Brain stem control of the phases of swallowing

Dysphagia

Volumn 24, Issue 3, 2009, Pages 333-348

  Lang, Ivan M ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Central pattern generator; Deglutition; Deglutition disorders; Deglutitive inhibition; Esophageal phase; Failed swallows; Oral phase; Pharyngeal phase; Reflexive swallow; Swallowing

Indexed keywords

AMBIGUUS NUCLEUS; ANATOMICAL VARIATION; ANESTHESIA; BRAIN NUCLEUS; BRAIN STEM; COORDINATION; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; ESOPHAGUS; FEEDBACK SYSTEM; HUMAN; MASTICATION; MOTONEURON; NEUROPHYSIOLOGY; NONHUMAN; PERISTALSIS; PHARYNX; PRIORITY JOURNAL; RETICULAR FORMATION; REVIEW; SENSORY NERVE CELL; SOLITARY TRACT NUCLEUS; STIMULUS; SWALLOWING; THALAMUS VENTRAL NUCLEUS; TRIGEMINAL NUCLEUS; DYSPHAGIA; ELECTROMYOGRAPHY; MANOMETRY; OROPHARYNX;

BRAIN STEM; DEGLUTITION; DEGLUTITION DISORDERS; ELECTROMYOGRAPHY; ESOPHAGUS; HUMANS; MANOMETRY; OROPHARYNX; PERISTALSIS;

EID: 69249216674     PISSN: 0179051X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00455-009-9211-6     Document Type: Review

References (98)

1. JB Palmer NJ Rudin G Lara AW Crompton 1992 Coordination of mastication and swallowing Dysphagia 7 187 200 10.1007/BF02493469
2. AJ Thexton 1992 Mastication and swallowing: an overview Br Dent J 173 197 206 10.1038/sj.bdj.4808002
3. WJ Dodds 1989 Physiology of swallowing Dysphagia 3 171 178 10.1007/BF02407219
4. WG Selley RE Ellis FC Flack WA Brooks 1990 Coordination of sucking, swallowing and breathing in the newborn: Its relationship to infant feeding and normal development Br J Disord Commun 25 311 327 10.3109/13682829009011980
5. JL Miller B Sonies C Macedonia 2003 Emergence of oropharyngeal, laryngeal and swallowing activity in the developing fetal upper aerodigestive tract: an ultrasound evaluation Early Hum Dev 71 61 87 10.1016/S0378-3782(02)00110-X (Pubitemid 36287094)
6. AJ Miller 1982 Deglutition Physiol Rev 62 129 184
7. A Jean 2001 Brain stem control of swallowing: neuronal network and cellular mechanisms Physiol Rev 81 929 969
8. Bieger D, Neuhuber W. Neural circuits and mediators regulating swallowing in the brainstem. GI Motility Online, 16 May 2006. doi: 10.1038/gimo74.
9. Jean A, Dallaporta M. Electrophysiologic characterization of the swallowing generator in the brainstem. GI Motility Online, 16 May 2006. doi: 10.1038/gimo9.
10. RW Doty JF Bosma 1956 An electromyographic analysis of reflex deglutition J Neurophysiol 19 44 60
11. RW Doty 1951 Influence of stimulus pattern on reflex deglutition Am J Physiol 166 142 158
12. AJ Thexton AW Crompton RZ German 2007 Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited J Appl Physiol 102 2 587 600 10.1152/japplphysiol.00456.2006 (Pubitemid 46220887)
13. MJ Beyak PI Collman DT Valdez S Xue NE Diamant 1997 Superior laryngeal nerve stimulation in the cat: effect on oropharyngeal swallowing, esophageal motility, and lower esophageal sphincter activity Neurogastroenterol Motil 9 117 127 10.1046/j.1365-2982.1997.d01-22.x
14. IM Lang BK Medda R Shaker 2001 Mechanisms of reflexes induced by esophageal distension Am J Physiol 281 G1246 G1263
15. Y Yoshida Y Tanaka M Hirano T Nakashima 2000 Sensory innervation of the pharynx and larynx Am J Med 108 Suppl 4a 51S 61S 10.1016/S0002-9343(99)00342-3 (Pubitemid 30133425)
16. GA Ciampini A Jean 1980 Role of glossopharyngeal and trigeminal afferents in the initiation and propagation of swallowing. II-Trigeminal afferents (author's transl) J Physiol (Paris) 76 49 60 (Pubitemid 10117821)
17. WJ Sinclair 1971 Role of pharyngeal plexus in initiation of swallowing Am J Physiol 221 1260 1263
18. 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. IM Lang J Marvig SK Sarna 1988 Electromyography (EMG) of the pharyngoesophageal junction (PEJ) during various physiological states Gastroenterology 94 A249
20. M Qureshi FL Vice VL Taciak JF Bosma IH Gewolb 2002 Changes in rhythmic suckle feeding patterns in term infants in the first month of life Dev Med Child Neurol 44 34 39 10.1017/S0012162201001621
21. G Schwartz S Enomoto C Valiquete JP Lund 1989 Mastication in the rabbit: a description of movement and muscle activity J Neurophysiol 62 273 287
22. IM Lang N Dana BK Medda R Shaker 2002 Mechanisms of airway protection during retching, vomiting, and swallowing Am J Physiol 283 G529 G536
23. AJ Thexton JD McGarrick 1988 Tongue movement of the cat during lapping Arch Oral Biol 33 331 339 10.1016/0003-9969(88)90066-0
24. LA Newman RH Cleveland JG Blickman RE Hillman D Jaramillo 1991 Videofluoroscopic analysis of the infant swallow Invest Radiol 26 870 873 10.1097/00004424-199110000-00005
25. T Sumi 1967 The nature and postnatal development of reflex deglutition in the kitten Jpn J Physiol 17 200 210
26. T Nishino 1993 Swallowing as a protective reflex for the upper respiratory tract Anesthesiology 79 588 601 10.1097/00000542-199309000-00024
27. R Shaker J Ren Z Zamir S Sarna J Liu Z Sui 1994 Effect of aging, position, and temperature on the threshold volume triggering pharyngeal swallows Gastroenterology 107 396 402
28. WJ Dodds WJ Hogan DP Reid ET Stewart RC Arndorfer 1973 A comparison between primary esophageal peristalsis following wet and dry swallows J Appl Physiol 35 851 857
29. JB Hollis DO Castell 1975 Effect of dry and wet swallows of different volumes on esophageal peristalsis J Appl Physiol 38 1161 1164
30. P Ask L Tibbling 1980 Effect of time interval between swallows on esophageal peristalsis Am J Physiol 238 G485 G490
31. AW Vanek NE Diamant 1987 Responses of the human esophagus to paired swallows Gastroenterology 92 643 650
32. GW Meyer DC Gerhardt DO Castell 1981 Human esophageal response to rapid swallowing: muscle refractory period or neural inhibition Am J Physiol 241 G129 G136
33. MA Hashim D Bieger 1989 Excitatory amino acid receptor-mediated activation of solitarial deglutitive loci Neuropharmacology 28 913 921 10.1016/0028-3908(89)90190-1 (Pubitemid 19224334)
34. YT Wang D Bieger 1991 Role of solitarial GABAergic mechanisms in control of swallowing Am J Physiol 261 R639 R646
35. JP Kessler A Jean 1991 Evidence that activation of N-methyl-d-aspartate (NMDA) and non-NMDA receptors within the nucleus tractus solitariii triggers swallowing Eur J Pharmacol 201 59 67 10.1016/0014-2999(91)90323-I
36. T Shingai K Shimada 1976 Reflex swallowing elicited by water and chemical substances applied in the oral cavity, pharynx, and larynx of the rabbit Jpn J Physiol 26 455 469
37. IM Lang BK Medda J Ren R Shaker 1998 Characterization and mechanisms of the pharyngoesophageal inhibitory reflex Am J Physiol 275 G1127 G1136
38. WT Pommerenke 1928 A study of the sensory areas eliciting the swallowing reflex Am J Physiol 84 36 41
39. I Mansson N Sandberg 1975 Oro-pharyngeal sensitivity and elicitation of swallowing in man Acta Otolaryngol 79 140 145 10.3109/00016487509124666
40. J Janssens P Valembois J Hellemans G Vantrappen W Pelemans 1974 Studies on the necessity of a bolus for the progression of secondary peristalsis in the canine esophagus Gastroenterology 67 245 252
41. EH Longhi PH Jordan 1971 Necessity of a bolus for propagation of primary peristalsis in the canine esophagus Am J Physiol 220 609 612
42. J Janssens I Wever G Vantrappen HO Agg J Hellemans 1976 Peristalsis in smooth muscle esophagus after transection and bolus diversion Gastroenterology 71 1004 1009
43. M Wank WL Neuhuber 2001 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 435 41 59 10.1002/cne.1192 (Pubitemid 32448721)
44. JKM Lennerz C Dentsch N Bernardini T Hummel WL Neuhuber PW Reeh 2007 Electrophysiological characterization of vagal afferents relevant to mucosal nociception in the rat upper oesophagus J Physiol 582 229 242 10.1113/jphysiol.2007.130823 (Pubitemid 46993572)
45. IM Lang BK Medda R Shaker 2006 The esophagus is topographically organized in the brainstem according to peripheral location as well as receptor type Gastroenterology 130 A444
46. M Falempin A Madhloum JP Rousseau 1986 Effects of vagal deafferentation on oesophageal motility and transit in the sheep J Physiol 372 425 436
47. RO Dantas MK Kern BT Massey WJ Dodds PJ Kahrilas JG Brasseur IJ Cook IM Lang 1990 Effect of swallowed bolus variables on oral and pharyngeal phases fo swallowing Am J Physiol 258 G675 G681
48. C Ertekin I Aydogdu N Yuceyar M Pehliva M Ertas B Uludag G Celebi 1997 Effects of bolus volume on oropharyngeal swallowing: an electrophysiologic study in man J Gastroenterol 92 2049 2053
49. IJ Cook WJ Dodds RO Dantas MK Kern BT Massey R Shaker WJ Hogan 1989 Timing of videofluoroscopic, manometric events, and bolus transit during oral and pharyngeal phases of swallowing Dysphagia 4 8 15
50. E Bardan P Xie J Ren K Dua R Shaker 1997 Effect of pharyngeal water stimulation on esophageal peristalsis and bolus transport Am J Physiol 272 G265 G271
51. A Trifan J Ren R Arndorfer C Hofmann E Bardan R Shaker 1999 Inhibition of progressing primary esophageal peristalsis by pharyngeal water stimulation in humans Gastroenterology 110 419 423
52. A Trifan R Shaker J Ren RK Mittal K Saeian K Dua M Kusano 1995 Inhibition of resting lower esophageal sphincter pressure by pharyngeal water stimulation in humans Gastroenterology 108 441 446
53. JM Freiman TY El-Sharkay NE Diamant 1981 Effect of bilateral vagosympathetic nerve blockade on response of the dog upper esophageal sphincter (UES) to intraesophageal distension and acid Gastroenterology 81 78 84
54. RPE Reynolds GW Effer MP Bendeck 1987 The upper esophageal sphincter in the cat: the role of central innervation assessed by transient vagal blockade Can J Physiol Pharmacol 65 96 99
55. DR Enzman GS Harell FF Zboralske 1977 Upper esophageal responses to intraluminal distension in man Gastroenterology 72 1292 1298
56. A Jean 1972 Localization and activity of medullary swallowing neurones J Physiol (Paris) 64 227 268 (article in French)
57. C Roman L Tieffenbach 1972 Recording the unit activity of vagal motor fibers innervating the baboon esophagus J Physiol (Paris) 64 479 506 (article in French)
58. C Roman 1966 Nervous control of esophageal peristalsis J Phsyiol (Paris) 58 79 108 (article in French)
59. KG Westberg G Scott KA Olsson JP Lund 2001 Discharge patterns of neurons in the medial pontobulbar reticular formation during fictive mastication in the rabbit Eur J Neurosci 14 1709 1718
60. A Tsuboi A Kolta CC Chen JP Lund 2003 Neurons of the trigeminal main sensory nucleus participate in the generation of rhythmic motor patterns Eur J Neurosci 17 229 238
61. D Peleg JA Goldman 1978 Fetal deglutition: a study of the anencephalic fetus Eur J Obstet Gynecol Reprod Biol 8 133 136
62. JA Pritchard 1965 Deglutition by normal and anencephalic fetuses J Obstet Gynecol 25 289 297
63. JP Lund 1991 Mastication and its control by the brain stem Cur Rev Oral Biol Med 2 33 64
64. Y Nakamura N Katakama 1995 Generation of masticatory rhythm in the brainstem Neurosci Res 23 1 19
65. T Athanassiadis KA Olsson A Kolta KG Westberg 2005 Identification of c-Fos immunoreactive brainstem neuron activated during fictive mastication in the rabbit Exp Brain Res 165 478 489
66. IM Lang C Dean BK Medda M Aslam R Shaker 2004 Differential activation of medullary vagal nuclei during different phases of swallowing in the cat Brain Res 1014 145 163
67. Q Sang RK Goyal 2001 Swallowing reflex and brain stem neurons activated by superior laryngeal nerve stimulation in the mouse Am J Physiol 280 G191 G200
68. A Amirali G Tsai D Weisz N Schrader I Sanders 2001 Mapping of brain stem neuronal circuitry active during swallowing Ann Otol Rhinol Laryngol 110 502 5134
69. SM Altschuler X Bao D Bieger DA Hopkins RR Miselis 1989 Viscerotopic representation of the upper alimentary tract in the rat sensory ganglia and nuclei of the solitary and spinal trigeminal tracts J Comp Neurol 283 248 268
70. X Bao RT Barrett SM Altschuler 1995 Transynaptic localization of pharyngeal premotor neurons in rat Brain Res 696 246 249
71. RT Barrett X Bao RR Miselis SM Altschuler 1994 Brain stem localization of rodent esophageal premotor neurons revealed by transsynaptic passage of pseudorabies virus Gastroenterology 107 728 737
72. JH McClean DA Hopkins 1981 A light and electron microscopic study of the dorsal motor nucleus of the vagus in the cat J Comp Neurol 195 157 175
73. D Bieger DA Hopkins 1987 Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus J Comp Neurol 262 546 562
74. T Frysack W Zenker D Kantner 1984 Afferent and efferent innervation of the rat esophagus Anat Embryol 170 63 70
75. PI Collman L Tremblay NE Diamant 1993 The central vagal efferent supply to the esophagus and lower esophageal sphincter of the cat Gastroenterology 104 1430 1438
76. G Holstege G Graveland C Bijker-Biemond I Scuddeboom 1983 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 23 47 62
77. AM Lawn 1966 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 127 293 306
78. DL Brousard RB Lynn EB Wiedner SM Altschuler 1998 Solitarial premotor neuron projections to the rat esophagus and pharynx: implications for control of swallowing Gastroenterology 114 1268 1275
79. D Bieger 1984 Muscarinic activation of rhomboencephalic neurones controlling oesophageal peristalsis in the rat Neuropharmacology 23 1451 1464
80. W Lu M Zhang RS Neuman D Bieger 1997 Fictive oesophageal peristalsis evoked by activation of muscarinic acetylcholine receptors in rat nucleus tractus solitarii Neurogastroenterol Motil 9 247 256
81. IM Lang ST Haworth BK Medda DL Roerig HV Forster R Shaker 2008 Airway responses to esophageal acidification Am J Physiol 294 R211 R219
82. R Shaker 1995 Airway protective reflexes: current concepts Dysphagia 10 216 227
83. J Hamamoto H Kohrogi O Kawano H Iwagoe K Fujii N Hirata M Ando 1997 Esophageal stimulation by hydrochloric acid causes neurogenic inflammation in the airways in guinea pigs J Appl Physiol 82 738 745
84. TE Dick Y Oku Jr Romaniuk NS Cherniak 1993 Interaction between central pattern generators for breathing and swallowing in the cat J Physiol (Lond) 465 715 730
85. TR Feroah HV Forster CG Fuentes IM Lang D Beste P Martino L Pan T Rice 2002 Effects of spontaneous swallows on breathing in awake goats J Appl Physiol 92 1923 1935
86. M Kalia MM Mesulam 1980 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 193 467 508
87. CD Rossiter WP Norman M Jain PJ Hornby S Benjamin RA Gillis 1990 Control of lower esophageal sphincter pressure by two sites in dorsal motor nucleus of the vagus Am J Physiol 259 G899 G906
88. ET Cunningham PE Sawchenko 1989 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 9 1668 1682
89. B Kruszewska J Lipski R Kanjhan 1994 An electrophysiological and morphological study of esophageal motoneurons in rats Am J Physiol 26 R622 R632
90. Q Sang RK Goyal 2000 Lower esophageal sphincter relaxation and activation of medullary neurons by subdiaphragmattic vagal stimulation in the mouse Gastroenterology 119 1600 1609
91. YT Wang RS Neuman D Bieger 1991 Nicotinic cholinergic-mediated excitation in ambigual motoneurons of the rat Neuroscience 40 759 767
92. A Jean 1984 Brainstem organization of the swallowing network Brain Behav Evol 25 109 116
93. T Umezaki T Matsuse T Shin 1998 Medullary swallowing-related neurons in the anesthetized cat NeuroReport 9 1793 1798
94. A Jean 1972 Effect of localized lesions of the medulla oblongata on the esophageal stage of deglutition J Physiol (Paris) 64 507 516
95. A Jean 1978 Localization and activity of oesophageal motoneurons in sheep (microelectrode study) (author's transl) J. Physiol (Paris) 74 737 742 (article in French)
96. A Car C Roman 2002 Effects of atropine on the central mechanism of deglutition in anesthetized sheep Exp Brain Res 142 496 503
97. H Dong CW Loomis D Bieger 2000 Distal and deglutitive inhibition in the rat esophagus: Role of inhibitory neurotransmission in the nucleus tractus solitarii Gastroenterology 118 328 336
98. OR Zoungrana M Amri A Car C Roman 1997 Intracellular activity of motoneurons of the rostral nucleus ambiguus during swallowing in sheep J Neurophysiol 77 909 922