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The brainstem esophagomotor network pattern generator: A rodent model

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Abstract

The evidence reviewed in this essay supports the following working model of the central function generator for esophageal peristalsis in the rat: solitarial subnucleus centralis (NTSc) neurons operate in a dual capacity as esophagomotor reflex interneurons and as command neurons programming respective outputs from nucleus ambiguus compact formation (AMBc) motoneurons during secondary and primary peristalsis. In both conditions, there is a critical requirement for cholinergic input which enables NTSc neurons to generate the timed sequence of AMBc motoneuronal activity. In primary peristalsis, the cholinergic coupling mechanism is activated centrally, probably via projections from deglutitive premotor neurons to the parvicellular reticular formation and thence to the NTS. In reflex (or secondary) peristalsis, the cholinergic input could in part be generated by cholinergic vagal viscerosensory fibers innervating the esophagus. Postulated connections between NTS deglutitive neurons and the parvicellular cholinergic neurons of the intermediate reticular formation have yet to be demonstrated. Premotor input from NTSc to AMBc is generated by somatostatinergic and excitatory aminoacidergic neurons. Coactivation of both inputs by cholinergic afferents is necessary to generate esophagomotor output from AMBc neurons. The model under study is derived from investigations into central mechanisms governing striated muscle peristaltic activity. Whether the basic operational principles revealed thus far apply to peristaltic pattern generation in species with a smooth muscle esophagus, requires further investigation.

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References

  1. Roman C: Nervous control of esophageal and gastric motility. In: Bertaccini G (ed.):Handbook of Experimental Pharmacology, Mediators and Drugs in Gastrointestinal Motility, I. Morphological and Neurophysiological Control, Springer, vol. 51 (I). New York: Springer-Verlag, 1982, pp 223–278

    Google Scholar 

  2. Christensen J: Motor functions of the pharynx and esophagus. In: Johnson LR (ed.):Physiology of the Gastrointestinal Tract, 2nd ed. New York: Raven Press, 1987, pp 595–612

    Google Scholar 

  3. Miller A: Swallowing: neurophysiologic control of the esophageal phase.Dysphagia 2:72–82, 1987

    Google Scholar 

  4. Diamant NE: Physiology of esophageal motor function.Gastroenterol Clin North Am 18(2):179–194, 1989

    Google Scholar 

  5. Goyal RK, Paterson WG: Esophageal motility. In:Handbook of Physiology. The Gastrointestinal System. Motility and Circulation. Bethesda, MD: American Physiological Society, section 6, vol 1, pt. 2, 1987, pp 865–908

    Google Scholar 

  6. Jean A: Brainstem control of swallowing. In: Taylor A (ed.)Neurophysiology of the Jaws and Teeth. London: MacMillan, 1990, pp 294–321

    Google Scholar 

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

    Google Scholar 

  8. Kauffmann P, Lierse W, Stark W, Stelzner F: Die Muskelanordnug in der Speiseröhre (Mensch, Rhesusaffe, Kaninchen, Maus, Ratte, Seehund)Erg Anat Entw-Gesch 40:3–33, 1968

    Google Scholar 

  9. Marsh DC, Bieger D: Cholinoceptor-mediated mechanical and electrical responses of rat oesophageal striated musculature. A comparison of two in vitro methods.Gen Pharmacol 18:657–663, 1987

    Google Scholar 

  10. Bieger D, Triggle CR: Pharmacological properties of mechanical responses of the rat oesophageal muscularis mucosae to vagal and field stimulation.Br J Pharmacol 84:93–106, 1985

    Google Scholar 

  11. Bieger D, Marsh DC: Substance P modulates vagal cholinergic transmission in rat oesophageal striated and smooth muscle.Eur J Pharmacol 183:2045, 1990

    Google Scholar 

  12. Bieger D: Muscarinic activation of rhombencephalic neurones controlling oesophageal peristalsis in the rat.Neuropharmacol 23:1451–1464, 1984

    Google Scholar 

  13. Lu WY, Bieger D: Secondary peristalsis in the rat. Dysphagia Res. Soc. Inaug. Mtg., Milwaukee, WI, 1992

    Google Scholar 

  14. Bieger D, Hopkins DA: Viscerotopic representation of the upper alimentary tract in the medulla oblongata.J Comp Neurol 252:546–562, 1987

    Google Scholar 

  15. Wang YT, Bieger D, Neuman RS: Activation of NMDA receptors is necessary for fast information transfer at brainstem vagal motoneurons.Brain Res 576:260–266, 1991

    Google Scholar 

  16. Altschuler JM, Bao XM, 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 283:248–268, 1989

    Google Scholar 

  17. Neuhuber WL: Sensory vagal innervation of the rat oesophagus and cardia: a light and electron microscopic anterograde tracing study.J Auton Nerv Syst 20:243–255, 1987

    Google Scholar 

  18. Green T, Dockray GJ: Calcitonin gene-related peptide and substance P in afferents to the upper gastrointestinal tract in the rat.Neursci Lett 76:151–156, 1987

    Google Scholar 

  19. Jean A: Effet de lésions localisées du bulbe rachidien sur le stae oesophagien de la dëglutition.J Physiol (Paris) 64:507–516, 1972

    Google Scholar 

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

    Google Scholar 

  21. Palouzier B, Barrit-Chamoin MC, Portalier P, Ternaux JP: Cholinergic neurons in the rat nodose ganglia.Neurosci Lett 80:147–152, 1987

    Google Scholar 

  22. Ternaux JP, Falempin M, Palouzier B, Chamoin MC, Portalier P: Presence of cholinergic neurons in the vagal afferent system: biochemical and immunohistochemical approaches.J Auton Nerv Syst 28:233–242, 1989

    Google Scholar 

  23. Falempin M, Ternaux JP, Palouzier B, Chamoin MC: Presence of cholinergic neurons in the vagal affernt system: involvement in a heterogenous reinnervation.J Auton Nerv Syst 28:243–250, 1989

    Google Scholar 

  24. 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-immuno-reac tive interneurons subserving reflex control of oesophageal motility.J Neurosci 9:1668–1682, 1989

    Google Scholar 

  25. Hashim MA, Vyas D, Bieger D: Solitarial deglutitive efferents in the rat (Abstract)Neurosci 14(2):793, 1988

    Google Scholar 

  26. Cunningham ET Jr, Simmons DM, Swanson LW, Sawchenko PE: Enkephalin-immunoreactivity and messenger RNA in a discrete projection from the nucleus of the solitary tract to the nucleus ambiguus in the rat.J Comp Neurol 307:1–16, 1991

    Google Scholar 

  27. Paterson WG, Hynna-Liepert TT, Selucky M: Comparison of primary and secondary esophageal peristalsis in humans: effect of atropine.Am J Physiol 260:G52-G57, 1991

    Google Scholar 

  28. Hashim MA, Bieger D: Excitatory amino acid receptor-mediated activation of solitarial deglutitive loci.Neuropharmacology 28:913–921, 1989

    Google Scholar 

  29. Wang YT, Bieger D: Role of solitarial GABA-ergic mechanisms in control of swallowing.Am J Physiol 261:R639-R646, 1991

    Google Scholar 

  30. Bieger D: Neuropharmacologic correlates of deglutition: lessons from fictive swallowing.Dysphagia 6:147–164, 1991

    Google Scholar 

  31. Levy RA, Anderson EG: The effect of the GABA antagonists bicuculline and picrotoxin on primary afferent terminal excitability.Brain Res 43:171–180, 1972

    Google Scholar 

  32. Curtis DR, Duggan AW, Felix B, Johnston GAR: Bicuculline, an antagonist of GABA and synaptic inhibition in the spinal cord of the rat.Brain Res 32:69–96, 1971

    Google Scholar 

  33. Lu WY, Neuman RS, Bieger D: Cholinergic innervation of esophageal premotoneurons-central vs. peripheral source. Dysphagia Res. Soc. Inaug. Mtg. Milwaukee, WI, 1992

    Google Scholar 

  34. Ross CA, Ruggiero DA, Reis DJ: Projections from the nucleus tractus solitarius to the rostral ventrolateral medulla.J Comp Neurol 245:511–534, 1985

    Google Scholar 

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

    Google Scholar 

  36. Zhang M, Wang YT, Vyas DM, Neuman RS, Bieger D: Nicotinic cholinoceptor-mediated EPSPs in rat nucleus ambiguus.Exp Brain Res (in press)

  37. Kessler J, Jean A: Identification of the medullary swallowing regions in the rat.Exp Brain Res 57:256–263, 1985

    Google Scholar 

  38. Tell F, Jean A: Activation of N-methyl-D-aspartate receptors induces endogenous rhythmic bursting activities in nucleus tractus solitaryryi neurons: an intracellular study on adult rat brainstem slices.Eur J Neurosci 3:1353–1365, 1991

    Google Scholar 

  39. Wang YT, Zhang M, Neuman RS, Bieger D: Somatostatin regulates excitatory amino acid receptor-mediated fast excitatory postsynaptic potential components in vagal motoneurons.Neuroscience 53(1):7–9, 1993

    Google Scholar 

  40. Blank E, Greenwood B, Dodds WJ: Cholinergic control of smooth muscle peristalsis in the cat esophagus.Am J Physiol 257:G517-G523, 1989

    Google Scholar 

  41. Kantrowitz PA, Siegel CI, Hendrix TR: Differences in motility of the upper and lower esophagus in man and its alteration by atropine.Bull Johns Hopkins Hosp 118:476–491, 1966

    Google Scholar 

  42. Bramble MG, Cunliffe J, Dellipiani AW: Evidence for a change in neurotransmitter affecting oesophageal motlity in Parkinson's disease.J Neural Neurosurg Psychiatry 41:709–712, 1978

    Google Scholar 

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  1. Faculty of Medicine, Memorial University of Newfoundland, A1B 3V6, St. John's, Newfoundland, Canada

    Detlef Bieger MD

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  1. Detlef Bieger MD
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This essay is dedicated to the memory of Martin W. Donner.

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Bieger, D. The brainstem esophagomotor network pattern generator: A rodent model. Dysphagia 8, 203–208 (1993). https://doi.org/10.1007/BF01354539

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