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The effect of mastication on human motor preparation processing: A study with CNV and MRCP
Neuroscience Research 64 (2009) 259–266
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The effect of mastication on human motor preparation processing: A study with CNV and MRCP Kiwako Sakamoto a,b,*, Hiroki Nakata a,c, Yukiko Honda a, Ryusuke Kakigi a,b a
Department of Integrative Physiology, National Institute for Physiological Sciences, Okazaki, Japan Department of Physiological Sciences, School of Life Sciences, The Graduate University for Advanced Studies, Hayama, Kanagawa, Japan c School of Health Sciences, Nagoya University, Nagoya, Japan b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 14 January 2009 Received in revised form 11 March 2009 Accepted 12 March 2009 Available online 25 March 2009
To clarify the effect of mastication on motor preparation processing using electroencephalography (EEG), we investigated the effect of mastication on contingent negative variation (CNV) and reaction time (RT) in Experiment 1, and movement-related cortical potentials (MRCPs) in Experiment 2. The twelve subjects performed four CNV or MRCP sessions, and in the Mastication condition chewed a gum base during the resting period between sessions, Pre (before chewing) and Post 1, 2, and 3 (after chewing). In the Control condition, the subjects performed the same sessions without chewing gum during the intervals between sessions on another day. In Experiment 1, the mean amplitudes of the early- and late-CNV were significantly larger in Mastication than Control at Post 2 and Post 3. RT also differed significantly between Mastication and Control at Post 3. By contrast, in Experiment 2, there were no significant differences between Mastication and Control for the mean amplitudes of MRCPs including Bereitschaftspotential (BP) and negative slope (NS0 ) in any session. These results suggest that mastication influences cognitive processing reflected by CNV with stimulus-triggered movement, rather than motor-related processing reflected by MRCPs relating to self-initiated movement, and provide evidence concerning the mechanisms for the effect of mastication on the human brain. ß 2009 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved.
Keywords: Electroencephalography EEG Chewing CNV MRCP Bereitschaftspotential
1. Introduction Some studies have reported an effect of mastication on psychological tests relating to arousal (Endo et al., 1982; Nageishi et al., 1993; Otomaru et al., 2003), energy expenditure and heart rate (Suzuki et al., 1992, 1994), choice reaction time (Chu, 1994), and working memory (Wilkinson et al., 2002; Baker et al., 2004; Stephens and Tunney, 2004; Hirano et al., 2008). Several neurophysiological studies have also tried to clarify the effect by recording background electroencephalographic (EEG) activity (Endo et al., 1982; Masumoto et al., 1999; Morinushi et al., 2000). There is however, evidence of no significant effect of gumchewing on memory (Tucha et al., 2004; Johnson and Miles, 2007), and background EEG activity (Suzuki et al., 1989; Masumoto et al., 1998); and the effect of mastication has been a matter of debate. Consequently, objective methods and indexes are needed to investigate the effect in detail.
* Corresponding author at: Department of Integrative Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki, 444-8585, Japan. Tel.: +81 564 55 7810; fax: +81 564 52 7913. E-mail address: [email protected] (K. Sakamoto).
In the present study, to evaluate the effect of mastication on the human brain, time-locked averaging EEG was employed. In particular, we focused on contingent negative variation (CNV) and movement-related cortical potentials (MRCPs), which have been widely studied and are considered to be linked to cognitive and motor preparation processing. CNV is an event-related potential (ERP), the amplitude of which increases during the interval between a first warning stimulus (S1) and a second imperative stimulus (S2). CNV has been associated with both motor preparation and cognitive processing including expectancy, motivation, attention and arousal (Brunia, 1988; van Boxtel and Brunia, 1994; Ikeda et al., 1996). CNV consists of at least two components, an early frontocentral dominant component (early-CNV) and a late centroparietal dominant component (lateCNV). MRCPs are recorded preceding self-initiated voluntary movement, and reflect movement preparation processing, not involving cognitive processing for an imperative stimulus (reviewed in Shibasaki and Hallett, 2006). These potentials begin with a slow rising negativity, called the Bereitschaftspotential (BP), and progress to a steeper, later negativity starting about 500 ms before movement onset, called the negativity slope (NS0 ). CNV and MRCPs show similar waveforms and phenomena concerning motor preparation, but indicate different brain activities.
0168-0102/$ – see front matter ß 2009 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved. doi:10.1016/j.neures.2009.03.008
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Therefore, in the present study, we compared the effect of mastication between CNV and MRCPs to investigate the influence on the human brain. The comparison provides four possibilities. The first is that the effect of mastication is evident on both CNV and MRCPs. If so, this result suggests that mastication influences both motor preparation and cognitive processing. The second is that the effect is evident on CNV but not MRCPs. This would indicate that Mastication affects cognitive processing rather than motor preparation processing in the human brain. The third is that the effect is evident on MRCPs but not CNV. In this case, it is likely that motor preparation processing is more important than cognitive processing under the effect of mastication. The fourth possibility is that the effect is evident on neither CNV nor MRCPs. The present study aimed to investigate whether the amplitudes of CNV and/or MRCPs were modulated by the effect of mastication. 2. Materials and methods 2.1. Participants Twelve normal right-handed subjects (twelve males; mean age 28.4 years, range 25–34) participated in this study. None of the subjects had a history of neurological or psychiatric disorder. Informed consent was obtained from all participants. The study was approved by the Ethics Committee of the National Institute for Physiological Sciences, Okazaki, Japan. 2.2. Experiment 1 (CNV) The subjects seated comfortably in a quiet room with their arms resting, performed a warning stimulus (S1)–imperative stimulus (S2) paradigm. S1 was an auditory pure tone of 1 kHz (55 dB SPL, 200 ms duration), presented binaurally through earphones, and S2 was a binaural 2-kHz tone (55 dB SPL, 200 ms duration). The subjects had to respond by pushing a button with their right thumb as quickly as possible after the presentation of S2. A pair of S1 and S2 stimuli was given to the subjects with an interval of 2 s. The S1– S1 interval was 10 s. During the recordings, the subjects were instructed to keep their eyes open and look at a small fixation point positioned in front of them at a distance of approximately 1 m. One session comprised 30 epochs of stimulation. The practice session consisted of 5 stimuli before the recordings. This experiment consisted of two conditions, Mastication and Control. Each condition was performed on a different day. Half of the participants began with the Mastication condition and half with the Control condition. The participants were tested at the same time of the day in each condition. The Mastication condition comprised four sessions of recordings at different times: Pre, Post 1, Post 2, and Post 3. In each session, the subjects performed a S1– S2 paradigm for approximately 5 min. After one session, the subjects were asked to chew gum for 5 min at a constant rate of approximately 1 Hz (Onozuka et al., 2002; Takada and Miyamoto, 2004); however, to avoid the effect of attention to mastication, the subjects were also instructed to relax, and not to worry about the frequency of chewing. In total, there were three gum-chewing intervals (Fig. 1). The Control condition included the same four sessions of the S1–S2 paradigm (Pre, Post 1, Post 2, and Post 3), but the subjects were instructed to relax without chewing gum for 5 min in each interval (Fig. 1). The present study used Post 2 and Post 3 as well as Post 1 for two reasons. First, we wondered whether the effect of mastication was found at Post 1 after only 5 min of mastication, compared to the Control. Second, if there was a true effect, we wanted to investigate how the effect changed in repeated sessions. For the mastication, a special gum base without odor and taste components was prepared (CAT21 Chewing Pellet, NAMITEC Co., Ltd., Osaka, Japan). This gum was made of polyvinyl
Fig. 1. Protocol for the Mastication and Control conditions in the present study. In each condition, the subjects performed four CNV sessions in Experiment 1, and MRCP sessions in Experiment 2. In Mastication, the subjects were asked to chew a gum without odor or taste during the session intervals for 5 min. In Control, the subjects were instructed to relax without gum-chewing during the intervals.
acetate, wax, and polyisobutylene, based on Japan food hygiene laws. EEGs were recorded with Ag/AgCl disk electrodes placed on the scalp at Fz, Cz, Pz, C3, and C4, according to the International 10–20 System. Each scalp electrode was referenced to linked earlobes. The ground electrode was placed at Fpz. To eliminate eye movements or blinks exceeding 100 mV, an electro-oculogram (EOG) was recorded bipolarly with a pair of electrodes placed 2 cm lateral to the lateral canthus of the right eye and 2 cm above the upper edge of the right orbit. The impedance was maintained at less than 5 kV. All of the EEG signals were collected on a signal processor (Neuropack MEB-2200 system, Nihon-Kohden, Tokyo, Japan). The analysis epoch for ERPs was 4 s including a prestimulus baseline period of 1 s before the onset of S1. The bandpass filter was set at 0.01–50 Hz and the sampling rate was 1000 Hz. No digital filter was applied off-line. We divided the CNV into two periods, early-CNV and late-CNV, and analyzed the effect of mastication on the amplitude of each period, separately, based on previous reports (Weerts and Lang, 1973; Rohrbaugh et al., 1976; Brunia, 1988; Ikeda et al., 1996). The amplitudes were analyzed from 0.5 to 1 s after the onset of S1 as the early-CNV, and from 1.5 to 2 s after the onset of S1 as the late-CNV. Early-CNV is found in association with attention, S1-stimulus orienting, and expectancy stimulus processing (Weerts and Lang, 1973; Rohrbaugh et al., 1976), while late-CNV is related to judgment, estimation, cognition, preparation, and motor processing (Brunia, 1988; Ikeda et al., 1996). Each period is thought to include brain activity concerning each characteristic within an S1–S2 interval of 2 s, and this was defined according to previous studies (Elbert et al., 1994; Ikeda et al., 1997; Kamijo et al., 2004). Reaction time (RT) was also recorded in all sessions. 2.3. Experiment 2 (MRCPs) The subjects performed brisk extension movements with the middle finger of their right hand. Each movement was repeated voluntarily at irregular self-paced intervals exceeding 6 s. Subjects were told not to count or engage in any other rhythmic activity during the recording. One session comprised 70 epochs of movement. The practice session consisted of 10 movements before the recordings. This experiment also consisted of two conditions, Mastication and Control. The procedure was the same as for Experiment 1 (Fig. 1). The electromyogram (EMG) was recorded from a pair of electrodes about 3 cm apart on the skin overlying the contraction
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muscle in the forearm. Electrodes were placed at Fz, Cz, Pz, C3, and C4, and the linked earlobes were used as a reference. EEG was averaged with reference to movement onset based on EMG activity, and the analysis epoch was 3 s from 2.5 to 0.5 s based on the onset. The baseline was calculated from 2.5 to 2 s before movement onset. The bandpass filter was set at 0.01–50 Hz and the sampling rate was 1000 Hz. No digital filter was applied off-line. The amplitudes of MRCPs were analyzed in two periods, from 1.5 to 0.5 s before movement onset as BP, and from 0.5 to 0 s before the onset as NS0 . There were two reasons for setting the period of analysis for each time frame. The first is that we wanted to define the amplitudes of BP and NS0 ‘without any bias of the experimenter’. The onset of BP and NS0 is often visually determined by the experimenter. But in this case, there was the possibility that the amplitudes of BP and NS0 would be affected by bias. On the other hand, in Experiment 1, the amplitudes of early-CNV and lateCNV were calculated ‘without bias’. Therefore, we also needed to define the onsets and amplitudes of BP and NS’ without such bias. Second, there is general agreement that BP is recorded from 1.5 to 0.5 s before EMG onset, and NS0 is observed from 0.5 to 0 s (reviewed in Hallett, 1994; Shibasaki and Hallett, 2006), and some previous studies have investigated the characteristics of the neural activity during these periods without visual inspection of BP and NS0 (Wasaka et al., 2003, 2005). Thus, we followed these previous studies.
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Fig. 2. Mean reaction time (RT) in each condition in Experiment 1 across all subjects. There was significant interaction of Condition–Session. Vertical lines indicate standard errors (S.E.). *p < 0.05, showing a significant difference between Mastication and Control.
2.4. Data analysis For the analysis of CNV and MRCPs, the data on mean amplitude were subjected to analyses of variance (ANOVA) with repeated measures using as within-subjects factors, Condition (Mastication vs. Control), Session (Pre, Post 1, Post 2, and Post 3), and Electrode of midline (Fz, Cz, and Pz). The behavioral data in the form of the mean RT in Experiment 1 was subjected to a two-way ANOVA with repeated measures using as within-subjects factors, Condition and Session. For all repeated measures factors with more than two levels, it was tested whether Mauchly’s sphericity assumption was violated. If the result of Mauchly’s test was significant and the assumption of sphericity was violated, the Greenhouse-Geisser adjustment was used for correction by altering the degrees of freedom with a correction coefficient epsilon. In addition, we performed post hoc Bonferroni multiple comparisons for differences in values between conditions. Statistical significance was set at p < 0.05. 3. Results 3.1. Experiment 1 (CNV) Fig. 2 shows behavioral data in the form of the mean RT with standard error (S.E.) in Experiment 1. There was significant interaction of Condition–Session (F(3, 33) = 3.062, p < 0.05), although there were no main effects of Condition (F(1, 11) = 0.682, p > 0.05) and Session (F(3, 33) = 0.221, p > 0.05). Post hoc testing revealed a significant difference (p < 0.05) between Mastication and Control at Post 3, but not at Pre, Post 1, or Post 2. Fig. 3A indicates the grand-averaged CNV waveforms at Pre in the Mastication and Control conditions. Two waveforms are superimposed and look remarkably similar. Fig. 3B shows the grand-averaged CNV at each session in Mastication and Control. Waveforms were recorded from all subjects in all sessions, and clearly differed in appearance between Mastication and Condition. In Mastication, the amplitudes of CNV gradually increased with repetitive sessions (Post 1, Post 2, and Post 3), compared to Pre. On the other hand, in Control, the amplitudes were almost the same or gradually decreased with repetitive sessions. These evaluations are
Fig. 3. (A) Grand-averaged waveforms of CNV in Pre across all subjects, measured at Fz, Cz, Pz, C3, and C4. (B) Grand-averaged CNV waveforms of each session. Black, red, green, and blue lines indicate waveforms of Pre, Post 1, Post 2, and Post 3, respectively. Thin and thick gray zones indicate early- and late-CNV, respectively. Early = early-CNV; Late = late-CNV.
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Fig. 4. Mean value of early- and late-CNV. Vertical lines indicate S.E. Significant differences between Mastication and Control are shown as ***p < 0.001, **p < 0.01, and *p < 0.05, respectively.
supported by the ANOVA for the mean amplitudes of the early- and late-CNV. ANOVA for early-CNV demonstrated significant main effects of Condition (F(1, 11) = 14.551, p < 0.01) and Electrode (F(2, 22) = 7.398, p < 0.01), and significant interaction of Condition– Session (F(3, 33) = 3.484, p < 0.05), while there was no significant main effect of Session (F(3, 33) = 2.741, p > 0.05). Further analysis of the effect of Condition with collapsing a factor of Electrode on each session demonstrated significant differences at Post 2 (F(1, 11) = 16.222, p < 0.01) and Post 3 (F(1, 11) = 13.276, p < 0.01). There were no significant differences between conditions at Pre (F(1, 11) = 1.800, p > 0.05) or Post 1 (F(1, 11) = 1.508, p > 0.05). Post hoc tests confirmed that the amplitude of Post 2 was significantly larger in Mastication than Control at Fz (p < 0.01), Cz
(p < 0.01), and Pz (p < 0.05). The amplitude of Post 3 was also significantly larger in Mastication than Control at Fz (p < 0.01), and Cz (p < 0.01) (Fig. 4). In addition, further analysis of the effect of Session with collapsing a factor of Electrode on each condition showed a significant difference at Mastication (F(3, 33) = 5.683, p < 0.01), but not at Control (F(3, 33) = 0.953, p > 0.05). Post hoc testing revealed that the amplitude was significantly larger at Post 2 than Pre and Post 1 for Fz (p < 0.05, respectively) and Cz (p < 0.01, and p < 0.05, respectively), and at Post 2 than Pre for Pz (p < 0.05). As for late-CNV amplitude, there were significant main effects of Condition (F(1, 11) = 11.299, p < 0.01), and Electrode (F(2, 22) = 11.376, p < 0.001), and a significant interaction of Condition– Session (F(3, 33) = 3.683, p < 0.05), but no significant main effect of
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Session (F(3, 33) = 1.244, p > 0.05). Further analysis of the effect of Condition with collapsing a factor of Electrode on each session demonstrated significant differences at Post 2 (F(1, 11) = 26.763, p < 0.001) and Post 3 (F(1, 11) = 11.568, p < 0.01). There were no significant differences between conditions at Pre (F(1, 11) = 0.069, p > 0.05) and Post 1 (F(1, 11) = 2.033, p > 0.05). Post hoc tests revealed that the amplitude of Post 2 was significantly larger in Mastication than Control at Fz (p < 0.001), Cz (p < 0.01), and Pz (p < 0.05). The amplitude of Post 3 was also significantly larger in Mastication than Control at Fz (p < 0.01), and Cz (p < 0.01) (Fig. 4). Moreover, further analysis of the effect of Session with collapsing a factor of Electrode on each condition showed a significant difference at Mastication (F(3, 33) = 4.572, p < 0.01), but not at Control (F(3, 33) = 1.164, p > 0.05). Post hoc tests for Mastication indicated that the amplitude was significantly larger at Post 2 than Pre and Post 1 for Fz (p < 0.05, respectively), and at Post 2 than Pre for Cz (p < 0.05). 3.2. Experiment 2 (MRCPs) Fig. 5A indicates the grand-averaged MRCPs at Pre in the Mastication and Control conditions. These waveforms are superimposed and look remarkably similar. Fig. 5B shows the grandaveraged MRCPs for each session in Mastication and Control. MRCPs waveforms were recorded from all subjects in all sessions. It is apparent that the waveforms did not change with repetitive sessions in Mastication or Control. This characteristic is supported by the ANOVA for the mean amplitudes of BP and NS0 .
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The ANOVA for the mean amplitude of BP revealed a main effect of Electrode (F(2, 22) = 12.972, p < 0.001), but there was no significant main effect of Condition (F(1, 11) = 0.530, p > 0.05) or Session (F(3, 33) = 0.844, p > 0.05), and no significant interactions. Post hoc tests indicated the amplitude to be significantly larger at Cz than Fz and Pz (p < 0.001, and p < 0.05, respectively). The ANOVA for the mean amplitude of NS0 also showed a main effect of Electrode (F(2, 22) = 26.023, p < 0.001), although there was no significant main effect of Condition (F(1, 11) = 1.240, p > 0.05) or Session (F(3, 33) = 0.799, p > 0.05), and no significant interactions. Post hoc testing revealed the amplitude to be significantly larger at Cz than Fz and Pz (p < 0.001, and p < 0.01, respectively). The amplitude was also significantly larger at Pz than Fz (p < 0.001) (Fig. 6). 4. Discussion Several studies have shown that the act of mastication, even without calorie intake, has beneficial psychological effects, alters the state of arousal, and increases scores in working memory tests (see Section 1). Masumoto and colleagues reported a change in some frequency components of the power spectrum in background EEGs after gum-chewing (Masumoto et al., 1999). They suggested that the chewing of gum had a relaxing effect. However, to our knowledge, there have been no neurophysiological studies evaluating the effect of mastication on the human brain by recording CNV and MRCPs. Based on this background, here we showed the effect of mastication on human motor preparation processing by recording CNV and MRCPs. In Experiment 1, the mean amplitudes of earlyand late-CNV were significantly different between the Mastication and Control conditions at Post 2 and Post 3. By contrast, in Experiment 2, there was no significant difference in the amplitude of BP and NS0 between Mastication and Control in any sessions. As mentioned in Section 1, we inferred that a comparison of the effect of mastication between CNV and MRCPs provided four possibilities, with our results indicating that mastication influenced cognitive processing rather than motor preparation processing in the human brain. 4.1. The difference in the effect of mastication on CNV and MRCPs
Fig. 5. (A) Grand-averaged waveforms of MRCPs in Pre across all subjects, measured at Fz, Cz, Pz, C3, and C4. (B) Grand-averaged MRCP waveforms of each session. Black, red, green, and blue lines indicate waveforms of Pre, Post 1, Post 2, and Post 3, respectively. Thin and thick gray zones indicate BP and NS0 , respectively. BP = Bereitschaftspotential; NS0 = negative slope.
The characteristics of early- and late-CNV have been well documented in the literature. Early-CNV is found in association with attention, S1-stimulus orienting, and expectancy stimulus processing (Weerts and Lang, 1973; Rohrbaugh et al., 1976), while late-CNV is thought to be related to judgment, estimation, cognition, preparation, and motor processing (Brunia, 1988; van Boxtel and Brunia, 1994; Ikeda et al., 1996; Yazawa et al., 1997). In the present study, the effect of mastication was found in both early- and late-CNV at Post 2 and Post 3, showing similar statistical results (Figs. 3 and 4); therefore, it is likely that multiple processing consisting of early- and late-CNV components can be affected by mastication during S1–S2 paradigms. Indeed, many previous studies have shown that several regions of the brain are related to the generation of CNV. Previous intracranial recordings of CNV demonstrated a role for the prefrontal cortex (PFC), orbitofrontal cortex, supplementary motor area (SMA), premotor area (PM), primary motor cortex (MI), primary somatosensory cortex (SI), cingulate gyrus, temporal area, parietooccipital lobes, insula, and subcortical structures, including the basal ganglia and thalamus (Ikeda et al., 1994, 1997; Lamarche et al., 1995; Hamano et al., 1997; Baresˇ and Rektor, 2001; Baresˇ et al., 2003). These activities have been confirmed in studies with dipole analyses (Pouthas et al., 2000), low resolution electromagnetic tomography (LORETA) (Go´mez et al., 2003, 2006), magnetoencephalography (MEG)
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Fig. 6. Mean values of BP and NS0 in MRCPs. Vertical lines indicate S.E. There were no main effects or interactions for BP and NS0 between Mastication and Control.
(Fenwick et al., 1993; Hultin et al., 1996), and monkeys (Donchin et al., 1971; Gemba et al., 1990). Moreover, the generation of CNV involves the ascending reticular activating system (ARAS) from the brain stem and midbrain, which is strongly related to arousal levels (McCallum et al., 1973). In the present study, we could not conclude which brain regions were affected by mastication in detail, but our data suggested that generator mechanisms for both early- and late-CNV were more activated during the mastication task. In contrast to CNV, MRCPs were not affected by mastication in any session of Experiment 2, even though CNV and MRCPs show similar waveforms and phenomena. This may be due to a difference in generators between CNV and MRCPs. The generation of MRCPs mainly involves movement-related regions. That is, BP and NS0 are generated from the pre-SMA, SMA, PM, MI, SI, anterior cingulate cortex (ACC), and subcortical structures including the basal ganglia and thalamus, as shown by intracranial recordings (Ikeda et al., 1994, 1996, 1997; Rektor et al., 2001; Lamarche et al.,
1995; Hamano et al., 1997), dipole modeling (Tarkka, 1994; Praamstra et al., 1996), MEG (Nagamine et al., 1994; Beisteiner et al., 2004), and studies with monkeys (Sasaki et al., 1979; Hashimoto et al., 1981). Taking these studies into consideration, a broader cortico-subcortical network is needed to generate CNV, compared to MRCPs. Clinical studies found that in some patients with lesions in the cerebellum, BP was completely absent while CNV remained normal (Ikeda et al., 1994). In patients with Parkinson’s disease, Ikeda and colleagues reported that BP remained normal but CNV was diminished (Ikeda et al., 1997). In addition, in a CNV paradigm without a motor task in response to an imperative stimulus (S2), well-pronounced negativity was recorded prior to S2 (Ruchkin et al., 1986; van Boxtel and Brunia, 1994). These studies have indicated that CNV is clearly different from MRCPs (Cui et al., 2000), although it shares some cortical generators with MRCPs and contains BP-like features. Our study may support this, since an effect of mastication was found on CNV, but not MRCPs. Moreover, our results suggest that the effect is
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associated with cognitive processing rather than movementrelated processing. Behavioral measurements of RT were also influenced by mastication; that is, RT in Mastication decreased slightly with repeated sessions, while that in Control increased gradually with repeated sessions (Fig. 2). Post hoc testing revealed a significant difference between Mastication and Condition at Post 3. RT is an important measure of sensorimotor performance in humans (Schmidt and Wrisberg, 2000), and is defined as the time from stimulus onset to the response, including components such as stimulus evaluation and response selection (Doucet and Stelmack, 1999). Therefore, our findings concerning the modulation of RT in Mastication indicate that sequential processing from stimulus input to response output is accelerated by the effect of mastication. 4.2. Explanations for the modulation of CNV in mastication There appear to be several possible explanations for the effect of mastication on CNV in Experiment 1. The first is that mastication influences arousal processing related to the level of vigilance, compared with the rest control. Arousal is adjusted by the neural activity of the brainstem, as clarified by Moruzzi and Magoun (1949) who electrically stimulated the mesencephalic reticular formation of cats when EEG signified a sleep-like state. On the onset of stimulation, there was a rapid and dramatic change in the EEG to the waveform of an awake brain (Moruzzi and Magoun, 1949; reviewed in Siegel, 2004). Based on their findings, the reticular formation in the brainstem and the neural pathways basic to the cortical arousal response became known as the ARAS. The ARAS has two pathways, dorsal and ventral. The dorsal pathway activates the cortex via the thalamus, and the ventral pathway, via the hypothalamus and basal forebrain. We considered that the ARAS should be affected by mastication, because rhythmic mastication is generated by the central pattern generator (CPG) in the brainstem (Nakamura and Katakura, 1995; Yamada et al., 2005). Studies have reported that the CPG drives not only mastication, but also cyclic movements such as stepping, walking, and pedaling (Dietz, 2003; Yuste et al., 2005; Zehr et al., 2007). After such exercises, some studies found that the amplitudes of ERP waveforms changed (Magnie´ et al., 2000; Hillman et al., 2003; Kamijo et al., 2004). Kamijo et al. (2004) suggest that the arousal (vigilance) level is an important factor influencing CNV waveforms. Therefore, mastication drove the neural activities in the CPG, and might have affected the waveforms of CNV in the Mastication condition of Experiment 1, but not in Control condition. In addition, there is evidence that mastication might directly affect cognitive processing. Some papers have reported effects of gum-chewing on working memory tasks (Wilkinson et al., 2002; Baker et al., 2004; Stephens and Tunney, 2004; Hirano et al., 2008). For instance, Baker et al. (2004) reported that gum-chewing during the encoding of a word list improved recall performance. Hirano et al. (2008), using functional magnetic resonance imaging (fMRI), showed more predominant neuronal activities in the PM, precuneus, thalamus, hippocampus, and inferior parietal lobule (IPL) during n-back tasks after gum-chewing. They suggested that gum-chewing accelerated or recovered the working memory process, including an arousal effect of the chewing motion, consequently enhancing cognitive performance. These studies would support our results that mastication affected the amplitude of CNV rather than that of MRCPs, and directly affected cognitive function. A second explanation is an effect of motor-related activities elicited by mastication. Repetitive electrical stimulation of a certain area of the cerebral cortex induces rhythmic jaw movements in many species, including monkeys (Lund and Lamarre, 1974; Huang et al., 1989), cats (Nakamura and Kubo, 1978; Iwata
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et al., 1985), guinea pigs (Goldberg and Tal, 1978; Nozaki et al., 1986), and rabbits (Lund et al., 1984; Liu et al., 1993). Such rhythmic jaw movements along with coordinated rhythmic movements of the tongue and facial organs as well as the secretion of saliva are called fictive mastication, and the cortical regions involved are termed the ‘cortical masticatory area (CMA)’ (Nakamura and Katakura, 1995; Yamada et al., 2005). At present, the descending input from the CMA has been considered the major source generating and activating the masticatory CPG (Nakamura and Katakura, 1995). The CMA includes several cortical regions, such as the face MI, the face SI, the area immediately lateral to the face MI, and an area deep in the CMA on the inner surface of the frontal operculum (Huang et al., 1989). Recent neuroimaging studies using fMRI and positron emission tomography (PET) have also found a neural network involving the MI, SI, SMA, PM, PFC, insula, posterior parietal cortex (PPC), thalamus, striatum, and cerebellum (Momose et al., 1997; Onozuka et al., 2002; Tamura et al., 2003; Takada and Miyamoto, 2004). Therefore, the sequential activities generated from the neural network including the CMA may affect the global neural activities in the brain. Of course, there is a possibility that more than one of the above explanations apply. In conclusion, this is the first study to investigate the effect of mastication on CNV and MRCPs relating to motor preparation. As a result, an effect was found on CNV, but not MRCPs, suggesting that mastication mainly affected non-motor or cognitive aspects of the CNV, rather than specifically motor preparation. These results provide evidence concerning the mechanisms for the effect of mastication on the human brain. They may also help to distinguish between CNV and MRCPs. Acknowledgement We are very grateful to Mr. Y. Takeshima for technical support during this study. References Baker, J.R., Bezance, J.B., Zellaby, E., Aggleton, J.P., 2004. Chewing gum can produce context-dependent effects upon memory. Appetite 43, 207–210. Baresˇ, M., Rektor, I., 2001. Basal ganglia involvement in sensory and cognitive processing. A depth electrode CNV study in human subjects. Clin. Neurophysiol. 112, 2022–2030. ˇ ovsky´, P., Streitova´, H., 2003. Cortical and subcortical Baresˇ, M., Rektor, I., Kan distribution of middle and long latency auditory and visual evoked potentials in a cognitive (CNV) paradigm. Clin. Neurophysiol. 114, 2447–2460. Beisteiner, R., Gartus, A., Erdler, M., Mayer, D., Lanzenberger, R., Deecke, L., 2004. Magnetoencephalography indicates finger motor somatotopy. Eur. J. Neurosci. 19, 465–472. Brunia, C.H.M., 1988. Movement and stimulus preceding negativity. Biol. Psychol. 26, 165–178. Chu, N.S., 1994. Effect of betel chewing on performance reaction time. J. Formos. Med. Assoc. 93, 343–345. Cui, R.Q., Egkher, A., Huter, D., Lang, W., Lindinger, G., Deecke, L., 2000. High resolution spatiotemporal analysis of the contingent negative variation in simple or complex motor tasks and a non-motor task. Clin. Neurophysiol. 111, 1847–1859. Dietz, V., 2003. Spinal cord pattern generators for locomotion. Clin. Neurophysiol. 114, 1379–1389. Donchin, E., Otto, D., Gerbrandt, L.K., Pribram, K.H., 1971. While a monkey waits: electrocortical events recorded during the foreperiod of a reaction time study. Electroencephalogr. Clin. Neurophysiol. 31, 115–127. Doucet, C., Stelmack, M.R., 1999. The effect of response execution on P3 latency, reaction time, and movement time. Psychophysiology 36, 351–363. Elbert, T., Rockstroh, B., Hampson, S., Pantev, C., Hoke, M., 1994. The magnetic counterpart of the contingent negative variation. Electroencephalogr. Clin. Neurophysiol. 92, 262–272. Endo, T., Tezuka, S., Sato, Y., 1982. An experimental study of a preventive measure against drowsiness in a car driving. J. Transport. Med. 36, 195–204 (in Japanese). Fenwick, P.B.C., Ioannides, A.A., Fenton, G.W., Lumsden, J., Grummich, P., Kober, H., Daun, A., Vieth, J., 1993. Estimates of brain activity using magnetic field tomography in a GO/NOGO avoidance paradigm. Brain Topogr. 5, 275–282. Gemba, H., Sasaki, K., Tsujimoto, T., 1990. Cortical field potentials associated with hand movements triggered by warning and imperative stimuli in the monkey. Neurosci. Lett. 113, 275–280.
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The effect of mastication on human motor preparation processing: A study with CNV and MRCP Kiwako Sakamoto a,b,*, Hiroki Nakata a,c, Yukiko Honda a, Ryusuke Kakigi a,b a
Department of Integrative Physiology, National Institute for Physiological Sciences, Okazaki, Japan Department of Physiological Sciences, School of Life Sciences, The Graduate University for Advanced Studies, Hayama, Kanagawa, Japan c School of Health Sciences, Nagoya University, Nagoya, Japan b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 14 January 2009 Received in revised form 11 March 2009 Accepted 12 March 2009 Available online 25 March 2009
To clarify the effect of mastication on motor preparation processing using electroencephalography (EEG), we investigated the effect of mastication on contingent negative variation (CNV) and reaction time (RT) in Experiment 1, and movement-related cortical potentials (MRCPs) in Experiment 2. The twelve subjects performed four CNV or MRCP sessions, and in the Mastication condition chewed a gum base during the resting period between sessions, Pre (before chewing) and Post 1, 2, and 3 (after chewing). In the Control condition, the subjects performed the same sessions without chewing gum during the intervals between sessions on another day. In Experiment 1, the mean amplitudes of the early- and late-CNV were significantly larger in Mastication than Control at Post 2 and Post 3. RT also differed significantly between Mastication and Control at Post 3. By contrast, in Experiment 2, there were no significant differences between Mastication and Control for the mean amplitudes of MRCPs including Bereitschaftspotential (BP) and negative slope (NS0 ) in any session. These results suggest that mastication influences cognitive processing reflected by CNV with stimulus-triggered movement, rather than motor-related processing reflected by MRCPs relating to self-initiated movement, and provide evidence concerning the mechanisms for the effect of mastication on the human brain. ß 2009 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved.
Keywords: Electroencephalography EEG Chewing CNV MRCP Bereitschaftspotential
1. Introduction Some studies have reported an effect of mastication on psychological tests relating to arousal (Endo et al., 1982; Nageishi et al., 1993; Otomaru et al., 2003), energy expenditure and heart rate (Suzuki et al., 1992, 1994), choice reaction time (Chu, 1994), and working memory (Wilkinson et al., 2002; Baker et al., 2004; Stephens and Tunney, 2004; Hirano et al., 2008). Several neurophysiological studies have also tried to clarify the effect by recording background electroencephalographic (EEG) activity (Endo et al., 1982; Masumoto et al., 1999; Morinushi et al., 2000). There is however, evidence of no significant effect of gumchewing on memory (Tucha et al., 2004; Johnson and Miles, 2007), and background EEG activity (Suzuki et al., 1989; Masumoto et al., 1998); and the effect of mastication has been a matter of debate. Consequently, objective methods and indexes are needed to investigate the effect in detail.
* Corresponding author at: Department of Integrative Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki, 444-8585, Japan. Tel.: +81 564 55 7810; fax: +81 564 52 7913. E-mail address: [email protected] (K. Sakamoto).
In the present study, to evaluate the effect of mastication on the human brain, time-locked averaging EEG was employed. In particular, we focused on contingent negative variation (CNV) and movement-related cortical potentials (MRCPs), which have been widely studied and are considered to be linked to cognitive and motor preparation processing. CNV is an event-related potential (ERP), the amplitude of which increases during the interval between a first warning stimulus (S1) and a second imperative stimulus (S2). CNV has been associated with both motor preparation and cognitive processing including expectancy, motivation, attention and arousal (Brunia, 1988; van Boxtel and Brunia, 1994; Ikeda et al., 1996). CNV consists of at least two components, an early frontocentral dominant component (early-CNV) and a late centroparietal dominant component (lateCNV). MRCPs are recorded preceding self-initiated voluntary movement, and reflect movement preparation processing, not involving cognitive processing for an imperative stimulus (reviewed in Shibasaki and Hallett, 2006). These potentials begin with a slow rising negativity, called the Bereitschaftspotential (BP), and progress to a steeper, later negativity starting about 500 ms before movement onset, called the negativity slope (NS0 ). CNV and MRCPs show similar waveforms and phenomena concerning motor preparation, but indicate different brain activities.
0168-0102/$ – see front matter ß 2009 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved. doi:10.1016/j.neures.2009.03.008
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Therefore, in the present study, we compared the effect of mastication between CNV and MRCPs to investigate the influence on the human brain. The comparison provides four possibilities. The first is that the effect of mastication is evident on both CNV and MRCPs. If so, this result suggests that mastication influences both motor preparation and cognitive processing. The second is that the effect is evident on CNV but not MRCPs. This would indicate that Mastication affects cognitive processing rather than motor preparation processing in the human brain. The third is that the effect is evident on MRCPs but not CNV. In this case, it is likely that motor preparation processing is more important than cognitive processing under the effect of mastication. The fourth possibility is that the effect is evident on neither CNV nor MRCPs. The present study aimed to investigate whether the amplitudes of CNV and/or MRCPs were modulated by the effect of mastication. 2. Materials and methods 2.1. Participants Twelve normal right-handed subjects (twelve males; mean age 28.4 years, range 25–34) participated in this study. None of the subjects had a history of neurological or psychiatric disorder. Informed consent was obtained from all participants. The study was approved by the Ethics Committee of the National Institute for Physiological Sciences, Okazaki, Japan. 2.2. Experiment 1 (CNV) The subjects seated comfortably in a quiet room with their arms resting, performed a warning stimulus (S1)–imperative stimulus (S2) paradigm. S1 was an auditory pure tone of 1 kHz (55 dB SPL, 200 ms duration), presented binaurally through earphones, and S2 was a binaural 2-kHz tone (55 dB SPL, 200 ms duration). The subjects had to respond by pushing a button with their right thumb as quickly as possible after the presentation of S2. A pair of S1 and S2 stimuli was given to the subjects with an interval of 2 s. The S1– S1 interval was 10 s. During the recordings, the subjects were instructed to keep their eyes open and look at a small fixation point positioned in front of them at a distance of approximately 1 m. One session comprised 30 epochs of stimulation. The practice session consisted of 5 stimuli before the recordings. This experiment consisted of two conditions, Mastication and Control. Each condition was performed on a different day. Half of the participants began with the Mastication condition and half with the Control condition. The participants were tested at the same time of the day in each condition. The Mastication condition comprised four sessions of recordings at different times: Pre, Post 1, Post 2, and Post 3. In each session, the subjects performed a S1– S2 paradigm for approximately 5 min. After one session, the subjects were asked to chew gum for 5 min at a constant rate of approximately 1 Hz (Onozuka et al., 2002; Takada and Miyamoto, 2004); however, to avoid the effect of attention to mastication, the subjects were also instructed to relax, and not to worry about the frequency of chewing. In total, there were three gum-chewing intervals (Fig. 1). The Control condition included the same four sessions of the S1–S2 paradigm (Pre, Post 1, Post 2, and Post 3), but the subjects were instructed to relax without chewing gum for 5 min in each interval (Fig. 1). The present study used Post 2 and Post 3 as well as Post 1 for two reasons. First, we wondered whether the effect of mastication was found at Post 1 after only 5 min of mastication, compared to the Control. Second, if there was a true effect, we wanted to investigate how the effect changed in repeated sessions. For the mastication, a special gum base without odor and taste components was prepared (CAT21 Chewing Pellet, NAMITEC Co., Ltd., Osaka, Japan). This gum was made of polyvinyl
Fig. 1. Protocol for the Mastication and Control conditions in the present study. In each condition, the subjects performed four CNV sessions in Experiment 1, and MRCP sessions in Experiment 2. In Mastication, the subjects were asked to chew a gum without odor or taste during the session intervals for 5 min. In Control, the subjects were instructed to relax without gum-chewing during the intervals.
acetate, wax, and polyisobutylene, based on Japan food hygiene laws. EEGs were recorded with Ag/AgCl disk electrodes placed on the scalp at Fz, Cz, Pz, C3, and C4, according to the International 10–20 System. Each scalp electrode was referenced to linked earlobes. The ground electrode was placed at Fpz. To eliminate eye movements or blinks exceeding 100 mV, an electro-oculogram (EOG) was recorded bipolarly with a pair of electrodes placed 2 cm lateral to the lateral canthus of the right eye and 2 cm above the upper edge of the right orbit. The impedance was maintained at less than 5 kV. All of the EEG signals were collected on a signal processor (Neuropack MEB-2200 system, Nihon-Kohden, Tokyo, Japan). The analysis epoch for ERPs was 4 s including a prestimulus baseline period of 1 s before the onset of S1. The bandpass filter was set at 0.01–50 Hz and the sampling rate was 1000 Hz. No digital filter was applied off-line. We divided the CNV into two periods, early-CNV and late-CNV, and analyzed the effect of mastication on the amplitude of each period, separately, based on previous reports (Weerts and Lang, 1973; Rohrbaugh et al., 1976; Brunia, 1988; Ikeda et al., 1996). The amplitudes were analyzed from 0.5 to 1 s after the onset of S1 as the early-CNV, and from 1.5 to 2 s after the onset of S1 as the late-CNV. Early-CNV is found in association with attention, S1-stimulus orienting, and expectancy stimulus processing (Weerts and Lang, 1973; Rohrbaugh et al., 1976), while late-CNV is related to judgment, estimation, cognition, preparation, and motor processing (Brunia, 1988; Ikeda et al., 1996). Each period is thought to include brain activity concerning each characteristic within an S1–S2 interval of 2 s, and this was defined according to previous studies (Elbert et al., 1994; Ikeda et al., 1997; Kamijo et al., 2004). Reaction time (RT) was also recorded in all sessions. 2.3. Experiment 2 (MRCPs) The subjects performed brisk extension movements with the middle finger of their right hand. Each movement was repeated voluntarily at irregular self-paced intervals exceeding 6 s. Subjects were told not to count or engage in any other rhythmic activity during the recording. One session comprised 70 epochs of movement. The practice session consisted of 10 movements before the recordings. This experiment also consisted of two conditions, Mastication and Control. The procedure was the same as for Experiment 1 (Fig. 1). The electromyogram (EMG) was recorded from a pair of electrodes about 3 cm apart on the skin overlying the contraction
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muscle in the forearm. Electrodes were placed at Fz, Cz, Pz, C3, and C4, and the linked earlobes were used as a reference. EEG was averaged with reference to movement onset based on EMG activity, and the analysis epoch was 3 s from 2.5 to 0.5 s based on the onset. The baseline was calculated from 2.5 to 2 s before movement onset. The bandpass filter was set at 0.01–50 Hz and the sampling rate was 1000 Hz. No digital filter was applied off-line. The amplitudes of MRCPs were analyzed in two periods, from 1.5 to 0.5 s before movement onset as BP, and from 0.5 to 0 s before the onset as NS0 . There were two reasons for setting the period of analysis for each time frame. The first is that we wanted to define the amplitudes of BP and NS0 ‘without any bias of the experimenter’. The onset of BP and NS0 is often visually determined by the experimenter. But in this case, there was the possibility that the amplitudes of BP and NS0 would be affected by bias. On the other hand, in Experiment 1, the amplitudes of early-CNV and lateCNV were calculated ‘without bias’. Therefore, we also needed to define the onsets and amplitudes of BP and NS’ without such bias. Second, there is general agreement that BP is recorded from 1.5 to 0.5 s before EMG onset, and NS0 is observed from 0.5 to 0 s (reviewed in Hallett, 1994; Shibasaki and Hallett, 2006), and some previous studies have investigated the characteristics of the neural activity during these periods without visual inspection of BP and NS0 (Wasaka et al., 2003, 2005). Thus, we followed these previous studies.
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Fig. 2. Mean reaction time (RT) in each condition in Experiment 1 across all subjects. There was significant interaction of Condition–Session. Vertical lines indicate standard errors (S.E.). *p < 0.05, showing a significant difference between Mastication and Control.
2.4. Data analysis For the analysis of CNV and MRCPs, the data on mean amplitude were subjected to analyses of variance (ANOVA) with repeated measures using as within-subjects factors, Condition (Mastication vs. Control), Session (Pre, Post 1, Post 2, and Post 3), and Electrode of midline (Fz, Cz, and Pz). The behavioral data in the form of the mean RT in Experiment 1 was subjected to a two-way ANOVA with repeated measures using as within-subjects factors, Condition and Session. For all repeated measures factors with more than two levels, it was tested whether Mauchly’s sphericity assumption was violated. If the result of Mauchly’s test was significant and the assumption of sphericity was violated, the Greenhouse-Geisser adjustment was used for correction by altering the degrees of freedom with a correction coefficient epsilon. In addition, we performed post hoc Bonferroni multiple comparisons for differences in values between conditions. Statistical significance was set at p < 0.05. 3. Results 3.1. Experiment 1 (CNV) Fig. 2 shows behavioral data in the form of the mean RT with standard error (S.E.) in Experiment 1. There was significant interaction of Condition–Session (F(3, 33) = 3.062, p < 0.05), although there were no main effects of Condition (F(1, 11) = 0.682, p > 0.05) and Session (F(3, 33) = 0.221, p > 0.05). Post hoc testing revealed a significant difference (p < 0.05) between Mastication and Control at Post 3, but not at Pre, Post 1, or Post 2. Fig. 3A indicates the grand-averaged CNV waveforms at Pre in the Mastication and Control conditions. Two waveforms are superimposed and look remarkably similar. Fig. 3B shows the grand-averaged CNV at each session in Mastication and Control. Waveforms were recorded from all subjects in all sessions, and clearly differed in appearance between Mastication and Condition. In Mastication, the amplitudes of CNV gradually increased with repetitive sessions (Post 1, Post 2, and Post 3), compared to Pre. On the other hand, in Control, the amplitudes were almost the same or gradually decreased with repetitive sessions. These evaluations are
Fig. 3. (A) Grand-averaged waveforms of CNV in Pre across all subjects, measured at Fz, Cz, Pz, C3, and C4. (B) Grand-averaged CNV waveforms of each session. Black, red, green, and blue lines indicate waveforms of Pre, Post 1, Post 2, and Post 3, respectively. Thin and thick gray zones indicate early- and late-CNV, respectively. Early = early-CNV; Late = late-CNV.
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Fig. 4. Mean value of early- and late-CNV. Vertical lines indicate S.E. Significant differences between Mastication and Control are shown as ***p < 0.001, **p < 0.01, and *p < 0.05, respectively.
supported by the ANOVA for the mean amplitudes of the early- and late-CNV. ANOVA for early-CNV demonstrated significant main effects of Condition (F(1, 11) = 14.551, p < 0.01) and Electrode (F(2, 22) = 7.398, p < 0.01), and significant interaction of Condition– Session (F(3, 33) = 3.484, p < 0.05), while there was no significant main effect of Session (F(3, 33) = 2.741, p > 0.05). Further analysis of the effect of Condition with collapsing a factor of Electrode on each session demonstrated significant differences at Post 2 (F(1, 11) = 16.222, p < 0.01) and Post 3 (F(1, 11) = 13.276, p < 0.01). There were no significant differences between conditions at Pre (F(1, 11) = 1.800, p > 0.05) or Post 1 (F(1, 11) = 1.508, p > 0.05). Post hoc tests confirmed that the amplitude of Post 2 was significantly larger in Mastication than Control at Fz (p < 0.01), Cz
(p < 0.01), and Pz (p < 0.05). The amplitude of Post 3 was also significantly larger in Mastication than Control at Fz (p < 0.01), and Cz (p < 0.01) (Fig. 4). In addition, further analysis of the effect of Session with collapsing a factor of Electrode on each condition showed a significant difference at Mastication (F(3, 33) = 5.683, p < 0.01), but not at Control (F(3, 33) = 0.953, p > 0.05). Post hoc testing revealed that the amplitude was significantly larger at Post 2 than Pre and Post 1 for Fz (p < 0.05, respectively) and Cz (p < 0.01, and p < 0.05, respectively), and at Post 2 than Pre for Pz (p < 0.05). As for late-CNV amplitude, there were significant main effects of Condition (F(1, 11) = 11.299, p < 0.01), and Electrode (F(2, 22) = 11.376, p < 0.001), and a significant interaction of Condition– Session (F(3, 33) = 3.683, p < 0.05), but no significant main effect of
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Session (F(3, 33) = 1.244, p > 0.05). Further analysis of the effect of Condition with collapsing a factor of Electrode on each session demonstrated significant differences at Post 2 (F(1, 11) = 26.763, p < 0.001) and Post 3 (F(1, 11) = 11.568, p < 0.01). There were no significant differences between conditions at Pre (F(1, 11) = 0.069, p > 0.05) and Post 1 (F(1, 11) = 2.033, p > 0.05). Post hoc tests revealed that the amplitude of Post 2 was significantly larger in Mastication than Control at Fz (p < 0.001), Cz (p < 0.01), and Pz (p < 0.05). The amplitude of Post 3 was also significantly larger in Mastication than Control at Fz (p < 0.01), and Cz (p < 0.01) (Fig. 4). Moreover, further analysis of the effect of Session with collapsing a factor of Electrode on each condition showed a significant difference at Mastication (F(3, 33) = 4.572, p < 0.01), but not at Control (F(3, 33) = 1.164, p > 0.05). Post hoc tests for Mastication indicated that the amplitude was significantly larger at Post 2 than Pre and Post 1 for Fz (p < 0.05, respectively), and at Post 2 than Pre for Cz (p < 0.05). 3.2. Experiment 2 (MRCPs) Fig. 5A indicates the grand-averaged MRCPs at Pre in the Mastication and Control conditions. These waveforms are superimposed and look remarkably similar. Fig. 5B shows the grandaveraged MRCPs for each session in Mastication and Control. MRCPs waveforms were recorded from all subjects in all sessions. It is apparent that the waveforms did not change with repetitive sessions in Mastication or Control. This characteristic is supported by the ANOVA for the mean amplitudes of BP and NS0 .
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The ANOVA for the mean amplitude of BP revealed a main effect of Electrode (F(2, 22) = 12.972, p < 0.001), but there was no significant main effect of Condition (F(1, 11) = 0.530, p > 0.05) or Session (F(3, 33) = 0.844, p > 0.05), and no significant interactions. Post hoc tests indicated the amplitude to be significantly larger at Cz than Fz and Pz (p < 0.001, and p < 0.05, respectively). The ANOVA for the mean amplitude of NS0 also showed a main effect of Electrode (F(2, 22) = 26.023, p < 0.001), although there was no significant main effect of Condition (F(1, 11) = 1.240, p > 0.05) or Session (F(3, 33) = 0.799, p > 0.05), and no significant interactions. Post hoc testing revealed the amplitude to be significantly larger at Cz than Fz and Pz (p < 0.001, and p < 0.01, respectively). The amplitude was also significantly larger at Pz than Fz (p < 0.001) (Fig. 6). 4. Discussion Several studies have shown that the act of mastication, even without calorie intake, has beneficial psychological effects, alters the state of arousal, and increases scores in working memory tests (see Section 1). Masumoto and colleagues reported a change in some frequency components of the power spectrum in background EEGs after gum-chewing (Masumoto et al., 1999). They suggested that the chewing of gum had a relaxing effect. However, to our knowledge, there have been no neurophysiological studies evaluating the effect of mastication on the human brain by recording CNV and MRCPs. Based on this background, here we showed the effect of mastication on human motor preparation processing by recording CNV and MRCPs. In Experiment 1, the mean amplitudes of earlyand late-CNV were significantly different between the Mastication and Control conditions at Post 2 and Post 3. By contrast, in Experiment 2, there was no significant difference in the amplitude of BP and NS0 between Mastication and Control in any sessions. As mentioned in Section 1, we inferred that a comparison of the effect of mastication between CNV and MRCPs provided four possibilities, with our results indicating that mastication influenced cognitive processing rather than motor preparation processing in the human brain. 4.1. The difference in the effect of mastication on CNV and MRCPs
Fig. 5. (A) Grand-averaged waveforms of MRCPs in Pre across all subjects, measured at Fz, Cz, Pz, C3, and C4. (B) Grand-averaged MRCP waveforms of each session. Black, red, green, and blue lines indicate waveforms of Pre, Post 1, Post 2, and Post 3, respectively. Thin and thick gray zones indicate BP and NS0 , respectively. BP = Bereitschaftspotential; NS0 = negative slope.
The characteristics of early- and late-CNV have been well documented in the literature. Early-CNV is found in association with attention, S1-stimulus orienting, and expectancy stimulus processing (Weerts and Lang, 1973; Rohrbaugh et al., 1976), while late-CNV is thought to be related to judgment, estimation, cognition, preparation, and motor processing (Brunia, 1988; van Boxtel and Brunia, 1994; Ikeda et al., 1996; Yazawa et al., 1997). In the present study, the effect of mastication was found in both early- and late-CNV at Post 2 and Post 3, showing similar statistical results (Figs. 3 and 4); therefore, it is likely that multiple processing consisting of early- and late-CNV components can be affected by mastication during S1–S2 paradigms. Indeed, many previous studies have shown that several regions of the brain are related to the generation of CNV. Previous intracranial recordings of CNV demonstrated a role for the prefrontal cortex (PFC), orbitofrontal cortex, supplementary motor area (SMA), premotor area (PM), primary motor cortex (MI), primary somatosensory cortex (SI), cingulate gyrus, temporal area, parietooccipital lobes, insula, and subcortical structures, including the basal ganglia and thalamus (Ikeda et al., 1994, 1997; Lamarche et al., 1995; Hamano et al., 1997; Baresˇ and Rektor, 2001; Baresˇ et al., 2003). These activities have been confirmed in studies with dipole analyses (Pouthas et al., 2000), low resolution electromagnetic tomography (LORETA) (Go´mez et al., 2003, 2006), magnetoencephalography (MEG)
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Fig. 6. Mean values of BP and NS0 in MRCPs. Vertical lines indicate S.E. There were no main effects or interactions for BP and NS0 between Mastication and Control.
(Fenwick et al., 1993; Hultin et al., 1996), and monkeys (Donchin et al., 1971; Gemba et al., 1990). Moreover, the generation of CNV involves the ascending reticular activating system (ARAS) from the brain stem and midbrain, which is strongly related to arousal levels (McCallum et al., 1973). In the present study, we could not conclude which brain regions were affected by mastication in detail, but our data suggested that generator mechanisms for both early- and late-CNV were more activated during the mastication task. In contrast to CNV, MRCPs were not affected by mastication in any session of Experiment 2, even though CNV and MRCPs show similar waveforms and phenomena. This may be due to a difference in generators between CNV and MRCPs. The generation of MRCPs mainly involves movement-related regions. That is, BP and NS0 are generated from the pre-SMA, SMA, PM, MI, SI, anterior cingulate cortex (ACC), and subcortical structures including the basal ganglia and thalamus, as shown by intracranial recordings (Ikeda et al., 1994, 1996, 1997; Rektor et al., 2001; Lamarche et al.,
1995; Hamano et al., 1997), dipole modeling (Tarkka, 1994; Praamstra et al., 1996), MEG (Nagamine et al., 1994; Beisteiner et al., 2004), and studies with monkeys (Sasaki et al., 1979; Hashimoto et al., 1981). Taking these studies into consideration, a broader cortico-subcortical network is needed to generate CNV, compared to MRCPs. Clinical studies found that in some patients with lesions in the cerebellum, BP was completely absent while CNV remained normal (Ikeda et al., 1994). In patients with Parkinson’s disease, Ikeda and colleagues reported that BP remained normal but CNV was diminished (Ikeda et al., 1997). In addition, in a CNV paradigm without a motor task in response to an imperative stimulus (S2), well-pronounced negativity was recorded prior to S2 (Ruchkin et al., 1986; van Boxtel and Brunia, 1994). These studies have indicated that CNV is clearly different from MRCPs (Cui et al., 2000), although it shares some cortical generators with MRCPs and contains BP-like features. Our study may support this, since an effect of mastication was found on CNV, but not MRCPs. Moreover, our results suggest that the effect is
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associated with cognitive processing rather than movementrelated processing. Behavioral measurements of RT were also influenced by mastication; that is, RT in Mastication decreased slightly with repeated sessions, while that in Control increased gradually with repeated sessions (Fig. 2). Post hoc testing revealed a significant difference between Mastication and Condition at Post 3. RT is an important measure of sensorimotor performance in humans (Schmidt and Wrisberg, 2000), and is defined as the time from stimulus onset to the response, including components such as stimulus evaluation and response selection (Doucet and Stelmack, 1999). Therefore, our findings concerning the modulation of RT in Mastication indicate that sequential processing from stimulus input to response output is accelerated by the effect of mastication. 4.2. Explanations for the modulation of CNV in mastication There appear to be several possible explanations for the effect of mastication on CNV in Experiment 1. The first is that mastication influences arousal processing related to the level of vigilance, compared with the rest control. Arousal is adjusted by the neural activity of the brainstem, as clarified by Moruzzi and Magoun (1949) who electrically stimulated the mesencephalic reticular formation of cats when EEG signified a sleep-like state. On the onset of stimulation, there was a rapid and dramatic change in the EEG to the waveform of an awake brain (Moruzzi and Magoun, 1949; reviewed in Siegel, 2004). Based on their findings, the reticular formation in the brainstem and the neural pathways basic to the cortical arousal response became known as the ARAS. The ARAS has two pathways, dorsal and ventral. The dorsal pathway activates the cortex via the thalamus, and the ventral pathway, via the hypothalamus and basal forebrain. We considered that the ARAS should be affected by mastication, because rhythmic mastication is generated by the central pattern generator (CPG) in the brainstem (Nakamura and Katakura, 1995; Yamada et al., 2005). Studies have reported that the CPG drives not only mastication, but also cyclic movements such as stepping, walking, and pedaling (Dietz, 2003; Yuste et al., 2005; Zehr et al., 2007). After such exercises, some studies found that the amplitudes of ERP waveforms changed (Magnie´ et al., 2000; Hillman et al., 2003; Kamijo et al., 2004). Kamijo et al. (2004) suggest that the arousal (vigilance) level is an important factor influencing CNV waveforms. Therefore, mastication drove the neural activities in the CPG, and might have affected the waveforms of CNV in the Mastication condition of Experiment 1, but not in Control condition. In addition, there is evidence that mastication might directly affect cognitive processing. Some papers have reported effects of gum-chewing on working memory tasks (Wilkinson et al., 2002; Baker et al., 2004; Stephens and Tunney, 2004; Hirano et al., 2008). For instance, Baker et al. (2004) reported that gum-chewing during the encoding of a word list improved recall performance. Hirano et al. (2008), using functional magnetic resonance imaging (fMRI), showed more predominant neuronal activities in the PM, precuneus, thalamus, hippocampus, and inferior parietal lobule (IPL) during n-back tasks after gum-chewing. They suggested that gum-chewing accelerated or recovered the working memory process, including an arousal effect of the chewing motion, consequently enhancing cognitive performance. These studies would support our results that mastication affected the amplitude of CNV rather than that of MRCPs, and directly affected cognitive function. A second explanation is an effect of motor-related activities elicited by mastication. Repetitive electrical stimulation of a certain area of the cerebral cortex induces rhythmic jaw movements in many species, including monkeys (Lund and Lamarre, 1974; Huang et al., 1989), cats (Nakamura and Kubo, 1978; Iwata
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et al., 1985), guinea pigs (Goldberg and Tal, 1978; Nozaki et al., 1986), and rabbits (Lund et al., 1984; Liu et al., 1993). Such rhythmic jaw movements along with coordinated rhythmic movements of the tongue and facial organs as well as the secretion of saliva are called fictive mastication, and the cortical regions involved are termed the ‘cortical masticatory area (CMA)’ (Nakamura and Katakura, 1995; Yamada et al., 2005). At present, the descending input from the CMA has been considered the major source generating and activating the masticatory CPG (Nakamura and Katakura, 1995). The CMA includes several cortical regions, such as the face MI, the face SI, the area immediately lateral to the face MI, and an area deep in the CMA on the inner surface of the frontal operculum (Huang et al., 1989). Recent neuroimaging studies using fMRI and positron emission tomography (PET) have also found a neural network involving the MI, SI, SMA, PM, PFC, insula, posterior parietal cortex (PPC), thalamus, striatum, and cerebellum (Momose et al., 1997; Onozuka et al., 2002; Tamura et al., 2003; Takada and Miyamoto, 2004). Therefore, the sequential activities generated from the neural network including the CMA may affect the global neural activities in the brain. Of course, there is a possibility that more than one of the above explanations apply. In conclusion, this is the first study to investigate the effect of mastication on CNV and MRCPs relating to motor preparation. As a result, an effect was found on CNV, but not MRCPs, suggesting that mastication mainly affected non-motor or cognitive aspects of the CNV, rather than specifically motor preparation. These results provide evidence concerning the mechanisms for the effect of mastication on the human brain. They may also help to distinguish between CNV and MRCPs. Acknowledgement We are very grateful to Mr. Y. Takeshima for technical support during this study. References Baker, J.R., Bezance, J.B., Zellaby, E., Aggleton, J.P., 2004. Chewing gum can produce context-dependent effects upon memory. Appetite 43, 207–210. Baresˇ, M., Rektor, I., 2001. Basal ganglia involvement in sensory and cognitive processing. A depth electrode CNV study in human subjects. Clin. Neurophysiol. 112, 2022–2030. ˇ ovsky´, P., Streitova´, H., 2003. Cortical and subcortical Baresˇ, M., Rektor, I., Kan distribution of middle and long latency auditory and visual evoked potentials in a cognitive (CNV) paradigm. Clin. Neurophysiol. 114, 2447–2460. Beisteiner, R., Gartus, A., Erdler, M., Mayer, D., Lanzenberger, R., Deecke, L., 2004. Magnetoencephalography indicates finger motor somatotopy. Eur. J. Neurosci. 19, 465–472. Brunia, C.H.M., 1988. Movement and stimulus preceding negativity. Biol. Psychol. 26, 165–178. Chu, N.S., 1994. Effect of betel chewing on performance reaction time. J. Formos. Med. Assoc. 93, 343–345. Cui, R.Q., Egkher, A., Huter, D., Lang, W., Lindinger, G., Deecke, L., 2000. High resolution spatiotemporal analysis of the contingent negative variation in simple or complex motor tasks and a non-motor task. Clin. Neurophysiol. 111, 1847–1859. Dietz, V., 2003. Spinal cord pattern generators for locomotion. Clin. Neurophysiol. 114, 1379–1389. Donchin, E., Otto, D., Gerbrandt, L.K., Pribram, K.H., 1971. While a monkey waits: electrocortical events recorded during the foreperiod of a reaction time study. Electroencephalogr. Clin. Neurophysiol. 31, 115–127. Doucet, C., Stelmack, M.R., 1999. The effect of response execution on P3 latency, reaction time, and movement time. Psychophysiology 36, 351–363. Elbert, T., Rockstroh, B., Hampson, S., Pantev, C., Hoke, M., 1994. The magnetic counterpart of the contingent negative variation. Electroencephalogr. Clin. Neurophysiol. 92, 262–272. Endo, T., Tezuka, S., Sato, Y., 1982. An experimental study of a preventive measure against drowsiness in a car driving. J. Transport. Med. 36, 195–204 (in Japanese). Fenwick, P.B.C., Ioannides, A.A., Fenton, G.W., Lumsden, J., Grummich, P., Kober, H., Daun, A., Vieth, J., 1993. Estimates of brain activity using magnetic field tomography in a GO/NOGO avoidance paradigm. Brain Topogr. 5, 275–282. Gemba, H., Sasaki, K., Tsujimoto, T., 1990. Cortical field potentials associated with hand movements triggered by warning and imperative stimuli in the monkey. Neurosci. Lett. 113, 275–280.
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