Rhythmic Jaw Movements Research Articles

Neuronal Activities of the Red Nucleus during Rhythmic Jaw Movements in the Rat

Neuronal Activities of the Red Nucleus during Rhythmic Jaw Movements in the Rat

The physiological and morphological characteristics of interneurons caudal to the trigeminal motor nucleus in rats

In this study we have characterized the membrane properties and morphology of interneurons which lie between the caudal pole of the trigeminal motor nucleus and the rostral border of the facial motor nucleus. Previous studies suggest that many of these interneurons may participate in the genesis of rhythmical jaw movements. Saggital brainstem slices were taken from rats aged 5-8 days. Interneurons lying caudal to the trigeminal motor nucleus were visualized using near-infrared differential interference contrast (DIC) microscopy, and were recorded from using patch pipettes filled with a K-gluconate- and biocytin-based solution. The 127 neurons recorded could be categorized into three subtypes on the basis of their responses to injection of depolarizing current pulses, namely tonic firing (type I), burst firing (type II) and spike-adaptive (type III) neurons. Type I interneurons had a higher input resistance and a lower rheobase than type II neurons. All three neuron subtypes showed 'sag' of the voltage response to injection of large-amplitude hyperpolarizing current pulses, and, in addition, also showed rectification of the voltage response to injection of depolarizing current pulses, with type II neurons showing significantly greater rectification than type I neurons. The axonal arborizations were reconstructed for 44 of 63 neurons labelled with tracer. Neurons of each subtype were found to issue axon collaterals terminating in the brainstem nuclei, including the parvocellular reticular nucleus (PCRt), the trigeminal motor nucleus (Vmot), the supratrigeminal nucleus or the trigeminal mesencephalic nucleus. Twenty-five of the 43 neurons issued collaterals which terminated in the Vmot and the other brainstem nuclei. When viewed under 100x magnification, the collaterals of some interneurons were seen to give off varicosities and end-terminations which passed close to the somata of unidentified neurons in the trigeminal motor nucleus and in the area close to the interneuron soma itself. This suggests that the interneurons may make synaptic contacts both on motoneurons and also on nearby interneurons. These results provide data on the membrane properties of trigeminal interneurons and evidence for their synaptic connections both with nearby interneurons and also with motoneurons. Thus, the interneurons examined could play roles in the shaping, and possibly also in the generation, of rhythmical signals to trigeminal motoneurons.

GABAergic Control of Action Potential Propagation along Axonal Branches of Mammalian Sensory Neurons

The main axons of mammalian sensory neurons are usually viewed as passive transmitters of sensory information. However, the spindle afferents of jaw-closing muscles behave as if action potential traffic along their central axons is phasically regulated during rhythmic jaw movements. In this paper, we used brainstem slices containing the cell bodies, stem axons, and central axons of these sensory afferents to show that GABA applied to the descending central (caudal) axon often abolished antidromic action potentials that were elicited by electrical stimulation of the tract containing the caudal axons of the recorded cells. This effect of GABA was most often not associated with a change in membrane potential of the soma and was still present in a calcium-free medium. It was mimicked by local applications of muscimol on the axons and was blocked by bath applications of picrotoxin, suggesting activation of GABA(A) receptors located on the descending axon. Antidromic action potentials could also be blocked by electrical stimulation of local interneurons, and this effect was prevented by bath application of picrotoxin, suggesting that it results from the activation of GABA(A) receptors after the release of endogenous GABA. We suggest that blockage is caused mainly by shunting within the caudal axon and that motor command circuits use this mechanism to disconnect the rostral and caudal compartments of the central axon, which allows the two parts of the neuron to perform different functions during movement.

Effect of cortical masticatory area stimulation on swallowing in anesthetized rabbits

The effects of stimulation of the cortical masticatory area (CMA) on swallowing evoked by superior laryngeal nerve (SLN) were studied in anesthetized rabbits. Electromyographic activity of the thyrohyoid, masseter, and digastric muscles and jaw-movement trajectories were recorded to monitor rhythmic jaw movements (RJMs) or swallowing. A systematic series of microelectrode penetrations within the CMA was made for each animal, and the effects of CMA stimulation on swallowing were tested by comparing the number of swallows evoked by stimulation of the CMA alone, the SLN alone, and simultaneous stimulation of the SLN and CMA. A significant facilitatory effect was observed in 49 (52%) of the 95 CMA loci tested. No significant effect was noted in the remaining 46 loci. Three different types of RJMs were evoked by CMA stimulation, and topographical organization was noted among CMA loci that evoked different types of RJMs. A high percentage of (77%) the CMA loci that evoked RJMs with a prominent horizontal excursion of the jaw facilitated swallowing and was located in the posterolateral and deep part of the CMA. A majority (88%) of the CMA loci that evoked RJMs with small circular jaw movements did not affect swallowing and was located in the anteromedial and shallow part of the CMA. The facilitatory effect of CMA stimulation on swallowing remained even after removal of peripheral sensory inputs by means of deafferentation of infraorbital and inferior alveolar nerves. Results suggest the existence of facilitatory descending pathways to the swallowing center from particular intracortical loci of CMA.

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.

Disturbed Jaw Behavior in Whiplash-associated Disorders during Rhythmic Jaw Movements

Disturbed Jaw Behavior in Whiplash-associated Disorders during Rhythmic Jaw Movements

Disturbed jaw behavior in whiplash-associated disorders during rhythmic jaw movements.

As shown previously, "functional jaw movements" are the result of coordinated activation of jaw as well as neck muscles, leading to simultaneous movements in the temporomandibular, atlanto-occipital, and cervical spine joints. In this study, the effect of neck trauma on natural jaw function was evaluated in 12 individuals suffering from whiplash-associated disorders (WAD). Spatiotemporal characteristics of mandibular and concomitant head movements were evaluated for three different modes of rhythmic jaw activities: self-paced continuous maximal jaw-opening/-closing movements, paced continuous maximal jaw-opening/-closing movements at 50 cycles/minute, and unilateral chewing. Compared with healthy subjects, the WAD group showed smaller magnitude and altered coordination pattern (a change in temporal relations) of mandibular and head movements. In conclusion, these results show that neck trauma can derange integrated jaw and neck behavior, and underline the functional coupling between the jaw and head-neck motor systems.

The sites of origin of projection fibers from the cerebral cortex to the jaw region of the striatum of the rat

Electrical microstimulation of the jaw region of the rat striatum (SJR) has been reported to provoke clear electromyographic activity in the anterior digastric muscle but not in the masseter muscle (Neurosci. Lett., 252 (1998) 79–82). Thus, in the present study, we examined the sites of origin of cortico-SJR fibers by the retrograde labeling. The SJR, identified by electrical microstimulation, was injected electrophoretically with cholera toxin B subunit. In the cerebral cortex ipsilateral to the injection, there existed two foci of retrograde labeling: One focus was centered on the lateral part of the sensorimotor area, while the other on the insular cortical area around the middle cerebral artery. These foci appeared to correspond to the reported two cortical areas, where two different types of rhythmical jaw movements were induced by repetitive electrical stimulation (Jap. J. Oral Biol., 32 (1990) 57–68).

Influence of oro-facial sensory input on the output of the cortical masticatory area in the anesthetized rabbit.

In order to study the role of sensory inputs to the cortical masticatory area (CMA) and plasticity in the CMA, the representation of sensory inputs and the change of sensory inputs and motor outputs in the CMA 16 days after trigeminal deafferentation in the rabbit were examined. Neuronal activity was recorded in response to mechanical and electrical stimulation of the oro-facial region and cortically-induced rhythmical jaw movements (CIRJMs) were analyzed. Cortical neurons with receptive fields in the deafferented region were not found in the CMA. However, the projection area of the intact lingual nerve extended both antero-posteriorly and medio-laterally in the CMA and included neurons with long latency responses to lingual nerve stimulation. In a previous study in the rabbit, CIRJMs were classified into two groups according to their similarity to normal masticatory patterns: one pattern resembled that occurring during the food transport stage (T-pattern), and the other resembled that occurring during the chewing stage (C-pattern). These two patterns of CIRJMs were evoked from different stimulation sites: T-patterns were induced from the dorsal CMA and C-patterns were induced from the ventral CMA. The relationship between the patterns of CIRJMs and the site of stimulation in the deafferented rabbits was similar to that observed in normal rabbits. This finding suggests that sensory inputs to the CMA may not directly influence the CMA motor outputs controlling jaw movements, despite a close spatial relationship between the input and output of this area.

Neural activities in the substantia nigra modulated by stimulation of the orofacial motor cortex and rhythmical jaw movements in the rat

Neurons related to jaw movements in the substantia nigra pars reticulata were explored by examining changes in their neural activities in response to electrical stimulation of the orofacial sensorimotor cortex and during rhythmical jaw movements induced by mechanical stimulation applied to the oral cavity in the rat. Out of 80 neurons tested, 59 showed changes in their firing patterns of activities in response to the electrical stimulation of the cortex. The responding neurons were mainly located in the dorsolateral part of the substantia nigra pars reticulata. The substantia nigra pars reticulata neurons showing responses were classified into the following five types according to their response patterns: (1) an inhibition preceded by an early excitation and followed by a late excitation ( n=26), (2) an inhibition preceded by an early excitation but not followed by a late excitation ( n=7), (3) an inhibition not preceded by an early excitation but followed by a late excitation ( n=2), (4) an inhibition without early or late excitations ( n=7) and (5) an excitation without an inhibition ( n=17). Out of 18 neurons responding to the cortical stimulation, 11 (61.1%) increased or decreased their neural activities during rhythmical jaw movements. Some of these neurons had a projection to the lateral part of the superior colliculus ( n=5) and/or to the parvicellular reticular formation ( n=2). These results provide first neurophysiological evidence for neurons in the dorsolateral part of the substantia nigra pars reticulata with inputs from and outputs to the areas related to jaw movements. These neurons may participate in the control of jaw movements in the rat.

Correlations between response properties of periodontal mechanosensitive neurones in the primary somatosensory cortex of the rabbit and cortically induced rhythmical jaw movements

The response properties of incisor- and molar-sensitive periodontal mechanosensitive (PM) neurones in the primary somatosensory (SI) cortex of rabbits were examined and rhythmical jaw movements induced by repetitive electrical stimulation of the recording sites of cortical PM neurones were observed. PM units were recorded from the rostromedial (RM) and rostrolateral (RL) areas of the SI cortex. In the RM area, most PMs (85%) were lower incisor-sensitive. Electrical stimulation of the RM area produced chopping-type rhythmical jaw movements. In the RL area, both incisor- and molar-sensitive PM units were recorded, and molar-sensitive units were located more rostromedially than incisor-sensitive units. More than half (66%) of the incisor-sensitive PM units were upper incisor-sensitive. The incidences of sustained-response type units were 8 and 10% for upper incisor- and lower incisor-sensitive units and 28 and 34% for upper molar- and lower molar-sensitive units, respectively. The optimal stimulus directions for the upper molar-sensitive units were predominantly labial or lingual, whereas those for most of the lower molar-sensitive units were lingual. Electrical stimulation of the PM unit-recording sites in the RL area induced grinding-type rhythmical jaw movements. Based on these findings, the lower incisor-sensitive neurones in the RM area of the SI cortex might mainly contribute to a neural network that controls jaw movements during ingestion. Furthermore, the response properties of molar-sensitive cortical neurones might be useful for discriminating the magnitude and direction of the biting force during grinding. Further studies are needed to clarify the role of upper incisor-sensitive neurones in the RL area in triggering grinding-type rhythmical jaw movements.

Electrophysiological analysis of rhythmic jaw movements in the freely moving mouse

Although rhythmic jaw movement in feeding has been studied in mammals, such as rats, rabbits and monkeys, the cellular and molecular mechanisms underlying it are not well understood. Transgenic and gene-targeting technologies enable direct control of the genetic makeup of the mouse, and have led to the development of a new category of reagents that have the potential to elucidate the cellular and molecular mechanisms of neural networks. The present study attempts to characterize rhythmic jaw movements in the mouse and to demonstrate its relevance to rhythmic jaw movements found in higher mammals using newly developed jaw-tracking systems and electromyograms of the masticatory muscles. The masticatory sequence of the mouse during feeding was classified into two stages, incision and chewing. Small and rapid (8 Hz) open–close jaw movements were observed during incision, while large and slow (5 Hz) open–close jaw movements were observed during chewing. Integrated electromyograms of the masseteric and digastric muscles were larger during chewing than those observed during incision. Licking behavior was associated with regular (8 Hz), small open–close jaw movements with smaller masseteric activity than those observed during mastication. Grooming showed variable patterns of jaw movement and electromyograms depending on the grooming site. These results suggest that there are neuronal mechanisms producing different frequencies of rhythmic jaw movements in the mouse, and we conclude that the mouse is useful for understanding rhythmic jaw movements in higher mammals.

Putative feed-forward control of jaw-closing muscle activity during rhythmic jaw movements in the anesthetized rabbit.

When a thin plastic test strip of various hardness is placed between the upper and lower teeth during rhythmical jaw movements induced by electrical stimulation of the cortical masticatory area (CMA) in anesthetized rabbits, electromyographic (EMG) activity of the masseter muscle is facilitated in a hardness-dependent manner. This facilitatory masseteric response (FMR) often occurred prior to contact of the teeth to the strip, and thus preceded the onset of the masticatory force. Since this finding suggests involvement of a feed-forward mechanism in the induction of the FMR, the temporal relationship between the onset of the FMR and that of the masticatory force was analyzed in five sequential masticatory cycles after application of the strip. The FMR was found to precede the onset of masticatory force from the second masticatory cycle after application of the strip, but never did in the first cycle. This finding supports the concept of a feed-forward control mechanism that modulates FMR timing. Furthermore, the FMR preceding the force onset disappeared after making a lesion of the mesencephalic trigeminal nucleus (MesV) where the ganglion cells of the muscle spindle afferents from the jaw-closing muscles are located. In contrast, no such change occurred after blocking periodontal afferents by transection of both the maxillary and the inferior alveolar nerves. The putative feed-forward control of the FMR is therefore dependent mainly on sensory inputs from the muscle spindles, but little on those from the periodontal receptors, if any. We further examined the involvement of the CMA with the putative feed-forward control of the FMR via the transcortical loop. For this purpose, rhythmical jaw movements were induced by stimulation of the pyramidal tract. No significant change in the timing of the FMR occurred after the CMA ablation, which strongly suggests that the CMA is not involved in the putative feed-forward control of the FMR. The FMR was also noted to increase significantly in a hardness-dependent manner even after the MesV lesion, although the rate of increment decreased significantly. Contribution of muscle spindles and periodontal receptors to the hardness-dependent change of the FMR is discussed.

Development of a three-dimensional jaw-tracking system implanted in the freely moving mouse

A high-resolution mandibular tracking system was designed and tested in a freely moving mouse. A sensor unit, which consisted of four small magnetic sensors, was employed to trace small magnet movements in the three-dimensional space. After the sensor's output-to-displacement transformation equations were obtained from a multiple regression analysis of pre-experimental calibration data, the magnet and the sensors were transferred to the mouse, being kept at the same configuration as determined in the calibration system. In order to measure the three-dimensional jaw movements, the magnet was glued on the mandibular surface of the mouse and the sensor unit was implanted in the nasal bone. Jaw-movement trajectories were obtained as electrical signals from the sensors after being compensated by the output-to-displacement transformation equations of the sensors with a personal computer. This sensor system, applied to the freely moving mouse, could trace the jaw trajectories with an accuracy of better than 20 μm in three-dimensional space. Consequently, the typical pattern of the rhythmical jaw movements of the mouse during mastication was obtained. The mouse protruded the mandible to the most anterior position in the jaw-opening phase and retruded to it the most posterior position in the jaw-closing phase. This tracking system may also be applied to other small animals.

Analysis of rhythmical jaw movements produced by taste stimulation in rats.

Taste stimulation of the mouth induces various oral movements. Sucrose or salt solution induces rhythmical jaw movements (RJM) or tongue protrusion as an ingestive behavior. Bitter taste induces a gaping or tongue retraction as an aversive behavior. There is no report that describes the precise pattern of jaw movements induced by taste stimulation. The purpose of the present study is to clarify the pattern of the taste-induced RJM with electromyographic activities of the masticatory muscles in the anesthetized rat. When water was injected into the mouth of the rat, an RJM was induced. In this type of RJM, the lower jaw swung right and left side in each open-close cycle alternately. The anterior digastric muscle was active in every opening phase, while activities of the jaw closing muscles were generally weak. The RJM induced by water was opening-dominant movements. Sucrose or salt solution induced a similar pattern of RJM to water-induced RJM. When acetic acid was injected, amplitude of the alternate lateral jaw movement was significantly larger than that in the water-induced RJM. The activity of the superficial temporalis muscle was large in those closing phases with ipsilateral side movement, while it was small in the closing phases with contralateral movement. The pattern of quinine-induced RJM was characterized by small lateral, large open-close and large antero-posterior movements. Tastes which are reported to induce ingestive behavior such as sweet or salty don't alter the pattern of RJM; however, the tastes which induce aversive behavior make the pattern of RJM different from the water-induced RJM.

Influence of food thickness and hardness on possible feed-forward control of the masseteric muscle activity in the anesthetized rabbit.

The facilitatory masseteric muscle response (FMR) elicited by polyurethane foam strip application between the opposing molars during cortically-induced rhythmic jaw movements (CRJMs) was induced earlier than masticatory force onset. The occurrence of this early response of the FMR (e-FMR) could not be explained by a simple reflex mechanism. One possible mechanism of the e-FMR is the involvement of a feed-forward control mechanism of the masticatory jaw movement. In the present study, experimentally designed polyurethane foam strips with various thickness and hardness were applied during CRJMs and analyzed in terms of how the e-FMR was modulated by the food hardness and thickness. The FMR onset was not related to the strip thickness or the strip hardness. However, the magnitude of the e-FMR increased in a thickness and a hardness-dependent manner. The sensory information of the food properties in the masticatory cycle may make the FMR adequate to chewing of the food in the following cycle, and such modulation may help chewing rhythms remain stable.

Two Types of Rhythmical Jaw Movements Produced by Mechanical Stimulation of the Oral Cavity.

Two Types of Rhythmical Jaw Movements Produced by Mechanical Stimulation of the Oral Cavity.

Effect of norepinephrine receptors on trigeminal rhythm generation in newborn rats

N-methyl-D,L-aspartate acid and bicuculline are required to enhance the trigeminal rhythmic activities in an in vitro isolated brainstem block preparation. In this study, we analyzed the effect of norepinephrine on the trigeminal neural circuit underlying rhythmic jaw movements. Rhythmic trigeminal activity is observed in brainstem preparations (inferior colliculus to obex) only following blockade of α 2-adrenoceptors with idazoxan. This observation, combined with the inhibition of rhythm by α 2-adrenoceptor agonists suggests endogenous α 2-adrenoceptor mediated inhibition of trigeminal networks. A complex noradrenergic modulation of trigeminal systems is further supported by the prazosin-sensitive potentiation of rhythm by bath application of the α 1-adrenoceptor agonist phenylephrine.

Sleep bruxism in patients with sleep-disordered breathing

The aim was to test the hypothesis of a direct association between sleep-disordered breathing and sleep bruxism. The frequency of masseter contraction (MC) episodes and rhythmic jaw movements (RJM) was measured in patients with mild and moderate obstructive sleep apnoea (OSA). The diagnosis of sleep bruxism was made from a combination of questionnaire, clinical observation and all-night polysomnographic recording which included masseter electromyography. A total of 21 patients (19 males/two females, mean age 40.0 years±9.2 SD) were randomly selected from a provisional diagnosis of snoring and OSA by a sleep physician. In the patients with mild OSA [ n=11, mean apnoea hypopnoea index (AHI)=8.0±4.1 SD, body mass index (BMI)=29.1±5.0], the diagnosis of sleep bruxism was made in six out of 11 patients (54%); similarly, four out of 10 patients (40%) with moderate OSA ( n=10, mean AHI=34.7±19.1, BMI=30.6±5.0) were identified as bruxists. Although the combination of clinical, subjective estimation and nocturnal electromyographic recording of masseter muscle might provide a more solid base for the diagnosis of sleep bruxism, the result is biased by the variation in the bruxing activity. MC episodes were associated with the termination of apnoea or hypopnoea episodes in only 3.5% of the mild group and 14.4% of the moderate group ( p<0.05). It appears that sleep bruxism is rarely directly associated with apnoeic events, but is rather related to the disturbed sleep of OSA patients.

Genioglossus muscle activity during rhythmic open-close jaw movements.

The purpose of this study was to examine genioglossus muscle activity during rhythmic open-close jaw movements. The electromyographic activity of the genioglossus muscle was recorded with a bipolar fine-wire electrode in six healthy males. The electromyographic activities of the ipsilateral masseter and digastric muscles were simultaneously recorded with bipolar surface electrodes. The subjects were instructed to perform rhythmic open-close jaw movements in time with a metronome set at 23, 27, 33, 42 and 50 beats/min. In all of the subjects, rhythmic electromyographic activity of the genioglossus muscle was recorded in both the jaw-opening and jaw-closing phases. The activity of the genioglossus muscle was predominantly recorded in the jaw-opening phase in two subjects, and in the jaw-closing phase in two subjects. The burst duration of the electromyographic activity of the genioglossus muscle changed linearly in accordance with the cycle duration. However, the latency from the onset of the electromyographic activity of the masseter or digastric muscle to that of the genioglossus muscle was almost constant, independent of the cycle duration. Based on these findings, we conclude that the activity of the human genioglossus muscle is closely linked to that of masticatory muscles under the control of a closely related central pattern generator.