Jin Magara

Role of tongue pressure production in oropharyngeal swallow biomechanics

The tongue is important for orofacial movements, including swallowing. Although numerous studies have focused on tongue pressure against the palate, its physiological role has not been fully evaluated. The tongue pressure generation may have the temporal coordination with the swallowing relational organs. The aim of this study was to clarify the physiological mechanisms of tongue pressure and to investigate the temporal relationship among tongue pressure, supra‐hyoid muscle activity, and videofluorographic (VF) images during swallowing. Fifteen healthy young subjects participated. Tongue pressure measured using a sensor sheet with five channels, electromyographic EMG, and VF was recorded synchronously during 4‐ml barium swallowing. Swallowing behavior in VF images with and without the sensor sheet was compared. Furthermore, the temporal relationship between events measured from tongue pressure, EMG, and VF was evaluated. Swallowing behavior on VF images was not affected by placement of the sensor sheet. Tongue pressure at the posterio‐lateral point of the hard palate tended to have biphasic peaks. Tongue pressure production with a monophasic pattern appeared during the same period as the second peak in the biphasic pattern. The onset of tongue pressure was later than the start of hyoid movement and onset of EMG, and offset was observed between the hyoid at the up‐forward position and reposition. Onset of tongue pressure at the anterior area was correlated with the start of slight hyoid elevation. Offset of tongue pressure at the posterio‐lateral points was strongly time locked with the hyoid at the up‐forward position. The present results suggested the temporal coordination of tongue pressure generation with the swallowing‐related organs. That is, the tongue pressure was produced for bolus propulsion, and was closely related to hyoid movement temporally during swallowing. These results may contribute to clarify the clinical state with the disorder of tongue kinetics.

Changes in jaw muscle activity and the physical properties of foods with different textures during chewing behaviors

This study aimed to investigate how the activity of the masseter (Mas) and suprahyoid (Hyoid) muscles is influenced by the physical properties of food, how changes in the rheological properties of food differ between different foods during the process of food reduction, and how different salivary flow rates affect bolus-making capability during masticatory behavior in healthy humans. Ten healthy adults participated in this study. Electromyographic (EMG) recordings were obtained from the Mas and Hyoid muscles, and 15 g of steamed rice and rice cake was prepared as test foods. In the ingestion test, the subjects were asked to eat each food in their usual manner. The chewing duration, number of chewing cycles before the first swallow, Mas and Hyoid EMG activity, and chewing cycle time were compared between the foods. Total chewing duration was divided into three substages: early, middle, and late; chewing cycle time and EMG activity per chewing cycle of each substage were compared between the foods and among the substages. In the spitting test, the rheological properties of the bolus at the end of each substage were compared between the foods and among the substages. Finally, stimulated salivary flow rates were measured and the relationships between salivary flow rate and chewing duration, EMG activity, and changes in physical food characteristics were investigated. There were significant differences in total chewing duration and the number of chewing cycles, but not in chewing cycle time, between the foods, which had similar hardness values. The EMG activity levels of the Mas and Hyoid per chewing cycle for the rice cake were significantly greater than for the steamed rice throughout the recording periods. While Mas activity did not change among the substages during chewing, Hyoid EMG activity decreased as chewing progressed. Chewing cycle time also gradually decreased as chewing progressed. The hardness of both foods initially increased, then gradually decreased back to baseline. The adhesiveness of the rice cake initially increased, and did not fall throughout the recording period; the adhesiveness of the steamed rice did not significantly change. Cohesiveness barely changed in either of the two foods during chewing, but was significantly greater for the rice cake than for the steamed rice. Finally, a correlation between the stimulated salivary flow rate and chewing performance was evident only in a change in Mas EMG activity. The current results demonstrate that the activities of the Mas and Hyoid muscles changed as chewing progressed, and were affected by hardness, adhesiveness, and cohesiveness. Salivary flow rate may affect the changes in Mas activity during the process of bolus formation.

Changes in the frequency of swallowing during electrical stimulation of superior laryngeal nerve in rats.

The aim of the present study was to investigate the adaptation of the swallowing reflex in terms of reduced swallowing reflex initiation following continuous superior laryngeal nerve stimulation. Forty-four male Sprague Dawley rats were anesthetized with urethane. To identify swallowing, electromyographic activity of the left mylohyoid and thyrohyoid muscles was recorded. To evoke the swallowing response, the superior laryngeal nerve (SLN), recurrent laryngeal nerve, or cortical swallowing area was electrically stimulated. Repetitive swallowing evoked by continuous SLN stimulation was gradually reduced, and this reduction was dependent on the resting time duration between stimulations. Prior SLN stimulation also suppressed subsequent swallowing initiation. The reduction in evoked swallows induced by recurrent laryngeal nerve or cortical swallowing area stimulation was less than that following superior laryngeal nerve stimulation. Decerebration had no effect on the reduction in evoked swallows. Prior subthreshold stimulation reduced subsequent initiation of swallowing, suggesting that there was no relationship between swallowing movement evoked by prior stimulation and the subsequent reduction in swallowing initiation. Overall, these data suggest that reduced sensory afferent nerve firing and/or trans-synaptic responses, as well as part of the brainstem central pattern generator, are involved in adaptation of the swallowing reflex following continuous stimulation of swallow-inducing peripheral nerves and cortical areas.

Peripheral and central control of swallowing initiation in healthy humans.

We investigated (1) how peripheral inputs might assist central inputs in the control of voluntary evoked swallowing, (2) inter-individual variation in involuntary and voluntary swallowing initiation, and (3) whether natural chewing behavior affects the initiation of involuntary swallowing in healthy humans. Eleven participants completed a repetitive saliva swallowing test (RSST), chewing test (CHEW), and rest period (REST). In RSST, participants repetitively swallowed as quickly as possible. In CHEW, subjects chewed gum freely. We delivered pharyngeal electrical stimulation (PEStim) to the laryngopharynx and compared the number of swallows that occurred with and without PEStim. PEStim significantly increased the number of voluntary evoked swallows in RSST, as well as the number of swallows in CHEW and REST trials, although this facilitatory effect was larger in REST trials. We found a positive correlation between the number of swallows at RSST without PEStim and that at REST with PEStim within individuals. Additionally, we found a significant positive correlation between the number of swallows at RSST with PEStim and the sum of that at RSST without PEStim and at REST with PES. Based on the current results, we suggest that (1) peripheral inputs within a certain range appear to facilitate the central inputs that control voluntary swallowing, (2) inter-individual variations in swallowing initiation may arise from differences in the excitability of the common neural network in the lower brainstem, and (3) during chewing, food reduction in the oral cavity is prioritized, such that the neural network associated with chewing may regulate swallowing initiation.

Phenotypes of articular disc cells in the rat temporomandibular joint as demonstrated by immunohistochemistry for nestin and GFAP

The articular disc is a dense collagenous tissue containing disc cells that are phenotypically described as chondrocyte‐like cells or fibrochondrocytes. Despite the possible existence of these phenotypes in systemic joints, little is known about the detailed classification of the articular disc cells in the temporomandibular joint. In this immunocytochemical study we examined the localization and distribution patterns of nestin and glial fibrillary acidic protein (GFAP) in the articular disc of the rat temporomandibular joint at postnatal day 1, and weeks 1, 2, 4 and 8, based on the status of tooth eruption and occlusion. Nestin and GFAP are intermediate filament proteins whose expression patterns are closely related to cell differentiation and cell migration. Both types of immunopositive cell greatly increased postnatally to a stable level after postnatal week 4, but they showed different distribution patterns and cell morphologies. Nestin‐reactive disc cells, which were characterized by a meagre cytoplasm and thin cytoplasmic processes, were scattered in the articular disc, whereas GFAP‐positive cells, characterized by broader processes, existed exclusively in the deeper area. In mature discs, the major proportion of articular disc cells exhibited GFAP immunoreactivity. Furthermore, a double‐immunostaining demonstrated that the nestin‐negative cells, consisting of GFAP‐positive and ‐negative cells, exhibited immunoreactions for heat shock protein 25. These findings indicate that the articular disc cells comprise at least three types in the rat temporomandibular joint and suggest that their expressions closely relate to mechanical loading forces within the joint, including occlusal force, as observed through postnatal development.

Differential response properties of peripherally and cortically evoked swallows by electrical stimulation in anesthetized rats

We compared onset latency, motor-response patterns, and the effect of electrical stimulation of the cortical masticatory area between peripherally and cortically evoked swallows by electrical stimulation in anesthetized rats. The number of swallows and the motor patterns were determined using electromyographic recordings from the thyrohyoid, digastric, and masseter muscles. The onset latency of the first swallow evoked by electrical stimulation of the cortical swallowing area (Cx) was significantly longer than that evoked by stimulation of the superior laryngeal nerve (SLN). The duration of thyrohyoid burst activity associated with SLN-evoked swallows was significantly longer than that associated with either Cx-evoked or spontaneous swallows. Combining Cx with SLN stimulation increased the number of swallows at low levels of SLN stimulation. Finally, A-area (the orofacial motor cortex) stimulation inhibited Cx-evoked swallows significantly more than it inhibited SLN-evoked swallows. These findings suggest that peripherally and cortically evoked swallows have different response properties and are affected differently by the mastication network.

Effects of chewing and swallowing behavior on jaw opening reflex responses in freely feeding rabbits.

It has been reported that the jaw opening reflex (JOR) evoked by intra-oral innocuous stimulation was suppressed during a reflex swallow in anesthetized animals only. However, the mechanism of JOR inhibition during swallowing has not yet been elucidated. The aim of the present study was to investigate the effects of peripheral nerve stimulation on masticatory behaviors, as well as the modulation of low threshold afferent evoked JOR responses during chewing and swallowing in freely feeding animals. The JOR in the digastric muscle was evoked by low threshold electrical stimulation of the inferior alveolar nerve (IAN). Changes in the peak-to-peak amplitude of digastric electromyographic responses were compared among the phases of chewing and swallowing. IAN stimulation did not produce any differences in cycle duration, gape of the jaw in one cycle, or swallowing interval, suggesting a minimal effect on feeding behaviors. The JOR amplitude during the fast-closing, slow-closing, and slow-opening phases of chewing was significantly smaller than that of the control (recorded when the animal was at rest) and fast-opening phase. During swallowing, the JOR amplitude was significantly less than the control. Inhibition of the JOR during swallowing is assumed to prevent unnecessary opposing jaw opening motion.

Alterations in intermediate filaments expression in disc cells from the rat temporomandibular joint following exposure to continuous compressive force

The articular disc in the temporomandibular joint (TMJ) that serves in load relief and stabilizing in jaw movements is a dense collagenous tissue consisting of extracellular matrices and disc cells. The various morphological configurations of the disc cells have given us diverse names, such as fibroblasts, chondrocyte‐like cells and fibrochondrocytes; however, the characteristics of these cells have remained to be elucidated in detail. The disc cells have been reported to exhibit heterogeneous immunoreaction patterns for intermediate filaments including glial fibrillary acidic protein (GFAP), nestin and vimentin in the adult rat TMJ. Because these intermediate filaments accumulate in the disc cells as tooth eruption proceeds during postnatal development, it might be surmised that the expression of these intermediate filaments in the disc cells closely relates to mechanical stress. The present study was therefore undertaken to examine the effect of a continuous compressive force on the immunoexpression of these intermediate filaments and an additional intermediate filament – muscle‐specific desmin – in the disc cells of the TMJ disc using a rat experimental model. The rats wore an appliance that exerts a continuous compressive load on the TMJ. The experimental period with the appliance was 5 days as determined by previous studies, after which some experimental animals were allowed to survive another 5 days after removal of the appliance. Histological observations demonstrated that the compressive force provoked a remarkable acellular region and a decrease in the thickness of the condylar cartilage of the mandible, and a sparse collagen fiber distribution in the articular disc. The articular disc showed a significant increase in the number of desmin‐positive cells as compared with the controls. In contrast, immunopositive cells for GFAP, nestin and vimentin remained unchanged in number as well as intensity. At 5 days after removal of the appliance, both the disc and cartilage exhibited immunohistological and histological features in a recovery process. These findings indicate that the mature articular cells are capable of producing desmin instead of the other intermediate filaments against mechanical stress. The desmin‐positive disc cells lacked α‐smooth muscle actin (α‐SMA) in this study, even though desmin usually co‐exists with α‐SMA in the vascular smooth muscle cells or pericytes. Because the precursor of a pericyte has such an immunoexpression pattern during angiogenesis, there is a further possibility that the formation of new vessels commenced in response to the extraordinary compressive force.

Effect of body posture on involuntary swallow in healthy volunteers

Clinically, reclining posture has been reported to reduce risk of aspiration. However, during involuntary swallow in reclining posture, changes in orofacial and pharyngeal movement before and during pharyngeal swallow should be considered. Further, the mechanisms underlying the effect of body posture on involuntary swallow remain unclear. The aim of the present study was to determine the effect of body posture on activity patterns of the suprahyoid muscles and on patterns of bolus transport during a natural involuntary swallow. Thirteen healthy male adults participated in a water infusion test and a chewing test. In the water infusion test, thickened water was delivered into the pharynx at a very slow rate until the first involuntary swallow was evoked. In the chewing test, subjects were asked to eat 10 g of gruel rice. In both tests, the recording was performed at four body postures between upright and supine positions. Results showed that reclining changed the location of the bolus head at the start of swallow and prolonged onset latency of the swallowing initiation. Muscle burst duration and whiteout time measured by videoendoscopy significantly increased with body reclining and prolongation of the falling time. In the chewing test, reclining changed the location of the bolus head at the start of swallow, and the frequency of bolus residue after the first swallow increased. Duration and area of EMG burst and whiteout time significantly increased with body reclining. These data suggest that body reclining may result in prolongation of pharyngeal swallow during involuntary swallow.

Central inhibition of initiation of swallowing by systemic administration of diazepam and baclofen in anaesthetized rats

Dysphagia is caused not only by neurological and/or structural damage but also by medication. We hypothesized memantine, dextromethorphan, diazepam, and baclofen, all commonly used drugs with central sites of action, may regulate swallowing function. Swallows were evoked by upper airway (UA)/pharyngeal distension, punctate mechanical stimulation using a von Frey filament, capsaicin or distilled water (DW) applied topically to the vocal folds, and electrical stimulation of a superior laryngeal nerve (SLN) in anesthetized rats and were documented by recording electromyographic activation of the suprahyoid and thyrohyoid muscles and by visualizing laryngeal elevation. The effects of intraperitoneal or topical administration of each drug on swallowing function were studied. Systemic administration of diazepam and baclofen, but not memantine or dextromethorphan, inhibited swallowing evoked by mechanical, chemical, and electrical stimulation. Both benzodiazepines and GABAA receptor antagonists diminished the inhibitory effects of diazepam, whereas a GABAB receptor antagonist diminished the effects of baclofen. Topically applied diazepam or baclofen had no effect on swallowing. These data indicate that diazepam and baclofen act centrally to inhibit swallowing in anesthetized rats.NEW & NOTEWORTHY Systemic administration of diazepam and baclofen, but not memantine or dextromethorphan, inhibited swallowing evoked by mechanical, chemical, and electrical stimulation. Both benzodiazepines and GABAA receptor antagonists diminished the inhibitory effects of diazepam, whereas a GABAB receptor antagonist diminished the effects of baclofen. Topical applied diazepam or baclofen was without effect on swallowing. Diazepam and baclofen act centrally to inhibit swallowing in anesthetized rats.