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Brainstem Control of Deglutition: Brainstem Neural Circuits and Mediators Regulating Swallowing

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Book cover Principles of Deglutition

Abstract

Swallowing requires coordination of several paired muscle groups in the head and neck including the diaphragm. Thus, motoneurons of the Vth, VIIth, IX through XIIth cranial, cervical spinal, and phrenic nerves are sequentially activated by a swallowing pattern generator (SPG) located in the lower brainstem for executing the oral, pharyngeal, and esophageal stages of swallowing. Independence of these stages from each other indicates distinct subcircuits, their coupling pointing to flexible links between them. Although intrinsically autonomous, the SPG depends on peripheral and suprabulbar afferents for proper functioning. Pivotal to both, integrating afferents and coordinating stage-specific subcircuits, are the nucleus tractus solitarii (NTS) with some of its subnuclei and their reciprocal interconnections with the brainstem reticular formation. This chapter provides a survey of the anatomical and functional organization of the SPG.

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References

  1. Bidder F. Beiträge zur Kenntniss der Wirkungen des Nervus laryngeus superior. Arch Anat Physiol Wissensch Med. 1856;322:492–507.

    Google Scholar 

  2. Mosso A. Über die Bewegungen der Speiserohre. Moleschotts Untersuch Naturlehre Menschen Thiere. 1876;11:327–49.

    Google Scholar 

  3. Miller FR, Sherrington CS. Some observations on the buccopharyngeal stage of reflex deglutition in the cat. Q J Exp Physiol. 1916;9:147–86.

    Google Scholar 

  4. Doty RW. The concept of neural centers. In: Fentress JC, editor. Simpler networks and behavior. Sunderland: Sinauer Associates; 1976. p. 251–65.

    Google Scholar 

  5. Miller AJ, Bieger D, Conklin J. Functional controls of deglutition. In: Perlman AL, Schulze-Delrieu K, editors. Deglutition and its disorders. San Diego: Singular; 1997. p. 43–97.

    Google Scholar 

  6. Paton JFR, Li Y-W, Kasparov S. Reflex response and convergence of pharyngoesophageal and peripheral chemoreceptors in the nucleus of the solitary tract. Neuroscience. 1999;93:143–54.

    Article  PubMed  CAS  Google Scholar 

  7. Salinas E, Abbott LF. Transfer of coded information from sensory to motor networks. J Neurosci. 1995;15:6461–74.

    PubMed  CAS  Google Scholar 

  8. Bieger D. Neuropharmacologic correlates of deglutition: lessons from fictive swallowing. Dysphagia. 1991;6:147–64.

    Article  PubMed  CAS  Google Scholar 

  9. Bieger D, Neuhuber WL. Neural circuits and mediators regulating swallowing in the brainstem. GI Motility online. 2006;doi:10.1038/gimo74.

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

    PubMed  CAS  Google Scholar 

  11. Lang IM. Brain stem control of the phases of swallowing. Dysphagia. 2009;24:333–48.

    Article  PubMed  Google Scholar 

  12. Doty RW. Neural organization of deglutition. In: Code CF, editor. Handbook of physiology, The alimentary canal, Section 6, vol IV. Washington, DC: American Physiological Society; 1968. p. 1861–902.

    Google Scholar 

  13. Rogers RC, Hermann GE, Travagli RA. Brainstem pathways responsible for oesophageal control of gastric motility and tone in the rat. J Physiol London. 1999;514:369–83.

    Article  PubMed  CAS  Google Scholar 

  14. Rossiter CD, Norman WP, Jain M, Hornby PJ, Benjamin S, Gillis RA. Control of lower esophageal sphincter pressure by two sites in dorsal motor nucleus of the vagus. Am J Physiol. 1990;259:G899–909.

    PubMed  CAS  Google Scholar 

  15. Sang Q, Goyal RK. Lower esophageal sphincter relaxation and activation of medullary neurons by subdiaphragmatic vagal stimulation in the mouse. Gastroenterology. 2000;119:1600–9.

    Article  PubMed  CAS  Google Scholar 

  16. Gordon DC, Richmond FJ. Distribution of motoneurons supplying dorsal suboccipital and intervertebral muscles in the cat neck. J Comp Neurol. 1991;304:343–56.

    Article  PubMed  CAS  Google Scholar 

  17. Gottschall J, Neuhuber W, Müntener M, Mysicka A. The ansa cervicalis and the infrahyoid muscles of the rat. II. Motor and sensory neurons. Anat Embryol. 1980;159:59–69.

    Article  PubMed  CAS  Google Scholar 

  18. Krammer EB, Lischka MF, Egger TP, Riedl M, Gruber H. The motoneuronal organization of the spinal accessory nuclear complex. Adv Anat Embryol Cell Biol. 1987;103:1–62.

    PubMed  CAS  Google Scholar 

  19. Richmond FJ, Scott DA, Abrahams VC. Distribution of motoneurons to the neck muscles, biventer cervicis, splenius and complexus in the cat. J Comp Neurol. 1978;181:451–63.

    Article  PubMed  CAS  Google Scholar 

  20. Altschuler SM. Laryngeal and respiratory protective reflexes. Am J Med. 2001;111(8A):90S–4.

    Article  PubMed  Google Scholar 

  21. Bieger D, Hopkins DA. Viscerotopic representation of the upper alimentary tract in the medulla oblongata of the rat: the nucleus ambiguus. J Comp Neurol. 1987;262:546–62.

    Article  PubMed  CAS  Google Scholar 

  22. Hopkins DA, Bieger D, DeVente J, Steinbusch HWM. Vagal efferent projections: viscerotopy, neurochemistry and effects of vagotomy. In: Holstege G, Bandler R, Saper CB, editors. The emotional motor system, Prog Brain Res. 107. p. 79–96.

    Google Scholar 

  23. Blessing WW, Oertel WH, Willoughby JO. Glutamic acid decarboxylase immunoreactivity is present in perikarya of neurons in nucleus tractus solitarius of rat. Brain Res. 1984;322:346–50.

    Article  PubMed  CAS  Google Scholar 

  24. Lewis DI. Dye-coupling between vagal motoneurones within the compact region of the adult rat nucleus ambiguus, in vitro. J Auton Nerv Syst. 1994;47:53–8.

    Article  PubMed  CAS  Google Scholar 

  25. Cunningham Jr ET, Sawchenko PE. Central neural control of esophageal motility: a review. Dysphagia. 1990;5:35–51.

    Article  PubMed  CAS  Google Scholar 

  26. Hopkins DA. Ultrastructure and synaptology of the nucleus ambiguus in the rat: the compact formation. J Comp Neurol. 1995;360:705–25.

    Article  PubMed  CAS  Google Scholar 

  27. Dütsch M, Eichhorn U, Wörl J, Wank M, Berthoud HR, Neuhuber WL. Vagal and spinal afferent innervation of the rat esophagus: a combined retrograde tracing and immunocytochemical study with special emphasis on calcium-binding proteins. J Comp Neurol. 1998;398:289–307.

    Article  PubMed  Google Scholar 

  28. Neuhuber WL, Wörl J, Berthoud HR, Conte B. NADPH-diaphorase-positive nerve fibers associated with motor end plates in the rat esophagus: evidence for co-innervation of striated muscle by enteric ganglia. Cell Tissue Res. 1994;276:23–30.

    Article  PubMed  CAS  Google Scholar 

  29. Wörl J, Neuhuber WL. Enteric co-innervation of motor endplates in the esophagus: state of the art ten years after. Histochem Cell Biol. 2005;123:117–30.

    Article  PubMed  CAS  Google Scholar 

  30. Boudaka A, Worl J, Shiina T, Neuhuber WL, Kobayashi H, Shimizu Y, Takewaki T. Involvement of TRPV1-dependent and -independent components in the regulation of vagally induced contractions in the mouse esophagus. Eur J Pharmacol. 2007;556:157–65.

    Article  PubMed  CAS  Google Scholar 

  31. Boudaka A, Wörl J, Shiina T, Shimizu Y, Takewaki T, Neuhuber WL. Galanin modulates vagally induced contractions in the mouse oesophagus. Neurogastroen­terol Motil. 2009;21:180–8.

    Article  PubMed  CAS  Google Scholar 

  32. Izumi N, Matsuyama H, Ko M, Shimizu Y, Takewaki T. Role of intrinsic nitrergic neurons on vagally mediated striated muscle contractions in the hamster oesophagus. J Physiol. 2003;551:287–94.

    Article  PubMed  CAS  Google Scholar 

  33. Wang YT, Neuman RS, Bieger D. Nicotinic cholinoceptor-mediated excitation in ambiguual motoneurons of the rat. Neuroscience. 1991;40:759–67.

    Article  PubMed  CAS  Google Scholar 

  34. Neuhuber WL, Raab M, Berthoud HR, Worl J. Innervation of the mammalian esophagus. Adv Anat Embryol Cell Biol. 2006;185:1–73.

    Article  PubMed  Google Scholar 

  35. Mittal RK. The crural diaphragm, an external lower esophageal sphincter: a definitive study. Gastroenterology. 1993;105:1565–7.

    Article  PubMed  CAS  Google Scholar 

  36. Pickering M, Jones JFX. The diaphragm: two physiological muscles in one. J Anat. 2002;201:305–12.

    Article  PubMed  Google Scholar 

  37. Niedringhaus M, Jackson PG, Evans SRT, Verbalis JG, Gillis RA, Sahibzada N. Dorsal motor nucleus of the vagus: a site for evoking simultaneous changes in crural diaphragm activity, lower esophageal sphincter pressure, and fundus tone. Am J Physiol Regul Integr Comp Physiol. 2008;294:R121–31.

    Article  PubMed  CAS  Google Scholar 

  38. Niedringhaus M, Jackson PG, Pearson R, Shi M, Dretchen K, Gillis RA, Sahibzada N. Brainstem sites controlling the lower esophageal sphincter and crural diaphragm in the ferret: a neuroanatomical study. Auton Neurosci. 2008;144:50–60.

    Article  PubMed  Google Scholar 

  39. Young RL, Page AJ, Cooper NJ, Frisby CL, Blackshaw LA. Sensory and motor innervation of the crural diaphragm by the vagus nerves. Gastroenterology. 2010;138:1091–101.

    Article  PubMed  Google Scholar 

  40. Yates BJ, Smail JA, Stocker ST, Card JP. Transneuronal tracing of neural pathways controlling activity of diaphragm motoneurons in the ferret. Neuroscience. 1999;90:1501–13.

    Article  PubMed  CAS  Google Scholar 

  41. Liu J, Yamamoto Y, Schirmer BD, Ross RA, Mittal RK. Evidence for a peripheral mechanism of esophagocrural diaphragm inhibitory reflex in cats. Am J Physiol. 2000;278:G281–8.

    CAS  Google Scholar 

  42. Marfurt CF, Rajchert DM. Trigeminal primary afferent projections to “non-trigeminal” areas of the rat central nervous system. J Comp Neurol. 1991;355:489–511.

    Article  Google Scholar 

  43. Pfaller K, Arvidsson J. Central distribution of trigeminal and upper cervical primary afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin. J Comp Neurol. 1988;268:91–108.

    Article  PubMed  CAS  Google Scholar 

  44. Dessem D, Luo P. Jaw-muscle spindle afferent feedback to the cervical spinal cord in the rat. Exp Brain Res. 1999;128:451–9.

    Article  PubMed  CAS  Google Scholar 

  45. Mehler WR. Observations on the connectivity of the parvicellular reticular formation with respect to a vomiting center. Brain Behav Evol. 1983;23:63–80.

    Article  PubMed  CAS  Google Scholar 

  46. Zhang J, Yang R, Pendlebery W, Luo P. Monosynaptic circuitry of trigeminal proprioceptive afferents coordinating jaw movement with visceral and laryngeal activities in rats. Neuroscience. 2005;135:497–505.

    Article  PubMed  CAS  Google Scholar 

  47. Zhang J, Luo P, Pendlebury WW. Light and electron microscopic observations of a direct projection from mesencephalic trigeminal nucleus neurons to hypoglossal motoneurons in the rat. Brain Res. 2001;917:67–80.

    Article  PubMed  CAS  Google Scholar 

  48. Altschuler SM, Bao X, Bieger D, Hopkins DA, Miselis RR. Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol. 1989;283:248–68.

    Article  PubMed  CAS  Google Scholar 

  49. Hamilton RB, Norgren R. Central projections of gustatory nerves in the rat. J Comp Neurol. 1984;222:560–77.

    Article  PubMed  CAS  Google Scholar 

  50. Hayakawa T, Takanaga A, Maeda S, Seki M, Yajima Y. Subnuclear distribution of afferents from the oral, pharyngeal and laryngeal regions in the nucleus tractus solitarii of the rat: a study using transganglionic transport of cholera toxin. Neurosci Res. 2001;39:221–32.

    Article  PubMed  CAS  Google Scholar 

  51. Nomura S, Mizuno N. Central distribution of efferent and afferent components of the cervical branches of the vagus nerve: a HRP study in the cat. Anat Embryol (Berl). 1983;166:1–18.

    Article  CAS  Google Scholar 

  52. Lu W-Y. Oesophageal premotor mechanisms in the rat. Ph.D. thesis, Memorial University of Newfoundland (1996).

    Google Scholar 

  53. Wank M, Neuhuber WL. Local differences in vagal afferent innervation of the rat esophagus are reflected by neurochemical differences at the level of sensory ganglia and by different brainstem projections. J Comp Neurol. 2001;435:41–59.

    Article  PubMed  CAS  Google Scholar 

  54. Wang YT, Bieger D. Role of solitarial GABA-ergic mechanisms in control of swallowing. Am J Physiol. 1991;161:R639–46.

    Google Scholar 

  55. Patrickson JW, Smith TE, Zhou S-S. Afferent projections of the superior and recurrent laryngeal nerves. Brain Res. 1991;539:169–74.

    Article  PubMed  CAS  Google Scholar 

  56. Neuhuber W, Sandoz PA. Vagal primary afferent terminals in the dorsal motor nucleus of the rat: are they making monosynaptic contact with preganglionic efferent neurons? Neurosci Lett. 1982;69:126–30.

    Article  Google Scholar 

  57. Rinaman L, Card JP, Schwaber JS, Miselis RR. Ultrastructural demonstration of a gastric monosynaptic vagal circuit in the nucleus of the solitary tract. J Neurosci. 1989;9:1985–96.

    PubMed  CAS  Google Scholar 

  58. Saha S, Batten TF, McWilliam PN. Glutamate- immunoreactivity in identified vagal afferent terminals of the cat: a study combining horseradish peroxidase tracing and postembedding electron microscopic immunogold staining. Exp Physiol. 1995;80:193–202.

    PubMed  CAS  Google Scholar 

  59. Paton JFR, Kasparov S. Sensory channel specific modulation in the nucleus of the solitary tract. J Autonom Nerv Syst. 2000;80:117–29.

    Article  CAS  Google Scholar 

  60. Hayakawa T, Takanaga A, Tanaka K, Maeda S, Seki M. Ultrastructure of the central subnucleus of the nucleus tractus solitarii and the esophageal afferent terminals in the rat. Anat Embryol. 2003;206:273–81.

    PubMed  Google Scholar 

  61. Mrini A, Jean A. Synaptic organization of the interstitial subdivision of the nucleus tractus solitarii and of its laryngeal afferents in the rat. J Comp Neurol. 1995;355:221–36.

    Article  PubMed  CAS  Google Scholar 

  62. Atkinson L, Batten TF, Corbett EK, Sinfield JK, Deuchars J. Subcellular localization of neuronal nitric oxide synthase in the rat nucleus of the solitary tract in relation to vagal afferent inputs. Neuroscience. 2003;118:115–22.

    Article  PubMed  CAS  Google Scholar 

  63. Broussard DL, Bao X, Altschuler SM. Somatostatin immunoreactivity in esophageal premotor neurons of the rat. Neurosci Lett. 1998;250:201–4.

    Article  PubMed  CAS  Google Scholar 

  64. Cunningham Jr ET, Sawchenko PE. A circumscribed projection from the nucleus of the solitary tract to the nucleus ambiguus in the rat: anatomical evidence for somatostatin-28-immunoreactive interneurons subserving reflex control of esophageal motility. J Neurosci. 1989;9:1668–82.

    PubMed  Google Scholar 

  65. Rogers RC, Travagli RA, Hermann GE. Noradrenergic neurons in the rat solitary nucleus participate in the esophageal-gastric relaxation reflex. Am J Physiol Integr Comp Physiol. 2003;285:R479–89.

    CAS  Google Scholar 

  66. Dong HH, Loomis CW, Bieger D. Distal and deglutitive inhibition in the rat esophagus: role of inhibitory neurotransmission in the nucleus tractus solitarii. Gastroenterology. 2000;118:328–36.

    Article  PubMed  CAS  Google Scholar 

  67. Broussard DL, Li X, Altschuler SM. Localization of GABAA alpha 1 mRNA subunit in the brainstem nuclei controlling esophageal peristalsis. Mol Brain Res. 1996;40:143–7.

    Article  PubMed  CAS  Google Scholar 

  68. Hayakawa T, Yajima Y, Zyo K. Ultrastructural characterization of pharyngeal and esophageal motoneurons in the nucleus ambiguus of the rat. J Comp Neurol. 1996;370:135–46.

    Article  PubMed  CAS  Google Scholar 

  69. Hayakawa T, Zheng JQ, Yajima Y. Direct synaptic projections to esophageal motoneurons in the nucleus ambiguus from the nucleus of the solitary tract of the rat. J Comp Neurol. 1997;381:18–30.

    Article  PubMed  CAS  Google Scholar 

  70. Hayakawa T, Zheng JQ, Seki M, Yajima Y. Synaptology of the direct projections from the nucleus of the solitary tract to pharyngeal motoneurons in the nucleus ambiguus of the rat. J Comp Neurol. 1998;393:391–401.

    Article  PubMed  CAS  Google Scholar 

  71. Saxon DW, Robertson GN, Hopkins DA. Ultrastructure and synaptology of the nucleus ambiguus in the rat: the semicompact and loose formations. J Comp Neurol. 1996;375:109–27.

    Article  PubMed  CAS  Google Scholar 

  72. Ross CA, Ruggiero DA, Reis DJ. Projections from the nucleus tractus solitarii to the rostral ventrolateral medulla. J Comp Neurol. 1985;242:511–34.

    Article  PubMed  CAS  Google Scholar 

  73. Cunningham Jr ET, Sawchenko PE. Dorsal medullary pathways subserving oromotor reflexes in the rat: implications for the central neural control of swallowing. J Comp Neurol. 2000;417:448–66.

    Article  PubMed  Google Scholar 

  74. Zerari-Mailly F, Pinganaud G, Dauvergne C, Buisseret P, Buisseret-Delmas C. Trigemino-reticulo-facial and trigemino-reticulo-hypoglossal pathways in the rat. J Comp Neurol. 2001;429:80–93.

    Article  PubMed  CAS  Google Scholar 

  75. Saxon DW, Hopkins DA. Efferent and collateral organization of paratrigeminal nucleus projections: an anterograde and retrograde fluorescent tracer study. J Comp Neurol. 1998;402:93–110.

    Article  PubMed  CAS  Google Scholar 

  76. Herbert H, Moga MM, Saper CB. Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J Comp Neurol. 1990;293:540–80.

    Article  PubMed  CAS  Google Scholar 

  77. Ruggiero DA, Giuliano R, Anwar M, Stornetta R, Reis DJ. Anatomical substrates of cholinergic-autonomic regulation in the rat. J Comp Neurol. 1990;292:1–53.

    Article  PubMed  CAS  Google Scholar 

  78. Tago H, McGeer PL, McGeer EG, Akiyama H, Hersh LB. Distribution of choline acetyltranferase immunopositive structures in the rat brainstem. Brain Res. 1989;495:271–97.

    Article  PubMed  CAS  Google Scholar 

  79. Amri M, Car A, Roman C. Axonal branching of medullary swallowing neurons projecting on the trigeminal and hypoglossal motor nuclei: demonstration by electrophysiological and fluorescent double labeling techniques. Exp Brain Res. 1990;81:384–90.

    Article  PubMed  CAS  Google Scholar 

  80. Li Y-Q, Takada M, Mizuno N. Premotor neurons projecting simultaneously to two orofacial motor nuclei by sending their branched axons. A study with a fluorescent retrograde double-labeling technique in the rat. Neurosci Lett. 1993;152:29–32.

    Article  PubMed  CAS  Google Scholar 

  81. Li Y-Q, Takada M, Mizuno N. Identification of premotor interneurons which project bilaterally to the trigeminal motor, facial and hypoglossal nuclei: a fluorescent retrograde double-labeling study in the rat. Brain Res. 1993;611:160–4.

    Article  PubMed  CAS  Google Scholar 

  82. Travers JB, Rinaman L. Identification of lingual motor control circuits using two strains of pseudorabies virus. Neuroscience. 2002;115:1139–51.

    Article  PubMed  CAS  Google Scholar 

  83. Beckman ME, Whitehead MC. Intramedullary connections of the rostral nucleus of the solitary tract in the hamster. Brain Res. 1991;557:265–79.

    Article  PubMed  CAS  Google Scholar 

  84. Hashim MA. Premotoneuronal organization of swallowing in the rat. Ph.D. thesis, Memorial University of Newfoundland (1989).

    Google Scholar 

  85. Hashim MA, Vyas D, Bieger D. Solitarial deglutitive efferents in the rat. Soc Neurosci Abstr. 1988;14:319.3.

    Google Scholar 

  86. Zhang M, Wang YT, Vyas DM, Neuman RS, Bieger D. Nicotinic cholinoceptor-mediated excitatory postsynaptic potentials in rat nucleus ambiguus. Exp Brain Res. 1993;96:83–8.

    PubMed  CAS  Google Scholar 

  87. Bao X, Wiedner EB, Altschuler SM. Transsynaptic localization of pharyngeal premotor neurons in the rat. Brain Res. 1995;696:246–9.

    Article  PubMed  CAS  Google Scholar 

  88. Broussard DL, Lynn RB, Wiedner EB, Altschuler SM. Solitarial premotor projections to the rat esophagus and pharynx: implications for control of swallowing. Gastroenterology. 1998;144:1268–75.

    Article  Google Scholar 

  89. Lang IM, Dean C, Medda BK, Aslam M, Shaker R. Differential activation of medullary vagal nuclei during different phases swallowing in the cat. Brain Res. 2004;1014:145–63.

    Article  PubMed  CAS  Google Scholar 

  90. Goyal RK, Padmanabhan R, San Q. Neural circuits in swallowing and abdominal vagal afferent-mediated lower esophageal sphincter relaxation. Am J Med. 2001;111(8A):95S–105.

    Article  PubMed  Google Scholar 

  91. Shihara M, Hori N, Hirooka Y, Eshima K, Akaike N, Takeshita A. Cholinergic systems in the nucleus of the solitary tract of rats. Am J Physiol. 1999;276:R1141–8.

    PubMed  CAS  Google Scholar 

  92. Hermann GE, Travagli RA, Rogers RC. Esophageal-gastric relaxation reflex in rat: dual control of peripheral nitrergic and cholinergic transmission. Am J Physiol Regul Integr Comp Physiol. 2006;290:R1570–6.

    Article  PubMed  CAS  Google Scholar 

  93. Gestreau C, Milano S, Bianchi AL, Grélot L. Activity of dorsal respiratory group inspiratory neurons during laryngeal-induced fictive coughing and swallowing in decerebrate cats. Exp Brain Res. 1996;108:247–56.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  95. Lu WY, Bieger D. Vagovagal reflex motility patterns of the rat esophagus. Am J Physiol Regul Integr Comp Physiol. 1998;274:R1425–35.

    CAS  Google Scholar 

  96. Lu WY, Bieger D. Vagal afferent transmission in the NTS mediating reflex responses of the rat esophagus. Am J Physiol Regul Integr Comp Physiol. 1998;274:R1436–45.

    CAS  Google Scholar 

  97. Jean A, Car A, Roman C. Comparison of activity in pontine vs. medullary neurones during swallowing. Exp Brain Res. 1975;22:211–20.

    Article  PubMed  CAS  Google Scholar 

  98. Martino R, Terrault N, Ezerzer F, Mikulis D, Diamant NE. Dysphagia in a patient with lateral medullary syndrome: insight into the central control of swallowing. Gastroenterology. 2001;121:420–6.

    Article  PubMed  CAS  Google Scholar 

  99. Amri M, Lamkadem M, Car A. Effects of lingual nerve and chewing cortex stimulation upon activity of the swallowing neurons located in the region of the hypoglossal motor nucleus. Brain Res. 1991;548:144–55.

    Article  Google Scholar 

  100. Gidda JS, Goyal RK. Swallow-evoked action potentials in vagal preganglionic efferents. J Neurophysiol. 1984;52:1169–80.

    PubMed  CAS  Google Scholar 

  101. Roman C, Tieffenbach L. Enrégistrement de l’activité unitaire des fibres motrices vagales destinées à l’oesophage du Babouin. J Physiol Paris. 1972;64:479–506.

    PubMed  CAS  Google Scholar 

  102. Zoungrana OR, Amri M, Car A, Roman C. Intracellular activity of motoneurons of the rostral nucleus ambiguus during swallowing in sheep. J Neurophysiol. 1997;77:909–22.

    PubMed  CAS  Google Scholar 

  103. Tomume N, Takata M. Excitatory and inhibitory postsynaptic potentials in cat hypoglossal motoneurons during swallowing. Exp Brain Res. 1988;71:262–72.

    Google Scholar 

  104. Amirali A, Tsai G, Schrader N, Weisz D, Sanders I. Mapping of brain stem neuronal circuitry active during swallowing. Ann Otol Rhinol Laryngol. 2001;110:502–13.

    PubMed  CAS  Google Scholar 

  105. Sang Q, Goyal RK. Swallowing reflex and brain stem neurons activated by superior laryngeal nerve stimulation in the mouse. Am J Physiol Gastrointest Liver Physiol. 2001;280:G191–200.

    PubMed  CAS  Google Scholar 

  106. Holstege G, Graveland G, Bijker-Biemond C, Schuddeboom I. Location of motoneurons innervating soft palate, pharynx and upper esophagus. Anatomical evidence for a possible swallowing center in the pontine reticular formation. An HRP and autoradiographical tracing study. Brain Behav Evol. 1983;32:47–62.

    Article  Google Scholar 

  107. Grélot L, Barillot JC, Bianchi AL. Central distribution of the efferent and afferent components of the pharyngeal branches of the vagus and glossopharyngeal nerves: an HRP study in the cat. Exp Brain Res. 1989;78:327–35.

    PubMed  Google Scholar 

  108. Aylwin ML, Horowitz JM, Bonham AC. NMDA receptors contribute to primary visceral afferent transmission in the nucleus of the solitary tract. J Neurophysiol. 1997;77:2239–48.

    Google Scholar 

  109. Jean A, Kessler JP, Tell F. Nucleus tractus solitarii and deglutition: monoamines, excitatory acids and cellular properties. In: Baracco RA, editor. Nucleus of the solitary tract. Boca Raton: CRC Press; 1994. p. 355–69.

    Google Scholar 

  110. Bieger D. Muscarinic activation of rhombencephalic neurons controlling esophageal peristalsis in the rat. Neuropharmacology. 1984;23:1451–64.

    Article  PubMed  CAS  Google Scholar 

  111. Hashim MA, Bieger D. Excitatory amino acid receptor-mediated activation of solitarial deglutitive loci. Neuropharmacology. 1989;28:913–21.

    Article  PubMed  CAS  Google Scholar 

  112. Lu WY, Bieger D, Neuman RS. Does nitric oxide contribute to control of esophagomotor activity? Dysphagia. 1994;9:263.

    Google Scholar 

  113. Lu WY, Zhang M, Neuman RS, Bieger D. Fictive oesophageal peristalsis evoked by activation of muscarinic acetylcholine receptors in rat nucleus tractus solitarii. Neurogastroenterol Motil. 1997;9:247–56.

    Article  PubMed  CAS  Google Scholar 

  114. Kessler JP, Jean A. Evidence that activation of N-methyl-D-aspartate (NMDA) and non-NMDA receptors in the nucleus tractus solitarii trigger swallowing. Eur J Pharmacol. 1991;201:59–67.

    Article  PubMed  CAS  Google Scholar 

  115. Broussard DL, Wiedner EB, Li X, Altschuler SM. NMDAR1 mRNA expression in the brainstem circuit controlling esophageal peristalsis. Mol Brain Res. 1994;27:329–32.

    Article  PubMed  CAS  Google Scholar 

  116. Colin I, Blondeau C, Baude A. Neurokinin release in the rat nucleus of the solitary tract via NMDA and AMPA receptors. Neuroscience. 2002;115:1023–33.

    Article  PubMed  CAS  Google Scholar 

  117. Young-Ho J, Bailey TW, Andresen MC. Cranial afferent glutamate heterosynaptically modulates GABA release onto second-order neurons via distinctly segregated metabotropic glutamate receptors. J Neurosci. 2004;24:9332–40.

    Article  CAS  Google Scholar 

  118. Blessing WW. Distribution of glutamate decarboxylase-containing neurons in rabbit medulla oblongata with attention to intramedullary and spinal projections. Neuroscience. 1990;37:171–85.

    Article  PubMed  CAS  Google Scholar 

  119. Dufour A, Tell F, Kessler JP, Baude A. Mixed GABA-glycine synapses delineate a specific topography in the nucleus tractus solitarii of adult rat. J Physiol. 2010;588:1097–115.

    Article  PubMed  CAS  Google Scholar 

  120. Meeley MP, Ruggiero DA, Ishitsuka T, Reis DJ. Intrinsic gamma-aminobutyric acid neurons in the nucleus of the solitary tract and the rostral ventrolateral medulla of the rat: an immunocytochemical and biochemical study. Neurosci Lett. 1985;58:83–9.

    Article  PubMed  CAS  Google Scholar 

  121. Saha S, Batten TF, McWilliam PN. Glycine-immunoreactive synaptic terminals in the nucleus tractus solitarii of the cat: ultrastructure and relationship to GABA-immunoreactive terminals. Synapse. 1999;33:192–206.

    Article  PubMed  CAS  Google Scholar 

  122. Sweazey RD. Distribution of GABA and glycine in the lamb nucleus of the solitary tract. Brain Res. 1996;737:275–86.

    Article  PubMed  CAS  Google Scholar 

  123. Tanaka I, Ezure K, Kondo M. Distribution of glycine transporter 2 mRNA-containing neurons in relation to glutamic acid decarboxylase mRNA-containing neurons in rat medulla. Neurosci Res. 2003;47:139–51.

    Article  PubMed  CAS  Google Scholar 

  124. Hockman CH, Weerasuriya A, Bieger D. GABA receptor-mediated inhibition of reflex deglutition in the cat. Dysphagia. 1996;11:209–15.

    Article  PubMed  CAS  Google Scholar 

  125. Tell F, Jean A. Ionic basis for endogenous rhythmic patterns induced by activation of N-methyl-D-aspartate receptors in neurons of the rat nucleus tractus solitarii. J Neurophysiol. 1993;70:2379–90.

    PubMed  CAS  Google Scholar 

  126. Greenwood B, Blank E, Dodds WJ. Nicotine stimulates esophageal peristaltic contractions in cats by a central mechanism. Am J Physiol. 1992;262:G567–71.

    PubMed  CAS  Google Scholar 

  127. Dodds WJ, Dent J, Hogan WJ, Arndorfer RC. Effect of atropine on esophageal motor function in humans. Am J Physiol. 1981;240:G290–6.

    PubMed  CAS  Google Scholar 

  128. Paterson WG, Hynna-Liepert TT, Selucky M. Comparison of primary and secondary peristalsis in humans: effect of atropine. Am J Physiol Gastrointest Liver Physiol. 1991;260:G52–7.

    CAS  Google Scholar 

  129. Wang YT, Bieger D, Neuman RS. Activation of NMDA receptors is necessary for fast information transfer at brainstem vagal motoneurons. Brain Res. 1991;597:260–6.

    Article  Google Scholar 

  130. Zagorodnyuk VP, Brookes SJ. Transduction sites of vagal mechanoreceptors in the Guinea pig esophagus. J Neuroscience. 2000;20:6249–55.

    CAS  Google Scholar 

  131. Wang YT, Neuman RS, Bieger D. Somatostatin inhibits nicotinic cholinoceptor mediated excitation in rat ambiguual motoneurons in vitro. Neurosci Lett. 1991;123:236–9.

    Article  PubMed  CAS  Google Scholar 

  132. Zheng H, Patterson LM, Berthoud HR. Orexin- A projections to the caudal medulla and orexin-induced c-Fos expression, food intake, and autonomic function. J Comp Neurol. 2005;485:127–42.

    Article  PubMed  CAS  Google Scholar 

  133. Kobashi M, Xuan SY, Fujita M, Mitoh Y, Matsuo R. Central ghrelin inhibits reflex swallowing elicited by activation of the superior laryngeal nerve in the rat. Regul Pept. 2010;160:19–25.

    Article  PubMed  CAS  Google Scholar 

  134. Félix B, Jean A, Roman C. Leptin inhibits swallowing in rats. Am J Physiol Regul Integr Comp Physiol. 2006;291:R657–63.

    Article  PubMed  CAS  Google Scholar 

  135. Cui RJ, Li X, Appleyard SM. Ghrelin inhibits visceral afferent activation of catecholamine neurons in the solitary tract nucleus. J Neurosci. 2011;31:3484–92.

    Article  PubMed  CAS  Google Scholar 

  136. Bariohay B, Tardivel C, Pio J, Jean A, Félix B. BDNF-TrkB signalling interacts with the GABAergic system to inhibit rhythmic swallowing in the rat. Am J Physiol Regul Integr Comp Physiol. 2008;295:R1050–9.

    Article  PubMed  CAS  Google Scholar 

  137. Hermann GE, Nasse JS, Rogers RC. Alpha-1 adrenergic input to solitary nucleus neurones: calcium oscillations, excitation and gastric reflex control. J Physiol. 2005;562(2):553–68.

    Article  PubMed  CAS  Google Scholar 

  138. Broussard DL, Bao X, Li X, Altschuler SM. Co-localization of NOS and NMDAR receptor in esophageal premotor neurons of the rat. Neuroreport. 1995;6:2073–6.

    Article  PubMed  CAS  Google Scholar 

  139. Ohta A, Takagi H, Matsui T, Hamai Y, Iida S, Esumi H. Localization of nitric oxide synthase-immunoreactive neurons in the solitary nucleus and ventrolateral medulla oblongata of the rat: their relation to catecholaminergic neurons. Neurosci Lett. 1993;158:33–5.

    Article  PubMed  CAS  Google Scholar 

  140. Ruggiero DA, Mtui EP, Otake K, Anwar M. Central and primary visceral afferents to nucleus tractus solitarii may generate nitric oxide as a membrane-permeant neuronal messenger. J Comp Neurol. 1996;364:51–67.

    Article  PubMed  CAS  Google Scholar 

  141. Lu WY, Bieger D, Neuman RS. Nitric oxide mediates crossed inhibition of rat esophageal premotoneurons. Dysphagia. 1995;10:137. abst.

    Google Scholar 

  142. Beyak MJ, Shuwen X, Collman PI, Valdez DT, Diamant NE. Central nervous system nitric oxide induces swallowing and esophageal peristalsis in the cat. Gastroenterology. 2000;119:377–85.

    Article  PubMed  CAS  Google Scholar 

  143. Wang YT, Zhang M, Neuman RS, Bieger D. Somatostatin regulates excitatory amino acid receptor-mediated fast excitatory postsynaptic potential components in vagal motoneurons. Neuroscience. 1993;53:7–9.

    Article  PubMed  CAS  Google Scholar 

  144. Shaker R, Ren J, Podvrsan B, Dodds WJ, Hogan WJ, Kern M, Hoffmann R, Hinz J. Effect of aging and bolus variables on pharyngeal and upper esophageal sphincter motor function. Am J Physiol. 1993;264:G427–32.

    PubMed  CAS  Google Scholar 

  145. Gross DR, Atwood Jr CW, Grayhack JP, Shaiman S. Lung volume effects on pharyngeal swallowing physiology. J Appl Physiol. 2003;95:2211–7.

    PubMed  Google Scholar 

  146. McFarland DH, Lund JP, Gagner M. Effects of posture on the coordination of respiration and swallowing. J Neurophysiol. 1994;72:2431–7.

    PubMed  CAS  Google Scholar 

  147. Shiina T, Shimizu Y, Boudaka A, Wörl J, Takewaki T. Tachykinins are involved in local reflex modulation of vagally mediated striated muscle contractions in the rat esophagus via tachykinin NK1 receptors. Neuroscience. 2006;139:495–503.

    Article  PubMed  CAS  Google Scholar 

  148. 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  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Anatomy, University of Erlangen-Nuremberg, Krankenhausstraße 9, Erlangen, 91054, Germany

    Winfried Neuhuber MD

  2. Health Science Centre, Memorial University, St. John’s, NL, Canada, A1B 3V6

    Detlef Bieger Dr. Med

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  1. Winfried Neuhuber MD
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Correspondence to Winfried Neuhuber MD .

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Editors and Affiliations

  1. Div. Gastroenterology & Hepatology, Medical College of Wisconsin, West Wisconsin Avenue 9200, Milwaukee, 53226, Wisconsin, USA

    Reza Shaker

  2. , Dpt Otolaryngology/Head & Neck Surg., UC Davis Medical Center, Stockton Blvd. 2521, Sacramento, 95817, California, USA

    Peter C. Belafsky

  3. Ctr for Voice, Airway & Swallowing Disor, Department of Otolaryngology, Georgia Health Sciences University, 15th Street 1120, Augusta, 30912, Georgia, USA

    Gregory N. Postma

  4. , Dpt of Communication Sciences & Disorder, University of Wisconsin-Milwaukee, East Hartford Ave 2400, Milwaukee, 53201, Wisconsin, USA

    Caryn Easterling

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Neuhuber, W., Bieger, D. (2013). Brainstem Control of Deglutition: Brainstem Neural Circuits and Mediators Regulating Swallowing. In: Shaker, R., Belafsky, P., Postma, G., Easterling, C. (eds) Principles of Deglutition. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3794-9_7

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