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. 1966 Feb;182(3):504–526. doi: 10.1113/jphysiol.1966.sp007834

The inhibitory innervation of the taenia of the guinea-pig caecum

G Burnstock, G Campbell, M J Rand
PMCID: PMC1357484  PMID: 5942999

Abstract

1. The inhibitory innervation of the taenia of the guinea-pig caecum has been studied, after blocking the responses to stimulation of excitatory cholinergic nerves with atropine.

2. Stimulation of the perivascular nerves supplying the taenia caused relaxations. These nerves had properties which were typical of sympathetic post-ganglionic adrenergic nerves. The relaxations caused by stimulation were maximal at frequencies of stimulation above 30 pulses/sec and they were abolished by bretylium, guanethidine and 1,1-dimethyl-4-phenylpiperazinium iodide (DMPP).

3. The taenia is also innervated by intramural inhibitory nerves with their cell bodies in Auerbach's plexus. These nerves can be excited by electrical stimulation of the taenia or by the application of ganglion-stimulating drugs.

4. The intramural inhibitory nerves have different properties from sympathetic adrenergic nerves. Relaxations in response to stimulation were maximal with frequencies of stimulation of about 5 pulses/sec and they were not blocked by bretylium, guanethidine or DMPP.

5. Preganglionic cholinergic fibres in the caecal wall make synaptic connexions with the intramural inhibitory neurones.

6. The role of the intramural inhibitory neurones in intestinal activity and their possible connexions with the central nervous system have been discussed.

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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., EDWARDS J. Reversal of nicotine action on the intestine by atropine. Br J Pharmacol Chemother. 1951 Jun;6(2):311–317. doi: 10.1111/j.1476-5381.1951.tb00644.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. AMBACHE N. Unmasking, after cholinergic paralysis by botulinum toxin, of a reversed action of nicotine on the mammalian intestine, revealing the probable presence of local inhibitory ganglion cells in the enteric plexuses. Br J Pharmacol Chemother. 1951 Mar;6(1):51–67. doi: 10.1111/j.1476-5381.1951.tb00619.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BENTLEY G. A. Studies on sympathetic mechanisms in isolated intestinal and vas deferens preparations. Br J Pharmacol Chemother. 1962 Aug;19:85–98. doi: 10.1111/j.1476-5381.1962.tb01429.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BORN G. V., BULBRING E. The movement of potassium between smooth muscle and the surrounding fluid. J Physiol. 1956 Mar 28;131(3):690–703. doi: 10.1113/jphysiol.1956.sp005494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. BUELBRING E., KURIYAMA H. THE EFFECT OF ADRENALINE ON THE SMOOTH MUSCLE OF GUINEA-PIG TAENIA COLI IN RELATION TO THE DEGREE OF STRETCH. J Physiol. 1963 Nov;169:198–212. doi: 10.1113/jphysiol.1963.sp007250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. BULBRING E. Correlation between membrane potential, spike discharge and tension in smooth muscle. J Physiol. 1955 Apr 28;128(1):200–221. doi: 10.1113/jphysiol.1955.sp005299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. BULBRING E., KURIYAMA H. Effects of changes in ionic environment on the action of acetylcholine and adrenaline on the smooth muscle cells of guinea-pig taenia coli. J Physiol. 1963 Apr;166:59–74. doi: 10.1113/jphysiol.1963.sp007090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. BULBRING E., KURIYAMA H. Effects of changes in the external sodium and calcium concentrations on spontaneous electrical activity in smooth muscle of guinea-pig taenia coli. J Physiol. 1963 Apr;166:29–58. doi: 10.1113/jphysiol.1963.sp007089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. BULBRING E. Measurements of oxygen consumption in smooth muscle. J Physiol. 1953 Oct;122(1):111–134. doi: 10.1113/jphysiol.1953.sp004983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. BURN J. H., GIBBONS W. R. THE SYMPATHETIC POSTGANGLIONIC FIBRE AND THE BLOCK BY BRETYLIUM; THE BLOCK PREVENTED BY HEXAMETHONIUM AND IMITATED BY MECAMYLAMINE. Br J Pharmacol Chemother. 1964 Jun;22:549–557. doi: 10.1111/j.1476-5381.1964.tb01709.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. BURN J. H., LEACH E. H., RAND M. J., THOMPSON J. W. Peripheral effects of nicotine and acetylcholine resembling those of sympathetic stimulation. J Physiol. 1959 Oct;148:332–352. doi: 10.1113/jphysiol.1959.sp006291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. BURNSTOCK G., CAMPBELL G., BENNETT M., HOLMAN M. E. INNERVATION OF THE GUINEA-PIG TAENIA COLI: ARE THERE INTRINSIC INHIBITORY NERVES WHICH ARE DISTINCT FROM SYMPATHETIC NERVES? Int J Neuropharmacol. 1964 May;3:163–166. doi: 10.1016/0028-3908(64)90003-6. [DOI] [PubMed] [Google Scholar]
  14. BURNSTOCK G. The action of adrenaline on excitability and membrane potential in the taenia coli of the guinea-pig and the effect of DNP on this action and on the action of acetylcholine. J Physiol. 1958 Aug 29;143(1):183–194. doi: 10.1113/jphysiol.1958.sp006052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. BURNSTOCK G. The effects of acetylcholine on membrane potential, spike frequency, conduction velocity and excitability in the taenia coli of the guinea-pig. J Physiol. 1958 Aug 29;143(1):165–182. doi: 10.1113/jphysiol.1958.sp006051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Bayliss W. M., Starling E. H. The movements and innervation of the small intestine. J Physiol. 1899 May 11;24(2):99–143. doi: 10.1113/jphysiol.1899.sp000752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Bennett M. R., Burnstock G., Holman M. E. Transmission from perivascular inhibitory nerves to the smooth muscle of the guinea-pig taenia coli. J Physiol. 1966 Feb;182(3):527–540. doi: 10.1113/jphysiol.1966.sp007835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Bennett M. R., Burnstock G., Holman M. Transmission from intramural inhibitory nerves to the smooth muscle of the guinea-pig taenia coli. J Physiol. 1966 Feb;182(3):541–558. doi: 10.1113/jphysiol.1966.sp007836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Brandon K. W., Rand M. J. Acetylcholine and the sympathetic innervation of the spleen. J Physiol. 1961 Jun;157(1):18–32. doi: 10.1113/jphysiol.1961.sp006702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. DALY M. D., SCOTT M. J. The effects of acetylcholine on the volume and vascular resistance of the dog's spleen. J Physiol. 1961 Apr;156:246–259. doi: 10.1113/jphysiol.1961.sp006673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Elliott T. R. Antiperistalsis and other muscular activities of the colon. J Physiol. 1904 Jun 30;31(3-4):272–304. doi: 10.1113/jphysiol.1904.sp001037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. FISHLOCK D. J., PARKS A. G. A STUDY OF HUMAN COLONIC MUSCLE IN VITRO. Br Med J. 1963 Sep 14;2(5358):666–667. doi: 10.1136/bmj.2.5358.666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. GILLESPIE J. S., MACKENNA B. R. The inhibitory action of nicotine on the rabbit colon. J Physiol. 1960 Jul;152:191–205. doi: 10.1113/jphysiol.1960.sp006481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. GOKHALE S. D., GULATI O. D., KELKAR V. V., JOSHI N. Y. EFFECT OF BRETYLIUM AND GUANETHIDINE ON SOME CHOLINERGIC EFFECTORS. Arch Int Pharmacodyn Ther. 1963 Sep 1;145:243–253. [PubMed] [Google Scholar]
  27. GOODFORD P. J. CHLORIDE CONTENT AND 36CL UPTAKE IN THE SMOOTH MUSCLE OF THE GUINEA-PIG TAENIA COLI. J Physiol. 1964 Mar;170:227–237. doi: 10.1113/jphysiol.1964.sp007326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. GOODFORD P. J. The sodium content of the smooth muscle of the guinea-pig taenia coli. J Physiol. 1962 Oct;163:411–422. doi: 10.1113/jphysiol.1962.sp006986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. HOLMAN M. E. Membrane potentials recorded with high-resistance micro-electrodes; and the effects of changes in ionic environment on the electrical and mechanical activity of the smooth muscle of the taenia coli of the guineapig. J Physiol. 1958 May 28;141(3):464–488. doi: 10.1113/jphysiol.1958.sp005989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. HUKUHARA T., YAMAGAMI M., NAKAYAMA S. On the intestinal intrinsic reflexes. Jpn J Physiol. 1958 Mar 30;8(1):9–20. doi: 10.2170/jjphysiol.8.9. [DOI] [PubMed] [Google Scholar]
  31. JARRETT R. J. Action of nicotine on the rabbit muscular organ (ileo-colic sphincter). Br J Pharmacol Chemother. 1962 Apr;18:397–404. doi: 10.1111/j.1476-5381.1962.tb01419.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. KOSTERLITZ H. W., LEES G. M. Action of bretylium on the isolated guinea-pig ileum. Br J Pharmacol Chemother. 1961 Aug;17:82–86. doi: 10.1111/j.1476-5381.1961.tb01106.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. KOTTEGODA S. R. The action of nicotine and acetylcholine on the vessels of the rabbit's ear. Br J Pharmacol Chemother. 1953 Jun;8(2):156–161. doi: 10.1111/j.1476-5381.1953.tb00770.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. KURIYAMA H. The influence of potassium, sodium and chloride on the membrane potential of the smooth muscle of taenia coli. J Physiol. 1963 Apr;166:15–28. doi: 10.1113/jphysiol.1963.sp007088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. LEE W. C., SHIDEMAN F. E. Mechanism of the positive inotropic response to certain ganglionic stimulants. J Pharmacol Exp Ther. 1959 Jul;126(3):239–249. [PubMed] [Google Scholar]
  36. LEVY J., MICHEL-BER E. Mécanisme de l'action de divers excito-ganglionnaires et intestin isolé de rongeurs. J Physiol (Paris) 1953;45(4):687–722. [PubMed] [Google Scholar]
  37. Langley J. N. On Inhibitory Fibres in the Vagus for the end of the OEsophagus and the Stomach. J Physiol. 1898 Dec 30;23(5):407–414. doi: 10.1113/jphysiol.1898.sp000737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. MCEWEN L. M. The effect on the isolated rabbit heart of vagal stimulation and its modification by cocaine, hexamethonium and ouabain. J Physiol. 1956 Mar 28;131(3):678–689. doi: 10.1113/jphysiol.1956.sp005493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. NAGASAWA J. THE EFFECTS OF CHANGE IN IONIC MILIEU AND ELECTRICAL STIMULATION ON THE IONIC MOVEMENTS IN SMOOTH MUSCLE. Tohoku J Exp Med. 1964 Mar 25;82:103–116. doi: 10.1620/tjem.82.103. [DOI] [PubMed] [Google Scholar]
  41. NAGASAWA J. THE EFFECTS OF TEMPERATURE AND SOME DRUGS ON THE IONIC MOVEMENTS IN THE SMOOTH MUSCLE OF GUINEA-PIG TAENIA COLI. Tohoku J Exp Med. 1963 Dec 25;81:222–237. doi: 10.1620/tjem.81.222. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. THOMPSON J. W. Studies on the responses of the isolated nictitating membrane of the cat. J Physiol. 1958 Apr 3;141(1):46–72. doi: 10.1113/jphysiol.1958.sp005954. [DOI] [PMC free article] [PubMed] [Google Scholar]

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