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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 Oral Biochemistry, Kanagawa Dental College, Yokosuka 238-8580, Japan; and
6 Business Center for Academic Societies of Japan, Tokyo 113-8622, Japan;
* corresponding author, onozuka{at}cc.gifu-u.ac.jp
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: fMRI • gum chewing • brain activation • aging • human
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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Functional magnetic resonance imaging (fMRI) has provided a new tool for the testing of specific hypotheses about the anatomical regions involved in processing sensory and motor information in the human brain (Pulvermuller, 1999; Yancey and Phelps, 2001). Blood oxygenation level-dependent (BOLD) contrast fMRI not only detects small signal changes that are related to changes in the magnetization of protons within the blood (Ogawa et al., 1992), but also provides enhanced spatial and temporal resolution (Meisenzahl and Schlosser, 2001).
In this study, we used fMRI to assess the effect of aging on brain regional activity associated with chewing in young adult, middle-aged, and aged intact humans.
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MATERIALS & METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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Task Paradigm
The task paradigm was periods of rhythmic chewing, at a rate of approximately 1 Hz, measured by means of a metronome (Kemsley et al., 2003), of moderately hard gum (5.6 x 104 poise) separated by periods of no chewing (see Suzuki et al., 1994; Onozuka et al., 2002). This gum, without odor and taste components, was specially prepared in the General Laboratory of Lotte Co. Ltd. (Saitama, Japan). Each subject performed 8 cycles of 32 sec of rhythmic chewing and 32 sec without chewing (see inset in Fig. A
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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 analytical 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 (Mazziotta and Cherry, 1993). Independently, a correction for head motion was also applied with the use of SPM99 software (Wellcome Department of Cognitive Neurology, London, UK). Furthermore, motion artifacts, which may have been due to chewing, were removed by a low-pass filter of 1.5 sec, with MEDx software. Finally, we confirmed that residual motion artifacts were less than 0.01 mm (0.267% of a voxel) in any direction.
The 128 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 with the use of SPM99. 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 peak height and spatial extent (> 20 voxels).
For quantitative evaluation of the increased fMRI signal seen 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.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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). In addition, increases were seen in the supplementary motor area, thalamus, insula, cerebellum, and right prefrontal area. 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 and the coordinates, as given in the Talairach and Tournoux (1988) atlas, are shown. In contrast, in middle-aged subjects, the signal increase was lower in the primary sensorimotor cortex, thalamus, and cerebellum, and higher in the right prefrontal area, than in the young adults (Fig. C). In the aged subjects, these differences were even greater (Fig. D). Furthermore, in only the aged subjects, gum-chewing caused activation of the parietal, temporal, and occipital association cortices (Fig. D, arrowheads), the exact regions varying between subjects (data not shown).
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). In the prefrontal area, the signal increase in middle-aged and aged subjects was, respectively, 174.3% (group effect: F2, 25 = 27.58, p < 0.05) and 412.7% (group effect: F2, 25 = 27.58, p < 0.0001) of that seen in young adults. However, no significant difference was seen in the supplementary motor area (group effect: F2, 25 = 0.36) or insula (group effect: F2, 25 = 1.01). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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Our new finding is that, in the primary sensorimotor cortex, cerebellum, and thalamus, the chewing-induced increase in the BOLD signal was attenuated in an age-dependent manner. Studies on aging and mastication have shown that the loss of teeth and the masticatory muscle power deficits seen with advancing age impair masticatory function, thereby causing a reduction in sensory input activity to the central nervous system (Okimoto et al., 1991). In the present experiments, biting force was highest in the young adult group, followed by the middle-aged group, and lowest in the aged group. A similar age-dependent decline was seen in the number of remaining teeth. Taken together with the fact that age-related degeneration of various brain regions, including the somatosensory cortex, occurs in humans (Godde et al., 2002), it may be suggested that the age-related attenuation of the signal seen in the above three regions results from an age-dependent decrease in both masticatory work and neuronal activity in the brain.
Surprisingly, our results indicate that, in all groups, gum-chewing resulted in an increased BOLD signal in the right prefrontal area, and in aged subjects, this increase was 4 times higher than that seen in young subjects. A previous PET study found that patients with early Alzheimer’s disease show increased activity in the prefrontal regions compared with healthy age-matched controls during cognitive tasks (Grady et al., 2001a). Furthermore, these authors also showed that increased right prefrontal cortex activity is associated with better memory performance in both groups (Grady et al., 2001b); this has been interpreted as compensatory re-allocation of cognitive resources (Grady et al., 2003). With respect to Alzheimer’s disease and aging, the single most vulnerable circuit in the cerebral cortex is the projection referred to as the perforant path (Squire and Zola-Morgan, 1991), which originates in the entorhinal cortex and terminates in the dentate gyrus, thus providing the key interconnection between the neocortex and hippocampus (Amaral and Witter, 1989; Witter et al., 1989). Thus, if the interpretation of Grady et al. is correct, it is possible that, in the elderly, chewing stimulates neuronal activity within a network between the right prefrontal cortex and the hippocampus, which might be useful in maintaining cognitive function.
However, the exact link between gum-chewing and activation of the parietal, temporal, and occipital association cortices is unclear at the present time, and further research is required.
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ACKNOWLEDGMENTS |
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Received August 12, 2002; Last revision March 7, 2003; Accepted May 7, 2003
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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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.
Godde B, Berkefeld T, David-Jurgens M, Dinse HR (2002). Age-related changes in primary somatosensory cortex of rats: evidence for parallel degenerative and plastic-adaptive processes. Neurosci Biobehav Rev 26:743–752.[ISI][Medline]
Grady CL, Furey ML, Pietrini P, Horwitz B, Rapoport SI. (2001a). Altered brain functional connectivity and impaired short-term memory in Alzheimer’s disease. Brain 124:739–756.
Grady CL, McIntosh AR, Beig S, Craik FI (2001b). An examination of the effects of stimulus type, encoding task, and functional connectivity on the role of right prefrontal cortex in recognition memory. Neuroimage 14:556–571.[ISI][Medline]
Grady CL, McIntosh AR, Beig S, Keightley ML, Burian HB, Black SE (2003). Evidence from functional neuroimaging of a compensatory prefrontal network in Alzheimer’s disease. J Neurosci 23:986–993.
Kemsley EK, Defernez M, Sprunt JC, Smith AC (2003). Electromyographic responses to prescribed mastication. J Electromyogr Kinesiol 13:197–207.[ISI][Medline]
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.[ISI][Medline]
Mazziotta RP, Cherry JC (1993). MRI-PET registration with automated algorithm. J Comp Assist Tomog 17:536–546.[ISI][Medline]
Meisenzahl EM, Schlosser R (2001). Functional magnetic resonance imaging research in psychiatry. Neuroimaging Clin N Am 11:365–374.[ISI][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.[ISI][Medline]
Nakamura Y, Katakura N (1995). Generation of masticatory rhythm in the brainstem. Neurosci Res 23:1–19.[ISI][Medline]
Nakata M (1998). Masticatory function and its effects on general health. Int Dent J 48:540–548.[Medline]
Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, et al. (1992). Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 89:5951–5955.
Okimoto K, Ieiri K, Matsuo K, Terada Y (1991). Ageing and mastication: the relationship between oral status and the progress of dementia at senile hospital. J Jpn Prosthodont Soc 35:931–943.
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.
Pulvermuller F (1999). Words in the brain’s language. Behav Brain Sci 22:253–336.[ISI][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–A128.
Squire LR, Zola-Morgan S (1991). The medial temporal lobe memory system. Science 253:1380–1386.
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.
Witter MP, van Hoesen GW, Amaral DG (1989). Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J Neurosci 9:216–228.[Abstract]
Yancey SW, Phelps EA (2001). Functional neuroimaging and episodic memory: a perspective. J Clin Exp Neuropsychol 23:32–48.[ISI][Medline]
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