Ó 2013 Eur J Oral Sci
Eur J Oral Sci 2014; 122: 42–48 DOI: 10.1111/eos.12101 Printed in Singapore. All rights reserved
European Journal of Oral Sciences
Repeated clenching causes plasticity in corticomotor control of jaw muscles Iida T, Komiyama O, Obara R, Baad-Hansen L, Kawara M, Svensson P. Repeated clenching causes plasticity in corticomotor control of jaw muscles. Eur J Oral Sci 2014; 122: 42–48. © 2013 Eur J Oral Sci This study tested the effect of short-term tooth-clenching on corticomotor excitability of the masseter muscle using transcranial magnetic stimulation (TMS). Fifteen subjects with normal stomatognathic function participated. All subjects performed a tooth-clenching task (TCT) on five consecutive days. The TCT consisted of 10, 20, and 40% of maximum voluntary contraction in a randomized order within 1 h. All subjects underwent TMS in four sessions: pretask day 1 (baseline), post-task day 1, pretask day 5, and post-task day 5. Motor-evoked potentials (MEPs) from the masseter and the first dorsal interosseous (FDI) muscles were obtained using TMS in four sessions. Motor thresholds decreased, after the TCT, for the masseter muscle MEPs. Masseter muscle MEPs were dependent on stimulus intensity and on session, whereas FDI muscle MEPs were only dependent on stimulus intensity. Post-hoc Tukey tests demonstrated significantly higher masseter muscle MEPs post-task on day 5 with 80 and 90% stimulus intensity and above when compared with pre- and post-task day 1 values. Our results suggest that the performance of repeated TCTs can trigger neuroplastic changes in the corticomotor control of the jaw-closing muscles and that such neuroplastic changes may contribute to the mechanism underlying the clinical manifestations of tooth clenching.
It is well known that the cortical control of the jaw motor system allows a fine control and accurate coordination of jaw movements in both animals and humans (1–5). Focal transcranial magnetic stimulation (TMS) with a figure-of eight coil of the primary motor cortex (M1) evokes bilateral responses in masseter muscles and provides conclusive proof of bilateral corticobulbar projections to the human trigeminal motoneuron pools (6– 11). In a TMS study using a tooth-clenching task (TCT), JABERZADEH et al. (12) compared features of the masseter cortical silent period evoked by TMS with previous reports from limb and other cranial muscles and suggested that intracortical inhibitory circuits have a relatively weak effect on corticotrigeminal neurons supplying the masseter muscle. Thus, TMS has been used to characterize the corticomotor control of the jaw muscles, but less is known about the influence of repeated TCTs (i.e. several days of simple motor exercise). TYC & BOYADJIAN (13) suggested that training of a coordinated movement involving several muscles and joints requires an activity-dependent coupling of cortical networks. In addition, CLASSEN et al. (14) suggested that training rapidly and transiently establishes a change in the cortical network representing the thumb, which encodes kinematic details of the practiced movement. In monkeys, SESSLE et al. (15, 16) have demonstrated neuroplasticity in the face M1 evoked by training of a
Takashi Iida1,2, Osamu Komiyama1, Ryoko Obara1, Lene Baad-Hansen2, Misao Kawara1, Peter Svensson2,3 1
Department of Oral Function and Rehabilitation, Nihon University School of Dentistry at Matsudo, Matsudo, Chiba, Japan; 2 Clinical Oral Physiology, Department of Dentistry, Aarhus University, Aarhus; 3Center for Functionally Integrative Neuroscience, Mind Laboratory, Aarhus University Hospital, Aarhus, Denmark
Takashi Iida, Department of Oral Function and Rehabilitation, Nihon University School of Dentistry at Matsudo, 2-870-1, Sakaechonishi, Matsudo, Chiba 271-8587, Japan E-mail: [email protected] Key words: corticomotor control; motor learning; neuroplasticity; transcranial magnetic stimulation; trigeminal physiology Accepted for publication September 2013
novel tongue-protrusion task . In accordance with these observations in animals, our previous studies showed that a specific plasticity of the corticomotor excitability related to the tongue motor control can be induced when human participants learn to perform tongue-protrusion tasks successfully (17–19). For jaw movements, our recent behavioral study compared the influence of visual feedback in spinal and trigeminal muscle activity between tooth clenching and finger-pinch training and suggested that short-term neuroplasticity of the corticomotor pathways related to the jaw muscles seem to occur with short-term tooth clenching training and to a similar extent with finger-pinch training in humans (20). HELLMANN et al. (21) also compared masticatory muscle activity during long-term jaw-movement training for 10 wk using electromygraphy. They found that, as a result of motor adaptations, the electromygraphic activity of masticatory muscle after 10 wk of training was significantly lower than before training (21). Although some studies investigated the relationship between the central nervous system and tooth clenching (22–24), there is currently little information on the effect of several days of repeated TCTs on the central nervous system related to the jaw muscles. The hypothesis of the present study was that repeated tooth clenching could trigger neuroplastic changes in the central nervous system. In this
Clenching causes plasticity in corticomotor
perspective it is therefore of interest to determine the effect of repeated and standardized TCTs on corticomotor excitability, as assessed using motor-evoked potentials (MEPs), in the masseter muscle with the use of TMS.
Material and methods Subjects The study was carried out in 15 volunteers (seven women and eight men; mean age standard error of the mean = 24.9 1.1 yr). All subjects had complete dentition (except for the third molars) and normal occlusion according to the Angle classification method. No participant reported any neurological disorders or abnormalities in stomatognathic function, based on a medical and dental history including standard questionnaires and an oral examination. Informed consent was obtained from all subjects before the start of the experiment. This protocol was approved by the Local Ethics Committee in Central Denmark Region Denmark (20110101), based on the guidelines set forth in the Declaration of Helsinki. The subjects were excluded if they had epilepsy, metal implants in the head, a pacemaker, an implanted medicine pump, or if they were pregnant (25). Tooth clenching task All participants performed a standardized TCT, which was repeated for five consecutive days (Fig. 1A). During the TCT, participants were instructed to clench their teeth or rest at a given auditory signal. Each day, participants performed a maximum TCT to determine the 100% maximum voluntary contraction (MVC) before the TCT. In the first and third series, participants received no visual feedback but were simply instructed to target different force levels. During the second series, visual feedback of the muscle activity level, via the electromygraphic data, was displayed to the subjects on a monitor. One series consisted of three measurements (10, 20, and 40% of the MVC), and one measurement consisted of one force level (10, 20, or 40% of the MVC) in randomized order (Fig. 1B). During all measurements, participants alternated between a 30-s rest block and a 30-s task block for 360 s (Fig. 1C). In the task block, participants alternated between a 5-s rest block and a 5-s task block, at a given auditory signal. The rationale for this design was the possibility to apply this type of masticatory muscle activation in subsequent functional magnetic resonance imaging (MRI) studies. To avoid masticatory muscle fatigue, there was a 30-s rest period between each series. Thus, participants performed TCTs for a total of 58 min each day. All subjects were instructed to keep the lower jaw in a natural and relaxed position with teeth apart during the rest blocks of the TCTs and to keep the hand in a natural and relaxed position during the TCT.
Electromyographic measurement The electromyographic activity from the right first dorsal interosseous (FDI), left masseter (LM), and right masseter (RM) muscles was recorded using disposable bipolar surface electrodes (Neuroline 720; Ambu, Copenhagen, Denmark).
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The surface electrodes were placed, 10-mm apart, over the hand on the FDI. In the jaw, the surface electromyographic electrodes were placed 10-mm apart along the central part of the muscle, midway between the anterior and posterior borders and the superior and inferior borders of the LM and RM muscles. The electromyographic signals were amplified 5,000 times (Disa 15C01; DISA Electronik, Skovlunde, Denmark) and filtered in the bandwidth 10 Hz to 1 kHz for offline analysis. The electromyographic activity during epochs of 5 s was quantified by calculation of the root-mean-square (RMS) amplitude from LM and RM muscles. To evaluate the performance each day, the coefficient of determination (r2; CD) and the slope of the target force level–electromygraphy curve from LM and RM muscles was calculated for each day for all subjects.
Recording of the MEP This part of the study consisted of four sessions of TMS and MEP measurements: first session, before the TCTs on the first day (pretask day 1); second session, 5 min after the TCTs on the first day (post-task day 1); third session, before the TCTs on the fifth day (pretask day 5); and fourth session, 5 min after the TCTs on the fifth day (post-task day 5; Fig. 1A). During TMS measurement, the subjects sat upright and relaxed in a dental chair with the head supported by a headrest. Electromygraphic activity was recorded from the RM and the right FDI muscles through the same electromygraphic electrodes placed for the TCTs. During the recording of the MEPs, subjects kept a special biting device between the anterior teeth in order to ensure constant pre-activation of the masseter muscles, which is required to elicit a MEP (8, 26). The biting device was calibrated to 10 N when the two parts were in contact, thus providing the subject with feedback on the targeted biteforce level. The electromygraphic signals were recorded, bandpassfiltered (10 Hz to 5 kHz), and stored on a Viking electromyograph (Viasys Healthcare, Madison, WI, USA). The TMS was performed using a Magstim 200 stimulator (Magstim, Whitland, Dyfed, UK) and a focal figure-ofeight stimulating coil. A flexible cap was placed over the head in a standardized way based on anatomical markers and in accordance with the International 10–20 Electrode Placement System (27). A co-ordinate system with a 1-cm solution was drawn on the cap. The coil of the stimulator was oriented 45° obliquely to the sagittal midline, so that the induced current flowed in a plane perpendicular to the estimated alignment of the central sulcus. Three markings on the coil helped to identify the position in relation to the scalp sites. The scalp sites at which electromygraphic responses were evoked in the masseter or FDI muscles at the lowest stimulus strength were determined. The motor threshold was measured and was defined as the lowest stimulus intensity that produced five out of 10 discrete MEPs clearly discernible from the background electromygraphic activity (17, 18). The MEPs were assessed in two ways: using a stimulus–response curve; and using a motor cortex map. Stimulus–response curves were constructed in increments of 10% of the motor threshold, from 30% up to a maximum of 90% of the maximum TMS stimulator output. Twelve stimuli were presented at each stimulus level with an interstimulus interval of 10–15 s. For motor cortex mapping, TMS stimuli were delivered at the sites over the scalp identified by the snugly fitting,
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Iida et al. trode placement system. The stimulator output was set at 20% above the motor threshold, and 12 stimuli were delivered to each site. The grid was stimulated in a fixed pattern, beginning at the center of the hot spot and then moving anterior, then posterior, at increasing and decreasing latitudes (the sites typically covered 5 cm from the vertex and 5 cm anterior and posterior to the interaural line, corresponding to 25 grids). Position Cz was defined as the center spot (X = 0, Y = 0). The MEP areas (cm2) of the masseter and FDI maps with MEP amplitudes greater than 10 lV (masseter) and 50 lV (FDI), respectively, were determined on the 1 9 1-cm grid. The center of gravity (COG) was calculated in accordance with RIDDING et al. (29). For TMS data analysis, the stimulus–response curves and motor cortex mapping were performed at four sessions: pre- and post-task day 1 and day 5.
A
B
Statistics All data were presented as mean values and standard errors of the mean. The electromygraphic RMS values during MVC were compared between the first and the fifth days using a paired t-test. The CDs calculated from the target force–actual force curve were analyzed using twoway ANOVA, with LM and RM muscles and session as repeated measures. The onset latencies of the masseter and FDI-MEPs at motor threshold in each session were analyzed using repeated-measures one-way ANOVA (RM-ANOVA). The motor thresholds of the masseter and FDI muscle MEPs in each session were analyzed using RMANOVA. The MEP amplitudes were analyzed using two-way ANOVA with stimulus intensity (percentage of maximum output) and task session (pre- and post-task day 1 and day 5) as factors. The COG measures and MEP areas were analyzed using RM-ANOVAs. When appropriate, the ANOVAs were followed by post-hoc Tukey tests to compensate for multiple comparisons. P values less than 0.05 were considered as statistically significant.
C
Results Fig. 1. (A) Overview of the study design. (B) Overview of the tooth clenching task. (C) Details of the tooth clenching task. MVC, maximum voluntary contraction; TMS, transcranial magnetic stimulation; VF, visual feedback.
flexible cap marked with the 1 9 1-cm grid in an anterior– posterior and lateral–medial coordinate system (28). The anterior–posterior grid lines were related to the vertex (Cz) in accordance with the 10–20 electroencephalographic elec-
Performance of the TCT
Table 1 shows electromyographic RMS values during MVC at the first and fifth days and CDs calculated from the target force–actual force curve in four sessions. All participants completed the 5 d of repeated submaximal contractions. There was no significant difference in the electromyographic RMS values during
Table 1 Electromyographic root-mean-square (EMG-RMS) values during maximum voluntary contraction (MVC) on Day 1 and Day 5, and coefficient of determination (CD) values calculated from the target force–actual force curve in four sessions EMG-RMS value during MVC (lV) Muscle type LM RM
Day 1
Day 5
1.21 0.27 1.14 0.30
1.28 0.29 1.07 0.06
LM, left masseter; RM, right masseter. *P < 0.05 compared with pretask day 1.
CD (r2) Pretask day 1
Post-task day 1
Pretask day 5
Post-task day 5
0.84 0.10 0.83 0.05
0.91 0.03* 0.92 0.03*
0.88 0.03* 0.09 0.03*
0.95 0.01* 0.96 0.03*
Clenching causes plasticity in corticomotor
MVC between the first and fifth days (P = 0.164; t-test). The CDs calculated from the target force–actual force curve were significantly different between the four sessions (P < 0.001; two-way ANOVA) and the CDs at pretask day 1 were significantly lower than the CDs at all other sessions (P < 0.05; Tukey), indicating improvement of the linear relationship between target force and actual force values. MEP recordings
The motor thresholds for the masseter MEPs at pretask day 1, post-task day 1, pretask day 5, and post-task day 5 were 39.3 2.3, 37.9 2.8, 36.4 1.9, and 33.6 1.5%, respectively (P < 0.01; RM-ANOVA) and post-hoc tests demonstrated that the motor thresholds at pre- and post-task day 5 were significantly lower than that at pre-task day 1 (P < 0.05; Tukey). The motor thresholds for the FDI-MEPs at pretask day 1, post-task day 1, pretask day 5, and post-task day 5 were 37.5 1.3, 35.8 1.5, 36.6 1.4, and 34.2 1.5%, respectively (P = 0.347; RM-ANOVA). The onset latency of the masseter muscle MEPs at pretask day 1, post-task day 1, pretask day 5, and post-task day 5 were 7.4 0.4, 7.4 0.4, 7.0 0.4, and 7.3 0.6 ms, respectively (P = 0.604; RM-ANOVA). The onset latency of the FDI-MEPs at pretask day 1, posttask day 1, pretask day 5, and post-task day 5 were 25.1 0.3, 26.4 0.5, 26.0 0.8, and 25.7 0.3 ms, respectively (P = 0.746; RM-ANOVA).
A
B
Fig. 2. Stimulus–response curves obtained by transcranial magnetic stimulation of the masseter motor cortex (A) and first dorsal interosseous (FDI) motor cortex (B) in 15 subjects. Values represent mean standard error of the mean. *Significantly higher at post-task Day 5 compared with pretask Day 1 and post-task Day 1 (P < 0.01; Tukey).
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Stimulus–response curves
The masseter MEPs were significantly dependent on stimulus intensity (P < 0.001; two-way ANOVA) and on task session (P < 0.001; two-way ANOVA), whereas the FDI-MEPs were dependent on stimulus intensity only (P < 0.001; two-way ANOVA) and not on task session (P = 0.972; two-way ANOVA; Fig. 2). Post-hoc tests demonstrated significantly higher masseter MEPs at post-task day 5 with 80 and 90% stimulus intensity and above when compared with pretask day 1 and post-task day 1 (P < 0.01; Tukey). Motor cortex maps
The masseter MEP areas were significantly different among the four sessions (P < 0.005; RM-ANOVA), with significantly larger areas at pretask (23.9 1.8 cm2) and post-task (24.3 0.5 cm2) day 5 compared with pretask day 1 (20.1 1.9 cm2; P < 0.01; Tukey). In contrast, the FDI-MEP areas were not significantly different between the four sessions (P = 0.318; RM-ANO2 VA; mean areas 8.4 0.4 cm ; Fig. 3). Table 2 shows the COG measures. There were no significant changes over time for any of the COG outcomes.
Discussion This TMS study for the first time demonstrated that repeated and standardized TCTs triggered significant neuroplastic changes in the corticomotor control of jaw-closing muscles but not of a hand muscle. The neuroplastic changes were manifested as a MEP facilitation of the masseter jaw-closing muscle and increased cortical excitability. Previously, we demonstrated specific neuroplasticity in the corticomotor excitability related to tongue muscle control after standardized tongue-protrusion tasks (17–19). Our present study applied a similar experimental design and demonstrated that the motor threshold of the masseter muscle MEP decreased over time, whereas the motor threshold of the FDI-MEP did not change between the four sessions. Moreover the masseter muscle motor cortex maps at day 5 were significantly larger than at day 1, whereas the FDI cortical motor maps were not significantly different between the four sessions. In addition, our present study found no significant changes over time for any of the COG outcomes of masseter MEP. Our MEP findings and hotspot localization are consistent with recent data on the motor threshold, onset latency, and motor cortex maps of the MEPs elicited by TMS in the tongue musculature (17, 18). Changes in the input/output curve over a period of time may be caused either by changes in the distribution of excitability in the corticospinal system or by changes in the spatial distribution of excitable elements in the cortex (30). Some TMS studies demonstrated that TMS maps of the motor cortex change following experimental intervention, and the major effect has been an increase in the size of the map, which may
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Iida et al. Table 2
A
Center of gravity measures from the masseter muscle (MM) and the first dorsal interosseous muscle (FDI) cortical motor maps Center of gravity measure (cm) Site MM Pretask day 1 Post-task day 1 Pretask day 5 Post-task day 5 FDI Pretask day 1 Post-task day 1 Pretask day 5 Post-task day 5
Ant–Post
Lat–Med
Length
2.0 1.9 2.0 2.0
0.1 0.1 0.2 0.1
7.0 7.0 7.0 7.0
0.1 0.1 0.1 0.1
9.9 9.9 9.9 9.9
0.1 0.1 0.1 0.2
1.2 1.4 1.4 1.2
0.1 0.2 0.2 0.1
5.8 5.8 5.8 5.8
0.2 0.2 0.2 0.1
8.3 8.2 8.3 8.3
0.2 0.1 0.2 0.2
Ant–Post, anterior–posterior; Lat–Med, lateral–medial.
B
Fig. 3. Masseter (A) and first dorsal interosseous (FDI; B) motor cortex maps generated in 15 subjects (mean amplitudes) by transcranial magnetic stimulation of multiple scalp sites arranged in a 1 9 1-cm grid. Arrows indicate directions (A, anterior; L, lateral; M, medial; P, posterior). The value zero on the y-axis corresponds to the Cz line (interaural line).
well indicate that there has been an increase in excitability of the corticospinal projection rather than a true reorganization (31–33). CLASSEN et al. (14) showed that repeated practice of an isolated thumb movement could alter the excitability of the corticospinal projections to thumb muscles and demonstrated a shift in cortical excitability produced by natural inputs as use-dependent plasticity. In addition, the change in cortical excitability induced by TMS is believed to represent associative plasticity induced in the motor cortex (34, 35). Thus, the present study also provided evidence of neuroplasticity of the corticomotor excitability of the masseter muscle evoked by a repeated TCT. As the TMS technique used in the present study does not permit a precise delineation of the actual cortical or subcortical regions involved in the plastic changes during the learning of the new motor skill (30), the
degree of subcortical excitability changes induced by standardized TCTs cannot be determined from the present study. In novel tongue-protrusion tasks, ARIMA et al. (19) demonstrated, using functional MRI (fMRI), that areas other than the primary motor area were activated by a tongue-protrusion task. It may be important to investigate further the plasticity of the subcortical excitability affected by standardized TCTs using other neuroimaging techniques using fMRI. On the other hand, SVENSSON et al. (17, 18) showed that tongue-task training is associated with plasticity of corticomotor excitability specifically related to the tongue musculature after 1 h of tongue training. BOUDREAU et al. (36) demonstrated that bidirectional tongue training and multidirectional tongue training differentially altered the excitability of the tongue motor cortex. These studies suggested that neuroplasticity in the motor cortex depends on duration, direction, and force level of the specific motor task. It may be important to investigate, in more detail, the minimum extent of jaw motor tasks that may lead to neuroplasticity of corticomotor excitability related to the jaw musculature. For example, LU et al. (37) have recently demonstrated that a single bout of low-level tooth-clenching activity (10 N) for 1 h, following the same protocol used for the tongue-protrusion task studies, failed to evoke any signs of neuroplasticity related to the control of the masseter muscle. As humans actively and unconsciously may clench their teeth in daily life, we applied a TCT with visual feedback as a passive task to control bite force and a TCT without visual feedback as an active task. Although we did not measure MVC after TCTs each day as a follow-up, we measured MVC before TCTs each day and compared the results obtained on the first day with those obtained on the fifth day. The present study demonstrated that although there was no significant difference in electromyographic RMS values during MVC between the first and the fifth days, there was a significant increase in CDs from pretask day 1
Clenching causes plasticity in corticomotor
to all other sessions, indicating improvements of the linear relationship between target-force and actual force values. HELLMANN et al. (21) also compared masticatory muscle activity during long-term jaw-movement training for 10 wk using electromyography, and they found that masticatory muscle activity was significant lower after 10 wk than before training when the participants produced the same bite force. The present results suggest that the ability to adjust the bite force accurately to different specific target levels after repeated practice may indeed be interpreted as a learning-induced effect. The motor cortical maps in the present study indicated that although FDI motor cortex maps were not significantly different between the four sessions, the FDI motor cortex maps at post-task day 5 tended to be slightly larger compared with pretask day 1 without hand motor training. Although our previous fMRI study showed that the somatotopic locations of sensorimotor cortex activity differed between hand and jaw movement (38), some investigators also demonstrated the effect of tooth clenching on the excitability of the hand motor area (39, 40). However, as our present study applied only a jaw-motor task, we did not expect to see an effect on the corticomotor control of the hand, in accordance with the findings from the tongueprotrusion task studies (17, 18). Further studies are needed to investigate the potential relationship of neuroplasticity in the motor cortices between jaw and other motor systems. BYRD et al. (41) classified participants, with and without parafunctional behavior, by self-reported history, clinical examination, evaluation of dental casts, and positive responses to the temporomandibular disorder history questionnaire, and they compared the cerebral activity during tooth clenching and tooth grinding between the two groups using fMRI. Their results showed significant differences in the cortical and subcortical activation patterns during tooth clenching and tooth grinding between the two groups (41). In addition, WONG et al. (42) also classified participants with and without a tooth-grinding behavior in daily life by self-reported parafunctional clench-and-grind behavior and clinical evidence of abnormal tooth wear and they also compared cerebral activity during tooth clenching between the two groups using fMRI. Their result suggested that the participants without a tooth-grinding behavior showed more extensive activity in the supplementary motor area than did those with a tooth-grinding behavior (42). Thus, these studies suggest that unconscious jaw-motor behavior in patients with sleep or awake bruxism is associated with specific alterations in the central nervous system. The long-term aim of our project is to elucidate mechanisms potentially underlying awake bruxism, which is characterized by frequent tooth clenching. In order to understand the importance of neuroplasticity in clinical conditions such as awake or sleep-related bruxism, it may be important to investigate, in more detail, the plasticity of the corticomotor excitability affected by standardized TCTs between patients with bruxism and normal subjects. In
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addition, this may have implications for jaw motorfunction rehabilitation in patients with acquired brain damage, (such as stroke, or neuromuscular disorders) as a new physiotherapy jaw exercise. In conclusion, our results suggest that the performance of repeated TCTs can trigger neuroplastic changes in the central nervous system, and such neuroplastic changes may contribute to the mechanism underlying the clinical manifestations of tooth clenching. Acknowledgements – The Danish Dental Association is acknowledged for their financial support of the study. Conflicts of interest – All authors declare that there are no conflicts of interest.
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29. RIDDING MC, BROUWER B, MILES TS, PITCHER JB, THOMPSON PD. Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res 2000; 131: 135–143. 30. SIEBNER HR, ROTHWELL J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 2003; 148: 1–16. 31. RIDDING MC, ROTHWELL JC. Reorganisation in human motor cortex. Can J Physiol Pharmacol 1995; 73: 218–222. 32. ZANETTE G, TINAZZI M, BONATO C, DI SUMMA A, MANGANOTTI P, POLO A, FIASCHI A. Reversible changes of motor cortical outputs following immobilization of the upper limb. Electroencephalogr Clin Neurophysiol 1997; 105: 269–279. 33. RIDDING MC, MCKAY DR, THOMPSON PD, MILES TS. Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans. Clin Neurophysiol 2001; 112: 1461–1469. 34. STEFAN K, KUNESCH E, COHEN LG, BENECKE R, CLASSEN J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 2000; 123: 572–584. 35. WOLTERS A, SANDBRINK F, SCHLOTTMANN A, KUNESCH E, STEFAN K, COHEN LG, BENECKE R, CLASSEN J. A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol 2003; 89: 2339–2345. 36. BOUDREAU SA, LONTIS ER, CALTENCO H, SVENSSON P, SESSLE BJ, ANDREASEN STRUIJK LN, ARENDT-NIELSEN L. Features of cortical neuroplasticity associated with multidirectional novel motor skill training: a TMS mapping study. Exp Brain Res 2013; 225: 513–526. 37. LU S, BAAD-HANSEN L, ZHANG Z, SVENSSON P. One hour jaw muscle training does not evoke plasticity in the corticomotor control of the masseter muscle. Arch Oral Biol 2013; 58: 1483–1490. 38. IIDA T, KATO M, KOMIYAMA O, SUZUKI H, ASANO T, KUROKI T, KANEDA T, SVENSSON P, KAWARA M. Comparison of cerebral activity during teeth clenching and fist clenching: a functional magnetic resonance imaging study. Eur J Oral Sci 2010; 118: 635–641. 39. FURUBAYASHI T, SUGAWARA K, KASAI T, HAYASHI A, HANAJIMA R, SHIIO Y, IWATA NK, UGAWA Y. Remote effects of selfpaced teeth clenching on the excitability of hand motor area. Exp Brain Res 2003; 148: 261–265. 40. SUGAWARA K, FURUBAYASHI T, TAKAHASHI M, NI Z, UGAWA Y, KASAI T. Remote effects of voluntary teeth clenching on excitability changes of the human hand motor area. Neurosci Lett 2005; 377: 25–30. 41. BYRD KE, ROMITO LM, DZEMIDZIC M, WONG D, TALAVAGE TM. fMRI study of brain activity elicited by oral parafunctional movements. J Oral Rehabil 2009; 36: 346–361. 42. WONG D, DZEMIDZIC M, TALAVAGE TM, ROMITO LM, BYRD KE. Motor control of jaw movements: an fMRI study of parafunctional clench and grind behavior. Brain Res 2011; 1383: 206–217.
Eur J Oral Sci 2014; 122: 42–48 DOI: 10.1111/eos.12101 Printed in Singapore. All rights reserved
European Journal of Oral Sciences
Repeated clenching causes plasticity in corticomotor control of jaw muscles Iida T, Komiyama O, Obara R, Baad-Hansen L, Kawara M, Svensson P. Repeated clenching causes plasticity in corticomotor control of jaw muscles. Eur J Oral Sci 2014; 122: 42–48. © 2013 Eur J Oral Sci This study tested the effect of short-term tooth-clenching on corticomotor excitability of the masseter muscle using transcranial magnetic stimulation (TMS). Fifteen subjects with normal stomatognathic function participated. All subjects performed a tooth-clenching task (TCT) on five consecutive days. The TCT consisted of 10, 20, and 40% of maximum voluntary contraction in a randomized order within 1 h. All subjects underwent TMS in four sessions: pretask day 1 (baseline), post-task day 1, pretask day 5, and post-task day 5. Motor-evoked potentials (MEPs) from the masseter and the first dorsal interosseous (FDI) muscles were obtained using TMS in four sessions. Motor thresholds decreased, after the TCT, for the masseter muscle MEPs. Masseter muscle MEPs were dependent on stimulus intensity and on session, whereas FDI muscle MEPs were only dependent on stimulus intensity. Post-hoc Tukey tests demonstrated significantly higher masseter muscle MEPs post-task on day 5 with 80 and 90% stimulus intensity and above when compared with pre- and post-task day 1 values. Our results suggest that the performance of repeated TCTs can trigger neuroplastic changes in the corticomotor control of the jaw-closing muscles and that such neuroplastic changes may contribute to the mechanism underlying the clinical manifestations of tooth clenching.
It is well known that the cortical control of the jaw motor system allows a fine control and accurate coordination of jaw movements in both animals and humans (1–5). Focal transcranial magnetic stimulation (TMS) with a figure-of eight coil of the primary motor cortex (M1) evokes bilateral responses in masseter muscles and provides conclusive proof of bilateral corticobulbar projections to the human trigeminal motoneuron pools (6– 11). In a TMS study using a tooth-clenching task (TCT), JABERZADEH et al. (12) compared features of the masseter cortical silent period evoked by TMS with previous reports from limb and other cranial muscles and suggested that intracortical inhibitory circuits have a relatively weak effect on corticotrigeminal neurons supplying the masseter muscle. Thus, TMS has been used to characterize the corticomotor control of the jaw muscles, but less is known about the influence of repeated TCTs (i.e. several days of simple motor exercise). TYC & BOYADJIAN (13) suggested that training of a coordinated movement involving several muscles and joints requires an activity-dependent coupling of cortical networks. In addition, CLASSEN et al. (14) suggested that training rapidly and transiently establishes a change in the cortical network representing the thumb, which encodes kinematic details of the practiced movement. In monkeys, SESSLE et al. (15, 16) have demonstrated neuroplasticity in the face M1 evoked by training of a
Takashi Iida1,2, Osamu Komiyama1, Ryoko Obara1, Lene Baad-Hansen2, Misao Kawara1, Peter Svensson2,3 1
Department of Oral Function and Rehabilitation, Nihon University School of Dentistry at Matsudo, Matsudo, Chiba, Japan; 2 Clinical Oral Physiology, Department of Dentistry, Aarhus University, Aarhus; 3Center for Functionally Integrative Neuroscience, Mind Laboratory, Aarhus University Hospital, Aarhus, Denmark
Takashi Iida, Department of Oral Function and Rehabilitation, Nihon University School of Dentistry at Matsudo, 2-870-1, Sakaechonishi, Matsudo, Chiba 271-8587, Japan E-mail: [email protected] Key words: corticomotor control; motor learning; neuroplasticity; transcranial magnetic stimulation; trigeminal physiology Accepted for publication September 2013
novel tongue-protrusion task . In accordance with these observations in animals, our previous studies showed that a specific plasticity of the corticomotor excitability related to the tongue motor control can be induced when human participants learn to perform tongue-protrusion tasks successfully (17–19). For jaw movements, our recent behavioral study compared the influence of visual feedback in spinal and trigeminal muscle activity between tooth clenching and finger-pinch training and suggested that short-term neuroplasticity of the corticomotor pathways related to the jaw muscles seem to occur with short-term tooth clenching training and to a similar extent with finger-pinch training in humans (20). HELLMANN et al. (21) also compared masticatory muscle activity during long-term jaw-movement training for 10 wk using electromygraphy. They found that, as a result of motor adaptations, the electromygraphic activity of masticatory muscle after 10 wk of training was significantly lower than before training (21). Although some studies investigated the relationship between the central nervous system and tooth clenching (22–24), there is currently little information on the effect of several days of repeated TCTs on the central nervous system related to the jaw muscles. The hypothesis of the present study was that repeated tooth clenching could trigger neuroplastic changes in the central nervous system. In this
Clenching causes plasticity in corticomotor
perspective it is therefore of interest to determine the effect of repeated and standardized TCTs on corticomotor excitability, as assessed using motor-evoked potentials (MEPs), in the masseter muscle with the use of TMS.
Material and methods Subjects The study was carried out in 15 volunteers (seven women and eight men; mean age standard error of the mean = 24.9 1.1 yr). All subjects had complete dentition (except for the third molars) and normal occlusion according to the Angle classification method. No participant reported any neurological disorders or abnormalities in stomatognathic function, based on a medical and dental history including standard questionnaires and an oral examination. Informed consent was obtained from all subjects before the start of the experiment. This protocol was approved by the Local Ethics Committee in Central Denmark Region Denmark (20110101), based on the guidelines set forth in the Declaration of Helsinki. The subjects were excluded if they had epilepsy, metal implants in the head, a pacemaker, an implanted medicine pump, or if they were pregnant (25). Tooth clenching task All participants performed a standardized TCT, which was repeated for five consecutive days (Fig. 1A). During the TCT, participants were instructed to clench their teeth or rest at a given auditory signal. Each day, participants performed a maximum TCT to determine the 100% maximum voluntary contraction (MVC) before the TCT. In the first and third series, participants received no visual feedback but were simply instructed to target different force levels. During the second series, visual feedback of the muscle activity level, via the electromygraphic data, was displayed to the subjects on a monitor. One series consisted of three measurements (10, 20, and 40% of the MVC), and one measurement consisted of one force level (10, 20, or 40% of the MVC) in randomized order (Fig. 1B). During all measurements, participants alternated between a 30-s rest block and a 30-s task block for 360 s (Fig. 1C). In the task block, participants alternated between a 5-s rest block and a 5-s task block, at a given auditory signal. The rationale for this design was the possibility to apply this type of masticatory muscle activation in subsequent functional magnetic resonance imaging (MRI) studies. To avoid masticatory muscle fatigue, there was a 30-s rest period between each series. Thus, participants performed TCTs for a total of 58 min each day. All subjects were instructed to keep the lower jaw in a natural and relaxed position with teeth apart during the rest blocks of the TCTs and to keep the hand in a natural and relaxed position during the TCT.
Electromyographic measurement The electromyographic activity from the right first dorsal interosseous (FDI), left masseter (LM), and right masseter (RM) muscles was recorded using disposable bipolar surface electrodes (Neuroline 720; Ambu, Copenhagen, Denmark).
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The surface electrodes were placed, 10-mm apart, over the hand on the FDI. In the jaw, the surface electromyographic electrodes were placed 10-mm apart along the central part of the muscle, midway between the anterior and posterior borders and the superior and inferior borders of the LM and RM muscles. The electromyographic signals were amplified 5,000 times (Disa 15C01; DISA Electronik, Skovlunde, Denmark) and filtered in the bandwidth 10 Hz to 1 kHz for offline analysis. The electromyographic activity during epochs of 5 s was quantified by calculation of the root-mean-square (RMS) amplitude from LM and RM muscles. To evaluate the performance each day, the coefficient of determination (r2; CD) and the slope of the target force level–electromygraphy curve from LM and RM muscles was calculated for each day for all subjects.
Recording of the MEP This part of the study consisted of four sessions of TMS and MEP measurements: first session, before the TCTs on the first day (pretask day 1); second session, 5 min after the TCTs on the first day (post-task day 1); third session, before the TCTs on the fifth day (pretask day 5); and fourth session, 5 min after the TCTs on the fifth day (post-task day 5; Fig. 1A). During TMS measurement, the subjects sat upright and relaxed in a dental chair with the head supported by a headrest. Electromygraphic activity was recorded from the RM and the right FDI muscles through the same electromygraphic electrodes placed for the TCTs. During the recording of the MEPs, subjects kept a special biting device between the anterior teeth in order to ensure constant pre-activation of the masseter muscles, which is required to elicit a MEP (8, 26). The biting device was calibrated to 10 N when the two parts were in contact, thus providing the subject with feedback on the targeted biteforce level. The electromygraphic signals were recorded, bandpassfiltered (10 Hz to 5 kHz), and stored on a Viking electromyograph (Viasys Healthcare, Madison, WI, USA). The TMS was performed using a Magstim 200 stimulator (Magstim, Whitland, Dyfed, UK) and a focal figure-ofeight stimulating coil. A flexible cap was placed over the head in a standardized way based on anatomical markers and in accordance with the International 10–20 Electrode Placement System (27). A co-ordinate system with a 1-cm solution was drawn on the cap. The coil of the stimulator was oriented 45° obliquely to the sagittal midline, so that the induced current flowed in a plane perpendicular to the estimated alignment of the central sulcus. Three markings on the coil helped to identify the position in relation to the scalp sites. The scalp sites at which electromygraphic responses were evoked in the masseter or FDI muscles at the lowest stimulus strength were determined. The motor threshold was measured and was defined as the lowest stimulus intensity that produced five out of 10 discrete MEPs clearly discernible from the background electromygraphic activity (17, 18). The MEPs were assessed in two ways: using a stimulus–response curve; and using a motor cortex map. Stimulus–response curves were constructed in increments of 10% of the motor threshold, from 30% up to a maximum of 90% of the maximum TMS stimulator output. Twelve stimuli were presented at each stimulus level with an interstimulus interval of 10–15 s. For motor cortex mapping, TMS stimuli were delivered at the sites over the scalp identified by the snugly fitting,
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Iida et al. trode placement system. The stimulator output was set at 20% above the motor threshold, and 12 stimuli were delivered to each site. The grid was stimulated in a fixed pattern, beginning at the center of the hot spot and then moving anterior, then posterior, at increasing and decreasing latitudes (the sites typically covered 5 cm from the vertex and 5 cm anterior and posterior to the interaural line, corresponding to 25 grids). Position Cz was defined as the center spot (X = 0, Y = 0). The MEP areas (cm2) of the masseter and FDI maps with MEP amplitudes greater than 10 lV (masseter) and 50 lV (FDI), respectively, were determined on the 1 9 1-cm grid. The center of gravity (COG) was calculated in accordance with RIDDING et al. (29). For TMS data analysis, the stimulus–response curves and motor cortex mapping were performed at four sessions: pre- and post-task day 1 and day 5.
A
B
Statistics All data were presented as mean values and standard errors of the mean. The electromygraphic RMS values during MVC were compared between the first and the fifth days using a paired t-test. The CDs calculated from the target force–actual force curve were analyzed using twoway ANOVA, with LM and RM muscles and session as repeated measures. The onset latencies of the masseter and FDI-MEPs at motor threshold in each session were analyzed using repeated-measures one-way ANOVA (RM-ANOVA). The motor thresholds of the masseter and FDI muscle MEPs in each session were analyzed using RMANOVA. The MEP amplitudes were analyzed using two-way ANOVA with stimulus intensity (percentage of maximum output) and task session (pre- and post-task day 1 and day 5) as factors. The COG measures and MEP areas were analyzed using RM-ANOVAs. When appropriate, the ANOVAs were followed by post-hoc Tukey tests to compensate for multiple comparisons. P values less than 0.05 were considered as statistically significant.
C
Results Fig. 1. (A) Overview of the study design. (B) Overview of the tooth clenching task. (C) Details of the tooth clenching task. MVC, maximum voluntary contraction; TMS, transcranial magnetic stimulation; VF, visual feedback.
flexible cap marked with the 1 9 1-cm grid in an anterior– posterior and lateral–medial coordinate system (28). The anterior–posterior grid lines were related to the vertex (Cz) in accordance with the 10–20 electroencephalographic elec-
Performance of the TCT
Table 1 shows electromyographic RMS values during MVC at the first and fifth days and CDs calculated from the target force–actual force curve in four sessions. All participants completed the 5 d of repeated submaximal contractions. There was no significant difference in the electromyographic RMS values during
Table 1 Electromyographic root-mean-square (EMG-RMS) values during maximum voluntary contraction (MVC) on Day 1 and Day 5, and coefficient of determination (CD) values calculated from the target force–actual force curve in four sessions EMG-RMS value during MVC (lV) Muscle type LM RM
Day 1
Day 5
1.21 0.27 1.14 0.30
1.28 0.29 1.07 0.06
LM, left masseter; RM, right masseter. *P < 0.05 compared with pretask day 1.
CD (r2) Pretask day 1
Post-task day 1
Pretask day 5
Post-task day 5
0.84 0.10 0.83 0.05
0.91 0.03* 0.92 0.03*
0.88 0.03* 0.09 0.03*
0.95 0.01* 0.96 0.03*
Clenching causes plasticity in corticomotor
MVC between the first and fifth days (P = 0.164; t-test). The CDs calculated from the target force–actual force curve were significantly different between the four sessions (P < 0.001; two-way ANOVA) and the CDs at pretask day 1 were significantly lower than the CDs at all other sessions (P < 0.05; Tukey), indicating improvement of the linear relationship between target force and actual force values. MEP recordings
The motor thresholds for the masseter MEPs at pretask day 1, post-task day 1, pretask day 5, and post-task day 5 were 39.3 2.3, 37.9 2.8, 36.4 1.9, and 33.6 1.5%, respectively (P < 0.01; RM-ANOVA) and post-hoc tests demonstrated that the motor thresholds at pre- and post-task day 5 were significantly lower than that at pre-task day 1 (P < 0.05; Tukey). The motor thresholds for the FDI-MEPs at pretask day 1, post-task day 1, pretask day 5, and post-task day 5 were 37.5 1.3, 35.8 1.5, 36.6 1.4, and 34.2 1.5%, respectively (P = 0.347; RM-ANOVA). The onset latency of the masseter muscle MEPs at pretask day 1, post-task day 1, pretask day 5, and post-task day 5 were 7.4 0.4, 7.4 0.4, 7.0 0.4, and 7.3 0.6 ms, respectively (P = 0.604; RM-ANOVA). The onset latency of the FDI-MEPs at pretask day 1, posttask day 1, pretask day 5, and post-task day 5 were 25.1 0.3, 26.4 0.5, 26.0 0.8, and 25.7 0.3 ms, respectively (P = 0.746; RM-ANOVA).
A
B
Fig. 2. Stimulus–response curves obtained by transcranial magnetic stimulation of the masseter motor cortex (A) and first dorsal interosseous (FDI) motor cortex (B) in 15 subjects. Values represent mean standard error of the mean. *Significantly higher at post-task Day 5 compared with pretask Day 1 and post-task Day 1 (P < 0.01; Tukey).
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Stimulus–response curves
The masseter MEPs were significantly dependent on stimulus intensity (P < 0.001; two-way ANOVA) and on task session (P < 0.001; two-way ANOVA), whereas the FDI-MEPs were dependent on stimulus intensity only (P < 0.001; two-way ANOVA) and not on task session (P = 0.972; two-way ANOVA; Fig. 2). Post-hoc tests demonstrated significantly higher masseter MEPs at post-task day 5 with 80 and 90% stimulus intensity and above when compared with pretask day 1 and post-task day 1 (P < 0.01; Tukey). Motor cortex maps
The masseter MEP areas were significantly different among the four sessions (P < 0.005; RM-ANOVA), with significantly larger areas at pretask (23.9 1.8 cm2) and post-task (24.3 0.5 cm2) day 5 compared with pretask day 1 (20.1 1.9 cm2; P < 0.01; Tukey). In contrast, the FDI-MEP areas were not significantly different between the four sessions (P = 0.318; RM-ANO2 VA; mean areas 8.4 0.4 cm ; Fig. 3). Table 2 shows the COG measures. There were no significant changes over time for any of the COG outcomes.
Discussion This TMS study for the first time demonstrated that repeated and standardized TCTs triggered significant neuroplastic changes in the corticomotor control of jaw-closing muscles but not of a hand muscle. The neuroplastic changes were manifested as a MEP facilitation of the masseter jaw-closing muscle and increased cortical excitability. Previously, we demonstrated specific neuroplasticity in the corticomotor excitability related to tongue muscle control after standardized tongue-protrusion tasks (17–19). Our present study applied a similar experimental design and demonstrated that the motor threshold of the masseter muscle MEP decreased over time, whereas the motor threshold of the FDI-MEP did not change between the four sessions. Moreover the masseter muscle motor cortex maps at day 5 were significantly larger than at day 1, whereas the FDI cortical motor maps were not significantly different between the four sessions. In addition, our present study found no significant changes over time for any of the COG outcomes of masseter MEP. Our MEP findings and hotspot localization are consistent with recent data on the motor threshold, onset latency, and motor cortex maps of the MEPs elicited by TMS in the tongue musculature (17, 18). Changes in the input/output curve over a period of time may be caused either by changes in the distribution of excitability in the corticospinal system or by changes in the spatial distribution of excitable elements in the cortex (30). Some TMS studies demonstrated that TMS maps of the motor cortex change following experimental intervention, and the major effect has been an increase in the size of the map, which may
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Iida et al. Table 2
A
Center of gravity measures from the masseter muscle (MM) and the first dorsal interosseous muscle (FDI) cortical motor maps Center of gravity measure (cm) Site MM Pretask day 1 Post-task day 1 Pretask day 5 Post-task day 5 FDI Pretask day 1 Post-task day 1 Pretask day 5 Post-task day 5
Ant–Post
Lat–Med
Length
2.0 1.9 2.0 2.0
0.1 0.1 0.2 0.1
7.0 7.0 7.0 7.0
0.1 0.1 0.1 0.1
9.9 9.9 9.9 9.9
0.1 0.1 0.1 0.2
1.2 1.4 1.4 1.2
0.1 0.2 0.2 0.1
5.8 5.8 5.8 5.8
0.2 0.2 0.2 0.1
8.3 8.2 8.3 8.3
0.2 0.1 0.2 0.2
Ant–Post, anterior–posterior; Lat–Med, lateral–medial.
B
Fig. 3. Masseter (A) and first dorsal interosseous (FDI; B) motor cortex maps generated in 15 subjects (mean amplitudes) by transcranial magnetic stimulation of multiple scalp sites arranged in a 1 9 1-cm grid. Arrows indicate directions (A, anterior; L, lateral; M, medial; P, posterior). The value zero on the y-axis corresponds to the Cz line (interaural line).
well indicate that there has been an increase in excitability of the corticospinal projection rather than a true reorganization (31–33). CLASSEN et al. (14) showed that repeated practice of an isolated thumb movement could alter the excitability of the corticospinal projections to thumb muscles and demonstrated a shift in cortical excitability produced by natural inputs as use-dependent plasticity. In addition, the change in cortical excitability induced by TMS is believed to represent associative plasticity induced in the motor cortex (34, 35). Thus, the present study also provided evidence of neuroplasticity of the corticomotor excitability of the masseter muscle evoked by a repeated TCT. As the TMS technique used in the present study does not permit a precise delineation of the actual cortical or subcortical regions involved in the plastic changes during the learning of the new motor skill (30), the
degree of subcortical excitability changes induced by standardized TCTs cannot be determined from the present study. In novel tongue-protrusion tasks, ARIMA et al. (19) demonstrated, using functional MRI (fMRI), that areas other than the primary motor area were activated by a tongue-protrusion task. It may be important to investigate further the plasticity of the subcortical excitability affected by standardized TCTs using other neuroimaging techniques using fMRI. On the other hand, SVENSSON et al. (17, 18) showed that tongue-task training is associated with plasticity of corticomotor excitability specifically related to the tongue musculature after 1 h of tongue training. BOUDREAU et al. (36) demonstrated that bidirectional tongue training and multidirectional tongue training differentially altered the excitability of the tongue motor cortex. These studies suggested that neuroplasticity in the motor cortex depends on duration, direction, and force level of the specific motor task. It may be important to investigate, in more detail, the minimum extent of jaw motor tasks that may lead to neuroplasticity of corticomotor excitability related to the jaw musculature. For example, LU et al. (37) have recently demonstrated that a single bout of low-level tooth-clenching activity (10 N) for 1 h, following the same protocol used for the tongue-protrusion task studies, failed to evoke any signs of neuroplasticity related to the control of the masseter muscle. As humans actively and unconsciously may clench their teeth in daily life, we applied a TCT with visual feedback as a passive task to control bite force and a TCT without visual feedback as an active task. Although we did not measure MVC after TCTs each day as a follow-up, we measured MVC before TCTs each day and compared the results obtained on the first day with those obtained on the fifth day. The present study demonstrated that although there was no significant difference in electromyographic RMS values during MVC between the first and the fifth days, there was a significant increase in CDs from pretask day 1
Clenching causes plasticity in corticomotor
to all other sessions, indicating improvements of the linear relationship between target-force and actual force values. HELLMANN et al. (21) also compared masticatory muscle activity during long-term jaw-movement training for 10 wk using electromyography, and they found that masticatory muscle activity was significant lower after 10 wk than before training when the participants produced the same bite force. The present results suggest that the ability to adjust the bite force accurately to different specific target levels after repeated practice may indeed be interpreted as a learning-induced effect. The motor cortical maps in the present study indicated that although FDI motor cortex maps were not significantly different between the four sessions, the FDI motor cortex maps at post-task day 5 tended to be slightly larger compared with pretask day 1 without hand motor training. Although our previous fMRI study showed that the somatotopic locations of sensorimotor cortex activity differed between hand and jaw movement (38), some investigators also demonstrated the effect of tooth clenching on the excitability of the hand motor area (39, 40). However, as our present study applied only a jaw-motor task, we did not expect to see an effect on the corticomotor control of the hand, in accordance with the findings from the tongueprotrusion task studies (17, 18). Further studies are needed to investigate the potential relationship of neuroplasticity in the motor cortices between jaw and other motor systems. BYRD et al. (41) classified participants, with and without parafunctional behavior, by self-reported history, clinical examination, evaluation of dental casts, and positive responses to the temporomandibular disorder history questionnaire, and they compared the cerebral activity during tooth clenching and tooth grinding between the two groups using fMRI. Their results showed significant differences in the cortical and subcortical activation patterns during tooth clenching and tooth grinding between the two groups (41). In addition, WONG et al. (42) also classified participants with and without a tooth-grinding behavior in daily life by self-reported parafunctional clench-and-grind behavior and clinical evidence of abnormal tooth wear and they also compared cerebral activity during tooth clenching between the two groups using fMRI. Their result suggested that the participants without a tooth-grinding behavior showed more extensive activity in the supplementary motor area than did those with a tooth-grinding behavior (42). Thus, these studies suggest that unconscious jaw-motor behavior in patients with sleep or awake bruxism is associated with specific alterations in the central nervous system. The long-term aim of our project is to elucidate mechanisms potentially underlying awake bruxism, which is characterized by frequent tooth clenching. In order to understand the importance of neuroplasticity in clinical conditions such as awake or sleep-related bruxism, it may be important to investigate, in more detail, the plasticity of the corticomotor excitability affected by standardized TCTs between patients with bruxism and normal subjects. In
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addition, this may have implications for jaw motorfunction rehabilitation in patients with acquired brain damage, (such as stroke, or neuromuscular disorders) as a new physiotherapy jaw exercise. In conclusion, our results suggest that the performance of repeated TCTs can trigger neuroplastic changes in the central nervous system, and such neuroplastic changes may contribute to the mechanism underlying the clinical manifestations of tooth clenching. Acknowledgements – The Danish Dental Association is acknowledged for their financial support of the study. Conflicts of interest – All authors declare that there are no conflicts of interest.
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