophysiological artifacts caused by contraction of the masticatory muscles. Thus, it seems inappropriate to investigate chewing-related cortical activation during chewing per se. Rather, it appears to be more appropriate to perform TM without activation of masticatory muscles, to avoid motion-related artifacts, since movements of the tongue and masticatory muscles are closely associated (Lowe et al., 1977; Schieppati et al., 1989; Takada et al., 1996; Palmer et al., 1997; Narita et al., 2002). Since it has been suggested that mastication induces an increase in cerebral blood flow (Senda et al., 1992; Sesay et al., 2000), it may be possible to show that mastication has biologically significant effects against the degenerative effects of aging on the masticatory system (Hector and Linden, 1987; Kubota et al., 1988).

Our aim in this study was, using the BOLD-fMRI technique, to assess the short-term effect of bilateral gum-chewing on cortical activation patterns during TMs, with special attention to the relationship with the CSP.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects
Seventeen healthy volunteers (14 males and three females, aged 24–31 yrs), with no history of psychiatric and/or neurological illness, were recruited for the study. They were all consistent right-handers as measured by the Edinburgh Handedness Inventory (Oldfield, 1971). Each subject was interviewed to determine the CSP, which was further confirmed by the deviation in the chewing pattern recorded with the use of a mandibular kinesiograph (K6-I Diagnostic System, Myo-tronics, Inc., Seattle, WA, USA). Of the 17 subjects, six reported that they predominantly used the left dentition, indicating a left CSP. The CSP that was subjectively reported by each subject was consistent with that objectively determined with the mandibular kinesiograph (Fig. 1AGo). Of the 17 subjects, six showed a strong (> 90% of total chewing strokes) left CSP, whereas two showed a weak left CSP, three showed a weak right CSP, and four showed a strong right CSP. The other two showed no CSP. The six subjects (three males and three females, aged 25–29 yrs) with a strong left CSP volunteered to participate in this study. All of the experimental procedures complied with the Code of Ethics of the World Medical Association (Declaration of Helsinki) and the standards established by the Institutional Ethical Review Board. Written informed consent was obtained from all of the subjects before the study, after the nature of the experimental procedures had been fully explained.



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  		Figure 1. (A) A representative coronal projection of mandibular movement in a subject, which was recorded with the use of a mandibular kinesiograph. The trajectory of the open-close movement in this subject shows a slight deviation to the right at the maximum gape (Aa). When the subject chewed gum without any instruction, the jaw trajectory shows a marked deviation to the left, indicating a strong left chewing-side preference (Ab). When the subject was instructed to chew the gum bilaterally, the laterality of the jaw trajectory disappeared (Ac). Green lines and downward arrows indicate jaw-opening trajectories, while red lines and upward arrows indicate jaw-closing trajectories. Several cycles are superimposed. L indicates the left side. Bars denote 5 mm. (B) Block design of the tongue movement paradigm.

 
Conditions and Training Session
During tongue protrusion (TP), the subjects were instructed to push the tongue tip lightly against the palatal surface of the maxillary incisors. During tongue movement to the right (TR) and left (TL), they were instructed to push the ipsilateral tongue edge lightly against the lingual surfaces of mandibular premolars with a similar degree of tongue pressure. The subjects underwent a vigorous training session for TMs so as not to produce major displacement and/or rotation of the tongue body, but rather to produce only minimal displacement of the tip or lateral edge of the tongue (Shinagawa et al., 2003). These TMs do not resemble natural TMs during feeding (Hiiemae and Palmer, 2003). The subjects executed TMs with negligible artifacts arising from the orofacial movement, which may affect acquired MR images.

Brain Scanning
After TM training, each subject performed two runs before and after gum-chewing in a 1.5-T apparatus (Magnetom Vision, Siemens AG, Erlangen, Germany) to obtain 40 transverse T2*-weighted slices with parameters identical to those in our previous study (Shinagawa et al., 2003). First, the subject performed a run that consisted of 290 scans before gum-chewing. The subject was then instructed to chew a gum base (Recaldent, Warner-Lambert Inc., Tokyo, Japan) voluntarily, not only on the preferred chewing side but also on the contralateral dentition, for 5 min. Immediately after chewing, the subject performed a second run that consisted of the same number of scans. The subject performed 36 blocks for each run (i.e., 10 scans for the first block and 8 scans for the remaining blocks). We discarded data from the first two scans of all blocks to eliminate transients that arose before dynamic equilibrium was achieved. The runs were measured with the use of a gradient echo-type echo planar imaging sequence with a head coil.

The subject performed each of three randomized TM tasks six times, and each was followed by a ‘rest’ period as a control (Fig. 1BGo). fMRI data obtained from each subject after gum-chewing were divided into two phases—the first 10 min, beginning immediately after gum-chewing, and the second 10 min. Each phase consisted of 144 scans.

Data Analysis
We used SPM99 software to analyze individual fMRI data. Statistically significant locations were expressed as coordinates and superimposed on a standard brain atlas (Talairach and Tournoux, 1988). Since head and body movements must be eliminated during MR imaging, because they cause problematic artifacts (Birn et al., 1999; Seto et al., 2001), artifacts were carefully eliminated as in our previous study (Shinagawa et al., 2003)—i.e., by full visual-feedback training for TMs to minimize electromyographic signals from masticatory muscles, fixation of the head and body with straps, immobilization of the mandible with reference to the maxilla by means of a splint, re-alignment by SPM99 to eliminate motion-related artifacts, and discarding of the first two scans for analysis. Therefore, it is reasonable to assume that the BOLD-fMRI signals obtained in this study were derived from neuronal activity associated with TMs. All sessions were included, because movement artifacts showed translations < ± 1.5 mm and rotations < ± 0.5 degrees in x-, y-, and z-coordinates. Statistical comparisons were performed for the group and for each subject and were used to identify regions with significantly increased activation during TMs relative to "rest" in three conditions before and after gum-chewing. The following subtractions were performed: (1) TM-"rest" before gum-chewing, (2) TM-"rest" in the first 10 min after gum-chewing, and (3) TM-"rest" in the second 10 min after gum-chewing.

The difference in the numbers of chewing strokes on the right and left sides of the dentition during bilateral gum-chewing was evaluated by the paired t test. We used an unpaired t test to compare the mean BOLD signal changes on the left and right S1/M1 for all TMs before and after gum-chewing. The main and interaction effects of gum-chewing and TMs on the mean BOLD signal changes in the S1/M1 of each hemisphere were tested by the F test and repeated two-way ANOVA followed by Fisher’s test. Statistical significance was established at p < 0.01. All procedures were carried out with the use of commercially available statistical software (StatView 5.0, Hulinks, Tokyo, Japan).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The number of strokes per minute during bilateral gum-chewing in the six subjects was 43.2 ± 6.4 (mean ± SD) on the right side and 43.6 ± 8.5 on the left side. There was no significant difference in the number of strokes during gum-chewing between the right and left sides.

Before gum-chewing, the S1/M1 was bilaterally activated during TM (Fig. 2Go). The area of activation in the S1/M1 during TM increased appreciably in size during the first 10 min after gum-chewing, and then decreased during the second 10 min. Several foci in the S1/M1 with similar three-dimensional coordinates were activated during TM before gum-chewing, and in the first and second 10-minute periods after gum-chewing (TableGo).



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  		Figure 2. Projections of the activation foci on the lateral aspect of the standard human brain during tongue protrusion and rightward and leftward tongue movements (n = 6). Activations of bilateral sensorimotor cortices that were statistically significant (p < 0.05 corrected for multiple comparisons) are shown. Color code denotes T-values. Abbreviations for Figs. 2Go and 3Go: TP, tongue protrusion; TR, rightward tongue movement; TL, leftward tongue movement; Before, before gum-chewing; After1st, the first 10-minute period beginning immediately after gum-chewing; After2nd, the second 10-minute period from 10 min to 20 min after gum-chewing.

 

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  		Table. x-, y-, and z-coordinates and T-values of Activation Focia in the S1/M1 during Various Tongue Movements (TP, TR, and TL) - "Rest" as Revealed by the Group Analysis
 
Before gum-chewing, the BOLD signal in the S1/M1 in the right hemisphere was significantly greater than that in the left. In the left hemisphere, the mean change in the BOLD signal in the S1/M1 significantly increased in the first 10 min after gum-chewing compared with those before chewing during TP, TR, and TL (Fig. 3Go). In the second 10 min after gum-chewing, the mean change in the BOLD signal in the S1/M1 significantly decreased compared with those in the first 10 min during TP and TL, while there was no significant change during TR. In contrast, in the right hemisphere, there were no significant increases in the mean change in the BOLD signal in the S1/M1 during any TM in the first 10 min. In the second 10 min, there was no significant change during TP or TR, whereas there was a significant decrease during TL. With regard to the main and interaction effects of gum-chewing and TMs on the mean BOLD signal changes in the S1/M1 of each hemisphere, only gum-chewing (p < 0.0001), not TMs (p = 0.14 for the left hemisphere and p = 0.67 for the right), had an effect on the mean BOLD signal changes in the S1/M1 of both hemispheres. In contrast, there were no significant interaction effects of gum-chewing and TMs (p = 0.38 for the left hemisphere and p = 0.19 for the right) on the mean BOLD signal changes in the S1/M1 of both hemispheres.



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  		Figure 3. Comparisons of the mean change in the BOLD signal in both the right and left primary sensorimotor cortices during tongue protrusion (TP) and rightward (TR) and leftward (TL) tongue movements (n = 6). Solid bars indicate standard errors of the mean. F values along with P values by repeated two-way ANOVA, as well as means and standard errors of the mean, are indicated. **p < 0.01.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The main finding of this study is that bilateral gum-chewing enhances activation of the S1/M1 ipsilateral to the CSP during TMs. We examined the change in the BOLD-signal intensity in the S1/M1 during "rest" blocks after gum-chewing, and found that there were no significant differences during "rest" between the first and second 10-minute periods after gum-chewing. Therefore, an increase in the activated S1/M1 area in the first 10 min, compared with both before gum-chewing and the second 10 min after gum-chewing, could not be attributed to an increase in baseline activity in the S1/M1. Rather, a net increase in neuronal activities in the S1/M1 during TM tasks might play a role. Although it is not clear why the area of activation in the S1/M1 increases after gum-chewing, bilateral gum-chewing may reinforce the sub-threshold neuronal activity related to mastication. Thus, once the tongue moves, the S1/M1 area, which controls masticatory muscles and receives sensory feedback from the orofacial region (Narita et al., 2002), shows excitation to co-ordinate the tongue and jaws.

Plasticity of the hand S1/M1 area has been reported in humans (Classen et al., 1998; Liepert et al., 1999). In these previous studies, rapid and short-term re-organization of the S1/M1 was induced by simple (Classen et al., 1998) or synchronized (Liepert et al., 1999) repetitive thumb movements. Jaw movement to chew gum bilaterally requires highly coordinated contraction and relaxation of many orofacial muscles. In addition, updated afferent information is always necessary if bilateral gum-chewing is to be performed smoothly. The increase in the TM-related activation of the S1/M1 after 5 min of chewing may be comparable with that reported for thumb movement (Classen et al., 1998; Liepert et al., 1999).

In this study, all six subjects were consistent right-handers and exhibited a strong left CSP. The TM-related activation of the S1/M1 before gum-chewing was greater on the right than the left, which is consistent with our previous study in subjects with a left CSP (Shinagawa et al., 2003). After gum-chewing, TM-related activation of the bilateral S1/M1 was equalized; a significant increase in the mean change in the BOLD signal was seen on the left, but not on the right (i.e., hemispheric effect). Although the neural mechanism for this is not clear, this finding is interesting in the context that chewing-related transient plasticity may be affected by long-term plastic change due to the left CSP. This assumption may be supported by the fact that there was no interaction effect between gum-chewing and the TM pattern; there was only a main effect of gum-chewing. The mean change in the BOLD signal in the bilateral S1/M1 significantly decreased in the second 10 min compared with that in the first 10 min after gum-chewing during TL. During this period, there was no hemispheric effect. Furthermore, it seemed that there were no effects of the TM pattern on the mean change in the BOLD signal in the S1/M1.

Strengthening of the existing neuronal circuit through changes in synaptic efficacy (Donoghue, 1995) may account for the increase in the activated area, since the three-dimensional co-ordinates of the maximum activated foci during TMs remained relatively constant without systematic displacement (Liepert et al., 1999) before and after gum-chewing, and the development of new neuro-anatomic connections to surrounding areas is less likely to occur (Liepert et al., 1999).

The present study has several limitations. Seventeen volunteers were initially recruited, and brain scanning was carried out in only six subjects. These subjects showed significant deviation (i.e., more than 90% of total strokes performed) in chewing stroke to the left while they were freely chewing gum. In contrast, only four subjects showed significant deviation in chewing stroke to the right, and seven showed no side preference. Therefore, subjects with a left CSP were studied. So that variability among subjects would be minimized, fMRI data were spatially normalized with state-of-the-art SPM99 software. Although the number of subjects is similar to those in other studies on functional brain imaging, and significant (p < 0.05) results were obtained in the S1/M1 of the left hemisphere, further studies should be performed to determine whether comparable results can be obtained in the S1/M1 of the right hemisphere in subjects with a right CSP.

The present findings suggest that bilateral gum-chewing modulates activation in the S1/M1 during TMs. Further, this activation occurs differentially in each hemisphere, depending on the CSP. This plasticity supports the existence of short-term memory for a recently practiced movement, and may be beneficial for rehabilitation of the injured brain (Bütefisch et al., 1995; Cioni et al., 2001) or for stimulating the aging brain (Adams, 1987).


   ACKNOWLEDGMENTS
 
The authors are grateful to Dr. Yasuo Ishiwata for a critical review of the manuscript. This study was supported by Grants-in-Aid 10307052 and 09470467 from the Japanese Ministry of Education, Culture, Sports, Science and Technology.

Received July 28, 2003; Last revision July 4, 2004; Accepted July 27, 2004


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