The Enteric Nervous System pp 11-19

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 891) | Cite as

A Personal Perspective on the Development of Our Understanding of the Myogenic Control Mechanisms of Gut Motor Function

Chapter

Abstract

Myogenic control mechanisms play a role in all motor activities of the gut. Myogenic control systems are defined here as control systems that are intrinsic to the smooth muscle cells and/or interstitial cells of Cajal (ICC) and that can operate without an essential contribution of the intrinsic (ENS) and extrinsic nervous systems. In vivo however, the ENS and the myogenic control systems always work in cooperation. Although myogenic control plays a role in every gut organ, this review focuses on the peristaltic and segmentation activity of the small intestine. It provides some historical perspectives and some discussion on the development of our understanding of the cooperative nature of the myogenic and neurogenic control mechanisms. It highlights how some influential papers inadvertently provided hindrance to full understanding, it discusses how the guinea pig model has hampered acceptance of myogenic control systems and it provides some background into the genesis of our understanding of control mechanisms involving ICC.

References

  1. Alvarez WC (1914) Functional variations in contractions of different parts of the small intestine. Am J Physiol 35:177–193Google Scholar
  2. Alvarez WC (1922) The myogenic nature of the contractions. Am J Physiol 59:421–430Google Scholar
  3. Bayliss WM, Starling EH (1899) The movements and innervation of the small intestine. J Physiol 24:99–143CrossRefPubMedPubMedCentralGoogle Scholar
  4. Cannon WB (1902) The movements of the intestines studied by means of the Röntgen rays. J Med Res 7:72–75PubMedPubMedCentralGoogle Scholar
  5. Code CF, Szurszewski J, Keith AK, Smith IB (1968) A concept of control of gastrointestinal motility. In: Code CF (ed) Handbook of physiology: alimentary canal. American Physiological Society, Washington, DC, pp 2881–2896Google Scholar
  6. Costa M (2006) All together now: from pacemakers to gastric peristalsis. J Physiol 571:1CrossRefPubMedPubMedCentralGoogle Scholar
  7. Costa M, Brookes SH (2008) Architecture of enteric neural circuits involved in intestinal motility. Eur Rev Med Pharmacol Sci 12(Suppl 1):3–19PubMedGoogle Scholar
  8. Der-Silaphet T, Malysz J, Hagel S, Arsenault LA, Huizinga JD (1998) Interstitial cells of Cajal direct normal propulsive contractile activity in the mouse small intestine. Gastroenterology 114:724–736CrossRefPubMedGoogle Scholar
  9. Diamant NE, Bortoff A (1969) Nature of the intestinal slow-wave frequency gradient. Am J Physiol 216:301–307PubMedGoogle Scholar
  10. Donnelly G, Jackson TD, Ambrous K, Ye J, Safdar A, Farraway L, Huizinga JD (2001) The myogenic component in distention-induced peristalsis in the guinea pig small intestine. Am J Physiol Gastrointest Liver Physiol 280:G491–G500PubMedGoogle Scholar
  11. Ellis M, Chambers JD, Gwynne RM, Bornstein JC (2013) Serotonin (5-HT) and cholecystokinin (CCK) mediate nutrient induced segmentation in guinea pig small intestine. Am J Physiol Gastrointest Liver Physiol 304:G749–G761CrossRefPubMedGoogle Scholar
  12. Ferens D, Baell J, Lessene G, Smith JE, Furness JB (2007) Effects of modulators of Ca(2+)-activated, intermediate-conductance potassium channels on motility of the rat small intestine, in vivo. Neurogastroenterol Motil 19:383–389CrossRefPubMedGoogle Scholar
  13. Furness JB (2006) The enteric nervous system. Blackwell, Oxford, EnglandGoogle Scholar
  14. Gomez-Pinilla PJ, Gibbons SJ, Bardsley MR, Lorincz A, Pozo MJ, Pasricha PJ, Van de Rijn M, West RB, Sarr MG, Kendrick ML, Cima RR, Dozois EJ, Larson DW, Ordog T, Farrugia G (2009) Ano1 is a selective marker of interstitial cells of Cajal in the human and mouse gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol 296:G1370–G1381CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gwynne RM, Bornstein JC (2007) Mechanisms underlying nutrient-induced segmentation in isolated guinea pig small intestine. Am J Physiol Gastrointest Liver Physiol 292:G1162–G1172CrossRefPubMedGoogle Scholar
  16. Gwynne RM, Thomas EA, Goh SM, Sjovall H, Bornstein JC (2004) Segmentation induced by intraluminal fatty acid in isolated guinea-pig duodenum and jejunum. J Physiol 556:557–569CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hall KE, El-Sharkawy TY, Diamant NE (1982) Vagal control of migrating motor complex in the dog. Am J Physiol 243:G276–G284PubMedGoogle Scholar
  18. Huizinga JD, Chen JH (2014) The myogenic and neurogenic components of the rhythmic segmentation motor patterns of the intestine. Front Neurosci 8:78CrossRefPubMedPubMedCentralGoogle Scholar
  19. Huizinga JD, Thuneberg L, Kluppel M, Malysz J, Mikkelsen HB, Bernstein A (1995) W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 373:347–349CrossRefPubMedGoogle Scholar
  20. Huizinga JD, Berezin I, Sircar K, Hewlett B, Donnelly G, Bercik P, Ross C, Algoufi T, Fitzgerald P, Der T, Riddell RH, Collins SM, Jacobson K (2001) Development of interstitial cells of Cajal in a full-term infant without an enteric nervous system. Gastroenterology 120:561–567CrossRefPubMedGoogle Scholar
  21. Huizinga JD, Chen JH, Zhu YF, Pawelka A, McGinn RJ, Bardakjian BL, Parsons SP, Kunze WA, Wu RY, Bercik P, Khoshdel A, Chen S, Yin S, Zhang Q, Yu Y, Gao Q, Li K, Hu X, Zarate N, Collins P, Pistilli M, Ma J, Zhang R, Chen D (2014) The origin of segmentation motor activity in the intestine. Nat Commun 5:3326CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hwang SJ, Blair PJ, Britton FC, O’Driscoll KE, Hennig G, Bayguinov YR, Rock JR, Harfe BD, Sanders KM, Ward SM (2009) Expression of anoctamin 1/TMEM16A by interstitial cells of Cajal is fundamental for slow wave activity in gastrointestinal muscles. J Physiol 587:4887–4904CrossRefPubMedPubMedCentralGoogle Scholar
  23. Koh SD, Sanders KM, Ward SM (1998) Spontaneous electrical rhythmicity in cultured interstitial cells of Cajal from the murine small intestine. J Physiol 513:203–213CrossRefPubMedPubMedCentralGoogle Scholar
  24. Komuro T, Zhou DS (1996) Anti-c-kit protein immunoreactive cells corresponding to the interstitial cells of Cajal in the guinea-pig small intestine. J Auton Nerv Syst 61:169–174CrossRefPubMedGoogle Scholar
  25. Maeda H, Yamagata A, Nishikawa S, Yoshinaga K, Kobayashi S, Nishi K (1992) Requirement of c-kit for development of intestinal pacemaker system. Development 116:369–375PubMedGoogle Scholar
  26. Pawelka AJ, Huizinga JD (2015) Induction of rhythmic transient depolarizations associated with waxing and waning of slow wave activity in intestinal smooth muscle. Am J Physiol Gastrointest Liver Physiol 308:G427–33Google Scholar
  27. Perdue MH, Masson S, Wershil BK, Galli SJ (1991) Role of mast cells in ion transport abnormalities associated with intestinal anaphylaxis. Correction of the diminished secretory response in genetically mast cell-deficient W/Wv mice by bone marrow transplantation. J Clin Invest 87:687–693CrossRefPubMedPubMedCentralGoogle Scholar
  28. Smith TK (1989) Spontaneous junction potentials and slow waves in the circular muscle of isolated segments of guinea-pig ileum. J Auton Nerv Syst 27:147–154CrossRefPubMedGoogle Scholar
  29. Suzuki N, Prosser CL, DeVos W (1986) Waxing and waning of slow waves in intestinal musculature. Am J Physiol 250:G28–G34PubMedGoogle Scholar
  30. Thomsen L, Robinson TL, Lee JC, Farraway LA, Hughes MJ, Andrews DW, Huizinga JD (1998) Interstitial cells of Cajal generate a rhythmic pacemaker current. Nat Med 4:848–851CrossRefPubMedGoogle Scholar
  31. Tort AB, Komorowski R, Eichenbaum H, Kopell N (2010) Measuring phase–amplitude coupling between neuronal oscillations of different frequencies. J Neurophysiol 104:1195–1210CrossRefPubMedPubMedCentralGoogle Scholar
  32. Trendelenburg P (2006) Physiological and pharmacological investigations of small intestinal peristalsis. Translation of the article “Physiologische und pharmakologische Versuche uber die Dunndarmperistaltik”, Arch. Exp. Pathol. Pharmakol. 81, 55–129, 1917. Naunyn Schmiedebergs Arch Pharmacol 373:101–133Google Scholar
  33. Ward SM, Burns AJ, Torihashi S, Sanders KM (1994) Mutation of the proto-oncogene c-kit blocks development of interstitial cells and electrical rhythmicity in murine intestine. J Physiol 480:91–97Google Scholar
  34. Wright GW, Parsons SP, Huizinga JD (2012) Ca(2+) sensitivity of the maxi chloride channel in interstitial cells of Cajal. Neurogastroenterol Motil 24:e221–e234CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of MedicineFarncombe Family Digestive Health Research Institute, McMaster UniversityHamiltonCanada

Personalised recommendations