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

Abstract

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.

Get full access to this article

View all access options for this article.

References

Adams I -1987-. Comparison of synaptic changes in the precentral and postcentral cerebral cortex of aging humans: a quantitative ultrastructural study. Neurobiol Aging 8:203–212.

Birn RM, Bandettini PA, Cox RW, Shaker R -1999-. Event-related fMRI of tasks involving brief motion. Hum Brain Mapp 7:106–114.

Bütefisch C, Hummelsheim H, Denzler P, Mauritz KH -1995-. Repetitive training of isolated movements improves the outcome of motor rehabilitation of the centrally paretic hand. J Neurol Sci 130:59–68.

Cioni G, Montanaro D, Tosetti M, Canapicchi R, Ghelarducci B -2001-. Reorganisation of the sensorimotor cortex after early focal brain lesion: a functional MRI study in monozygotic twins. Neuroreport 12:1335–1340.

Classen J, Liepert J, Wise SP, Hallett M, Cohen LG -1998-. Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79:1117–1123.

Donoghue JP -1995-. Plasticity of adult sensorimotor representations. Curr Opin Neurobiol 5:749–754.

Funakoshi M, Kawamura S, Fujiwara H, Katsukawa H -1989-. Effects of mastication on post-natal development of brain. In: Mechanobiological Research on the Masticatory System. Kubota K, editor. Berlin: VEB Verlag für Medizin und Biologie, pp. 162–167.

Hector MP, Linden RW -1987-. The possible role of periodontal mechanoreceptors in the control of parotid secretion in man. Q J Exp Physiol 72:285–301.

Hiiemae KM, Palmer JB -2003-. Tongue movements in feeding and speech. Crit Rev Oral Biol Med 146:413–429.

10.

Kubota K, Shimizu T, Nagae K, Shibanai S, Iseki H, Odagiri N, et al. -1988-. Degenerative changes of primary neurons following tooth extraction. Ann Anat 166:133–139.

11.

Liepert J, Terborg C, Weiller C -1999-. Motor plasticity induced by synchronized thumb and foot movements. Exp Brain Res 125:435–439.

12.

Lowe AA, Gurza S, Sessle BJ -1977-. Regulation of genioglossus and masseter muscle activity in man. Arch Oral Biol 22:579–584.

13.

Mioche L, Hiiemae KM, Palmer JB -2002-. A postero-anterior videofluorographic study of the intra-oral management of food in man. Arch Oral Biol 47:267–280.

14.

Momose T, Nishikawa J, Watanabe T, Sasaki Y, Senda M, Kubota K, et al. -1997-. Effect of mastication on regional cerebral blood flow in humans examined by positron-emission tomography with ¹⁵O-labelled water and magnetic resonance imaging. Arch Oral Biol 42:57–61.

15.

Narita N, Yamamura K, Yao D, Martin RE, Masuda Y, Sessle BJ -2002-. Effects on mastication of reversible bilateral inactivation of the lateral pericentral cortex in the monkey -Macaca fascicularis-. Arch Oral Biol 47:673–688.

16.

Oldfield RC -1971-. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1:97–113.

17.

Onozuka M, Fujita M, Watanabe K, Hirano Y, Niwa M, Nishiyama K, et al. -2002-. Mapping brain region activity during chewing: a functional magnetic resonance imaging study. J Dent Res 81:743–746.

18.

Onozuka M, Fujita M, Watanabe K, Hirano Y, Niwa M, Nishiyama K, et al. -2003-. Age-related changes in brain regional activity during chewing: a functional magnetic resonance imaging study. J Dent Res 82:657–660.

19.

Palmer JB, Hiiemae KM, Liu J -1997-. Tongue-jaw linkages in human feeding: a preliminary videofluorographic study. Arch Oral Biol 42:429–441.

20.

Pond LH, Barghi N, Barnwell GM -1986-. Occlusion and chewing side preference. J Prosthet Dent 55:498–500.

21.

Schieppati M, Di Francesco G, Nardone A -1989-. Patterns of activity of perioral facial muscles during mastication in man. Exp Brain Res 77:103–112.

22.

Senda M, Ishiyama N, Ishii K, Toyama H, Oda K, Momose T, et al. -1992-. Changes in regional cerebral blood flow during mastication in young and old normal subjects measured with positron emission tomography [abstract in English]. J Masticat Health Soc 2:49–54.

23.

Sesay M, Tanaka A, Ueno Y, Lecaroz P, De Beaufort DG -2000-. Assessment of regional cerebral blood flow by xenon-enhanced computed tomography during mastication in humans. Keio J Med 49-Suppl 1-:A125–A128.

24.

Seto E, Sela G, McIlroy WE, Black SE, Staines WR, Bronskill MJ, et al. -2001-. Quantifying head motion associated with motor tasks used in fMRI. NeuroImage 14:284–297.

25.

Shinagawa H, Ono T, Ishiwata Y, Honda E, Sasaki T, Taira M, et al. -2003-. Hemispheric dominance of tongue control depends on the chewing-side preference. J Dent Res 82:278–283.

26.

Takada K, Yashiro K, Sorihashi Y, Morimoto T, Sakuda M -1996-. Tongue, jaw, and lip muscle activity and jaw movement during experimental chewing efforts in man. J Dent Res 75:1598–1606.

27.

Talairach J, Tournoux P -1988-. Co-planar stereotaxic atlas of the human brain. New York: Thieme.

28.

Tamura T, Kanayama T, Yoshida S, Kawasaki T -2003-. Functional magnetic resonance imaging of human jaw movements. J Oral Rehabil 30:614–622.

29.

Zarzecki P, Shinoda Y, Asanuma H -1978-. Projection from area 3a to the motor cortex by neurons activated from group I muscle afferents. Exp Brain Res 33:269–282.