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. 1983 Aug;72(2):551–559. doi: 10.1172/JCI111003

Neural control of the sphincter of Oddi. A physiological role of 5-hydroxytryptamine in the regulation of basal sphincter of Oddi motor activity in the cat.

J Behar, P Biancani
PMCID: PMC1129213  PMID: 6874956

Abstract

The effect of 5-hydroxytryptamine (5-HT) on the sphincter of Oddi (SO) was studied in the cat. The SO had two motor responses to 5-HT: the most common was an initial contraction followed by a more prolonged relaxation, and the other was an exclusive relaxation. Tetrodotoxin did not impair the magnitude of the net contraction induced by 5-HT, but it completely blocked the relaxation. Methysergide partially inhibited the SO contraction in response to submaximal doses of 5-HT (5-20 micrograms/kg). Atropine decreased the SO excitatory response to all doses of 5-HT. The combination of atropine and methysergide completely antagonized the 5-HT excitatory effect, which changed the SO biphasic response to an exclusive relaxation. After tetrodotoxin, the effect of 5-HT was almost completely antagonized by methysergide alone. The SO contraction and relaxation caused by 5-HT were almost completely blocked by 5-HT tachyphylaxis. In contrast, a 5-HT depletion with reserpine enhanced the sensitivity of the SO to 5-HT, responding to doses a thousand times smaller than in control animals. Hexamethonium, phentolamine, propranolol, and 5-methoxy-N,N-dimethyltryptamine did not antagonize the 5-HT-induced contraction or relaxation. These findings indicate that 5-HT caused SO contraction by stimulating postganglionic cholinergic neurons and the smooth muscle directly and caused relaxation by stimulating postganglionic, noncholinergic, nonadrenergic inhibitory neurons. 5-HT blockade or depletion resulted in a significant reduction in basal tonic pressures and in the amplitude of phasic contractions, which suggested that serotonergic neurons may play a physiologic role in the regulation of basal SO motor activity.

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Selected References

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  1. Behar J., Biancani P. Effect of cholecystokinin and the octapeptide of cholecystokinin on the feline sphincter of Oddi and gallbladder. Mechanisms of action. J Clin Invest. 1980 Dec;66(6):1231–1239. doi: 10.1172/JCI109974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burks T. F. Mediation by 5-hydroxytryptamine of morphine stimulant actions in dog intestine. J Pharmacol Exp Ther. 1973 Jun;185(3):530–539. [PubMed] [Google Scholar]
  3. Bülbring E., Gershon M. D. Serotonin participation in the vagal inhibitory pathway to the stomach. Adv Pharmacol. 1968;6(Pt A):323–333. doi: 10.1016/s1054-3589(08)61188-6. [DOI] [PubMed] [Google Scholar]
  4. Costa M., Furness J. B. On the possibility that an indoleamine is a neurotransmitter in the gastrointestinal tract. Biochem Pharmacol. 1979 Mar 1;28(5):565–571. doi: 10.1016/0006-2952(79)90136-9. [DOI] [PubMed] [Google Scholar]
  5. Costa M., Furness J. B. The peristaltic reflex: an analysis of the nerve pathways and their pharmacology. Naunyn Schmiedebergs Arch Pharmacol. 1976 Jul;294(1):47–60. doi: 10.1007/BF00692784. [DOI] [PubMed] [Google Scholar]
  6. Costa M., Furness J. B. The sites of action of 5-hydroxytryptamine in nerve-muscle preparations from the guinea-pig small intestine and colon. Br J Pharmacol. 1979 Feb;65(2):237–248. doi: 10.1111/j.1476-5381.1979.tb07824.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dingledine R., Goldstein A. Effect of synaptic transmission blockade on morphine action in the guinea-pig myenteric plexus. J Pharmacol Exp Ther. 1976 Jan;196(1):97–106. [PubMed] [Google Scholar]
  8. Dingledine R., Goldstein A., Kendig J. Effects of narcotic opiates and serotonin on the electrical behavior of neurons in the guinea pig myenteric plexus. Life Sci. 1974 Jun 1;14(11):2299–2309. doi: 10.1016/0024-3205(74)90111-8. [DOI] [PubMed] [Google Scholar]
  9. Drakontides A. B., Gershon M. D. 5-hydroxytryptamine receptors in the mouse duodenum. Br J Pharmacol Chemother. 1968 Jul;33(3):480–492. doi: 10.1111/j.1476-5381.1968.tb00496.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. FELDBERG W., TOH C. C. Distribution of 5-hydroxytryptamine (serotonin, enteramine) in the wall of the digestive tract. J Physiol. 1953 Feb 27;119(2-3):352–362. doi: 10.1113/jphysiol.1953.sp004850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. GYERMEK L. 5-hydroxytryptamine antagonists. Pharmacol Rev. 1961 Sep;13:399–439. [PubMed] [Google Scholar]
  12. Gershon M. D. Effects of tetrodotoxin on innervated smooth muscle preparations. Br J Pharmacol Chemother. 1967 Mar;29(3):259–279. doi: 10.1111/j.1476-5381.1967.tb01958.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gershon M. D., Erde S. M. The nervous system of the gut. Gastroenterology. 1981 Jun;80(6):1571–1594. [PubMed] [Google Scholar]
  14. Gershon M. D., Robinson R. G., Ross L. L. Serotonin accumulation in the guinea-pig myenteric plexus: ion dependence, structure-activity relationship and the effect of drugs. J Pharmacol Exp Ther. 1976 Sep;198(3):548–561. [PubMed] [Google Scholar]
  15. Green R. D., 3rd, Fleming W. W., Schmidt J. L. Sensitivity changes in the isolated ileum of the guinea pig after pretreatment with reserpine. J Pharmacol Exp Ther. 1968 Aug;162(2):270–276. [PubMed] [Google Scholar]
  16. Johnson S. M., Katayama Y., North R. A. Multiple actions of 5-hydroxytryptamine on myenteric neurones of the guinea-pig ileum. J Physiol. 1980 Jul;304:459–470. doi: 10.1113/jphysiol.1980.sp013336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jonakait G. M., Tamir H., Gintzler A. R., Gershon M. D. Release of [3H]serotonin and its binding protein from enteric neurons. Brain Res. 1979 Sep 28;174(1):55–69. doi: 10.1016/0006-8993(79)90803-5. [DOI] [PubMed] [Google Scholar]
  18. Kao C. Y. Pharmacology of tetrodotoxin and saxitoxin. Fed Proc. 1972 May-Jun;31(3):1117–1123. [PubMed] [Google Scholar]
  19. North R. A., Henderson G., Katayama Y., Johnson S. M. Electrophysiological evidence for presynaptic inhibition of acetylcholine release by 5-hydroxytryptamine in the enteric nervous system. Neuroscience. 1980;5(3):581–586. doi: 10.1016/0306-4522(80)90055-x. [DOI] [PubMed] [Google Scholar]
  20. Rattan S., Goyal R. K. Effects of 5-hydroxytryptamine on the lower esophageal sphincter in vivo: evidence for multiple sites of action. J Clin Invest. 1977 Jan;59(1):125–133. doi: 10.1172/JCI108609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rattan S., Goyal R. K. Evidence of 5-HT participation in vagal inhibitory pathway to opossum LES. Am J Physiol. 1978 Mar;234(3):E273–E276. doi: 10.1152/ajpendo.1978.234.3.E273. [DOI] [PubMed] [Google Scholar]

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