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. 1967 Oct;192(3):823–846. doi: 10.1113/jphysiol.1967.sp008334

5-Hydroxytryptamine participation in the vagal inhibitory innervation of the stomach

Edith Bülbring, M D Gershon
PMCID: PMC1365545  PMID: 4383454

Abstract

1. Intraluminal pressure was recorded from the isolated guinea-pig and mouse stomach with the vagus and sympathetic nerves attached.

2. The response to vagal stimulation, which consists of an excitatory and an inhibitory component, resembled the response to 5-hydroxytryptamine (5-HT), which has no direct action on the muscle but acts on intrinsic excitatory and inhibitory ganglia.

3. In the presence of hyoscine, the effect of vagal stimulation, of nicotinic compounds and of 5-HT were all purely relaxant. Competitive block of ganglionic receptors for acetylcholine reduced the vagal relaxation without antagonizing 5-HT. Specific desensitization of ganglionic receptors for 5-HT reduced the vagal relaxation without antagonizing nicotinic compounds.

4. During the early phase of the blocking action of nicotine, responses to vagal stimulation and to 5-HT were both abolished. As the non-specific antagonism changed to the later phase of specific antagonism to acetylcholine, the inhibitory (but not the excitatory) component of the vagal response recovered partially, in parallel with the recovery of the relaxant effect of 5-HT.

5. The vagal inhibitory effect was completely abolished only when competitive block of acetylcholine receptors was combined with desensitization of 5-HT receptors.

6. Stimulation of the mouse stomach (after asphyxiation of the mucosa and exclusion of the luminal content) in the presence of hyoscine caused the release of 5-HT; this release was blocked by tetrodotoxin.

7. The results, together with previous observations that 5-HT is contained within preganglionic nerve fibres in the myenteric plexus, are consistent with the hypothesis that 5-HT, with acetylcholine, may be a neurotransmitter in the vagal inhibitory innervation of the stomach.

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Selected References

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

  1. BIRMINGHAM A. T., WILSON A. B. AN ANALYSIS OF THE BLOCKING ACTION OF DIMETHYLPHENYLPIPERAZINIUM IODINE ON THE INHIBITION OF ISOLATED SMALL INTESTINE PRODUCED BY STIMULATION OF SYMPATHETIC NERVES. Br J Pharmacol Chemother. 1965 Apr;24:375–386. doi: 10.1111/j.1476-5381.1965.tb01725.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BROWNLEE G., JOHNSON E. S. THE RELEASE OF ACETYLCHOLINE FROM THE ISOLATED ILEUM OF THE GUINEA-PIG INDUCED BY 5-HYDROXYTRYPTAMINE AND DIMETHYLPHENYLPIPERAZINIUM. Br J Pharmacol Chemother. 1965 Jun;24:689–700. doi: 10.1111/j.1476-5381.1965.tb01624.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BROWNLEE G., JOHNSON E. S. THE SITE OF THE 5-HYDROXYTRYPTAMINE RECEPTOR ON THE INTRAMURAL NERVOUS PLEXUS OF THE GUINEA-PIG ISOLATED ILEUM. Br J Pharmacol Chemother. 1963 Oct;21:306–322. doi: 10.1111/j.1476-5381.1963.tb01529.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BULBRING E., CREMA A. The release of 5-hydroxytryptamine in relation to pressure exerted on the intestinal mucosa. J Physiol. 1959 Apr 23;146(1):18–28. doi: 10.1113/jphysiol.1959.sp006175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bennett A., Bucknell A., Dean A. C. The release of 5-hydroxytryptamine from the rat stomach in vitro. J Physiol. 1966 Jan;182(1):57–65. doi: 10.1113/jphysiol.1966.sp007808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Burnstock G., Campbell G., Rand M. J. The inhibitory innervation of the taenia of the guinea-pig caecum. J Physiol. 1966 Feb;182(3):504–526. doi: 10.1113/jphysiol.1966.sp007834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bülbring E., Gershon M. D. 5-hydroxytryptamine participation in vagal relaxation of the stomach. J Physiol. 1966 Oct;186(2):95P–96P. [PubMed] [Google Scholar]
  8. Bülbring E., Tomita T. Properties of the inhibitory potential of smooth muscle as observed in the response to field stimulation of the guinea-pig taenia coli. J Physiol. 1967 Apr;189(2):299–315. doi: 10.1113/jphysiol.1967.sp008169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Campbell G. The inhibitory nerve fibres in the vagal supply to the guinea-pig stomach. J Physiol. 1966 Aug;185(3):600–612. doi: 10.1113/jphysiol.1966.sp008004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. FASTIER F. N., McDOWALL M. A., WAAL H. Pharmacological properties of phenyldiguanide and other amidine derivatives in relation to those of 5-hydroxytryptamine. Br J Pharmacol Chemother. 1959 Dec;14:527–535. doi: 10.1111/j.1476-5381.1959.tb00960.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. GADDUM J. H., PICARELLI Z. P. Two kinds of tryptamine receptor. Br J Pharmacol Chemother. 1957 Sep;12(3):323–328. doi: 10.1111/j.1476-5381.1957.tb00142.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. GADDUM J. H. Tryptamine receptors. J Physiol. 1953 Feb 27;119(2-3):363–368. doi: 10.1113/jphysiol.1953.sp004851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. GERSHON M. D., DRAKONTIDES A. B., ROSS L. L. SEROTONIN: SYNTHESIS AND RELEASE FROM THE MYENTERIC PLEXUS OF THE MOUSE INTESTINE. Science. 1965 Jul 9;149(3680):197–199. doi: 10.1126/science.149.3680.197. [DOI] [PubMed] [Google Scholar]
  15. GYERMEK L. A NEW CLASS OF 5-HYDROXYTRYPTAMINE ANTAGONISTS. J Med Chem. 1964 May;7:280–284. doi: 10.1021/jm00333a007. [DOI] [PubMed] [Google Scholar]
  16. GYERMEK L. ACTION OF GUANIDINE DERIVATIVES ON AUTONOMIC GANGLIA. Arch Int Pharmacodyn Ther. 1964 Aug 1;150:570–581. [PubMed] [Google Scholar]
  17. 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]
  18. Gershon M. D. Inhibition of gastrointestinal movement by sympathetic nerve stimulation: the site of action. J Physiol. 1967 Apr;189(2):317–327. doi: 10.1113/jphysiol.1967.sp008170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gershon M. D., Ross L. L. Location of sites of 5-hydroxytryptamine storage and metabolism by radioautography. J Physiol. 1966 Oct;186(2):477–492. doi: 10.1113/jphysiol.1966.sp008047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gershon M. D., Ross L. L. Radioisotopic studies of the binding, exchange, and distribution of 5-hydroxytryptamine synthesized from its radioactive precursor. J Physiol. 1966 Oct;186(2):451–476. doi: 10.1113/jphysiol.1966.sp008046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. HERTZLER E. C. 5-Hydroxytryptamine and transmission in sympathetic ganglia. Br J Pharmacol Chemother. 1961 Dec;17:406–413. doi: 10.1111/j.1476-5381.1961.tb01126.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. JOHNSON E. S. AN INDEPENDENT NERVE-PATHWAY FOR 5-HYDROXYTRYPTAMINE IN THE GUINEA-PIG ILEUM. J Pharm Pharmacol. 1964 Nov;16:760–763. doi: 10.1111/j.2042-7158.1964.tb07402.x. [DOI] [PubMed] [Google Scholar]
  23. KURIYAMA H. ELECTROPHYSIOLOGICAL OBSERVATIONS ON THE MOTOR INNERVATION OF THE SMOOTH MUSCLE CELLS IN THE GUINEA-PIG VAS DEFERENS. J Physiol. 1963 Nov;169:213–228. doi: 10.1113/jphysiol.1963.sp007251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. LESSIN A. W., LONG R. F., PARKES M. W. CENTRAL STIMULANT ACTIONS OF ALPHA-ALKYL SUBSTITUTED TRYPTAMINES IN MICE. Br J Pharmacol Chemother. 1965 Feb;24:49–67. doi: 10.1111/j.1476-5381.1965.tb02079.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. LING H. W. Actions of dimethylphenylpiperazinium. Br J Pharmacol Chemother. 1959 Dec;14:505–511. doi: 10.1111/j.1476-5381.1959.tb00957.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Martinson J. Vagal relaxation of the stomach. Experimental re-investigation of the concept of the transmission mechanism. Acta Physiol Scand. 1965 Aug;64(4):453–462. doi: 10.1111/j.1748-1716.1965.tb04204.x. [DOI] [PubMed] [Google Scholar]
  27. McSwiney B. A., Robson J. M. The response of smooth muscle to stimulation of the vagus nerve. J Physiol. 1929 Oct 23;68(2):124–131. doi: 10.1113/jphysiol.1929.sp002599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. PATON W. D. M., PERRY W. L. M. The relationship between depolarization and block in the cat's superior cervical ganglion. J Physiol. 1953 Jan;119(1):43–57. doi: 10.1113/jphysiol.1953.sp004827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. PATON W. D., RANG H. P. THE UPTAKE OF ATROPINE AND RELATED DRUGS BY INTESTINAL SMOOTH MUSCLE OF THE GUINEA-PIG IN RELATION TO ACETYLCHOLINE RECEPTORS. Proc R Soc Lond B Biol Sci. 1965 Aug 24;163:1–44. doi: 10.1098/rspb.1965.0058. [DOI] [PubMed] [Google Scholar]
  30. PATON W. D. The response of the guineapig ileum to electrical stimulation by coaxial electrodes. J Physiol. 1955 Feb 28;127(2):40–1P. [PubMed] [Google Scholar]
  31. PATON W. D., VANE J. R. Analysis of he responses of the isolated stomach to electrical stimulation and to drugs. J Physiol. 1963 Jan;165:10–46. doi: 10.1113/jphysiol.1963.sp007040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. RANG H. P. STIMULANT ACTIONS OF VOLATILE ANAESTHETICS ON SMOOTH MUSCLE. Br J Pharmacol Chemother. 1964 Apr;22:356–365. doi: 10.1111/j.1476-5381.1964.tb02040.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. TRENDELENBURG U. Modification of transmission through the superior cervical ganglion of the cat. J Physiol. 1956 Jun 28;132(3):529–541. doi: 10.1113/jphysiol.1956.sp005546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. TRENDELENBURG U. Reaktion sympathischer Ganglien während der Ganglienblockade durch Nicotin. Naunyn Schmiedebergs Arch Exp Pathol Pharmakol. 1957;230(5):448–456. [PubMed] [Google Scholar]
  35. TRENDELENBURG U. The action of 5-hydroxytryptamine on the nictitating membrane and on the superior cervical ganglion of the cat. Br J Pharmacol Chemother. 1956 Mar;11(1):74–80. doi: 10.1111/j.1476-5381.1956.tb01031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. VANE J. R. A sensitive method for the assay of 5-hydroxytryptamine. Br J Pharmacol Chemother. 1957 Sep;12(3):344–349. doi: 10.1111/j.1476-5381.1957.tb00146.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. VANE J. R. The relative activities of some tryptamine analogues on the isolated rat stomach strip preparation. Br J Pharmacol Chemother. 1959 Mar;14(1):87–98. doi: 10.1111/j.1476-5381.1959.tb00933.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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