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. 1986 Mar;372:501–520. doi: 10.1113/jphysiol.1986.sp016022

Electrophysiology of smooth muscle of the small intestine of some mammals.

Y Hara, M Kubota, J H Szurszewski
PMCID: PMC1192776  PMID: 3723415

Abstract

Intracellular recordings were made from cells located in the longitudinal, inner and outer circular muscle layers of the dog, cat, rabbit, opossum and human small intestine. In whole-thickness preparations in all five species, longitudinal muscle cells generated slow waves and spikes. However, in isolated longitudinal muscle preparations, all cells tested were electrically silent. In whole-thickness and in isolated preparations, cells in the inner circular muscle layer generated spontaneous spikes superimposed on slow potentials. However, the occurrence of spikes and slow potentials was more regular in whole-thickness preparations. In whole-thickness preparations, cells in the outer circular muscle layer generated slow waves which were coupled with phasic contractions. However, in isolated outer circular muscle preparations, all cells tested were electrically silent and spontaneous phasic contractions were absent. In whole-thickness preparations, non-neural cells located on the serosal side of the outer circular muscle layer generated slow waves. The data suggest that spontaneous slow waves of the small intestine of the dog, cat, rabbit, opossum and human are generated in non-neural cells located between the longitudinal and outer circular muscle layer and by non-neural cells located between the outer and inner circular muscle layers.

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Selected References

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  1. Bolton T. B. On the nature of the oscillations of the membrane potential (slow waves) produced by acetylcholine or carbachol in intestinal smooth muscle. J Physiol. 1971 Jul;216(2):403–418. doi: 10.1113/jphysiol.1971.sp009532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bortoff A. Electrical transmission of slow waves from longitudinal to circular intestinal muscle. Am J Physiol. 1965 Dec;209(6):1254–1260. doi: 10.1152/ajplegacy.1965.209.6.1254. [DOI] [PubMed] [Google Scholar]
  3. Bortoff A., Michaels D., Mistretta P. Dominance of longitudinal muscle in propagation of intestinal slow waves. Am J Physiol. 1981 Mar;240(3):C135–C147. doi: 10.1152/ajpcell.1981.240.3.C135. [DOI] [PubMed] [Google Scholar]
  4. Bortoff A., Sachs F. Electrotonic spread of slow waves in circular muscle of small intestine. Am J Physiol. 1970 Feb;218(2):576–581. doi: 10.1152/ajplegacy.1970.218.2.576. [DOI] [PubMed] [Google Scholar]
  5. Cheung D. W., Daniel E. E. Comparative study of the smooth muscle layers of the rabbit duodenum. J Physiol. 1980 Dec;309:13–27. doi: 10.1113/jphysiol.1980.sp013490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Code C. F., Szurszewski J. H. The effect of duodenal and mid small bowel transection on the frequency gradient of the pacesetter potential in the canine small intestine. J Physiol. 1970 Apr;207(2):281–289. doi: 10.1113/jphysiol.1970.sp009061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Connor J. A., Kreulen D., Prosser C. L., Weigel R. Interaction between longitudinal and circular muscle in intestine of cat. J Physiol. 1977 Dec;273(3):665–689. doi: 10.1113/jphysiol.1977.sp012116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Connor J. A., Prosser C. L., Weems W. A. A study of pace-maker activity in intestinal smooth muscle. J Physiol. 1974 Aug;240(3):671–701. doi: 10.1113/jphysiol.1974.sp010629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. DANIEL E. E., HONOUR A. J., BOGOCH A. Electrical activity of the longitudinal muscle of dog small intestine studied in vivo using microelectrodes. Am J Physiol. 1960 Jan;198:113–118. doi: 10.1152/ajplegacy.1960.198.1.113. [DOI] [PubMed] [Google Scholar]
  10. Daniel E. E., Sarna S. The generation and conduction of activity in smooth muscle. Annu Rev Pharmacol Toxicol. 1978;18:145–166. doi: 10.1146/annurev.pa.18.040178.001045. [DOI] [PubMed] [Google Scholar]
  11. El-Sharkawy T. Y. Electrical activities of the muscle layers of the canine colon. J Physiol. 1983 Sep;342:67–83. doi: 10.1113/jphysiol.1983.sp014840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gabella G. Intercellular junctions between circular and longitudinal intestinal muscle layers. Z Zellforsch Mikrosk Anat. 1972;125(2):191–199. doi: 10.1007/BF00306788. [DOI] [PubMed] [Google Scholar]
  13. Gabella G. Special muscle cells and their innervation in the mammalian small intestine. Cell Tissue Res. 1974;153(1):63–77. doi: 10.1007/BF00225446. [DOI] [PubMed] [Google Scholar]
  14. Hara Y., Szurszewski J. H. Effect of potassium and acetylcholine on canine intestinal smooth muscle. J Physiol. 1986 Mar;372:521–537. doi: 10.1113/jphysiol.1986.sp016023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Henderson R. M., Duchon G., Daniel E. E. Cell contacts in duodenal smooth muscle layers. Am J Physiol. 1971 Aug;221(2):564–574. doi: 10.1152/ajplegacy.1971.221.2.564. [DOI] [PubMed] [Google Scholar]
  16. KAO C. Y., NISHIYAMA A. OVARIAN HORMONES AND RESTING POTENTIAL OF RABBIT UTERINE SMOOTH MUSCLE. Am J Physiol. 1964 Oct;207:793–799. doi: 10.1152/ajplegacy.1964.207.4.793. [DOI] [PubMed] [Google Scholar]
  17. Kitamura K. Comparative aspects of membrane properties and innervation of longitudinal and circular muscle layers of rabbit jejunum. Jpn J Physiol. 1978;28(5):583–601. doi: 10.2170/jjphysiol.28.583. [DOI] [PubMed] [Google Scholar]
  18. Kobayashi M., Nagai T., Prosser C. L. Electrical interaction between muscle layers of cat intestine. Am J Physiol. 1966 Dec;211(6):1281–1291. doi: 10.1152/ajplegacy.1966.211.6.1281. [DOI] [PubMed] [Google Scholar]
  19. Kobayashi M., Prosser C. L., Nagai T. Electrical properties of intestinal muscle as measured intracellularly and extracellularly. Am J Physiol. 1967 Jul;213(1):275–286. doi: 10.1152/ajplegacy.1967.213.1.275. [DOI] [PubMed] [Google Scholar]
  20. Kuriyama H., Osa T., Toida N. Electrophysiological study of the intestinal smooth muscle of the guinea-pig. J Physiol. 1967 Jul;191(2):239–255. doi: 10.1113/jphysiol.1967.sp008248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Li P. L. The intramural nervous system of the small intestine with special reference to the innervation of the inner subdivision of its circular muscle. J Anat. 1940 Apr;74(Pt 3):348–359. [PMC free article] [PubMed] [Google Scholar]
  22. Morgan K. G., Muir T. C., Szurszewski J. H. The electrical basis for contraction and relaxation in canine fundal smooth muscle. J Physiol. 1981 Feb;311:475–488. doi: 10.1113/jphysiol.1981.sp013599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Morgan K. G., Szurszewski J. H. Mechanisms of phasic and tonic actions of pentagastrin on canine gastric smooth muscle. J Physiol. 1980 Apr;301:229–242. doi: 10.1113/jphysiol.1980.sp013201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sanders K. M. Excitation-contraction coupling without Ca2+ action potentials in small intestine. Am J Physiol. 1983 May;244(5):C356–C361. doi: 10.1152/ajpcell.1983.244.5.C356. [DOI] [PubMed] [Google Scholar]
  25. Taylor A. B., Kreulen D., Prosser C. L. Electron microscopy of the connective tissues between longitudinal and circular muscle of small intestine of cat. Am J Anat. 1977 Nov;150(3):427–441. doi: 10.1002/aja.1001500305. [DOI] [PubMed] [Google Scholar]
  26. Thuneberg L. Interstitial cells of Cajal: intestinal pacemaker cells? Adv Anat Embryol Cell Biol. 1982;71:1–130. [PubMed] [Google Scholar]
  27. el-Sharkawy T. Y., Morgan K. G., Szurszewski J. H. Intracellular electrical activity of canine and human gastric smooth muscle. J Physiol. 1978 Jun;279:291–307. doi: 10.1113/jphysiol.1978.sp012345. [DOI] [PMC free article] [PubMed] [Google Scholar]

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