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. 1968 Jan;194(1):13–33. doi: 10.1113/jphysiol.1968.sp008392

The origin of acetylcholine released from guinea-pig intestine and longitudinal muscle strips

W D M Paton, M Aboo Zar
PMCID: PMC1365672  PMID: 4295753

Abstract

1. Strips of longitudinal muscle can be obtained from guinea-pig ileum either retaining or free from Auerbach's plexus.

2. The denervated strip is unresponsive to electrical stimulation by brief shocks, whether given singly or in trains; it also fails to respond to nicotine or dimethylphenylpiperazinium iodide (DMPP), and eserine causes no spasm.

3. Denervated strips neither contain detectable acetylcholine (< 0·4 ng/mg), nor release it spontaneously (< 5 pg/mg/min) or in response to stimulation (< 31 pg/mg/min). The acetylcholine metabolism of the innervated strip is therefore that of the adherent Auerbach's plexus. Innervated strips had a mean acetylcholine content of 28 ng/mg, a mean resting output of 94 pg/mg/min and an output in response to stimulation at 10 c/s of 700-1200 pg/mg/min.

4. By comparing the responses of innervated and denervated strips it was concluded that arecoline, methylfurmethide, α,β-ethylal-γ-tri-methylammonium propanediol iodide (2268 F), muscarine, histamine, tremorine, oxytocin, and substance P, like acetylcholine, act primarily on the smooth muscle directly; and that angiotensin, barium, potassium, m-bromophenyl choline ether and 5-hydroxytryptamine have a progressively increasing proportionate effect on the nerve plexus. Nicotine and DMPP were inactive in the absence of the plexus.

5. The longitudinal muscle with its accompanying plexus contains about one quarter of the acetylcholine of the whole ileum, and is responsible for about one fifth of the output to electrical stimulation.

6. The volley output of acetylcholine by the innervated strip declines sharply as rate of stimulation increases. Output of acetylcholine was reduced by morphine and by cocaine, particularly when resting or when stimulated at low rates.

7. Acetylcholine output by whole ileum from guinea-pig declines in the absence of glucose, but is insulin-independent. Output by strips of ileum from rats made diabetic with alloxan was similar to that from normal rats.

8. The similarity in properties of acetylcholine output from innervated strips, where it must come from nervous tissue, to that from whole ileum, and the insulin-independence of output from whole ileum suggest that the whole of the acetylcholine output of intestine is nervous in origin.

9. Comparison of the acetylcholine metabolism of the innervated strip with that of the superior cervical ganglion suggests that the typical features of the former (high resting output, high volley output at low rates, low minute output at high rates of stimulation, and sensitivity to morphine) may be linked with the absence of specialized neuro-effector junctions and represent a relatively primitive transmission process.

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Selected References

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

  1. AMBACHE N., LESSIN A. W. Classification of intestinomotor drugs by means of type D botulinum toxin. J Physiol. 1955 Mar 28;127(3):449–478. doi: 10.1113/jphysiol.1955.sp005270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. AMBACHE N. Separation of the longitudinal muscle of the rabbit's ileum as a broad sheet. J Physiol. 1954 Aug 27;125(2):53–5P. [PubMed] [Google Scholar]
  3. AXELSSON J., THESLEFF S. A study of supersensitivity in denervated mammalian skeletal muscle. J Physiol. 1959 Jun 23;147(1):178–193. doi: 10.1113/jphysiol.1959.sp006233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ambache N. Interaction of drugs and the effect of cooling on the isolated mammalian intestine. J Physiol. 1946 Jan 15;104(3):266–287. doi: 10.1113/jphysiol.1946.sp004120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. BIRKS R. I. THE ROLE OF SODIUM IONS IN THE METABOLISM OF ACETYLCHOLINE. Can J Biochem Physiol. 1963 Dec;41:2573–2597. [PubMed] [Google Scholar]
  6. BRISCOE S., BURN J. H. The formation of an acetylcholine-like substance of the isolated rabbit heart. J Physiol. 1954 Oct 28;126(1):181–190. doi: 10.1113/jphysiol.1954.sp005202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. BURBRING E., BURN J. H., SHELLEY H. J. Acetylcholine and ciliary movement in the gill plates of Mytilus edulis. Proc R Soc Lond B Biol Sci. 1953 Sep;141(905):445–466. doi: 10.1098/rspb.1953.0053. [DOI] [PubMed] [Google Scholar]
  8. CROSSLAND J., ELLIOTT K. A., PAPPIUS H. M. Acetylcholine content of brain during insulin hypoglycemia. Am J Physiol. 1955 Oct;183(1):32–34. doi: 10.1152/ajplegacy.1955.183.1.32. [DOI] [PubMed] [Google Scholar]
  9. DAY M. The release of substances like acetylcholine and adrenaline by the isolated rabbit heart. J Physiol. 1956 Dec 28;134(3):558–568. doi: 10.1113/jphysiol.1956.sp005665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DAY M., VANE J. R. An analysis of the direct and indirect actions of drugs on the isolated guinea-pig ileum. Br J Pharmacol Chemother. 1963 Feb;20:150–170. doi: 10.1111/j.1476-5381.1963.tb01306.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. EVANS D. H. L., SCHILD H. O. The reactions of plexus-free circular muscle of cat jejunum to drugs. J Physiol. 1953 Mar;119(4):376–399. doi: 10.1113/jphysiol.1953.sp004853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. EVANS D. H., SCHILD H. O. Reactions of nerve-free and chronically denervated plain muscle to drugs. J Physiol. 1953;122(Suppl):63P–63P. [PubMed] [Google Scholar]
  13. FELDBERG W. Effects of ganglion-blocking substances on the small intestine. J Physiol. 1951 May;113(4):483–505. doi: 10.1113/jphysiol.1951.sp004590. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. FELDBERG W., LIN R. C. Y. The effect of cocaine on the acetylcholine output of the intestinal wall. J Physiol. 1949 Sep;109(3-4):475–487. doi: 10.1113/jphysiol.1949.sp004410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Feldberg W., Lin R. C. Synthesis of acetylcholine in the wall of the digestive tract. J Physiol. 1950 Apr 15;111(1-2):96–118. doi: 10.1113/jphysiol.1950.sp004467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Feldberg W., Solandt O. M. The effects of drugs, sugar and allied substances on the isolated small intestine of the rabbit. J Physiol. 1942 Aug 18;101(2):137–171. doi: 10.1113/jphysiol.1942.sp003972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HEBB C. O. Biochemical evidence for the neural function of acetylcholine. Physiol Rev. 1957 Apr;37(2):196–220. doi: 10.1152/physrev.1957.37.2.196. [DOI] [PubMed] [Google Scholar]
  18. Hebb C. O., Ratković D. Choline acetylase in the placenta of man and other species. J Physiol. 1962 Sep;163(2):307–313. doi: 10.1113/jphysiol.1962.sp006976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. JOHNSON E. S. THE ORIGIN OF THE ACETYLCHOLINE RELEASED SPONTANEOUSLY FROM THE GUINEA-PIG ISOLATED ILEUM. Br J Pharmacol Chemother. 1963 Dec;21:555–568. doi: 10.1111/j.1476-5381.1963.tb02023.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kahlson G., Macintosh F. C. Acetylcholine synthesis in a sympathetic ganglion. J Physiol. 1939 Aug 14;96(3):277–292. doi: 10.1113/jphysiol.1939.sp003776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. MACINTOSH F. C. SYNTHESIS AND STORAGE OF ACETYLCHOLINE IN NERVOUS TISSUE. Can J Biochem Physiol. 1963 Dec;41:2555–2571. [PubMed] [Google Scholar]
  22. MILEDI R. The acetylcholine sensitivity of frog muscle fibres after complete or partial devervation. J Physiol. 1960 Apr;151:1–23. [PMC free article] [PubMed] [Google Scholar]
  23. NORBERG K. A. ADRENERGIC INNERVATION OF THE INTESTINAL WALL STUDIED BY FLUORESCENCE MICROSCOPY. Int J Neuropharmacol. 1964 Sep;3:379–382. doi: 10.1016/0028-3908(64)90067-x. [DOI] [PubMed] [Google Scholar]
  24. PATON W. D. CHOLINERGIC TRANSMISSION AND ACETYLCHOLINE OUTPUT. Can J Biochem Physiol. 1963 Dec;41:2637–2653. [PubMed] [Google Scholar]
  25. PATON W. D. The action of morphine and related substances on contraction and on acetylcholine output of coaxially stimulated guinea-pig ileum. Br J Pharmacol Chemother. 1957 Mar;12(1):119–127. doi: 10.1111/j.1476-5381.1957.tb01373.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Quastel J. H., Tennenbaum M., Wheatley A. H. Choline ester formation in, and choline esterase activities of, tissues in vitro. Biochem J. 1936 Sep;30(9):1668–1681. doi: 10.1042/bj0301668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. SCHAUMANN W. Inhibition by morphine of the release of acetylcholine from the intestine of the guinea-pig. Br J Pharmacol Chemother. 1957 Mar;12(1):115–118. doi: 10.1111/j.1476-5381.1957.tb01372.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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