Tongue and jaw muscle activities during chewing and swallowing in freely behaving rabbits

doi:10.1016/S0006-8993(01)02848-7

Brain Research

Volume 915, Issue 2, 12 October 2001, Pages 185-194

https://doi.org/10.1016/S0006-8993(01)02848-7 Get rights and content

Abstract

To study the function of the tongue and the coordination among jaw, tongue, and hyoid muscles during chewing and swallowing, we recorded the electromyographic activities from the masseter (Mas), digastric (Dig), mylohyoid (Myl), thyrohyoid (Thy), genioglossus (Gg) and styloglossus (Sg) muscles as well as jaw movement trajectories in the freely behaving rabbit. Three phases were identified in the chewing cycle (fast- and slow-closing and opening phases). The Gg (main tongue protruder) was active synchronously with the Dig during opening. The Sg (tongue retractor) showed two peaks in each cycle, one in the opening phase and the other in the closing phase. The latter may have a role in retracting the tongue during jaw closing. The co-contraction of the antagonists (i.e. Gg and Sg) during opening may contribute to shape the tongue to be appropriate to gather the foodstuff. In the swallowing cycle, five phases were identified, two in the closing phase and three in the opening phase. Regression analysis revealed that swallowing cycles had a longer cycle duration than that of the chewing cycles due to an extra phase (a pause) inserted in the opening phase, where there was a small co-activation in the jaw opening and closing muscles. The findings suggest that the swallowing center affects masticatory center in the central nervous system, and may also support the view that the masticatory burst timing begins with the Dig activities in the middle of the opening phase.

Introduction

Ingestion can be accomplished by the coordinated activities of the jaw, hyoid, tongue, and perioral muscles. It includes several motor behaviors such as mastication (chewing), food transportation, and swallowing (see Ref. [4], [16] for review). Although complete feeding sequences have been studied in humans with the use of videofluorography [6], [14], details in the burst timing of the participating muscles are still unclear. To understand the neural mechanism underlying the control of the oral motor behaviors, the activity of jaw and hyoid muscles have been studied during natural chewing and swallowing in animals [11], [12], [18], but the activity pattern of the tongue muscles and perioral muscles (e.g. facial muscles) during these orofacial movements have not been clarified due to methodological problems. Our objectives in the present study were to define the activity pattern of tongue muscles during chewing and swallowing and to elucidate the coordination among jaw, tongue, and hyoid muscle activities during these movements. To accomplish our objectives, jaw movements and the burst patterns and interactions of three muscle groups; jaw (masseter: Mas, digastric: Dig), extrinsic tongue (styloglossus: Sg, genioglossus: Gg), and hyoid (mylohyoid: Myl, thyrohyoid: Thy) muscles were studied during natural chewing and swallowing in the freely behaving animal.

Section snippets

Surgical preparation

The methods for animal preparation, recording and data analysis have been extensively detailed [12], [18], [19] and so only a brief description follows. The experiments were carried out in five male rabbits (Japanese white, 2.0–2.5 kg) in accordance with the Guide for the Care and Use of Laboratory Animal Care (NIH Publication #86-23, revised 1996). The animal protocols were approved by the Intramural Animal Care and Veterinary Science Committee of the Niigata University. Before the necessary

Properties of jaw movements and muscle activities during chewing cycles

Chewing cycles in the early stage of a masticatory sequence were characterized with simple open-close movements having little horizontal movement and smaller EMG activities in the jaw muscles compared those during the latter cycles. Here we termed the chewing cycles two-phase cycles that may be identical to the term ‘preparatory series’ [15] or ‘type I’ [13] chewing cycles named by other groups. The two-phase cycles were followed by the chewing cycles configured with larger movements in both

Discussion

The present study has documented the activity pattern of the jaw, hyoid and tongue muscles during natural chewing and swallowing. In the chewing cycles, Gg (main tongue protruder) was active synchronously with jaw-opening muscle, and Sg (tongue retractor) was active both in the opening and closing phases. In the swallowing cycles, dramatic changes were observed in the activity patterns of hyoid muscles (i.e. Thy and Myl). The duration of the swallowing cycles was significantly longer than that

Acknowledgements

The authors thank Professor B.J. Sessle for his help in reviewing this manuscript. The authors also thank Mr. H. Hirano and Mr. Y. Takahashi for their technical assistance. This study was partly supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture and Science of Japan (#11470389 to Y.Y.).

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Cited by (49)

Tongue, palatal, hyoid and pharyngeal muscle activity during chewing, swallowing, and respiration
2024, Archives of Oral Biology
Chewing, swallowing, and respiration are synchronized oropharyngeal functions. This study aimed to analyze the dynamics and coordination during natural chewing and swallowing in relation to respiratory phases.
Eight oropharyngeal muscles in minipigs were recorded using electromyography, X-ray fluoroscopy, and nasopharyngeal dynamics. Chewing cycles and swallowing episodes were analyzed for timing and activity amplitude along respiratory cycles. Digastric and middle pharyngeal constrictor were used as zero-points for timing analysis in chewing cycles and swallowing episodes, respectively. The beginning of these cycles and episodes were used as the zero-point for timing analysis in respiration during feeding.
The timing of jaw closing (57.8%) was longer than opening (42.2%) during chewing. Muscle activity occurred 20% later than digastric onsets and 15% earlier than jaw closing phase. Duration of muscle activity was shorter in ipsilateral than contralateral sides except for palatal muscles. Pharyngeal, palatal, and hyoid muscles showed longer durations than tongue muscles in jaw opening (p < 0.05). Palatal and hyoid muscles showed 2-phased activity in chewing while hyoid muscles showed higher amplitude in chewing and swallowing than other muscles. About 80% of the chewing cycles and swallowing episodes occurred in expiration. Nasopharyngeal airflow velocity increased from jaw opening to swallowing while airflow pressure decreased.
These findings indicate key activity of palatal and pharyngeal muscles mostly in chewing. The respiratory cycle changes in chewing and swallowing simultaneously with the activation of the tongue, palatal, and pharyngeal muscles. These findings will be useful for further understanding the mechanisms in swallowing and breathing disorders.
Beyond language: The unspoken sensory-motor representation of the tongue in non-primates, non-human and human primates
2022, Neuroscience and Biobehavioral Reviews
The English idiom “on the tip of my tongue” commonly acknowledges that something is known, but it cannot be immediately brought to mind. This phrase accurately describes sensorimotor functions of the tongue, which are fundamental for many tongue-related behaviors (e.g., speech), but often neglected by scientific research. Here, we review a wide range of studies conducted on non-primates, non-human and human primates with the aim of providing a comprehensive description of the cortical representation of the tongue’s somatosensory inputs and motor outputs across different phylogenetic domains. First, we summarize how the properties of passive non-noxious mechanical stimuli are encoded in the putative somatosensory tongue area, which has a conserved location in the ventral portion of the somatosensory cortex across mammals. Second, we review how complex self-generated actions involving the tongue are represented in more anterior regions of the putative somato-motor tongue area. Finally, we describe multisensory response properties of the primate and non-primate tongue area by also defining how the cytoarchitecture of this area is affected by experience and deafferentation.
Effect of peripherally and cortically evoked swallows on jaw reflex responses in anesthetized rabbits
2018, Brain Research
This study aimed to investigate whether the jaw-opening (JOR) and jaw-closing reflexes (JCR) are modulated during not only peripherally, but also centrally, evoked swallowing. Experiments were carried out on 24 adult male Japanese white rabbits. JORs were evoked by trigeminal stimulation at 1 Hz for 30 s. In the middle 10 s, either the superior laryngeal nerve (SLN) or cortical swallowing area (Cx) was simultaneously stimulated to evoke swallowing. The peak-to-peak JOR amplitude was reduced during the middle and late 10-s periods (i.e., during and after SLN or Cx stimulation), and the reduction was dependent on the current intensity of SLN/Cx stimulation: greater SLN/Cx stimulus current resulted in greater JOR inhibition. The reduction rate was significantly greater during Cx stimulation than during SLN stimulation. The amplitude returned to baseline 2 min after 10-s SLN/Cx stimulation. The effect of co-stimulation of SLN and Cx was significantly greater than that of SLN stimulation alone. There were no significant differences in any parameters of the JCR between conditions. These results clearly showed that JOR responses were significantly suppressed, not only during peripherally evoked swallowing but also during centrally evoked swallowing, and that the inhibitory effect is likely to be larger during centrally compared with peripherally evoked swallowing. The functional implications of these results are discussed.
Tongue exercise and ageing effects on morphological and biochemical properties of the posterior digastric and temporalis muscles in a Fischer 344 Brown Norway rat model
2018, Archives of Oral Biology
This study sought to examin effects of age and tongue exercise on the posterior digastric (opener) and the temporalis (closer). We hypothesized 1) age would result in differing morphological (cross sectional area) and biochemical (myosin heavy chain isoform) components of these muscles; 2) tongue exercise would result in coactivation of these muscles inducing a decrease in age-related differences between age groups.
Young adult (9 months) and old (32 months) Fischer 344 Brown Norway rats were randomized into a tongue exercise or control group. Post-training, posterior digastric and temporalis muscles were harvested and analyzed using: 1) Sodium Dodecyl Sulfate-Polyacrylamide Gel Electrophoresis (SDS-PAGE) to assess percent myosin heavy chain (MyHC) content; 2) Immunohistochemical staining to determine cross sectional area (CSA).
A larger proportion of slowly contracting MyHC isoforms in the posterior digastric and temporalis muscles were found in old. No significant main effects for age or exercise in fiber size were found in posterior digastric muscle. An interaction between age and exercise for temporalis cross sectional area indicated the old exercise group had smaller average cross sectional area than all other groups.
suggest that: 1) Increasing age induces biochemical changes in muscles of the jaw, specifically showing an increase the proportion of slower contracting MyHC isoforms; 2) Increasing age and tongue exercise induce a reduction in muscle fiber cross sectional area in the temporalis muscle only. However, continued study of these cranial muscle systems is warranted to better understand these changes that occur with age and exercise.
Effects of aging on evoked retrusive tongue actions
2015, Archives of Oral Biology
Citation Excerpt :
Stimulation of the medial branch of the hypoglossal nerve will elicit a tongue protrusion,20,21 while stimulation of the lateral branch elicits tongue retrusion, via the hyoglossus and styloglossus muscles.21 The hyoglossus, styloglossus, and the genioglossus are active during oral preparation and retrograde movement of the bolus to the hypopharynx.18,22,23 Thus, both protrusive and retrusive tongue muscle actions are relevant to the swallow.
Tongue strength, timing, and coordination deficits may underlie age-related swallowing function. Retrusive tongue actions are likely important in retrograde bolus transport. However, age-related changes in retrusive tongue muscle contractile properties have not been identified in animal studies. Because previous studies employed whole hypoglossal nerve stimulation that activated both protrusive and retrusive tongue muscles, co-contraction may have masked retrusive muscle force decrements. The hypotheses of this study were: (1) retrusive tongue muscle contraction forces would be diminished and temporal characteristics prolonged in old rats when lateral nerves were selectively activated, and (2) greater muscle contractile forces with selective lateral branch stimulation would be found relative to whole hypoglossal nerve stimulation.
Nineteen Fischer 344/Brown Norway rats (9 old, 10 young adult) underwent tongue muscle contractile property recording elicited by: (1) bilateral whole hypoglossal nerve stimulation, and (2) selective lateral branch stimulation. Twitch contraction time (CT), half-decay time, maximal twitch and tetanic forces, and a fatigue index were measured.
For whole nerve stimulation, CT was significantly longer in the old group. No significant age group differences were found with selective lateral nerve stimulation. Significantly reduced twitch forces (old group only), increased tetanic forces and significantly less fatigue were found with selective lateral nerve stimulation than with whole hypoglossal stimulation.
Retrusive tongue forces are not impaired in old rats. Deficits observed in swallowing with aging may be due to other factors such as inadequate bolus propulsive forces, mediated by protrusive tongue muscles, or timing/coordination of muscle actions.
Jaw-opening and -closing premotoneurons in the nucleus of the solitary tract making contacts with laryngeal and pharyngeal afferent terminals in rats
2013, Brain Research
This study clarified the neural mechanisms underlying jaw movements in pharyngolaryngeal reflexes such as swallowing in rats. After retrograde tracer injections into the ventromedial division (Vmovm) of the trigeminal motor nucleus (Vmo) containing jaw-opening (JO) motoneurons or into the dorsolateral division (Vmodl) of Vmo containing jaw-closing (JC) motoneurons, JO and JC premotoneurons were labeled with an ipsilateral predominance in the medial and intermediate subnuclei of the rostrocaudal middle two-thirds of the nucleus of the solitary tract (Sol); JC premotoneurons were also in the lateral subnucleus of Sol. After anterograde tracer injections into the Sol, axons were labeled with an ipsilateral predominance in the Vmovm and Vmodl, prominently in the ipsilateral Vmovm. After transganglionic tracer applications to the superior laryngeal nerve (SLN) or the cervical trunk of the glossopharyngeal nerve (GpN-ct), labeled afferents were seen in the medial, intermediate, lateral and interstitial subnuclei of Sol at the rostral three-fourths of Sol, indicating considerable overlap with the JO and JC premotoneurons in the Sol. Double labeling experiments demonstrated contacts between the afferent terminals and the JO and JC premotoneurons. The present study has for the first time revealed the differential distribution of JO and JC premotoneurons in the Sol and features of their projections from the Sol, as well as their connections with SLN and GpN-ct afferent inputs. The JO and JC premotoneurons in the Sol may play an important role in generation and organization of jaw movements in pharyngolaryngeal reflexes evoked by SLN and GpN-ct inputs, such as swallowing.

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Brain Research

Abstract

Introduction

Section snippets

Surgical preparation

Properties of jaw movements and muscle activities during chewing cycles

Discussion

Acknowledgements

References (20)

Activity of extrinsic tongue muscles during swallowing in sheep

Brain Res.

Short electromyographic bursts in the rabbit digastric muscle during the jaw-closing phase

Arch. Oral Biol.

Mandibular joint control of genioglossus muscle activity in the cat (Felis domesticus) and monkey (Macaca irus)

Arch. Oral Biol.

The neural regulation of tongue movements

Prog. Neurobiol.

Characteristics of rhythmic jaw movements of the rabbit

Arch. Oral Biol.

The coordination of rhythmical drinking behavior with swallowing in rabbits

Physiol. Behav.

Two-dimensional jaw tracking and EMG recording system implanted in the freely moving rabbit

J. Neurosci. Methods

Possible factors which may affect phase durations in the natural chewing rhythm

Brain Res.

Videofluorographic analysis of tongue movement in the rabbit (Oryctolagus cuniculus)

J. Morphol.

An electromyographic analysis of reflex deglutition

J. Neurophysiol.

Cited by (49)

Tongue, palatal, hyoid and pharyngeal muscle activity during chewing, swallowing, and respiration

Beyond language: The unspoken sensory-motor representation of the tongue in non-primates, non-human and human primates

Effect of peripherally and cortically evoked swallows on jaw reflex responses in anesthetized rabbits

Tongue exercise and ageing effects on morphological and biochemical properties of the posterior digastric and temporalis muscles in a Fischer 344 Brown Norway rat model

Effects of aging on evoked retrusive tongue actions

Jaw-opening and -closing premotoneurons in the nucleus of the solitary tract making contacts with laryngeal and pharyngeal afferent terminals in rats

Research reportTongue and jaw muscle activities during chewing and swallowing in freely behaving rabbits

Abstract

Introduction

Section snippets

Surgical preparation

Properties of jaw movements and muscle activities during chewing cycles

Discussion

Acknowledgements

Brain Res.

Arch. Oral Biol.

Arch. Oral Biol.

Prog. Neurobiol.

Arch. Oral Biol.

Physiol. Behav.

J. Neurosci. Methods

Brain Res.

Videofluorographic analysis of tongue movement in the rabbit (Oryctolagus cuniculus)

J. Morphol.

An electromyographic analysis of reflex deglutition

J. Neurophysiol.

Research report
Tongue and jaw muscle activities during chewing and swallowing in freely behaving rabbits