Skip to main content
Top
Published in: Dysphagia 3/2009

01-09-2009 | Review Article

Brain Stem Control of the Phases of Swallowing

Author: Ivan M. Lang

Published in: Dysphagia | Issue 3/2009

Login to get access

Abstract

The phases of swallowing are controlled by central pattern-generating circuitry of the brain stem and peripheral reflexes. The oral, pharyngeal, and esophageal phases of swallowing are independent of each other. Although central pattern generators of the brain stem control the timing of these phases, the peripheral manifestation of these phases depends on sensory feedback through reflexes of the pharynx and esophagus. The dependence of the esophageal phase of swallowing on peripheral feedback explains its absence during failed swallows. Reflexes that initiate the pharyngeal phase of swallowing also inhibit the esophageal phase which ensures the appropriate timing of its occurrence to provide efficient bolus transport and which prevents the occurrence of multiple esophageal peristaltic events. These inhibitory reflexes are probably partly responsible for deglutitive inhibition. Three separate sets of brain stem nuclei mediate the oral, pharyngeal, and esophageal phases of swallowing. The trigeminal nucleus and reticular formation probably contain the oral phase pattern-generating neural circuitry. The nucleus tractus solitarius (NTS) probably contains the second-order sensory neurons as well as the pattern-generating circuitry of both the pharyngeal and esophageal phases of swallowing, whereas the nucleus ambiguus and dorsal motor nucleus contain the motor neurons of the pharyngeal and esophageal phases of swallowing. The ventromedial nucleus of the NTS may govern the coupling of the pharyngeal phase to the esophageal phase of swallowing.
Literature
4.
7.
go back to reference Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81:929–69.PubMed Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81:929–69.PubMed
8.
go back to reference Bieger D, Neuhuber W. Neural circuits and mediators regulating swallowing in the brainstem. GI Motility Online, 16 May 2006. doi:10.1038/gimo74. Bieger D, Neuhuber W. Neural circuits and mediators regulating swallowing in the brainstem. GI Motility Online, 16 May 2006. doi:10.​1038/​gimo74.
9.
go back to reference Jean A, Dallaporta M. Electrophysiologic characterization of the swallowing generator in the brainstem. GI Motility Online, 16 May 2006. doi: 10.1038/gimo9. Jean A, Dallaporta M. Electrophysiologic characterization of the swallowing generator in the brainstem. GI Motility Online, 16 May 2006. doi: 10.​1038/​gimo9.
10.
go back to reference Doty RW, Bosma JF. An electromyographic analysis of reflex deglutition. J Neurophysiol. 1956;19:44–60.PubMed Doty RW, Bosma JF. An electromyographic analysis of reflex deglutition. J Neurophysiol. 1956;19:44–60.PubMed
11.
go back to reference Doty RW. Influence of stimulus pattern on reflex deglutition. Am J Physiol. 1951;166:142–58.PubMed Doty RW. Influence of stimulus pattern on reflex deglutition. Am J Physiol. 1951;166:142–58.PubMed
14.
go back to reference Lang IM, Medda BK, Shaker R. Mechanisms of reflexes induced by esophageal distension. Am J Physiol. 2001;281:G1246–63. Lang IM, Medda BK, Shaker R. Mechanisms of reflexes induced by esophageal distension. Am J Physiol. 2001;281:G1246–63.
16.
go back to reference Ciampini GA, Jean A. Role of glossopharyngeal and trigeminal afferents in the initiation and propagation of swallowing. II–Trigeminal afferents (author’s transl). J Physiol (Paris). 1980;76:49–60. Ciampini GA, Jean A. Role of glossopharyngeal and trigeminal afferents in the initiation and propagation of swallowing. II–Trigeminal afferents (author’s transl). J Physiol (Paris). 1980;76:49–60.
17.
go back to reference Sinclair WJ. Role of pharyngeal plexus in initiation of swallowing. Am J Physiol. 1971;221:1260–3.PubMed Sinclair WJ. Role of pharyngeal plexus in initiation of swallowing. Am J Physiol. 1971;221:1260–3.PubMed
18.
go back to reference Goyal RK, Paterson WG. Esophageal motility. In: Wood JD, editor. Handbook of physiology, Sect. 6: the gastrointestinal system. Volume 1: motility and circulation. Bethesda, MD: American Physiological Society; 1989. p. 865–908. Goyal RK, Paterson WG. Esophageal motility. In: Wood JD, editor. Handbook of physiology, Sect. 6: the gastrointestinal system. Volume 1: motility and circulation. Bethesda, MD: American Physiological Society; 1989. p. 865–908.
19.
go back to reference Lang IM, Marvig J, Sarna SK. Electromyography (EMG) of the pharyngoesophageal junction (PEJ) during various physiological states. Gastroenterology. 1988;94:A249. Lang IM, Marvig J, Sarna SK. Electromyography (EMG) of the pharyngoesophageal junction (PEJ) during various physiological states. Gastroenterology. 1988;94:A249.
21.
go back to reference Schwartz G, Enomoto S, Valiquete C, Lund JP. Mastication in the rabbit: a description of movement and muscle activity. J Neurophysiol. 1989;62:273–87.PubMed Schwartz G, Enomoto S, Valiquete C, Lund JP. Mastication in the rabbit: a description of movement and muscle activity. J Neurophysiol. 1989;62:273–87.PubMed
22.
go back to reference Lang IM, Dana N, Medda BK, Shaker R. Mechanisms of airway protection during retching, vomiting, and swallowing. Am J Physiol. 2002;283:G529–36. Lang IM, Dana N, Medda BK, Shaker R. Mechanisms of airway protection during retching, vomiting, and swallowing. Am J Physiol. 2002;283:G529–36.
25.
go back to reference Sumi T. The nature and postnatal development of reflex deglutition in the kitten. Jpn J Physiol. 1967;17:200–10.PubMed Sumi T. The nature and postnatal development of reflex deglutition in the kitten. Jpn J Physiol. 1967;17:200–10.PubMed
27.
go back to reference Shaker R, Ren J, Zamir Z, Sarna S, Liu J, Sui Z. Effect of aging, position, and temperature on the threshold volume triggering pharyngeal swallows. Gastroenterology. 1994;107:396–402.PubMed Shaker R, Ren J, Zamir Z, Sarna S, Liu J, Sui Z. Effect of aging, position, and temperature on the threshold volume triggering pharyngeal swallows. Gastroenterology. 1994;107:396–402.PubMed
28.
go back to reference Dodds WJ, Hogan WJ, Reid DP, Stewart ET, Arndorfer RC. A comparison between primary esophageal peristalsis following wet and dry swallows. J Appl Physiol. 1973;35:851–7.PubMed Dodds WJ, Hogan WJ, Reid DP, Stewart ET, Arndorfer RC. A comparison between primary esophageal peristalsis following wet and dry swallows. J Appl Physiol. 1973;35:851–7.PubMed
29.
go back to reference Hollis JB, Castell DO. Effect of dry and wet swallows of different volumes on esophageal peristalsis. J Appl Physiol. 1975;38:1161–4.PubMed Hollis JB, Castell DO. Effect of dry and wet swallows of different volumes on esophageal peristalsis. J Appl Physiol. 1975;38:1161–4.PubMed
30.
go back to reference Ask P, Tibbling L. Effect of time interval between swallows on esophageal peristalsis. Am J Physiol. 1980;238:G485–90.PubMed Ask P, Tibbling L. Effect of time interval between swallows on esophageal peristalsis. Am J Physiol. 1980;238:G485–90.PubMed
31.
go back to reference Vanek AW, Diamant NE. Responses of the human esophagus to paired swallows. Gastroenterology. 1987;92:643–50.PubMed Vanek AW, Diamant NE. Responses of the human esophagus to paired swallows. Gastroenterology. 1987;92:643–50.PubMed
32.
go back to reference Meyer GW, Gerhardt DC, Castell DO. Human esophageal response to rapid swallowing: muscle refractory period or neural inhibition. Am J Physiol. 1981;241:G129–36.PubMed Meyer GW, Gerhardt DC, Castell DO. Human esophageal response to rapid swallowing: muscle refractory period or neural inhibition. Am J Physiol. 1981;241:G129–36.PubMed
34.
go back to reference Wang YT, Bieger D. Role of solitarial GABAergic mechanisms in control of swallowing. Am J Physiol. 1991;261:R639–46.PubMed Wang YT, Bieger D. Role of solitarial GABAergic mechanisms in control of swallowing. Am J Physiol. 1991;261:R639–46.PubMed
36.
go back to reference Shingai T, Shimada K. Reflex swallowing elicited by water and chemical substances applied in the oral cavity, pharynx, and larynx of the rabbit. Jpn J Physiol. 1976;26:455–69.PubMed Shingai T, Shimada K. Reflex swallowing elicited by water and chemical substances applied in the oral cavity, pharynx, and larynx of the rabbit. Jpn J Physiol. 1976;26:455–69.PubMed
37.
go back to reference Lang IM, Medda BK, Ren J, Shaker R. Characterization and mechanisms of the pharyngoesophageal inhibitory reflex. Am J Physiol. 1998;275:G1127–36.PubMed Lang IM, Medda BK, Ren J, Shaker R. Characterization and mechanisms of the pharyngoesophageal inhibitory reflex. Am J Physiol. 1998;275:G1127–36.PubMed
38.
go back to reference Pommerenke WT. A study of the sensory areas eliciting the swallowing reflex. Am J Physiol. 1928;84:36–41. Pommerenke WT. A study of the sensory areas eliciting the swallowing reflex. Am J Physiol. 1928;84:36–41.
40.
go back to reference Janssens J, Valembois P, Hellemans J, Vantrappen G, Pelemans W. Studies on the necessity of a bolus for the progression of secondary peristalsis in the canine esophagus. Gastroenterology. 1974;67:245–52.PubMed Janssens J, Valembois P, Hellemans J, Vantrappen G, Pelemans W. Studies on the necessity of a bolus for the progression of secondary peristalsis in the canine esophagus. Gastroenterology. 1974;67:245–52.PubMed
41.
go back to reference Longhi EH, Jordan PH. Necessity of a bolus for propagation of primary peristalsis in the canine esophagus. Am J Physiol. 1971;220:609–12.PubMed Longhi EH, Jordan PH. Necessity of a bolus for propagation of primary peristalsis in the canine esophagus. Am J Physiol. 1971;220:609–12.PubMed
42.
go back to reference Janssens J, Wever I, Vantrappen G, Agg HO, Hellemans J. Peristalsis in smooth muscle esophagus after transection and bolus diversion. Gastroenterology. 1976;71:1004–9.PubMed Janssens J, Wever I, Vantrappen G, Agg HO, Hellemans J. Peristalsis in smooth muscle esophagus after transection and bolus diversion. Gastroenterology. 1976;71:1004–9.PubMed
43.
go back to reference Wank M, Neuhuber WL. Local differences in vagal afferent innervation of the rat esophagus are reflected by neurochemical differences at the level of the sensory ganglia and by different brainstem projections. J Comp Neurol. 2001;435:41–59. doi:10.1002/cne.1192.PubMedCrossRef Wank M, Neuhuber WL. Local differences in vagal afferent innervation of the rat esophagus are reflected by neurochemical differences at the level of the sensory ganglia and by different brainstem projections. J Comp Neurol. 2001;435:41–59. doi:10.​1002/​cne.​1192.PubMedCrossRef
44.
45.
go back to reference Lang IM, Medda BK, Shaker R. The esophagus is topographically organized in the brainstem according to peripheral location as well as receptor type. Gastroenterology. 2006;130:A444. Lang IM, Medda BK, Shaker R. The esophagus is topographically organized in the brainstem according to peripheral location as well as receptor type. Gastroenterology. 2006;130:A444.
46.
go back to reference Falempin M, Madhloum A, Rousseau JP. Effects of vagal deafferentation on oesophageal motility and transit in the sheep. J Physiol. 1986;372:425–36.PubMed Falempin M, Madhloum A, Rousseau JP. Effects of vagal deafferentation on oesophageal motility and transit in the sheep. J Physiol. 1986;372:425–36.PubMed
47.
go back to reference Dantas RO, Kern MK, Massey BT, Dodds WJ, Kahrilas PJ, Brasseur JG, et al. Effect of swallowed bolus variables on oral and pharyngeal phases fo swallowing. Am J Physiol. 1990;258:G675–81.PubMed Dantas RO, Kern MK, Massey BT, Dodds WJ, Kahrilas PJ, Brasseur JG, et al. Effect of swallowed bolus variables on oral and pharyngeal phases fo swallowing. Am J Physiol. 1990;258:G675–81.PubMed
48.
go back to reference Ertekin C, Aydogdu I, Yuceyar N, Pehliva M, Ertas M, Uludag B, et al. Effects of bolus volume on oropharyngeal swallowing: an electrophysiologic study in man. J Gastroenterol. 1997;92:2049–53. Ertekin C, Aydogdu I, Yuceyar N, Pehliva M, Ertas M, Uludag B, et al. Effects of bolus volume on oropharyngeal swallowing: an electrophysiologic study in man. J Gastroenterol. 1997;92:2049–53.
49.
go back to reference Cook IJ, Dodds WJ, Dantas RO, Kern MK, Massey BT, Shaker R, et al. Timing of videofluoroscopic, manometric events, and bolus transit during oral and pharyngeal phases of swallowing. Dysphagia. 1989;4:8–15.PubMedCrossRef Cook IJ, Dodds WJ, Dantas RO, Kern MK, Massey BT, Shaker R, et al. Timing of videofluoroscopic, manometric events, and bolus transit during oral and pharyngeal phases of swallowing. Dysphagia. 1989;4:8–15.PubMedCrossRef
50.
go back to reference Bardan E, Xie P, Ren J, Dua K, Shaker R. Effect of pharyngeal water stimulation on esophageal peristalsis and bolus transport. Am J Physiol. 1997;272:G265–71.PubMed Bardan E, Xie P, Ren J, Dua K, Shaker R. Effect of pharyngeal water stimulation on esophageal peristalsis and bolus transport. Am J Physiol. 1997;272:G265–71.PubMed
51.
go back to reference Trifan A, Ren J, Arndorfer R, Hofmann C, Bardan E, Shaker R. Inhibition of progressing primary esophageal peristalsis by pharyngeal water stimulation in humans. Gastroenterology. 1999;110:419–23.CrossRef Trifan A, Ren J, Arndorfer R, Hofmann C, Bardan E, Shaker R. Inhibition of progressing primary esophageal peristalsis by pharyngeal water stimulation in humans. Gastroenterology. 1999;110:419–23.CrossRef
52.
go back to reference Trifan A, Shaker R, Ren J, Mittal RK, Saeian K, Dua K, et al. Inhibition of resting lower esophageal sphincter pressure by pharyngeal water stimulation in humans. Gastroenterology. 1995;108:441–6.PubMedCrossRef Trifan A, Shaker R, Ren J, Mittal RK, Saeian K, Dua K, et al. Inhibition of resting lower esophageal sphincter pressure by pharyngeal water stimulation in humans. Gastroenterology. 1995;108:441–6.PubMedCrossRef
53.
go back to reference Freiman JM, El-Sharkay TY, Diamant NE. Effect of bilateral vagosympathetic nerve blockade on response of the dog upper esophageal sphincter (UES) to intraesophageal distension and acid. Gastroenterology. 1981;81:78–84.PubMed Freiman JM, El-Sharkay TY, Diamant NE. Effect of bilateral vagosympathetic nerve blockade on response of the dog upper esophageal sphincter (UES) to intraesophageal distension and acid. Gastroenterology. 1981;81:78–84.PubMed
54.
go back to reference Reynolds RPE, Effer GW, Bendeck MP. The upper esophageal sphincter in the cat: the role of central innervation assessed by transient vagal blockade. Can J Physiol Pharmacol. 1987;65:96–9.PubMed Reynolds RPE, Effer GW, Bendeck MP. The upper esophageal sphincter in the cat: the role of central innervation assessed by transient vagal blockade. Can J Physiol Pharmacol. 1987;65:96–9.PubMed
55.
go back to reference Enzman DR, Harell GS, Zboralske FF. Upper esophageal responses to intraluminal distension in man. Gastroenterology. 1977;72:1292–8. Enzman DR, Harell GS, Zboralske FF. Upper esophageal responses to intraluminal distension in man. Gastroenterology. 1977;72:1292–8.
56.
go back to reference Jean A. Localization and activity of medullary swallowing neurones. J Physiol (Paris). 1972;64:227–68 (article in French). Jean A. Localization and activity of medullary swallowing neurones. J Physiol (Paris). 1972;64:227–68 (article in French).
57.
go back to reference Roman C, Tieffenbach L. Recording the unit activity of vagal motor fibers innervating the baboon esophagus. J Physiol (Paris). 1972;64:479–506 (article in French). Roman C, Tieffenbach L. Recording the unit activity of vagal motor fibers innervating the baboon esophagus. J Physiol (Paris). 1972;64:479–506 (article in French).
58.
go back to reference Roman C. Nervous control of esophageal peristalsis. J Phsyiol (Paris). 1966;58:79–108 (article in French). Roman C. Nervous control of esophageal peristalsis. J Phsyiol (Paris). 1966;58:79–108 (article in French).
59.
go back to reference Westberg KG, Scott G, Olsson KA, Lund JP. Discharge patterns of neurons in the medial pontobulbar reticular formation during fictive mastication in the rabbit. Eur J Neurosci. 2001;14:1709–18.PubMedCrossRef Westberg KG, Scott G, Olsson KA, Lund JP. Discharge patterns of neurons in the medial pontobulbar reticular formation during fictive mastication in the rabbit. Eur J Neurosci. 2001;14:1709–18.PubMedCrossRef
60.
go back to reference Tsuboi A, Kolta A, Chen CC, Lund JP. Neurons of the trigeminal main sensory nucleus participate in the generation of rhythmic motor patterns. Eur J Neurosci. 2003;17:229–38.PubMedCrossRef Tsuboi A, Kolta A, Chen CC, Lund JP. Neurons of the trigeminal main sensory nucleus participate in the generation of rhythmic motor patterns. Eur J Neurosci. 2003;17:229–38.PubMedCrossRef
61.
go back to reference Peleg D, Goldman JA. Fetal deglutition: a study of the anencephalic fetus. Eur J Obstet Gynecol Reprod Biol. 1978;8:133–6.PubMedCrossRef Peleg D, Goldman JA. Fetal deglutition: a study of the anencephalic fetus. Eur J Obstet Gynecol Reprod Biol. 1978;8:133–6.PubMedCrossRef
62.
go back to reference Pritchard JA. Deglutition by normal and anencephalic fetuses. J Obstet Gynecol. 1965;25:289–97. Pritchard JA. Deglutition by normal and anencephalic fetuses. J Obstet Gynecol. 1965;25:289–97.
63.
go back to reference Lund JP. Mastication and its control by the brain stem. Cur Rev Oral Biol Med. 1991;2:33–64. Lund JP. Mastication and its control by the brain stem. Cur Rev Oral Biol Med. 1991;2:33–64.
64.
go back to reference Nakamura Y, Katakama N. Generation of masticatory rhythm in the brainstem. Neurosci Res. 1995;23:1–19.PubMed Nakamura Y, Katakama N. Generation of masticatory rhythm in the brainstem. Neurosci Res. 1995;23:1–19.PubMed
65.
go back to reference Athanassiadis T, Olsson KA, Kolta A, Westberg KG. Identification of c-Fos immunoreactive brainstem neuron activated during fictive mastication in the rabbit. Exp Brain Res. 2005;165:478–89.PubMedCrossRef Athanassiadis T, Olsson KA, Kolta A, Westberg KG. Identification of c-Fos immunoreactive brainstem neuron activated during fictive mastication in the rabbit. Exp Brain Res. 2005;165:478–89.PubMedCrossRef
66.
go back to reference Lang IM, Dean C, Medda BK, Aslam M, Shaker R. Differential activation of medullary vagal nuclei during different phases of swallowing in the cat. Brain Res. 2004;1014:145–63.PubMedCrossRef Lang IM, Dean C, Medda BK, Aslam M, Shaker R. Differential activation of medullary vagal nuclei during different phases of swallowing in the cat. Brain Res. 2004;1014:145–63.PubMedCrossRef
67.
go back to reference Sang Q, Goyal RK. Swallowing reflex and brain stem neurons activated by superior laryngeal nerve stimulation in the mouse. Am J Physiol. 2001;280:G191–200. Sang Q, Goyal RK. Swallowing reflex and brain stem neurons activated by superior laryngeal nerve stimulation in the mouse. Am J Physiol. 2001;280:G191–200.
68.
go back to reference Amirali A, Tsai G, Weisz D, Schrader N, Sanders I. Mapping of brain stem neuronal circuitry active during swallowing. Ann Otol Rhinol Laryngol. 2001;110:502–5134.PubMed Amirali A, Tsai G, Weisz D, Schrader N, Sanders I. Mapping of brain stem neuronal circuitry active during swallowing. Ann Otol Rhinol Laryngol. 2001;110:502–5134.PubMed
69.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
70.
go back to reference Bao X, Barrett RT, Altschuler SM. Transynaptic localization of pharyngeal premotor neurons in rat. Brain Res. 1995;696:246–9.PubMedCrossRef Bao X, Barrett RT, Altschuler SM. Transynaptic localization of pharyngeal premotor neurons in rat. Brain Res. 1995;696:246–9.PubMedCrossRef
71.
go back to reference Barrett RT, Bao X, Miselis RR, Altschuler SM. Brain stem localization of rodent esophageal premotor neurons revealed by transsynaptic passage of pseudorabies virus. Gastroenterology. 1994;107:728–37.PubMed Barrett RT, Bao X, Miselis RR, Altschuler SM. Brain stem localization of rodent esophageal premotor neurons revealed by transsynaptic passage of pseudorabies virus. Gastroenterology. 1994;107:728–37.PubMed
72.
go back to reference McClean JH, Hopkins DA. A light and electron microscopic study of the dorsal motor nucleus of the vagus in the cat. J Comp Neurol. 1981;195:157–75.CrossRef McClean JH, Hopkins DA. A light and electron microscopic study of the dorsal motor nucleus of the vagus in the cat. J Comp Neurol. 1981;195:157–75.CrossRef
73.
go back to reference Bieger D, Hopkins DA. Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus. J Comp Neurol. 1987;262:546–62.PubMedCrossRef Bieger D, Hopkins DA. Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus. J Comp Neurol. 1987;262:546–62.PubMedCrossRef
74.
go back to reference Frysack T, Zenker W, Kantner D. Afferent and efferent innervation of the rat esophagus. Anat Embryol. 1984;170:63–70.CrossRef Frysack T, Zenker W, Kantner D. Afferent and efferent innervation of the rat esophagus. Anat Embryol. 1984;170:63–70.CrossRef
75.
go back to reference Collman PI, Tremblay L, Diamant NE. The central vagal efferent supply to the esophagus and lower esophageal sphincter of the cat. Gastroenterology. 1993;104:1430–8.PubMed Collman PI, Tremblay L, Diamant NE. The central vagal efferent supply to the esophagus and lower esophageal sphincter of the cat. Gastroenterology. 1993;104:1430–8.PubMed
76.
go back to reference Holstege G, Graveland G, Bijker-Biemond C, Scuddeboom I. Location of motoneurons innervating soft palate, pharynx and upper esophagus. Anatomical evidence for a possible swallowing center in the pontine reticular formation. Brain Behav Evol. 1983;23:47–62. Holstege G, Graveland G, Bijker-Biemond C, Scuddeboom I. Location of motoneurons innervating soft palate, pharynx and upper esophagus. Anatomical evidence for a possible swallowing center in the pontine reticular formation. Brain Behav Evol. 1983;23:47–62.
77.
go back to reference Lawn AM. The localization, in the nucleus ambiguus of the rabbit, of the cells of origin of motor nerve fibers in the glossopharyngeal nerve and various branches of the vagus nerve by means of retrograde degeneration. J Comp Neurol. 1966;127:293–306.PubMedCrossRef Lawn AM. The localization, in the nucleus ambiguus of the rabbit, of the cells of origin of motor nerve fibers in the glossopharyngeal nerve and various branches of the vagus nerve by means of retrograde degeneration. J Comp Neurol. 1966;127:293–306.PubMedCrossRef
78.
go back to reference Brousard DL, Lynn RB, Wiedner EB, Altschuler SM. Solitarial premotor neuron projections to the rat esophagus and pharynx: implications for control of swallowing. Gastroenterology. 1998;114:1268–75.CrossRef Brousard DL, Lynn RB, Wiedner EB, Altschuler SM. Solitarial premotor neuron projections to the rat esophagus and pharynx: implications for control of swallowing. Gastroenterology. 1998;114:1268–75.CrossRef
79.
go back to reference Bieger D. Muscarinic activation of rhomboencephalic neurones controlling oesophageal peristalsis in the rat. Neuropharmacology. 1984;23:1451–64.PubMedCrossRef Bieger D. Muscarinic activation of rhomboencephalic neurones controlling oesophageal peristalsis in the rat. Neuropharmacology. 1984;23:1451–64.PubMedCrossRef
80.
go back to reference Lu W, 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.PubMedCrossRef Lu W, 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.PubMedCrossRef
81.
go back to reference Lang IM, Haworth ST, Medda BK, Roerig DL, Forster HV, Shaker R. Airway responses to esophageal acidification. Am J Physiol. 2008;294:R211–9. Lang IM, Haworth ST, Medda BK, Roerig DL, Forster HV, Shaker R. Airway responses to esophageal acidification. Am J Physiol. 2008;294:R211–9.
83.
go back to reference Hamamoto J, Kohrogi H, Kawano O, Iwagoe H, Fujii K, Hirata N, et al. Esophageal stimulation by hydrochloric acid causes neurogenic inflammation in the airways in guinea pigs. J Appl Physiol. 1997;82:738–45.PubMed Hamamoto J, Kohrogi H, Kawano O, Iwagoe H, Fujii K, Hirata N, et al. Esophageal stimulation by hydrochloric acid causes neurogenic inflammation in the airways in guinea pigs. J Appl Physiol. 1997;82:738–45.PubMed
84.
go back to reference Dick TE, Oku Y, Romaniuk JR, Cherniak NS. Interaction between central pattern generators for breathing and swallowing in the cat. J Physiol (Lond). 1993;465:715–30. Dick TE, Oku Y, Romaniuk JR, Cherniak NS. Interaction between central pattern generators for breathing and swallowing in the cat. J Physiol (Lond). 1993;465:715–30.
85.
go back to reference Feroah TR, Forster HV, Fuentes CG, Lang IM, Beste D, Martino P, et al. Effects of spontaneous swallows on breathing in awake goats. J Appl Physiol. 2002;92:1923–35.PubMed Feroah TR, Forster HV, Fuentes CG, Lang IM, Beste D, Martino P, et al. Effects of spontaneous swallows on breathing in awake goats. J Appl Physiol. 2002;92:1923–35.PubMed
86.
go back to reference Kalia M, Mesulam MM. Brain stem projections of sensory and motor components of the vagus complex in the cat. I. Laryngeal, tracheobronchial, pulmonary, cardiac, and gastrointestinal branches. J Comp Neurol. 1980;193:467–508. Kalia M, Mesulam MM. Brain stem projections of sensory and motor components of the vagus complex in the cat. I. Laryngeal, tracheobronchial, pulmonary, cardiac, and gastrointestinal branches. J Comp Neurol. 1980;193:467–508.
87.
go back to reference 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:G899–906.PubMed 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:G899–906.PubMed
88.
go back to reference Cunningham 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 Cunningham 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
89.
go back to reference Kruszewska B, Lipski J, Kanjhan R. An electrophysiological and morphological study of esophageal motoneurons in rats. Am J Physiol. 1994;26:R622–32. Kruszewska B, Lipski J, Kanjhan R. An electrophysiological and morphological study of esophageal motoneurons in rats. Am J Physiol. 1994;26:R622–32.
90.
go back to reference Sang Q, Goyal RK. Lower esophageal sphincter relaxation and activation of medullary neurons by subdiaphragmattic vagal stimulation in the mouse. Gastroenterology. 2000;119:1600–9.PubMedCrossRef Sang Q, Goyal RK. Lower esophageal sphincter relaxation and activation of medullary neurons by subdiaphragmattic vagal stimulation in the mouse. Gastroenterology. 2000;119:1600–9.PubMedCrossRef
91.
go back to reference Wang YT, Neuman RS, Bieger D. Nicotinic cholinergic-mediated excitation in ambigual motoneurons of the rat. Neuroscience. 1991;40:759–67.PubMedCrossRef Wang YT, Neuman RS, Bieger D. Nicotinic cholinergic-mediated excitation in ambigual motoneurons of the rat. Neuroscience. 1991;40:759–67.PubMedCrossRef
92.
93.
go back to reference Umezaki T, Matsuse T, Shin T. Medullary swallowing-related neurons in the anesthetized cat. NeuroReport. 1998;9:1793–8.PubMedCrossRef Umezaki T, Matsuse T, Shin T. Medullary swallowing-related neurons in the anesthetized cat. NeuroReport. 1998;9:1793–8.PubMedCrossRef
94.
go back to reference Jean A. Effect of localized lesions of the medulla oblongata on the esophageal stage of deglutition. J Physiol (Paris). 1972;64:507–16. Jean A. Effect of localized lesions of the medulla oblongata on the esophageal stage of deglutition. J Physiol (Paris). 1972;64:507–16.
95.
go back to reference Jean A. Localization and activity of oesophageal motoneurons in sheep (microelectrode study) (author’s transl). J. Physiol (Paris). 1978;74:737–42 (article in French). Jean A. Localization and activity of oesophageal motoneurons in sheep (microelectrode study) (author’s transl). J. Physiol (Paris). 1978;74:737–42 (article in French).
96.
go back to reference Car A, Roman C. Effects of atropine on the central mechanism of deglutition in anesthetized sheep. Exp Brain Res. 2002;142:496–503.PubMedCrossRef Car A, Roman C. Effects of atropine on the central mechanism of deglutition in anesthetized sheep. Exp Brain Res. 2002;142:496–503.PubMedCrossRef
97.
go back to reference Dong H, 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.PubMedCrossRef Dong H, 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.PubMedCrossRef
98.
go back to reference 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 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
Metadata
Title
Brain Stem Control of the Phases of Swallowing
Author
Ivan M. Lang
Publication date
01-09-2009
Publisher
Springer-Verlag
Published in
Dysphagia / Issue 3/2009
Print ISSN: 0179-051X
Electronic ISSN: 1432-0460
DOI
https://doi.org/10.1007/s00455-009-9211-6

Other articles of this Issue 3/2009

Dysphagia 3/2009 Go to the issue