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. 1977 Jun;267(3):767–789. doi: 10.1113/jphysiol.1977.sp011837

The site and receptors responsible for the inhibition by sympathetic nerves of intestinal smooth muscle and its parasympathetic motor nerves

J S Gillespie 1, M A Khoyi 1,*
PMCID: PMC1283639  PMID: 874878

Abstract

1. The effects of three inhibitory stimuli, sympathetic nerve stimulation, noradrenaline (NA) and isoprenaline have been examined on three forms of motor activity in the rabbit colon, the response to pelvic (parasympathetic) nerve stimulation, acetylcholine (ACh) and spontaneous tone.

2. The response to pelvic nerve stimulation is most effectively inhibited by sympathetic nerve stimulation, much less effectively by NA and hardly at all by isoprenaline. The sympathetic nerves can inhibit the pelvic response at frequencies of stimulation which do not affect spontaneous tone. The inhibitory effect of sympathetic stimulation, and of NA, on the pelvic response is reduced by phentolamine 5 × 10-6 M and unaffected by propranolol 5 × 10-6 M suggesting the effect is mediated via α receptors.

3. The response to ACh is inhibited by all three stimuli equally. The inhibitory effect of sympathetic nerve stimulation and of isoprenaline is reduced by propranolol 5 × 10-6 M. The inhibitory effect of NA is also reduced by propranolol but to a lesser extent. Phentolamine 5 × 10-6 M has a small effect in reducing the inhibitory effect of sympathetic nerve stimulation or of NA. This effect of phentolamine is lost if the participation of motor nerves in the response to ACh is excluded by either tetrodotoxin 10-7 g/ml. or cold storage for 10-14 days. These results suggest that inhibition of the ACh response takes place mainly at the muscle by activation of β receptors but that ACh may have a small indirect stimulant action through motor nerves and this is susceptible to inhibition through α receptors.

4. All three stimuli are equally effective in lowering smooth muscle tone. This inhibitory effect of sympathetic nerve stimulation and of isoprenaline is reduced by propranolol 5 × 10-6 M and unaffected by phentolamine 5 × 10-6 M. The inhibitory effect of NA is reduced by propranolol but again is less sensitive to block than the other two inhibitory stimuli. Phentolamine is without effect on the inhibitory action of NA and the combination of phentolamine with propranolol is no more effective than propranolol alone. These results suggest that NA liberated by sympathetic nerves and isoprenaline inhibit myogenic tone in the smooth muscle by an action on β receptors but the action of NA added to the bath cannot be fully explained in this way.

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Selected References

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

  1. AHLQUIST R. P., LEVY B. Andrenergic receptive mechanism of canine ileum. J Pharmacol Exp Ther. 1959 Oct;127:146–149. [PubMed] [Google Scholar]
  2. Antonio A. The relaxing effect of bradykinin on intestinal smooth muscle. Br J Pharmacol Chemother. 1968 Jan;32(1):78–86. doi: 10.1111/j.1476-5381.1968.tb00431.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BUCKNELL A., WHITNEY B. A PRELIMINARY INVESTIGATION OF THE PHARMACOLOGY OF THE HUMAN ISOLATED TAENIA COLI PREPARATION. Br J Pharmacol Chemother. 1964 Aug;23:164–175. doi: 10.1111/j.1476-5381.1964.tb01576.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bartlet A. L., Hassan T. Adrenoceptors of the chick rectum. Br J Pharmacol. 1970 Aug;39(4):817–821. doi: 10.1111/j.1476-5381.1970.tb09908.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beani L., Bianchi C., Crema A. The effect of catecholamines and sympathetic stimulation on the release of acetylcholine from the guinea-pig colon. Br J Pharmacol. 1969 May;36(1):1–17. doi: 10.1111/j.1476-5381.1969.tb08298.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bowman W. C., Hall M. T. Inhibition of rabbit intestine mediated by alpha- and beta-adrenoceptors. Br J Pharmacol. 1970 Feb;38(2):399–415. doi: 10.1111/j.1476-5381.1970.tb08528.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brody T. M., Diamond J. Blockade of the biochemical correlates of contraction and relaxation in uterine and intestinal smooth muscle. Ann N Y Acad Sci. 1967 Feb 10;139(3):772–780. doi: 10.1111/j.1749-6632.1967.tb41245.x. [DOI] [PubMed] [Google Scholar]
  8. Crema A., Frigo G. M., Lecchini S. A pharmacological analysis of the peristaltic reflex in the isolated colon of the guinea-pig or cat. Br J Pharmacol. 1970 Jun;39(2):334–345. doi: 10.1111/j.1476-5381.1970.tb12897.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dale H. H., Gaddum J. H. Reactions of denervated voluntary muscle, and their bearing on the mode of action of parasympathetic and related nerves. J Physiol. 1930 Sep 18;70(2):109–144. doi: 10.1113/jphysiol.1930.sp002682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Day M. D., Warren P. R. A pharmacological analysis of the responses to transmural stimulation in isolated intestinal preparations. Br J Pharmacol Chemother. 1968 Feb;32(2):227–240. doi: 10.1111/j.1476-5381.1968.tb00967.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dzoljić M. Stimulatory effect of tolazoline on smooth muscle. Br J Pharmacol Chemother. 1967 Jun;30(2):203–212. doi: 10.1111/j.1476-5381.1967.tb02126.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. GARRY R. C., GILLESPIE J. S. The responses of the musculature of the colon of the rabbit to stimulation, in vitro, of the parasympathetic and of the sympathetic outflows. J Physiol. 1955 Jun 28;128(3):557–576. doi: 10.1113/jphysiol.1955.sp005325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Gillespie J. S., Khoyl M. A. A pharmacological analysis of the inhibitory effects of the sympathetic nerves on the rabbit colon. J Physiol. 1975 Jan;244(1):42P–43P. [PubMed] [Google Scholar]
  15. Hirst G. D., Holman M. E., Spence I. Two types of neurones in the myenteric plexus of duodenum in the guinea-pig. J Physiol. 1974 Jan;236(2):303–326. doi: 10.1113/jphysiol.1974.sp010436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hirst G. D., McKirdy H. C. Presynaptic inhibition at mammalian peripheral synapse? Nature. 1974 Aug 2;250(465):430–431. doi: 10.1038/250430a0. [DOI] [PubMed] [Google Scholar]
  17. Jenkinson D. H., Morton I. K. The effect of noradrenaline on the permeability of depolarized intestinal smooth muscle to inorganic ions. J Physiol. 1967 Feb;188(3):373–386. doi: 10.1113/jphysiol.1967.sp008144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kosterlitz H. W., Lydon R. J., Watt A. J. The effects of adrenaline, noradrenaline and isoprenaline on inhibitory alpha- and beta-adrenoceptors in the longitudinal muscle of the guinea-pig ileum. Br J Pharmacol. 1970 Jun;39(2):398–413. doi: 10.1111/j.1476-5381.1970.tb12903.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lawson W. R., Mackenna B. R. The inhibitory adrenergic receptors of the rabbit intestine. J Physiol. 1969 May;202(1):35P–36P. [PubMed] [Google Scholar]
  20. McDOUGAL M. D., WEST G. B. The inhibition of the peristaltic reflex by sympathomimetic amines. Br J Pharmacol Chemother. 1954 Jun;9(2):131–137. doi: 10.1111/j.1476-5381.1954.tb00831.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Nishi S., North R. A. Presynaptic action of noradrenaline in the myenteric plexus. J Physiol. 1973 May;231(1):29P–30P. [PubMed] [Google Scholar]
  23. Ohkawa H., Prosser C. L. Functions of neurons in enteric plexuses of cat intestine. Am J Physiol. 1972 Jun;222(6):1420–1426. doi: 10.1152/ajplegacy.1972.222.6.1420. [DOI] [PubMed] [Google Scholar]
  24. Paton W. D., Vizi E. S. The inhibitory action of noradrenaline and adrenaline on acetylcholine output by guinea-pig ileum longitudinal muscle strip. Br J Pharmacol. 1969 Jan;35(1):10–28. doi: 10.1111/j.1476-5381.1969.tb07964.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. SCHAUMANN W. Zusammenhänge zwischen der Wirkung der Analgetica und Sympathicomimetica auf den Meerschweinchen-Dunndarm. Naunyn Schmiedebergs Arch Exp Pathol Pharmakol. 1958;233(1):112–124. [PubMed] [Google Scholar]
  26. de Groat W. C., Krier J. An electrophysiological study of the sacral parasympathetic pathway to the colon of the cat. J Physiol. 1976 Sep;260(2):425–445. doi: 10.1113/jphysiol.1976.sp011523. [DOI] [PMC free article] [PubMed] [Google Scholar]

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