Skip to main content
Log in

Control of human colonic motor function

  • Review Article
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Human colonic motility is governed by control mechanisms involving the electrical activity of the smooth muscle cell membranes, the intrinsic and extrinsic nervous activity, and hormonal action. The structural bases for neural and myogenic control have not been demonstrated. However gap junctions are lacking between muscle cells, and nerves are not close to smooth muscle cells. The myogenic control, as observedin vitro, is described and compared with results obtained from differentin vivo techniques.In vitro andin vivo measurements are critically evaluated, and a reconciliation between them attempted. No appropriate animal model is available to help resolve different findings and interpretations. Neural control of colon motility is exerted probably through modulation of myogenic activity as well as directly. The activities of extrinsic nerves, intrinsic motor nerves and afferent nerves are integrated within the colon, at prevertebral ganglia and in the spinal cord in animals, but similar data are not available for the human. There is a lack of studies directly relating transit to motility and conventional beliefs need reexamination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Daniel EE: Symposium on colonic function: Electrophysiology of the colon. Gut 16:298–306, 1975

    Google Scholar 

  2. Fraser ID, Condon RE, Schulte WJ, DeCosse JJ, Cowles VE: Longitudinal muscle of muscularis externa in human and nonhuman primate colon. Arch Surg 116:61–63, 1981

    Google Scholar 

  3. Daniel EE, Bowes K, Duchon G: The structural basis for control of gastrointestinal motility in man.In Proceedings of the 5th International Symposium on Gastrointestinal Motility. G Vantrappen (ed). Herentals, Belgium, Typoff-Press, 1975, pp 142–151

    Google Scholar 

  4. Oki M, Daniel EE: Ultrastructural basis for electrical coupling in the dog stomach.In Proceedings of the 4th International Symposium on Gastrointestinal Motility. EE Daniel (ed). Vancouver, Canada, Mitchell Press, 1974, pp 85–95

    Google Scholar 

  5. Henderson RM, Duchon G, Daniell EE: Cell controls in duodenal smooth muscle layers. Am J Physiol 221:564–574, 1971

    Google Scholar 

  6. Gabella G: Intracellular junctions between circular and longitudinal intestinal muscle layers. Z Zellforsch 125: 191–199, 1972

    Google Scholar 

  7. Kannan MS, Jager LP, Daniel EE: Electrical properties of the smooth muscle cell membrane of opossum esophagus. Am J Physiol 248:G342-G346, 1985

    Google Scholar 

  8. Cheung DW, Daniel EE: Comparative study of the smooth muscle layers of the rabbit duodenum. J Physiol 309:13–27, 1980

    Google Scholar 

  9. Daniel EE, Sarna SK: The generation and conduction of activity in smooth muscle. Annu Rev Pharmacol Toxicol 18:145–166, 1978

    Google Scholar 

  10. Gabella G: Structure of the Autonomic Nervous System. London, Chapman & Hall, 1976

    Google Scholar 

  11. Abe Y, Tomita J: Cable properties of smooth muscle. J Physiol (London) 196:87–100, 1968

    Google Scholar 

  12. Fry GN, Devine CE, Burnstock G: Freeze fracture studies of nexuses between smooth muscle cells: Close relationship to sarcoplasmic reticulum. J Cell Biol 72:26–36, 1977

    Google Scholar 

  13. Daniel EE, Daniel VP, Duchon G, Garfield RE, Nichols M, Malhotra SK, Oki M: Is the nexus necessary for cell-to-cell coupling in smooth muscle? J Membr Biol 28:207–239, 1976

    Google Scholar 

  14. Sperelakis N: The possibility of propagation between myocardial cells not connected by low resistance pathways. Adv Exp Med Biol 161:1–23, 1983

    Google Scholar 

  15. Taylor AB, Kreulen D, Prosser CL: Electron microscopy of the connective tissues between longitudinal and circular muscle of small intestine. Am J Anat 150:427–442, 1977

    Google Scholar 

  16. Elden L, Bortoff A: Electrical coupling of longitudinal and circular intestinal muscle. Am J Physiol 246:G618-G626, 1984

    Google Scholar 

  17. Bortoff A: Electrical transmission of slow waves from longitudinal to circular intestinal muscle. Am J Physiol 209:1254–1260, 1965

    Google Scholar 

  18. Thuneberg L: Interstitial cells of Cajal: intestinal pacemaker cells? Adv Anat Embryol Cell Biol 71:1–130, 1982

    Google Scholar 

  19. Thuneberg L, Rumessen JJ, Mikkelsen HB: Interstitial cells of Cajal—an intestinal impulse generation and conduction system? Scand J Gastroenterol (Suppl) 71:143–144, 1982

    Google Scholar 

  20. Huizinga JD, Stern H, Chow E, Diamant NE, El-Sharkawy TY: Electrophysiological control of motility in the human colon. Gastroenterology 88:500–511, 1985

    Google Scholar 

  21. Burnstock G: Neurotransmitters and trophic factors in the autonomic nervous system. J Physiol (London) 313:1–35, 1981

    Google Scholar 

  22. Daniel EE, Posey-Daniel V: Neuromuscular structures in opossum esophagus: Role of interstitial cells of Cajal. Am J Physiol 246:G305–315, 1984

    Google Scholar 

  23. Jones TR, Kannan MS, Daniel EE: Ultrastructural study of guinea pig tracheal smooth muscle and its innervation. Can J Physiol Pharmacol 58:1102–1113, 1980

    Google Scholar 

  24. Daniel EE, Taylor GS, Daniel VP, Holman ME: Can nonadrenergic inhibitory varicosities be identified structurally? Can J Physiol Pharmacol 55:243–250, 1977

    Google Scholar 

  25. Gannon BJ, Noblet HR, Burnstock G: Adrenergic innervation of bowel in Hirschsprung's disease. Br Med J 3:338–340, 1969

    Google Scholar 

  26. Garrett JR, Howard ER: Electron microscopy of myenteric nerves in Hirshsprung's disease and in normal bowel. Gut 11:1007–1014, 1970

    Google Scholar 

  27. Burnstock G: Do some sympathetic neurones release both nonadrenaline and acetylcholine. Prog Neurobiol 11:205–222 1978

    Google Scholar 

  28. Barajas L, Wang P: Demonstration of acetylcholinesterase in the adrenergic nerves of the renal glomerular arterioles. J Ultrastruct Res 53:244–253, 1975

    Google Scholar 

  29. Barajas L, Wang P: Simultaneous ultrastructural visualization of acetylcholinesterase activity and tritiated norepinephrine uptake in renal nerves. Anat Rec 205:185–195, 1983

    Google Scholar 

  30. Norberg KA: Adrenergic innervation of the intestinal wall by fluorescence microscopy. Int J Neuropharmacol 3:379–382, 1967

    Google Scholar 

  31. Rostad H: Colonic motility in the cat. II Extrinsic nervous control. Acta Physiol Scand 89:91–103, 1973

    Google Scholar 

  32. Tranzer JP, Thoenen H: Significance of “empty vesicles” in postganglionic sympathetic nerve lumen. Experientia 23: 123–124, 1967

    Google Scholar 

  33. Tranzer JP, Thoenen H: Electron microscopic licalization of 5-hydroxydopamine (3,4,5-trihydroxyphenylethylamine) a new “false” sympathetic transmitter. Experientia 23:743–745, 1967

    Google Scholar 

  34. Gibbins IL: Lack of correlation between ultrastructural and pharmacological types of nonadrenergic autonomic nerves. Cell Tissue Res 221:551–581, 1982

    Google Scholar 

  35. Llewellyn-Smith IJ, Furness JB, Murphy R, O'Brien PE, Costa M: Substance P-containing nerves in the human small intestine. Distribution, ultrastructure, and characterization of the immunoreactive peptides. Gastroenterology86:421–435, 1984

    Google Scholar 

  36. Larsson LI: Ultrastructural localization of a new neuronal peptide (VIP). Histochemistry 54:173–176, 1977

    Google Scholar 

  37. Costa M, Furness JB: Neuronal peptides in the gut. Br Med Bull 38:247–252, 1982

    Google Scholar 

  38. Rumessen JJ, Thuneberg L, Mikkelsen HB: Plexus muscularis profundus and associated interstitial cells. II. Ultrastructural studies of mouse small intestine. Anat Rec 203:129–146, 1982

    Google Scholar 

  39. Komuro J: The interstitial cells in the colon of the rabbit. Scanning and transmission electron microscopy. Cell Tissue Res 222:41–51, 1982

    Google Scholar 

  40. Duthie HL, Kirk D: Electrical activity of human colonic smooth musclein vitro. J Physiol (London) 283:319–330, 1978

    Google Scholar 

  41. Van Merwyk AJ, Duthie HL: Characteristics of human colonic smooth muscle in vitro.In Gastrointestinal Motility J Christensen (ed). New York, Raven Press, 1979, pp 473–478

    Google Scholar 

  42. Kubota M, Ito Y, Ikeda K: Membrane properties and innervation of smooth muscle cells in Hirschsprung's disease. Am J Physiol 244:G406–415, 1983

    Google Scholar 

  43. Chambers MM, Bowes KL, Kingma YL, Bannister C, Cote KR:In vitro electrical activity in human colon. Gastroenterology 81:502–508, 1981

    Google Scholar 

  44. Huizinga JD, Stern HS, Chow E, Diamant NE, El-Sharkawy TY: Electrical basis of excitation and inhibition of human colonic smooth muscle. Gastroenterology, 1986, in press

  45. Huizinga JD, Diamant NE, El-Sharkawy, TY: Electrical basis of contractions in the muscle layers of the pig colon. Am J Physiol 245:G482-G491, 1983

    Google Scholar 

  46. El-Sharkawy TY: Electrical activities of the muscle layers of the canine colon. J Physiol (London) 342:67–83, 1983

    Google Scholar 

  47. Daniel EE, Huizinga JD: Physiology of colonic motility.In Small Intestinal and Colonic Motility. P Poitras (ed). Montreal, Jouveinal Laboratories, 1985, pp 69–84

    Google Scholar 

  48. Sarna SK, Bardakjian BL, Waterfall WE, Lind JF: Human colonic electrical control activity (ECA). Gastroenterology 78:1526–1536, 1980

    Google Scholar 

  49. Sarna S, Latimer P, Campbell D, Waterfall WE: Electrical and contractile activities of the human rectosigmoid. Gut 23:698–705, 1982

    Google Scholar 

  50. Sarna SK, Waterfall WE, Bardakjian BL, Lind JF: Tupes of human colonic electrical activity recorded postoperatively. Gastroenterology 81:61–70, 1981

    Google Scholar 

  51. Snape WJ, Carlson GM, Cohen S: Colonic myelectric activity in the irritable bowel syndrome. Gastroenterology 70:326–330, 1976

    Google Scholar 

  52. Snape WJ Jr, Carlson GM, Matarazzo SA, Cohen S: Evidence that abnormal myoelectric activity produces colonic dysfunction in the irritable bowel syndrome. Gastroenterology 72:383–387, 1977

    Google Scholar 

  53. Taylor I, Duthie HL, Smallwood R, Linkens D: Large bowel myoelectrical activity in man. Gut 19:808–814, 1975

    Google Scholar 

  54. Snape WJ, Carlson GM, Cohen S: Human colonic myoelectric activity in response to prostigmine and the gastrointestinal hormones. Am J Dig Dis 22:881–887, 1977

    Google Scholar 

  55. Frieri G, Parisi F, Corazziari E, Caprilli R:Colonic electromyography in chronic constipation. Gastroenterology 84:737–740, 1983

    Google Scholar 

  56. Latimer P, Sarna S, Campbell D, Latimer M, Waterfall W, Daniel EE: Colonic motor and myoelectrical activity: A comparative study of normal subjects, psychoneurotic patients, and patients with irritable bowel syndrome. Gastroenterology 80:893–901, 1981

    Google Scholar 

  57. Altaparmakov I, Wienbeck M: Local inhibition of myoelectrical activity of human colon by loperamide. Dig Dis Sci 29:232–238, 1984

    Google Scholar 

  58. Taylor I, Duthie HL, Smallwood R, Brown BH, Linkens D: The effect of stimulation on the myoelectrical activity of the rectosigmoid in man. Gut 15:599–607, 1974

    Google Scholar 

  59. Provenzale L, Pisano M: Methods for recording electrical activity of the human colonin vivo. Am J Dig Dis 16:712–722, 1971

    Google Scholar 

  60. Snape WJ Jr, Matarazzo SA, Cohen S: Abnormal gastrocolonic response in patients with ulcerative colitis. Gut 21:392–396, 1980

    Google Scholar 

  61. Wienbeck M: The electrical activity of the cat colonin vivo. II. The effects of bethanechol and morphine. Res Exp Med 158:280–287, 1972

    Google Scholar 

  62. El-Sharkawy TY, Bardakjian BL, MacDonald WM, Diamant NE: Origins of the multiple patterns of electrical control activity in the colon.In Motility of the Digestive Tract. M Wienbeck (ed). New York, Raven Press, 1982, pp 491–497

    Google Scholar 

  63. Kocylowski M, Bowes KL, Kingma YL: Electrical and mechanical activity in theex vivo perfused total canine colon. Gastroenterology 77:1021–1026, 1979

    Google Scholar 

  64. Fioramonti J, Bueno L, Sarna SK, Ruckebusch Y: Origin of high slow wave frequency in the dog colon. Reprod Nutr Dev 20:983–990, 1982

    Google Scholar 

  65. Brown BH, Smallwood RH, Duthie HL, Stoddard CJ: Intestinal smooth muscle electrical potentials recorded from surface electrodes. Med Biol Eng 13:97–103, 1975

    Google Scholar 

  66. Volkers ACW, Van der Schee EJ, Grashuis JL: Electrogastrography in the dog: Waveform analysis by a coherent averaging technique. Med Biol Eng Comp 4:56–64, 1983

    Google Scholar 

  67. Christensen J, Caprilli R, Lund GF: Electrical slow waves in circular muscle of cat colon. Am J Physiol 217:771–776, 1969

    Google Scholar 

  68. Huizinga JD, Chang G, Diamant NE, El-Sharkawy TY: The electrophysiological basis of excitation of canine colonic circular muscle by cholinergic agents and substance P. Am J Pharm Exp Ther 231:692–699, 1984

    Google Scholar 

  69. Huizinga JD, Chang G, Diamant NE, El-Sharkawy TY: The effects of cholecystokinin-octapeptide and pentagastrin on the electrical and motor activities of canine colonic circular muscle. Can J Physiol Pharmacol 62:1440–1447, 1984

    Google Scholar 

  70. Bueno L, Fioramonti J, Ruckebusch Y, Frexinos J, Coulom P: Evaluation of colonic myoelectrical activity in health and functional disorders. Gut 21:480–485, 1980

    Google Scholar 

  71. Schang JC, Devroede G: Fasting and postprandial myoelectric spiking activity in the human sigmoid. Gastroenterology 85:1048–1053, 1983

    Google Scholar 

  72. Sunshine A, Ouyang R, Baker PL, Reynolds J, Cohen S: Colonic slow wave analysis: Limitations of the Fast Fourier Transform (FFT). Dig Dis Sci 30:797, 1985

    Google Scholar 

  73. Waterfall WE, Shannon S: Human colonic electrical activity: Transverse and human colons. Clin Invest Med 8:A104, 1985

    Google Scholar 

  74. Huizinga JD, Stern HS, Waterfall WE, El-Sharkawy TY, Diamant NE: Electrical activities apparently propagating in the circular muscle layer of the human colon. Dig Dis Sci 30:773, 1985

    Google Scholar 

  75. Hulten L: Extrinsic nervous control of colonic motility and blood flow. An experimental study in the cat. Acta Physiol Scand Suppl 335:1, 1969

    Google Scholar 

  76. Daniel EE: Pharmacology of the gastrointestinal tract.In Handbook of Physiology: Alimentary Canal, Vol IV. CF Code (ed). Am Phys Soc, Washington, 1968, pp 2267–2324

    Google Scholar 

  77. Fasth S, Hulten L, Nordgren S: Evidence for a dual pelvic nerve influence on large bowel motility in the cat. J Physiol (London) 298:159–169, 1980

    Google Scholar 

  78. Daniel EE: Pharmacology of adrenergic, cholinergic and drugs acting on other receptors in gastrointestinal muscle.In Hand Exp Pharmacol. G Bertaccini (ed). Berlin, Springer Verlag, 59:249–322, 1982

    Google Scholar 

  79. Fulgraff G, Schmidt L, Azokwu P: Uber die atropinresistente neuromuskulare ubertragung am pelvicuscolon-praeparat der katze. Arch Int Pharmacodyn 149:537–551, 1964

    Google Scholar 

  80. Goldenberg MM, Burns RN: Effect of atropine on parasympathetic responses of the gastrointestinal tract of the dog. Arch Int Pharmacodyn 1974:342–349, 1968

    Google Scholar 

  81. Fulgraff G, Schmidt L: Untersuchungen uber die atropinresistente Ubertragung am Pelvicus-Colon-Praparat der katze in vitro. Arch Int Pharmacodyn Ther 149:552–559, 1964

    Google Scholar 

  82. Jule Y: Nerve-mediated descending inhibition in the proximal colon of the rabbit. J Physiol (London) 309:487–498, 1980

    Google Scholar 

  83. Daniel EE: Nonadrenergic, noncholinergic (NANC) neuronal inhibitory interactions with smooth muscle.In Calcium and contractility. AK Grover, EE Daniel (ed). The Humana Press, Clifton, NJ,1985, pp 427–455

    Google Scholar 

  84. Bertaccini G: Gastrointestinal hormones.In Mediators and Drugs in Gastrointestinal Motility. Vol II. G Bertaccini (ed). Berlin, Springer-Verlag, 1982, pp 11

    Google Scholar 

  85. Rostad H: Colonic motility in the cat. IV. Peripheral pathways mediating the effects induced by hypothalamic and mesencephalic stimulation. Acta Physiol Scand 89:154–68, 1973

    Google Scholar 

  86. Rostad HV: Influence of telencephalic stimulation and the peripheral pathways mediating the effects. Acta Physiol Scand 89:169–181, 1973

    Google Scholar 

  87. Oscasson O: On the functional organization of the two presynaptic systems to the colonic nerve neurons of the inferior mesenteric ganglion in the cat. Acta Physiol Scand 35:153–166, 1955

    Google Scholar 

  88. Crowsroft PJ, Holman ME, Szurszewski JH: Excitory input from the distal colon to the inferior mesenteric ganglion in the guinea pig. J Physiol (London) 219:443–461, 1971

    Google Scholar 

  89. Szurszewski JH, Weems WA: A study of peripheral input to and its control by postganglionic neurones of the inferior mesenteric ganglion. J Physiol (London) 256:541–556, 1976

    Google Scholar 

  90. Weems WA, Szurszewski JH: Modulation of colonic motility by peripheral neural inputs to neurons of the inferior mesenteric ganglia. Gastroenterology 73:273–278, 1977

    Google Scholar 

  91. Kuntz A, Saccomanno G: Reflex inhibition of intestinal motility mediated through decentralized prevertebral ganglia. J Neurophysiol 1:163–170, 1944

    Google Scholar 

  92. Matthews MR, Cuello AC: Substances P-immunoreactive peripheral branches of sensory neurons innervate guinea pig sympathetic neurons. Proc Natl Acad Sci USA 79:1668–1672, 1982

    Google Scholar 

  93. Dun NJ, Minota S: Effects of substance P on neurons of the inferior mesenteric ganglion of the guinea pig. J Physiol (London) 321:259–271, 1981

    Google Scholar 

  94. DeGroat WC, Krier J: The sacral parasympathetic reflex pathway regulating colonic motility and defecation in the cat. J Physiol (London) 276:481–500, 1978

    Google Scholar 

  95. Krier J, Hartman DA: Electrical properties and sympathetic connections to neurons in parasympathetic colonic ganglia of the cat. Am J Physiol 247:G52-G61, 1984

    Google Scholar 

  96. Chaudhary NA, Truelove SC: Human colonic motility: A comparative study of normal subjects, patients with ulcerative colitis, and patients with the irritable colon syndrome. I. Resting patterns of motility. Gastroenterology 40:1–17, 1961

    Google Scholar 

  97. Chaudhary NA, Truelove SC: Human colonic motility: A comparative study of normal subjects, patients with ulcerative colitis, and patients with the irritable colon syndrome. II. The effect of prostigmin. Gastroenterology 40:18–26, 1961

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huizinga, J.D., Daniel, E.E. Control of human colonic motor function. Digest Dis Sci 31, 865–877 (1986). https://doi.org/10.1007/BF01296057

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01296057

Keywords

Navigation