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Inhibition of Water-Evoked Swallowing During Noxious Mechanical Stimulation of Tongue in Anesthetized Rats

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Abstract

Dysphagia is sometimes accompanied by pain. Because orofacial structures subserve mastication and swallowing, orofacial pain might impair both functions. Tongue biting can occur not only accidentally while eating but also in some pathological conditions. However, it remains unclear whether noxious mechanical stimulation of the tongue affects swallowing. To explore this question, we evaluated the effects of lingual pinch stimulation on the initiation of swallowing evoked by distilled water (DW) infusion with a flow rate of 5.0 µL/s for 20 s into the pharyngolaryngeal region in anesthetized rats. The swallowing reflex was identified by electromyographic (EMG) bursts in the suprahyoid muscles which include the anterior belly of the digastric muscle, mylohyoid and geniohyoid muscles, and laryngeal elevation by visual inspection. The number of DW-evoked swallows during pinch stimulation was significantly smaller than that in a control condition or during pressure stimulation. The onset latency of the first swallow during pinch stimulation was significantly longer than that in the control condition. DW-evoked swallowing was almost abolished following bilateral transection of the superior laryngeal nerve (SLN) compared with the control condition, suggesting that the SLN plays a crucial role in the initiation of DW-evoked swallowing. Finally, electrophysiological data indicated that some SLN-responsive neurons in the nucleus tractus solitarii (nTS) exhibited delayed latency from a single SLN stimulation during lingual pinch stimulation. These results suggest that noxious mechanical stimulation of the tongue inhibits the initiation of swallowing and modulates neuronal activity in the nTS.

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References

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

    Article  CAS  PubMed  Google Scholar 

  2. Ariji Y, Gotoh M, Kimura Y, Naitoh M, Kurita K, Natsume N, Ariji E. Odontogenic infection pathway to the submandibular space: imaging assessment. Int J Oral Maxillofac Surg. 2002;31:165–9.

    Article  CAS  PubMed  Google Scholar 

  3. Simoes J, Romao J, Cunha A, Paiva S, Migueis A. Neck pain and acute dysphagia. Dysphagia. 2017;32:123–5.

    Article  PubMed  Google Scholar 

  4. Svensson P, Arendt-Nielsen L, Houe L. Muscle pain modulates mastication: an experimental study in humans. J Orofac Pain. 1998;12:7–16.

    CAS  PubMed  Google Scholar 

  5. Fassicollo CE, Machado BCZ, Garcia DM, de Felicio CM. Swallowing changes related to chronic temporomandibular disorders. Clin Oral Investig. 2018;23(8):3287.

    Article  PubMed  Google Scholar 

  6. Vaiman M, Nahlieli O, Eliav E. Oynophagia in patients after dental extraction: surface electromyography study. Head Face Med. 2006;2:34.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Zoungrana OR, Lamkadem M, Amri M, Car A, Roman C. Effects of lingual nerve afferents on swallowing in sheep. Exp Brain Res. 2000;132:500–9.

    Article  CAS  PubMed  Google Scholar 

  8. Tominaga M, Tominaga T. Structure and function of TRPV1. Pflugers Arch. 2005;451:143–50.

    Article  CAS  PubMed  Google Scholar 

  9. van Amerongen G, de Boer MW, Groeneveld GJ, Hay JL. A literature review on the pharmacological sensitivity of human evoked hyperalgesia pain models. Br J Clin Pharmacol. 2016;82:903–22.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Benemei S, Patacchini R, Trevisani M, Geppetti P. TRP channels. Curr Opin Pharmacol. 2015;22:18–23.

    Article  CAS  PubMed  Google Scholar 

  11. Tsujimura T, Kitagawa J, Ueda K, Iwata K. Inhibition of swallowing reflex following phosphorylation of extracellular signal-regulated kinase in nucleus tractus solitarii neurons in rats with masseter muscle nociception. Neurosci Lett. 2009;450:361–4.

    Article  CAS  PubMed  Google Scholar 

  12. Tsujimura T, Kondo M, Kitagawa J, Tsuboi Y, Saito K, Tohara H, Ueda K, Sessle BJ, Iwata K. Involvement of ERK phosphorylation in brainstem neurons in modulation of swallowing reflex in rats. J Physiol. 2009;587:805–17.

    Article  CAS  PubMed  Google Scholar 

  13. Tsujimura T, Inoue M. Evaluation of the association between orofacial pain and dysphagia. J Oral Sci. 2020;62:156–9.

    Article  CAS  PubMed  Google Scholar 

  14. Fukumoto Y, Miyama T, Tanei ZI, Saito Y, Ota Y. Reactive bite-related tongue lesions in cognitively impaired epilepsy patients: a report of two cases. Spec Care Dentist. 2020;40:285–90.

    Article  PubMed  Google Scholar 

  15. Kajii Y, Shingai T, Kitagawa J, Takahashi Y, Taguchi Y, Noda T, Yamada Y. Sour taste stimulation facilitates reflex swallowing from the pharynx and larynx in the rat. Physiol Behav. 2002;77:321–5.

    Article  CAS  PubMed  Google Scholar 

  16. Tsujimura T, Suzuki T, Yoshihara M, Sakai S, Koshi N, Ashiga H, Shiraishi N, Tsuji K, Magara J, Inoue M. Involvement of hypoglossal and recurrent laryngeal nerves on swallowing pressure. J Appl Physiol. 1985;124(1148–1154):2018.

    Google Scholar 

  17. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 6th ed. Amsterdam: Elsevier; 2007.

    Google Scholar 

  18. Shimizu K, Asano M, Kitagawa J, Ogiso B, Ren K, Oki H, Matsumoto M, Iwata K. Phosphorylation of extracellular signal-regulated kinase in medullary and upper cervical cord neurons following noxious tooth pulp stimulation. Brain Res. 2006;1072:99–109.

    Article  CAS  PubMed  Google Scholar 

  19. Sunakawa M, Chiang YC, Sessle JB, Hu JW. Jaw electromyographic activity induced by the application of algesic chemicals to the rat tooth pulp. Pain. 1999;80:493–501.

    Article  CAS  PubMed  Google Scholar 

  20. Bellingham MC, Lipski J. Morphology and electrophysiology of superior laryngeal nerve afferents and postsynaptic neurons in the medulla oblongata of the cat. Neuroscience. 1992;48:205–16.

    Article  CAS  PubMed  Google Scholar 

  21. Umezaki T, Matsuse T, Shin T. Medullary swallowing-related neurons in the anesthetized cat. NeuroReport. 1998;9:1793–8.

    Article  CAS  PubMed  Google Scholar 

  22. Wang K, Arendt-Nielsen L, Svensson P. Capsaicin-induced muscle pain alters the excitability of the human jaw-stretch reflex. J Dent Res. 2002;81:650–4.

    Article  CAS  PubMed  Google Scholar 

  23. Peddireddy A, Wang K, Svensson P, Arendt-Nielsen L. Effect of experimental posterior temporalis muscle pain on human brainstem reflexes. Clin Neurophysiol. 2005;116:1611–20.

    Article  PubMed  Google Scholar 

  24. Hirata K, Nishiki Y, Goto R, Inagaki M, Oshima K, Shimazu Y, Takeda M. Resveratrol suppresses nociceptive jaw-opening reflex via 5HT3 receptor-mediated GABAergic inhibition. Neurosci Res. 2020;160:25–31.

    Article  CAS  PubMed  Google Scholar 

  25. Yang J, Turker KS. Jaw reflexes evoked by mechanical stimulation of teeth in humans. J Neurophysiol. 1999;81:2156–63.

    Article  CAS  PubMed  Google Scholar 

  26. Hill RZ, Bautista DM. Getting in touch with mechanical pain mechanisms. Trends Neurosci. 2020;43:311–25.

    Article  CAS  PubMed  Google Scholar 

  27. Tsujimura T, Ueha R, Yoshihara M, Takei E, Nagoya K, Shiraishi N, Magara J, Inoue M. Involvement of the epithelial sodium channel in initiation of mechanically evoked swallows in anaesthetized rats. J Physiol. 2019;597:2949–63.

    Article  CAS  PubMed  Google Scholar 

  28. Mazzone SB, Undem BJ. Vagal afferent innervation of the airways in health and disease. Physiol Rev. 2016;96:975–1024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Kupari J, Haring M, Agirre E, Castelo-Branco G, Ernfors P. An atlas of vagal sensory neurons and their molecular specialization. Cell Rep. 2019;27:2508.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Corson J, Aldridge A, Wilmoth K, Erisir A. A survey of oral cavity afferents to the rat nucleus tractus solitarii. J Comp Neurol. 2012;520:495–527.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Van Giersbergen P, Palkovits M, De Jong W. Involvement of neurotransmitters in the nucleus tractus solitarii in cardiovascular regulation. Physiol Rev. 1992;72:789–824.

    Article  PubMed  Google Scholar 

  32. Kessler JP, Jean A. Identification of the medullary swallowing regions in the rat. Exp Brain Res. 1985;57:256–63.

    Article  CAS  PubMed  Google Scholar 

  33. Saito Y, Ezure K, Tanaka I. Swallowing-related activities of respiratory and non-respiratory neurons in the nucleus of solitary tract in the rat. J Physiol. 2002;540:1047–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Sugiyama Y, Shiba K, Nakazawa K, Suzuki T, Umezaki T, Ezure K, Abo N, Yoshihara T, Hisa Y. Axonal projections of medullary swallowing neurons in guinea pigs. J Comp Neurol. 2011;519:2193–211.

    Article  PubMed  Google Scholar 

  35. Boscan P, Paton JF. Integration of cornea and cardiorespiratory afferents in the nucleus of the solitary tract of the rat. Am J Physiol Heart Circ Physiol. 2002;282:H1278-1287.

    Article  CAS  PubMed  Google Scholar 

  36. Barraco R, El-Ridi M, Ergene E, Parizon M, Bradley D. An atlas of the rat subpostremal nucleus tractus solitarius. Brain Res Bull. 1992;29:703–65.

    Article  CAS  PubMed  Google Scholar 

  37. Kalia M, Sullivan JM. Brainstem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol. 1982;211:248–65.

    Article  CAS  PubMed  Google Scholar 

  38. Jacquin MF, Semba K, Egger MD, Rhoades RW. Organization of HRP-labeled trigeminal mandibular primary afferent neurons in the rat. J Comp Neurol. 1983;215:397–420.

    Article  CAS  PubMed  Google Scholar 

  39. Marfurt CF, Rajchert DM. Trigeminal primary afferent projections to “non-trigeminal” areas of the rat central nervous system. J Comp Neurol. 1991;303:489–511.

    Article  CAS  PubMed  Google Scholar 

  40. Zhang WB, Li JS, Li HM. SP-like immunoreactivity in the primary trigeminal neurons projecting to the nucleus tractus solitarii. Brain Res. 1991;558:87–9.

    Article  CAS  PubMed  Google Scholar 

  41. Caous CA, de Sousa BH, Lindsey CJ. Neuronal connections of the paratrigeminal nucleus: a topographic analysis of neurons projecting to bulbar, pontine and thalamic nuclei related to cardiovascular, respiratory and sensory functions. Auton Neurosci. 2001;94:14–24.

    Article  CAS  PubMed  Google Scholar 

  42. de Sousa BH, Caous CA, Lindsey CJ. Projections of the paratrigeminal nucleus to the ambiguus, rostroventrolateral and lateral reticular nuclei, and the solitary tract. Auton Neurosci. 2001;87:187–200.

    Article  Google Scholar 

  43. Yamazaki Y, Ren K, Shimada M, Iwata K. Modulation of paratrigeminal nociceptive neurons following temporomandibular joint inflammation in rats. Exp Neurol. 2008;214:209–18.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Canning BJ, Mazzone SB, Meeker SN, Mori N, Reynolds SM, Undem BJ. Identification of the tracheal and laryngeal afferent neurones mediating cough in anaesthetized guinea-pigs. J Physiol. 2004;557:543–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ma WL, Zhang WB, Xiong KH, Guo F. Visceral and orofacial somatic afferent fiber terminals converge onto the same neuron in paratrigeminal nucleus: an electron microscopic study in rats. Auton Neurosci-Basic. 2007;131:45–9.

    Article  Google Scholar 

  46. Sugiyama Y, Shiba K, Mukudai S, Umezaki T, Sakaguchi H, Hisa Y. Role of the retrotrapezoid nucleus/parafacial respiratory group in coughing and swallowing in guinea pigs. J Neurophysiol. 2015;114:1792–805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Bonis JM, Neumueller SE, Krause KL, Pan LG, Hodges MR, Forster HV. Contributions of the Kolliker-Fuse nucleus to coordination of breathing and swallowing. Respir Physiol Neurobiol. 2013;189:10–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Bonis JM, Neumueller SE, Marshall BD, Krause KL, Qian B, Pan LG, Hodges MR, Forster HV. The effects of lesions in the dorsolateral pons on the coordination of swallowing and breathing in awake goats. Respir Physiol Neurobiol. 2011;175:272–82.

    Article  CAS  PubMed  Google Scholar 

  49. Bautista TG, Dutschmann M. Ponto-medullary nuclei involved in the generation of sequential pharyngeal swallowing and concomitant protective laryngeal adduction in situ. J Physiol. 2014;592:2605–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Dutschmann M, Bautista TG, Trevizan-Bau P, Dhingra RR, Furuya WI. The pontine Kolliker-Fuse nucleus gates facial, hypoglossal, and vagal upper airway related motor activity. Respir Physiol Neurobiol. 2021;284:103563.

    Article  CAS  PubMed  Google Scholar 

  51. McGovern AE, Driessen AK, Simmons DG, Powell J, Davis-Poynter N, Farrell MJ, Mazzone SB. Distinct brainstem and forebrain circuits receiving tracheal sensory neuron inputs revealed using a novel conditional anterograde transsynaptic viral tracing system. J Neurosci. 2015;35:7041–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was supported in part by a grant from JSPS KAKENHI (Grant Numbers 20KK0353 to T.T.). We thank Mamoru Takeda at Azabu University for advice on pain behavior and Benjamin Knight, MSc., from Edanz (https://jp.edanz.com/ac) for editing a draft of this manuscript.

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Authors and Affiliations

  1. Division of Dysphagia Rehabilitation, Niigata University Graduate School of Medical and Dental Sciences, Chuo-ku, Niigata, 951-8514, Japan

    Takanori Tsujimura, Yuta Nakajima, Titi Chotirungsan, Satomi Kawada, Yuhei Tsutsui, Midori Yoshihara, Taku Suzuki, Kouta Nagoya, Jin Magara & Makoto Inoue

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  1. Takanori Tsujimura
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Correspondence to Takanori Tsujimura.

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Tsujimura, T., Nakajima, Y., Chotirungsan, T. et al. Inhibition of Water-Evoked Swallowing During Noxious Mechanical Stimulation of Tongue in Anesthetized Rats. Dysphagia 38, 965–972 (2023). https://doi.org/10.1007/s00455-022-10522-5

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