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Hemispheric Dominance of Tongue Control Depends on the Chewing-side Preference

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; and
⁵ Department of Oral and Maxillofacial Radiology, the University of Tokushima, Tokushima 770-8503, Japan;

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

	ABSTRACT

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Blood-oxygenation-level-dependent (BOLD)-functional magnetic resonance imaging (fMRI) is known to be a non-invasive technique for studying human brain function. The purpose of this study was to apply BOLD-fMRI to identify brain areas responsible for producing tongue movements and their relation to chewing-side preference in 15 normal right-handed volunteers. A marked increase in BOLD signals was detected in primary sensorimotor cortices upon protrusion and in rightward and leftward tongue movements compared with at rest. In 10 subjects with an evident chewing-side preference, the BOLD signal change in the primary sensorimotor cortex was significantly greater on the side contralateral to the preferred chewing side. The results suggest that there is a relationship between hemispheric dominance and chewing-side preference in primary sensorimotor cortices responsible for tongue movements.

KEY WORDS: tongue movement • sensorimotor cortex • chewing-side preference • fMRI • human

	INTRODUCTION

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The human tongue is an essential component of several precisely coordinated movements such as mastication, deglutition, and articulation. Penfield and Boldrey (1937) used electrical stimulation to examine the somatotopic representation of the tongue in the cerebral cortex of epileptic patients and demonstrated that the tongue was bilaterally represented in the inferior region of the motor cortex. This area mediates the voluntary control of tongue movement via corticobulbar fibers, which finally impinge on the hypoglossal nucleus (Kuypers, 1958). Later, electrical stimulation of the cortical motor area in the rat was shown to evoke tongue movements associated with licking, chewing, and swallowing (Kaku, 1984). Neurons in the primary motor cortex (M1) fired in relation to tongue movements in monkeys (Murray and Sessle, 1992). However, only limited information is available on the cortical area that is activated during various kinds of voluntary tongue movement in humans. Recently, brain activation during tongue protrusion was found to be bilateral in the sensorimotor cortex (S1/M1), cerebellum, supplementary motor area, operculum, insula, putamen, and thalamus (Corfield et al., 1999). However, it is unclear whether lateral excursion of the tongue is associated with unilateral focal activation of the brain. Therefore, the current body of knowledge regarding the cortical control of tongue movement does not permit a definite description of the hemispheric lateralization during voluntary tongue movements.

It has been reported that unilateral chewing occurs in 70% of consecutive masticatory cycles (Wictorin et al., 1971). A chewing-side preference, which is a preference for one side of the dentition where mastication is performed consistently and predominantly, is hypothesized to be an expression of motivational and/or sensorimotor behavior in humans (Helkimo et al., 1978; Christensen and Radue, 1985; Pond et al., 1986). Recently, Mioche and colleagues (2002) performed a videofluorographic study of the intra-oral management of food in humans. They found that 66% of chewing occurred on one side only, and the food sample was replaced on either occlusal table by a combination of alternate tongue- and cheek-pushing movements during the unilateral chewing cycle (Mioche et al., 2002). However, little is known about whether the chewing-side preference is associated with tongue movement.

The aims of this study were: (1) to identify cortical areas responsible for producing various tongue movements, including lateral excursion of the tongue, by using functional magnetic resonance imaging (fMRI); and (2) to determine their relationship to the individual chewing-side preference in humans.

	MATERIALS & METHODS

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Fifteen normal volunteers (12 males, aged 24-30 yrs) participated in this study. They were all consistent right-handers (mean laterality quotient, +92; range, +70 - +100) according to the Edinburgh Handedness Inventory (Oldfield, 1971). 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 subjects before the study but after the nature of the experimental procedures had been fully explained.

Tongue movements were designed to produce minimal or no displacement of the tongue or jaw to minimize artifacts due to movement of the orofacial area on acquired MR images. All of the subjects were trained to perform tongue movements with visual feedback consisting of electromyographic (EMG) activities of orofacial muscles before fMRI data acquisition (Fig. 1). For this training session, a soft custom-made polycarbonate occlusal splint was fabricated for each subject to keep the mandible in the resting position during MR imaging. A pair of small pressure sensors was embedded bilaterally in the palatal aspect of the occlusal splint near the maxillary first molars. Surface electrodes were placed on the bilateral anterior and posterior temporalis, masseter, and digastric muscles for EMG recording. EMG recordings were performed during tongue movement to the right (T_R) and left (T_L), and during clenching and swallowing. Lateral movement of the tongue consisted of a self-paced (ca. 1 Hz) light pushing of the tongue against the lateral portion of the occlusal splint. Visual feedback of tongue pressure on the bilateral pressure sensors was used to reproduce the movement. For the control condition, the tongue was relaxed in the resting position. After this training, tongue movements could be performed with little co-activation of the jaw muscles (Fig. 1).

View larger version (17K): [in this window] [in a new window]   Figure 1. Representative simultaneous recordings of electromyographic activities of orofacial muscles and tongue pressure during visual feedback training of tongue movements. Electromyographic activities were recorded from bilateral anterior and posterior temporalis, masseter, and digastric muscles, and tongue pressure was recorded bilaterally by a pressure transducer. The subject performed tongue movement (i.e., lateral excursion of the tongue tip to touch the ipsilateral pressure transducer) between the two arrows. Note that while bilateral activation of several orofacial muscles was seen with tongue moments during clenching and swallowing, lateral tongue movements could be performed (between arrows) with a minimum activation of orofacial muscles and without touching the contralateral pressure transducer. The horizontal bar denotes 1.0 sec. Vertical bars denote 50 mV for TR and TL, 200 mV for clenching and swallowing in EMG records, and 20 g/cm2 for tongue pressure. Abbreviations: TR, tongue movement to the right; TL, tongue movement to the left.

All of the subjects performed the following 4 tasks in the block design (Fig. 2A): tongue protrusion (T_P), T_R, T_L, and "rest" as a control. During T_P, the subject pushed the tongue against the palatal surface of the maxillary incisors. During T_R and T_L, the subject performed lateral movement of the tongue to either side, mimicking the tongue movement that had been trained beforehand. One of the tongue-movement blocks occurred randomly between two "rest" blocks. The subject performed each tongue-movement block 6 times, and the "rest" block 18 times (i.e., 10 scans for the first "rest" block and 8 scans for the remaining blocks). Indications for the individual tongue movements (T_P, T_R, and T_L) and "rest" were displayed at the center of the visual field projected from the operation room immediately before each task. A time-series of 290 scans was obtained from each subject. Data from the first 2 scans within the first "rest" task were discarded to eliminate transients arising before dynamic equilibrium was achieved.

View larger version (78K): [in this window] [in a new window]   Figure 2. Task design and brain activities. (A) Experimental design of the tongue-movement paradigm indicating the alternation of "rest" and tongue-movement tasks. See text for details. (B) Projections of the activation foci on the lateral surface of a standard human brain atlas during tongue movements (i.e., TP, TR, and TL) revealed by a random-effect analysis. a, TP-"rest"; b, TR-"rest"; c, TL-"rest". Significant activations (p < 0.001 uncorrected for multiple comparisons) of bilateral S1/M1 cortices are shown. Note that there were no marked differences in activation foci for the 3 different tongue movements in terms of size or location. (C) Representative activation patterns in the S1/M1 of subjects with evident chewing-side preferences on the given sectional planes (z = 30). a, subject with a chewing-side preference exclusively on the left. b, subject with a chewing-side preference exclusively on the right. Activations of bilateral S1/M1 cortices that were significant (p < 0.05 corrected) are shown. Color code denotes T-values. Abbreviations: Tp, tongue protrusion; TR, tongue movement to the right; TL, tongue movement to the left; R, right side.

In this study, statistical comparisons were made, first for the group and for each subject, which identified regions that had significantly increased activations during tongue movements relative to the "rest" condition. We used subtraction in the following comparisons: (1) T_P+R+L (i.e., the sum of T_P, T_R, and T_L)-"rest"; (2) T_P-"rest"; (3) T_R-"rest"; and (4) T_L-"rest". Second-level random-effects analyses (Holmes and Friston, 1998) were used (uncorrected p < 0.001). The statistically significant locations were expressed as coordinates and superimposed on a standard brain atlas (Talairach and Tournoux, 1988).

After fMRI data acquisition, all 15 subjects were interviewed with regard to chewing-side preference, and subgrouped accordingly (n = 3 for "always right", n = 2 for "usually right", n = 5 for "either side", n = 3 for "usually left", and n = 2 for "always left"). Subjects who reported the chewing-side preference as "always right" or "usually right" were pooled as the right chewing-side preference group (n = 5). Likewise, subjects who reported the chewing-side preference as "always left" or "usually left" were pooled as the left chewing-side preference group (n = 5). All of the subjects were then divided into two groups with (n = 10) and without (n = 5) an evident chewing-side preference. The mean percentage change in blood-oxygen-level-dependent (BOLD) signal for a voxel containing the coordinate that showed maximum activation in the S1/M1 of both hemispheres was calculated by extraction of the time-series voxels. We performed the above calculations for each subject by taking the difference in the mean percentage change in BOLD signal between the average of 6 scans, excluding the first 2 scans, from each TM block. We used the Mann-Whitney U-test to compare mean BOLD signal changes in S1/M1 of each hemisphere for the group with an evident chewing-side preference. Statistical significance was established at p < 0.05. All procedures were carried out with the use of commercially available statistical software (StatView 5.0, Hulinks, Tokyo, Japan).

	RESULTS

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The regions activated during T_P+R+L were detected bilaterally in the S1/M1, cerebellum, supplementary motor area, operculum, insula, putamen, and thalamus. Further, to investigate the activation pattern in individual cortices, we segregated the tongue movements into T_P, T_R, and T_L. Notable focal activations were seen in the bilateral S1/M1 during the three tasks (Fig. 2B). Activation foci in the bilateral S1/M1 showed no remarkable differences with regard to three-dimensional coordinates across the three tongue movements (Table). Fig. 2C shows representative activation patterns in the S1/M1 during tongue movements in two subjects with an evident chewing-side preference. In the subject who reported his chewing-side preference as being "always left", the right S1/M1 was more strongly activated than the left S1/M1 during T_P, T_R, and T_L (Fig. 2Ca). In contrast, the left S1/M1 was more strongly activated than the right S1/M1 during the three tongue-movement tasks in the subject who reported his chewing-side preference as being "always right" (Fig. 2Cb).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS & METHODS RESULTS DISCUSSION REFERENCES

 
The two main findings in this study are, first, areas of the bilateral S1/M1 were significantly activated regardless of the kind of tongue movement, and, second, in subjects with an evident chewing-side preference, the signal intensity in the S1/M1 was significantly greater in the side contralateral to the chewing-side preference.

In studying juvenile chewing patterns, Ahlgren (1967) reported that each individual had a characteristic chewing pattern. Occlusal factors such as the area of occlusal contact may have an effect when the physiologic chewing pattern is being developed in children (Gisel, 1988). Occlusal factors are not the chief determinants of the chewing-side preference (Pond et al., 1986). Although several objective and subjective methods for determining the chewing-side preference have been proposed, their reliability varies. Since a questionnaire is used in one of the methods (Ogimoto et al., 1998; Hiyama et al., 1999), a subjective interview was used to determine the chewing-side preference in this study.

Brief orofacial movements that induce artifacts may be problematic in fMRI (Birn et al., 1999). Moreover, such movement could produce an activation-related signal if the movement was correlated with the activation condition (Hajnal et al., 1994). We were careful to eliminate such effects from our data—i.e., full visual-feedback training for tongue movements to minimize EMG signals from jaw muscles (Fig. 1), 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 the first 2 scans for analysis. Therefore, it is likely that the BOLD-fMRI signals obtained in this study were due to neuronal activity associated with tongue movements. All sessions were included, because movement artifacts showed translation < ± 1.5 mm and rotation < ± 0.5 degrees in x-, y-, and z-coordinates.

We segregated T_P+R+L into 3 individual tasks and performed a random-effect analysis to investigate whether there were differences in the location and size of activated cortical regions in relation to the tasks. The S1/M1 area in the left hemisphere that was activated during various tongue movements in our study appeared to be larger than that in the right hemisphere. This asymmetrical tongue representation may be explained by dominance in language, for which the tongue is specialized (Picard and Olivier, 1983); however, further studies are needed to clarify this issue.

Primary afferents from trigeminal receptors in intra-oral structures, including the tongue surface, gingiva, and periodontal ligaments, project to the ipsilateral principal sensory nucleus and the spinal tract nucleus of the trigeminal nerve. Afferents from these nuclei secondarily project to the S1 via the ventral posteromedial nucleus of the thalamus. Thus, the trigeminal afferents from intra-oral receptors project to the sensory cortex with contralateral dominance. However, the existence of hemispheric dominance in human tongue function is still controversial, while contralateral dominance in cerebral hemispheric organization has been established (Kim et al., 1993). In the random-effect analysis, the S1/M1 areas of both hemispheres were activated during the three kinds of tongue-movement, and there were no remarkable differences in the x-, y-, and z-coordinates of activation foci. This suggests that sensory inputs from intra-oral structures of different locations during T_P, T_R, and T_L may activate distinctive areas in the bilateral S1. Therefore, we analyzed T_P+R+L as well as the individual tasks to cancel the differential effects of trigeminal sensory inputs elicited by different tasks, even though there appeared to be no significant differences in sensory inputs from the tongue to the bilateral S1 (Pardo et al., 1997).

With regard to the lateralization of sensory cortical representation of the human tongue, Picard and Olivier (1983) demonstrated that sensory responses could be peripherally recorded by stimulation of both anterior and posterior regions of the central sulcus. In contrast, an fMRI study revealed that electrical stimulation of the tongue tip off the midline activated the contralateral S1 (Sakai et al., 1995). Pardo and colleagues (1997) showed that there were no significant hemispheric differences in cortical projection to the S1 from the bilateral tongue surface. In addition, they used a cluster analysis, which we also used in our study, to determine the mean signal intensity, since they found that it was impossible to segregate the S1 and M1 completely (Pardo et al., 1997). Therefore, we did not differentiate between the S1 and the M1 when we interpreted the data, as in a previous study on motor control of the tongue (Corfield et al., 1999). Voluntary movement requires the coordinated activity of several components of the motor system, including the M1, basal ganglia, cerebellum, and spinal cord (Middleton and Strick, 2000). Murray and co-workers (1991) showed that reversible inactivation by cooling the primate face and tongue areas of the M1 significantly reduced the successful execution of a trained task for the tongue, which involved the tongue muscles via the bilateral hypoglossal nucleus (Chen et al., 1999).

When we dichotomized the subjects based on the presence of a chewing-side preference and performed a group analysis for the 10 subjects with an evident chewing-side preference regardless of the side, we found significant contralateral dominance for T_P+R+L. This is the first study to demonstrate clearly that the S1/M1 contralateral to chewing-side preference is dominant in tongue motor function. This positive relationship between chewing-side preference and tongue movement may indicate that the masticatory system concurrently maximizes jaw and tongue function.

View larger version (25K): [in this window] [in a new window]   Figure 3, Comparisons of BOLD signals. (A) a, Comparisons of the mean BOLD signal change between the right and left S1/M1 during TP, TR, and TL (a) as well as TP+R+L (b) in all 15 subjects. (B) Comparisons of the mean BOLD signal change in the S1/M1 between the hemispheres contralateral and ipsilateral to the preferred chewing side during TP+R+L in the five subjects with an evident left chewing-side preference. (C) Comparisons of the mean BOLD signal change in the S1/M1 between the hemispheres contralateral and ipsilateral to the preferred chewing side during TP+R+L in the five subjects with an evident right chewing-side preference. (D) Comparisons of the mean BOLD signal change in the S1/M1 between the hemispheres contralateral and ipsilateral to the preferred chewing side during TP+R+L in the subjects with an evident chewing-side preference. Solid bars indicate standard deviations. Abbreviations: CSP, chewing-side preference; right, right hemisphere; left, left hemisphere: contra, the hemisphere contralateral to the preferred chewing side; ipsi, the hemisphere ipsilateral to the preferred chewing side. *p < 0.05, ***p < 0.001.

	ACKNOWLEDGMENTS

Received January 2, 2002; Last revision November 22, 2002; Accepted December 3, 2002

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