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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1984 Jun;81(11):3595–3599. doi: 10.1073/pnas.81.11.3595

Intramural mechanism of esophageal peristalsis: roles of cholinergic and noncholinergic nerves.

J Crist, J S Gidda, R K Goyal
PMCID: PMC345556  PMID: 6587375

Abstract

We examined the role of peripheral cholinergic and noncholinergic mechanisms in esophageal peristalsis. Intramural nerve elements in rings of circular muscle from six different levels of the opossum esophagus were stimulated transmurally so as to cause neurally mediated muscle contractions. Stimulus frequency was varied from 2 to 40 Hz. An increase in stimulus frequency caused an increase in latencies of contractions in rings from distal esophageal sites and a decrease in latencies in rings from proximal sites. This resulted in a marked slowing of the calculated peristaltic speed. Increasing stimulus frequency also caused an increase in duration and amplitude of contractions. These effects were reversed by atropine (0.1 microM), suggesting that higher stimulus frequencies recruited more cholinergic nerves. In the presence of atropine, increasing the stimulus frequency caused an increase in latencies of contraction at all sites, suggesting that increasing stimulation frequency applied to noncholinergic nerves causes an increase in latencies of contraction at all sites. The results of this study indicate that both noncholinergic and cholinergic nerves play a role in the peripheral mechanism of esophageal peristalsis. Cholinergic nerve stimulation reduces the latency and enhances the amplitude and duration of contractions seen with noncholinergic nerve stimulation alone. The influence of cholinergic innervation is most prominent proximally and decreases distally along the smooth muscle portion of the esophagus. This peripherally located gradient of cholinergic innervation plays an important role in determining the speed and amplitude of esophageal peristalsis.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Christensen J., Arthur C., Conklin J. L. Some determinants of latency of off-response to electrical field stimulation in circular layer of smooth muscle of opossum esophagus. Gastroenterology. 1979 Oct;77(4 Pt 1):677–681. [PubMed] [Google Scholar]
  2. Christensen J., Iskandarani M. Neuromuscular functions in esophageal smooth muscle of opossums as differently affected by veratrum alkaloids. Gastroenterology. 1981 Nov;81(5):866–871. [PubMed] [Google Scholar]
  3. Christensen J., Lund G. F. Esophageal responses to distension and electrical stimulation. J Clin Invest. 1969 Feb;48(2):408–419. doi: 10.1172/JCI105998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Christensen J., Robison B. A. Anatomy of the myenteric plexus of the opossum esophagus. Gastroenterology. 1982 Nov;83(5):1033–1042. [PubMed] [Google Scholar]
  5. Cohen S., Green F. Force-velocity characteristics of esophageal muscle: effect of acetylcholine and norepinephrine. Am J Physiol. 1974 May;226(5):1250–1256. doi: 10.1152/ajplegacy.1974.226.5.1250. [DOI] [PubMed] [Google Scholar]
  6. Crist J., Gidda J. S., Goyal R. K. Characteristics of "on" and "off" contractions in esophageal circular muscle in vitro. Am J Physiol. 1984 Feb;246(2 Pt 1):G137–G144. doi: 10.1152/ajpgi.1984.246.2.G137. [DOI] [PubMed] [Google Scholar]
  7. Daniel E. E., Helmy-Elkholy A., Jager L. P., Kannan M. S. Neither a purine nor VIP is the mediator of inhibitory nerves of opossum oesophageal smooth muscle. J Physiol. 1983 Mar;336:243–260. doi: 10.1113/jphysiol.1983.sp014579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Decktor D. L., Ryan J. P. Transmembrane voltage of opossum esophageal smooth muscle and its response to electrical stimulation of intrinsic nerves. Gastroenterology. 1982 Feb;82(2):301–308. [PubMed] [Google Scholar]
  9. Diamant N. E., El-Sharkawy T. Y. Neural control of esophageal peristalsis. A conceptual analysis. Gastroenterology. 1977 Mar;72(3):546–556. [PubMed] [Google Scholar]
  10. Dodds W. J., Christensen J., Dent J., Arndorfer R. C., Wood J. D. Pharmacologic investigation of primary peristalsis in smooth muscle portion of opossum esophagus. Am J Physiol. 1979 Dec;237(6):E561–E566. doi: 10.1152/ajpendo.1979.237.6.E561. [DOI] [PubMed] [Google Scholar]
  11. Dodds W. J., Christensen J., Dent J., Wood J. D., Arndorfer R. C. Esophageal contractions induced by vagal stimulation in the opossum. Am J Physiol. 1978 Oct;235(4):E392–E401. doi: 10.1152/ajpendo.1978.235.4.E392. [DOI] [PubMed] [Google Scholar]
  12. Dodds W. J., Dent J., Hogan W. J., Arndorfer R. C. Effect of atropine on esophageal motor function in humans. Am J Physiol. 1981 Apr;240(4):G290–G296. doi: 10.1152/ajpgi.1981.240.4.G290. [DOI] [PubMed] [Google Scholar]
  13. Dodds W. J., Stef J. J., Stewart E. T., Hogan W. J., Arndorfer R. C., Cohen E. B. Responses of feline esophagus to cervical vagal stimulation. Am J Physiol. 1978 Jul;235(1):E63–E73. doi: 10.1152/ajpendo.1978.235.1.E63. [DOI] [PubMed] [Google Scholar]
  14. Gidda J. S., Cobb B. W., Goyal R. K. Modulation of esophageal peristalsis by vagal efferent stimulation in opossum. J Clin Invest. 1981 Dec;68(6):1411–1419. doi: 10.1172/JCI110392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gidda J. S., Goyal R. K. Influence of successive vagal stimulations on contractions in esophageal smooth muscle of opossum. J Clin Invest. 1983 May;71(5):1095–1103. doi: 10.1172/JCI110859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Goyal R. K., Rattan S. Genesis of basal sphincter pressure: effect of tetrodotoxin on lower esophageal sphincter pressure in opossum in vivo. Gastroenterology. 1976 Jul;71(1):62–67. [PubMed] [Google Scholar]
  17. Goyal R. K., Rattan S., Said S. I. VIP as a possible neurotransmitter of non-cholinergic non-adrenergic inhibitory neurones. Nature. 1980 Nov 27;288(5789):378–380. doi: 10.1038/288378a0. [DOI] [PubMed] [Google Scholar]
  18. Lund G. F., Christensen J. Electrical stimulation of esophageal smooth muscle and effects of antagonists. Am J Physiol. 1969 Nov;217(5):1369–1374. doi: 10.1152/ajplegacy.1969.217.5.1369. [DOI] [PubMed] [Google Scholar]
  19. Lundberg J. M., Anggård A., Fahrenkrug J., Hökfelt T., Mutt V. Vasoactive intestinal polypeptide in cholinergic neurons of exocrine glands: functional significance of coexisting transmitters for vasodilation and secretion. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1651–1655. doi: 10.1073/pnas.77.3.1651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mukhopadhyay A. K., Weisbrodt N. W. Neural organization of esophageal peristalsis: role of vagus nerve. Gastroenterology. 1975 Mar;68(3):444–447. [PubMed] [Google Scholar]
  21. Rattan S., Gidda J. S., Goyal R. K. Membrane potential and mechanical responses of the opossum esophagus to vagal stimulation and swallowing. Gastroenterology. 1983 Oct;85(4):922–928. [PubMed] [Google Scholar]
  22. Rattan S., Grady M., Goyal R. K. Vasoactive intestinal peptide causes peristaltic contractions in the esophageal body. Life Sci. 1982 May 3;30(18):1557–1563. doi: 10.1016/0024-3205(82)90244-2. [DOI] [PubMed] [Google Scholar]
  23. Ryan J. P., Snape W. J., Jr, Cohen S. Influence of vagal cooling on esophageal function. Am J Physiol. 1977 Feb;232(2):E159–E164. doi: 10.1152/ajpendo.1977.232.2.E159. [DOI] [PubMed] [Google Scholar]
  24. Schulze K., Hajjar J. J., Christensen J. Regional differences in potassium content of smooth muscle from opossum esophagus. Am J Physiol. 1978 Dec;235(6):E709–E713. doi: 10.1152/ajpendo.1978.235.6.E709. [DOI] [PubMed] [Google Scholar]
  25. Weisbrodt N. W., Christensen J. Gradients of contractions in the opossum esophagus. Gastroenterology. 1972 Jun;62(6):1159–1166. [PubMed] [Google Scholar]

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