| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
RESEARCH REPORT |
1 Departments of Anatomy and Basic Neuroscience and
2 Physiology, Gifu University School of Medicine, 40 Tsukasa-machi, Gifu 500-8705, Japan;
3 Department of Veterinary Physiology, Faculty of Agriculture, Gifu University, Gifu 501-1193, Japan;
4 Department of Radiology, Yoro Central Hospital, Yoro 503-0013, Japan;
5 Department of Biochemistry, Kanagawa Dental College, Yokosuka 238-8580, Japan; and
6 Oral Health Association of Japan, Tokyo 170-0003, Japan;
* corresponding author, onozuka{at}cc.gifu-u.ac.jp
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
KEY WORDS: functional magnetic resonance imaging • gum chewing • masticatory system • brain activation • human
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
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.
|
MATERIALS & METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Task Paradigm
The task paradigm was the rhythmic chewing, at a rate of approximately 1 Hz, of two kinds of gum, moderately hard (X type, 5.6 x 104 poise) and hard (G type, 2.3 x 105 poise) (see Suzuki et al., 1994). These gums, essentially chewing gum without the odor and taste components, were specially prepared in the General Laboratory of Lotte Co. Ltd. (Saitama, Japan). Each subject performed 4 cycles of 32 sec of rhythmic chewing and 32 sec without chewing (see inset in Fig. 1A
).
|
Data Analysis
For data analysis, the first 8 volumes were discarded because of instability of magnetization. Head motion was monitored with the use of an analysis software package (MEDx, Sensor Systems, Inc., Sterling, VA, USA), and studies were rejected if a shift of greater than 0.75 mm (20% of voxel size) over the scanning time period was detected in any direction, since excess movement reduces both the spatial resolution and spatial fidelity. If head motion was < 0.75 mm, we applied a motion correction program, AIR 3.0, to the obtained images (Woods et al., 1992). Independently, head motion was also corrected by the application of SPM99 software (Wellcome Department of Cognitive Neurology, London, UK). Furthermore, motion artifacts, which may be due to chewing, were removed by a low-pass filter of 1.5 sec with MEDx software. Finally, we confirmed that motion artifacts were less than 0.01 mm (0.267% of a voxel) in any direction.
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.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
). 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.
|
, 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).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
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.
|
ACKNOWLEDGMENTS |
|---|
Received June 13, 2002; Last revision August 26, 2002; Accepted September 6, 2002
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Friston KL, Holmes AP, Worsley KP, Poline JP, Frith CD, Frackwiak RSJ (1995). Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210.
Kubota K, Nagae K, Shibanai S, Hosaka K, Iseki H, Odagiri N, et al. (1988). Degenerative changes of primary neurons following tooth extraction. Anat Anz 166:133–139.[Medline]
Lund JP, Olsson KA (1983). The importance of reflexes and their control during jaw movement. TINS 6:458–463.
Lund JP, Sasamoto K, Murakami T, Olsson KA (1984). Analysis of rhythmical jaw movements produced by electrical stimulation of motor-sensory cortex of rabbits. J Neurophysiol 52:1014–1029.
Lutz K, Specht K, Shah NJ, Jäncke L (2000). Tapping movements according to regular and irregular visual timing signals investigated with fMRI. Neuroreport 11:1301–1306.[Medline]
Meisenzahl EM, Schlosser R (2001). Functional magnetic resonance imaging research in psychiatry. Neuroimaging Clin N Am 11:365–374.[Medline]
Momose I, 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.[Medline]
Nakamura Y, Katakura N (1995). Generation of masticatory rhythm in the brainstem. Neurosci Res 23:1–19.[Medline]
Nakata M (1998). Masticatory function and its effects on general health. Int Dent J 48:540–548.[Medline]
Passingham RE (1993). The frontal lobes and voluntary action. Oxford: Oxford University Press.
Penfield W, Boldrey E (1938). Somatic motor and sensory representation in the cerebral cortex as studied by electrical stimulation. Brain 15:389–443.
Proschel PA, Raum J (2001). Preconditions for estimation of masticatory forces from dynamic EMG and isometric bite force-activity relations of elevator muscles. Int J Prosthodont 14:563–569.[Medline]
Pulvermuller F (1999). Words in the brain’s language. Behav Brain Sci 22:253–336.[Medline]
Rossignol S, Dubuc R (1994). Spinal pattern generation. Curr Opin Neurobiol 4:894–902.[Medline]
Sasaki A (2001). Influence of mastication on the amount of hemoglobin in human brain tissue. Kokubyo Gakkai Zasshi 68:72–81.[Medline]
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):A125–128.
Suzuki M, Shibata M, Sato Y (1992). Energy metabolism and endocrine responses to gum-chewing. J Mastica Health Sci 2:55–62.
Suzuki M, Ishiyama I, Takiguchi T, Ishikawa H, Suzuki Y, Sato Y (1994). Effects of gum hardness on the response of common carotid blood flow volume, oxygen uptake, heart rate and blood pressure to gum-chewing. J Mastica Health Sci 4:9–20.
Talairach J, Tournoux P (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme.
Watanabe I, Ishiyama N, Senda M (1992). Cerebral blood flow during mastication measures with positron emission tomography. Geriatric Dent 6:148–150.
Woods RP, Cherry SR, Mazziotta JC (1992). Rapid automated algorithm for aligning and reslicing PET images. J Comput Assist Tomogr 16:620–633.[Medline]
Yancey SW, Phelps EA (2001). Functional neuroimaging and episodic memory: a perspective. J Clin Exp Neuropsychol 23:32–48.[Medline]
This article has been cited by other articles:
|
|
 |
|
  D. P. DePaola, F. A. Curro, and D. T. Zero Saliva: The precious body fluid J Am Dent Assoc, May 1, 2008; 139(suppl_2): 5S - 10S. [Full Text] [PDF]
|
|
|
|
|
|
F. A. Curro Gum chewing as an adjunct to use of medications J Am Dent Assoc, May 1, 2008; 139(suppl_2): 6S - 8S. [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Hasegawa, T. Ono, K. Hori, and T. Nokubi Influence of Human Jaw Movement on Cerebral Blood Flow J. Dent. Res., January 1, 2007; 86(1): 64 - 68. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Haggman-Henrikson, E. Nordh, H. Zafar, and P.-O. Eriksson Head Immobilization can Impair Jaw Function. J. Dent. Res., November 1, 2006; 85(11): 1001 - 1005. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. G. Piancino, F. Talpone, P. Dalmasso, C. Debernardi, A. Lewin, and P. Bracco Reverse-sequencing chewing patterns before and after treatment of children with a unilateral posterior crossbite Eur J Orthod, October 1, 2006; 28(5): 480 - 484. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Shinagawa, T. Ono, E. Honda, T. Sasaki, M. Taira, A. Iriki, T. Kuroda, and K. Ohyama Chewing-side Preference is Involved in Differential Cortical Activation Patterns during Tongue Movements after Bilateral Gum-chewing: a Functional Magnetic Resonance Imaging Study J. Dent. Res., October 1, 2004; 83(10): 762 - 766. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Onozuka, M. Fujita, K. Watanabe, Y. Hirano, M. Niwa, K. Nishiyama, and S. Saito Age-related Changes in Brain Regional Activity during Chewing: A Functional Magnetic Resonance Imaging Study J. Dent. Res., August 1, 2003; 82(8): 657 - 660. [Abstract] [Full Text]
|
|
|
|
 |
|
 G.J. Lavigne, T. Kato, A. Kolta, and B.J. Sessle NEUROBIOLOGICAL MECHANISMS INVOLVEDIN SLEEP BRUXISM Crit. Rev. Oral. Biol. Med., January 1, 2003; 14(1): 30 - 46. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| IADR Journals | Advances in Dental Research ® |
| Journal of Dental Research ® | Critical Reviews (1990-2004) |
