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The Digastric Muscle is Less Involved in Pharyngeal Swallowing in Rabbits

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Abstract

The swallowing reflex is centrally programmed by the lower brain stem, the so-called swallowing central pattern generator (CPG), and once the reflex is initiated, many muscles in the oral, pharyngeal, laryngeal, and esophageal regions are systematically activated. The mylohyoid (MH) muscle has been considered to be a “leading muscle” according to previous studies, but the functional role of the digastric (DIG) muscle in the swallowing reflex remains unclear. In the present study, therefore, the activities of single units of MH and DIG neurons were recorded extracellularly, and the functional involvement of these neurons in the swallowing reflex was investigated. The experiments were carried out on eight adult male Japanese white rabbits anesthetized with urethane. To identify DIG and MH neurons, the peripheral nerve (either DIG or MH) was stimulated to evoke action potentials of single motoneurons. Motoneurons were identified as such if they either (1) responded to antidromic nerve stimulation of DIG or MH in an all-or-none manner at threshold intensities and (2) followed stimulation frequencies of up to 0.5 kHz. As a result, all 11 MH neurons recorded were synchronously activated during the swallowing reflex, while there was no activity in any of the 7 DIG neurons recorded during the swallowing reflex. All neurons were anatomically localized ventromedially at the level of the caudal portion of the trigeminal motor nucleus, and there were no differences between the MH and DIG neuron sites. The present results strongly suggest that at least in the rabbit, DIG motoneurons are not tightly controlled by the swallowing CPG and, hence, the DIG muscle is less involved in the swallowing reflex.

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References

  1. Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81:929–69.

    PubMed  CAS  Google Scholar 

  2. Doty RW, Bosma JF. An electromyographic analysis of reflex deglutition. J Neurophysiol. 1956;19:44–60.

    PubMed  CAS  Google Scholar 

  3. Thexton AJ, Crompton AW, German RZ. Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited. J Appl Physiol. 2007;102:587–600.

    Article  PubMed  CAS  Google Scholar 

  4. Naganuma K, Inoue M, Yamamura K, Hanada K, Yamada Y. Tongue and jaw muscle activities during chewing and swallowing in freely behaving rabbits. Brain Res. 2001;915:185–94.

    Article  PubMed  CAS  Google Scholar 

  5. Takata H. A comparative anatomical study on suprahyoid muscles. Kyushu Dental Soc. 1989;43:899–913.

    Google Scholar 

  6. Inoue M, Nozawa-Inoue K, Donga R, Yamada Y. Convergence of selected inputs from sensory afferents to trigeminal premotor neurons with possible projections to masseter motoneurons in the rabbit. Brain Res. 2002;957:183–91.

    Article  PubMed  CAS  Google Scholar 

  7. Donga R, Lund JP, Veilleux D. An electrophysiological study of trigeminal commissural interneurons in the anaesthetized rabbit. Brain Res. 1990;515:351–4.

    Article  PubMed  CAS  Google Scholar 

  8. Landgren S, Olsson KA. Localization of evoked potentials in the digastric, masseteric, supra- and intertrigeminal subnuclei of the cat. Exp Brain Res. 1976;26:299–318.

    Article  PubMed  CAS  Google Scholar 

  9. Meessen H, Olszewski J. Cytoarchitektonischer Atlas des Rautenhirns des Kaninchens. Basel: Karger; 1949.

    Google Scholar 

  10. Weijs WA, Dantuma R. Functional anatomy of the masticatory apparatus in the rabbit. Netherlands J Zool. 1981;31:99–147.

    Article  Google Scholar 

  11. Fukuhara T, Tsujimura T, Kajii Y, Yamamura K, Inoue M. Effects of electrical stimulation of the superior laryngeal nerve on the jaw-opening reflex. Brain Res. 2011;1391:44–53.

    Article  PubMed  CAS  Google Scholar 

  12. Sumi T. Modification of cortically evoked rhythmic jaw movements by reflex deglutition in rabbits. Jpn J Physiol. 1977;27:391–8.

    Article  PubMed  CAS  Google Scholar 

  13. Takagi M, Noda T, Yamada Y. Comparison of SLN-evoked swallows during rest and chewing in the freely behaving rabbit. Brain Res. 2002;956:74–80.

    Article  PubMed  CAS  Google Scholar 

  14. Lund JP. Mastication and its control by the brain stem. Crit Rev Oral Biol Med. 1991;2:33–64.

    PubMed  CAS  Google Scholar 

  15. Nakamura Y, Katakura N. Generation of masticatory rhythm in the brainstem. Neurosci Res. 1995;23:1–19.

    PubMed  CAS  Google Scholar 

  16. Yamada Y, Yamamura K, Inoue M. Coordination of cranial motoneurons during mastication. Respir Physiol Neurobiol. 2005;147:177–89.

    Article  PubMed  Google Scholar 

  17. Amarasena J, Ootaki S, Yamamura K, Yamada Y. Effect of cortical masticatory area stimulation on swallowing in anesthetized rabbits. Brain Res. 2003;965:222–38.

    Article  PubMed  CAS  Google Scholar 

  18. Meng Y, Uchida K, Sato T, Yamamura K, Yamada Y. Difference in the burst patterns of digastric and mylohyoid activities during feeding in the freely behaving rabbit. Dysphagia. 1999;14:78–84.

    Article  PubMed  CAS  Google Scholar 

  19. Konow N, Thexton A, Crompton AW, German RZ. Regional differences in length change and electromyographic heterogeneity in sternohyoid muscle during infant mammalian swallowing. J Appl Physiol. 2010;109:439–48.

    Article  PubMed  Google Scholar 

  20. Umapathi T, Venketasubramanian N, Leck KJ, Tan CB, Lee WL, Tjia H. Tongue deviation in acute ischaemic stroke: a study of supranuclear twelfth cranial nerve palsy in 300 stroke patients. Cerebrovasc Dis. 2000;10:462–5.

    Article  PubMed  CAS  Google Scholar 

  21. van Lunteren E, Dick TE. Heterogeneity within geniohyoid motor unit subpopulations in firing patterns during breathing. Respir Physiol. 2001;124:23–33.

    Article  PubMed  Google Scholar 

  22. Baisden RH, Woodruff ML, Whittington DL, Benson AE. The motor innervation of the single-bellied digastric muscle in the rabbit: a retrograde horseradish peroxidase study. Neurosci Lett. 1985;56:129–36.

    Article  PubMed  CAS  Google Scholar 

  23. German RZ, Campbell-Malone R, Crompton AW, Ding P, Holman S, Konow N, Thexton AJ. The concept of hyoid posture. Dysphagia. 2011;26(2):97–8.

    Article  PubMed  Google Scholar 

  24. Matsuda K, Uemura M, Kume M, Matsushima R, Mizuno N. Topographical representation of masticatory muscles in the motor trigeminal nucleus in the rabbit: a HRP study. Neurosci Lett. 1978;8:1–4.

    Article  PubMed  CAS  Google Scholar 

  25. Inoue M, Ariyasinghe S, Yamamura K, Harasawa Y, Yamada Y. Extrinsic tongue and suprahyoid muscle activities during mastication in freely feeding rabbits. Brain Res. 2004;1021:173–82.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Mr. Hidetoshi Hirano for technical assistance. This study was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (#23659982 to M.I.).

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Correspondence to Makoto Inoue.

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Tsujimura, T., Yamada, A., Nakamura, Y. et al. The Digastric Muscle is Less Involved in Pharyngeal Swallowing in Rabbits. Dysphagia 27, 271–276 (2012). https://doi.org/10.1007/s00455-011-9363-z

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  • DOI: https://doi.org/10.1007/s00455-011-9363-z

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