Takafumi Kato

Neurobiological Mechanisms Involved in Sleep Bruxism

Sleep bruxism (SB) is reported by 8% of the adult population and is mainly associated with rhythmic masticatory muscle activity (RMMA) characterized by repetitive jaw muscle contractions (3 bursts or more at a frequency of 1 Hz). The consequences of SB may include tooth destruction, jaw pain, headaches, or the limitation of mandibular movement, as well as tooth-grinding sounds that disrupt the sleep of bed partners. SB is probably an extreme manifestation of a masticatory muscle activity occurring during the sleep of most normal subjects, since RMMA is observed in 60% of normal sleepers in the absence of grinding sounds. The pathophysiology of SB is becoming clearer, and there is an abundance of evidence outlining the neurophysiology and neurochemistry of rhythmic jaw movements (RJM) in relation to chewing, swallowing, and breathing. The sleep literature provides much evidence describing the mechanisms involved in the reduction of muscle tone, from sleep onset to the atonia that characterizes rapid eye movement (REM) sleep. Several brainstem structures (e.g., reticular pontis oralis, pontis caudalis, parvocellularis) and neurochemicals (e.g., serotonin, dopamine, gamma aminobutyric acid [GABA], noradrenaline) are involved in both the genesis of RJM and the modulation of muscle tone during sleep. It remains unknown why a high percentage of normal subjects present RMMA during sleep and why this activity is three times more frequent and higher in amplitude in SB patients. It is also unclear why RMMA during sleep is characterized by co-activation of both jaw-opening and jaw-closing muscles instead of the alternating jaw-opening and jaw-closing muscle activity pattern typical of chewing. The final section of this review proposes that RMMA during sleep has a role in lubricating the upper alimentary tract and increasing airway patency. The review concludes with an outline of questions for future research.

Sleep Bruxism: An Oromotor Activity Secondary to Micro-arousal:

Spontaneous rhythmic masticatory muscle activity (RMMA) during sleep occurs in relation to transient activation in the cerebral and autonomic nervous systems of normal subjects and in patients with sleep bruxism (SB). In this study, we made a quantitative assessment of the sequential changes in cortical electroencephalographic (EEG) and autonomic-cardiac activities associated with micro-arousals preceding RMMA episodes. We matched 10 SB patients with 10 normal subjects. The onset of RMMA episodes was defined in terms of the onset of activation in the suprahyoid muscles. In SB patients, an increase in cortical EEG activity was observed 4 seconds before the onset of suprahyoid activity in 79% of episodes. A significant acceleration in heart rate was initiated one cardiac cycle before RMMA onset. A clear sequence of cortical to autonomic-cardiac activation precedes jaw motor activity in SB patients. This suggests that SB is a powerful oromotor manifestation secondary to micro-arousal.

Rhythmic Masticatory Muscle Activity during Sleep in Humans

Rhythmic Masticatory Muscle Activity (RMMA) is frequently observed during sleep in normal subjects and sleep bruxers. We hypothesized that some normal subjects exhibit RMMA at a lower frequency than sleep bruxers. Polysomnographic data from 82 normal subjects were compared with data from 33 sleep bruxers. RMMA episodes were defined as three or more consecutive bursts of masseter EMG activity, with or without tooth-grinding. Such episodes were observed in nearly 60% of normal subjects. A lower frequency of episodes was noted in normal subjects than in bruxers. Sleep organization was similar between groups. Bruxers had twice as many masseter muscle bursts per episode and episodes of higher amplitude compared with controls with RMMA. The high prevalence of RMMA observed in normal subjects suggests that this activity is related to certain sleep-related physiological functions, including autonomic activation.

Evidence that Experimentally Induced Sleep Bruxism is a Consequence of Transient Arousal

Spontaneous rhythmic masticatory muscle activity (RMMA) during sleep occurs more frequently following spontaneous transient micro-arousal in patients with sleep bruxism (SB) and normal controls. Here, we tested the hypothesis that an experimental arousal would be followed by an increase in RMMA. We identified RMMA on polygraphic recordings taken before and after sensory stimulation to induce experimental arousal in eight SB patients and eight matched normal subjects. The rate of experimental arousal and the level of resting electromyographic activity in masseter and suprahyoid muscles during sleep did not differ between the groups. In both, muscle tone and heart rate increased during the experimental arousal. Although post-arousal RMMA occurred in all SB patients, it was seen in only one normal subject. Moreover, tooth-grinding occurred during 71% of the evoked RMMA in SB patients. These results support the hypothesis that SB is an exaggerated form of oromotor activity associated with sleep micro-arousal.

Sleep bruxism is associated to micro-arousals and an increase in cardiac sympathetic activity

Sleep bruxism (SB) subjects show a higher incidence of rhythmic masticatory muscle activity (RMMA) than control subjects. RMMA is associated with sleep micro‐arousals. This study aims to: (i) assess RMMA/SB episodes in relation to sleep cycles; (ii) establish if RMMA/SB and micro‐arousals occur in relation to the slow wave activity (SWA) dynamics; (iii) analyze the association between RMMA/SB and autonomic cardiac activity across sleep cycles. Two nights of polygraphic recordings were made in three study groups (20 subjects each): moderate to high SB, low SB and control. RMMA episodes were considered to occur in clusters when several groups of RMMA or non‐specific oromotor episodes were separated by less than 100 s. Correlations between sleep, RMMA/SB index and heart rate variability variables were assessed for the first four sleep cycles of each study group. Statistical analyses were done with SYSTAT and SPSS. It was observed that 75.8% of all RMMA/SB episodes occurred in clusters. Micro‐arousal and SB indexes were highest during sleep cycles 2 and 3 (P < 0.001). Within each cycle, micro‐arousal and RMMA/SB indexes showed an increase before each REM sleep (P ≤ 0.02). The cross‐correlation plot for micro‐arousal index showed positive association from 4 min preceding SB onset in the moderate to high SB subjects (P ≤ 0.06). The cross‐correlation plot revealed that SWA decreases following SB onset (P ≤ 0.05). Further cross‐correlation analysis revealed that a shift in sympatho‐vagal balance towards increased sympathetic activity started 8 min preceding SB onset (P ≤ 0.03). In moderate to severe SB subjects, a clear increase in sympathetic activity precedes SB onset.

Experimental pain perception remains equally active over all sleep stages

&NA; The literature on sensory perception during sleep suggests that light sleep (Stage 2) is more responsive to external sensory stimulation (e.g. sound, electrical shock) than deep sleep (Stages 3 and 4) and REM sleep. The main objective of this study was to characterize the specificity of nociceptive stimulation to trigger sleep arousal–awakening over all sleep stages. Thirteen healthy adults (e.g. without pain or sleep problems; six female and seven male of a mean age of 24.2±1.3 years) were included in the study. The responses to noxious intramuscular 5% hypertonic infusion were compared to innocuous vibrotactile and to respective control stimulations: isotonic infusion and auditory stimulations. These stimulations were applied during wakefulness and were repeated during sleep. Polygraphic signals (e.g. brain activity, heart rate) signals were recorded to score sleep arousal over all sleep stages. A subjective assessment of sleep quality was made on next morning. No overnight sensitization or habituation occurred with any of the experimental stimulations. The vibratory–auditory stimulations and the noxious hypertonic infusions triggered significantly (P<0.05) more awakenings in sleep Stage 2 and in REM than their respective control stimulations. In sleep Stage 2, both vibratory+auditory stimulations and the noxious hypertonic infusions has the same awakening response frequency (≈30%), however, with the noxious infusions the response frequency were similar in sleep Stages 3 and 4 (P<0.05) and in REM (trend). Compared to the baseline night, sleep quality was lower following the night with noxious stimulation (90.1±2.7 and 73.3±7.4 mm, respectively; P<0.03). These data suggest that pain during sleep could trigger a sleep awaking response over all sleep stages and not only in light sleep.

Idiopathic myoclonus in the oromandibular region during sleep: a possible source of confusion in sleep bruxism diagnosis.

As part of a larger study, polysomnographic and audiovisual data were recorded over 2 nights in 41 subjects with a clinical diagnosis of sleep bruxism (SB). Electromyographic (EMG) events related to SB were scored according to standard criteria (Lavigne et al. J Dent Res 1996;75:546–552). Post hoc analysis revealed that rapid shock‐like contractions with the characteristics of myoclonus in the jaw muscles were observed in four subjects. EMG bursts characterized as myoclonus were significantly shorter in duration than bursts classified as SB. None of the subjects had any history of myoclonus while awake. Myoclonic episodes were more frequent in sleep stages 1 and 2 than in REM. Half of the episodes contained one or two contractions whereas the other half had three or more repetitive contractions. SB and myoclonus coexisted in one subject. To rule out sleep epilepsy, full electroencephalogram montage was done in three subjects and no epileptic spikes were noted. Our results suggest that approximately 10% of subjects clinically diagnosed as SB could present oromandibular myoclonus during sleep.

Experimentally induced arousals during sleep: a cross-modality matching paradigm

Micro‐arousals occur spontaneously or in response to exogenous and endogenous sensory input during sleep. The function of micro‐arousals remains unclear, for example, whether it reflects a disturbance or a preparatory response to environmental changes. The goal of this study was to assess arousal responsiveness when two types of sensory stimulations were used: auditory (AD) alone and the addition of a vibrotactile (VT) sensation. Ten normal sleepers participated in three nights of polygraphic recordings. The first night was for habituation and to rule out sleep disorders, and the second to collect baseline sleep data. During the third night, AD and VT + AD stimuli, with three levels of intensities for auditory and vibratory signals, were randomly given to induce arousal responses in sleep stages 2, 3 and 4 and rapid eye movement (REM). The frequency of the arousal responses increased with stimulus intensity for all sleep stages and was lowest in stages 3 and 4. In non‐REM (NREM) sleep, combined VT + AD stimulation induced more frequent and more intense arousal responses than AD alone. In REM sleep, more frequent micro‐arousals rather than awakenings were triggered by combined stimulations. In stage 2, the response rate of total induced K‐complexes did not differ between both types of stimulations while more K‐complexes followed by arousals were evoked by the combined VT + AD stimulation than by the AD alone. The induced arousals were associated with an increase in heart rate in all sleep stages. An increase in suprahyoid muscle tone was observed in NREM sleep only, REM being not associated with a rise in muscle tone following experimental stimulation. Most leg and body movements occurred in response to induced awakenings. These results suggest that the cross‐modality sensory stimuli triggered more arousal responses in comparison with single‐modality stimuli. In an attempt to wake a sleeping subject, the addition of a tactile stimulation, such as shaking the shoulder, is an effective strategy that increases the arousal probability.

Lower number of K-complexes and K-alphas in sleep bruxism: a controlled quantitative study

OBJECTIVES Although patients with sleep bruxism (SB) show a higher incidence of rhythmic masticatory muscle activity (RMMA) during sleep than matched normal controls, they are good sleepers. Sleep macrostructure (e.g. total sleep time, sleep latency, number of awakenings or sleep stage shifts and sleep stage duration) is similar between groups. Differences in sleep microstructure between SB patients and normals have been investigated only in few studies. The aim of the present study was to quantify number of microarousals, K-complexes, K-alphas, EEG spindles, and the density of slow wave activity, in both groups, in order to better understand the pathophysiology of SB. METHODS Ten normal sleepers were matched for age and gender with 10 patients who exhibited frequent tooth-grinding during sleep. Using quantitative polysomnographic measures, we compared the above-mentioned sleep variables in both groups. Data are presented as indices for total sleep and for consecutive non-rapid eye movement (non-REM) episodes over non-REM to rapid eye movement (REM) cycles and per hour of sleep. RESULTS SB patients showed 6 times more RMMA episodes per hour of sleep than normals (P<0.001), with a higher frequency in the second and third non-REM to REM cycles. SB patients presented 42.7% fewer K-complexes per hour of stage 2 sleep, but only normals showed a decline from the first to fourth non-REM episode. Only 24% of SB-RMMA episodes were associated with K-complexes in 60 s. The number of K-alphas was 61% lower in SB patients, no change across non-REM episodes was noted. While no difference in electroencephalographic (EEG) spindles or slow wave activity (SWA) was observed between groups, EEG spindles increased and SWA decreased linearly over consecutive non-REM to REM cycles. CONCLUSIONS According to our observations, good sleep in SB patients is characterized by a low incidence of K-complexes or K-alphas and by the absence of any difference in other sleep microstructure variables or SWA.

Quantitative analysis of surface EMG activity of cranial and leg muscles across sleep stages in human.

OBJECTIVE The aim of this study was to make a quantitative analysis of the changes in cranial and limb muscle activity from wakefulness to light and deep sleep stages and during rapid eye movement (REM) sleep of normal subjects. METHODS Polysomnographic recordings were made of the sleep of 9 healthy human subjects, including electromyograms of the suprahyoid, temporalis and masseter cranial muscles and the anterior tibialis limb muscle. Quantitative assessments of EMG activity were carried out with root mean square (RMS) and frequency-spectral analysis (FSA) methods. RESULTS From wakefulness to sleep, a significant reduction (-25.2 to -71.2%; P < 0.01) was observed in EMG activity (for both RMS and FSA) of the 3 cranial muscles using both methods of analysis. The EMG activity of suprahyoid muscle further decreased from non-REM to REM sleep (-17.8 to -43.0%; P < 0.01). In contrast, the EMG activity of the anterior tibialis muscle was only slightly reduced across sleep stages and did not further reduce during REM sleep. During REM sleep, all the 4 muscles maintained minimal activity. CONCLUSIONS The maintenance of muscle activity during REM sleep suggests that a minimal level of activity is required to preserve physiological functions (e.g. airway patency, posture) related to homeostasis and bodily protection. SIGNIFICANCE This study suggests that quantitative sleep EMG analysis is important for understanding the mechanisms of sleep-related movement disorders or when objective assessment of changes in EMG activity are needed for diagnostic purposes or for the assessment of drug efficiency.