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Enteric neural modulation of slow-wave activity in cat colon

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Abstract

These studies test the hypothesis that the generation of colonic slow waves can be modulated by stimulation of intrinsic enteric nerves and attempt to identify a neurotransmitter that may be responsible for this change in slow-wave activity. Isolated segments from the mid-colon of the cat generated regular, continuous slow waves at 6.5±1.1 cpm. Activation of the intrinsic nerves by electrical field stimulation transiently reduced the rate of slow-wave generation to 4.7±0.7 cpm (P<0.001). The response to electrical stimulation was blocked by tetrodotoxin and α-chymotrypsin. The following antagonists were not effective in blocking the response: atropine, hexamethonium, phenoxybenzamine, propranolol, methysergide, naloxone, or imidazole. Vasoactive intestinal polypeptide (5×10−7 M) decreased slow wave frequency to 4.5±0.4 cpm. Vasoactive intestinal polypeptide (VIP) fragment 10-28 inhibited the effect of electrical field stimulation but also decreased the slow-wave frequency. VIP-immunoreactive nerves were much more abundant in the plexus submucosus extremus than in the circular muscle of the muscularis externa. Thus, pacemakers for colonic slow waves may be modulated by intrinsic colonic nerves, and vasoactive intestinal polypeptide may be the neurotransmitter responsible for this modulation.

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References

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

    Google Scholar 

  2. Sanders KM, Smith TK: Enteric neural regulation of slow waves in circular muscle of the canine proximal colon. J Physiol (London) 377:297–313, 1986

    Google Scholar 

  3. Sanders KM, Smith TK: Motoneurons of the submucous plexus regulate electrical activity of the circular muscle of canine proximal colon. J Physiol (London) 380:293–310, 1986

    Google Scholar 

  4. Smith TK, Reed JB, Sanders KM: Electrical pacemakers of canine proximal colon are functionally innervated by inhibitory motor neurons. Am J Physiol 256:C466-C477, 1989

    Google Scholar 

  5. Christensen J, Anuras S, Arthur C: Influence of intrinsic nerves on electromyogram of cat colonin vitro. Am J Physiol 234:E641-E647, 1978

    Google Scholar 

  6. Huizinga JD, Chang G, Diamant NE, El-Sharkaway TY: Electrophysiological basis of excitation of canine colonic circular muscle by cholinergic agents and substance P. J Pharmacol Exp Ther 231:692–699, 1980

    Google Scholar 

  7. Durdle NG, Kingma YJ, Bowes KL, Chambers MM: Origin of slow waves in the canine colon. Gastroenterology 84:375–382, 1983

    Google Scholar 

  8. Smith TK, Reed JB, Sanders KM: Origin and propagation of electrical slow waves in circular muscle of canine proximal colon. Am J Physiol 252:C215-C224, 1987

    Google Scholar 

  9. Du C, Conklin JL: Origin of slow waves in the isolated proximal colon of the rat. J Auton Nerv Syst 28:167–178, 1989

    Google Scholar 

  10. Barajas-Lopez C, Berezin I, Daniel EE, Huizinga JD: Pacemaker activity recorder in interstitial cells of Cajal of the gastrointestinal tract. Am J Physiol 257:C830-C835, 1989

    Google Scholar 

  11. Langton P, Ward SM, Carl A, Norell MA, Sanders KS: Spontaneous electrical activity of interstitial cells of Cajal isolated from canine proximal colon. Proc Natl Acad Sci USA 86:7280–7284, 1989

    Google Scholar 

  12. Christensen J, Rick GA: Intrinsic nerves in the mammalian colon: Confirmation of a novel plexus at the circular muscle-submucosal border. J Auton Nerv Syst 21:223–231, 1987

    Google Scholar 

  13. Faussone-Pellegrini M: Comparative study of interstitial cells of Cajal. Acta Anat 130:109–126, 1987

    Google Scholar 

  14. Stach W: Der plexus entericus extremus des Dickerdarmes und seine Beziehungen zu den interstitiellen zellen (Cajal). Z Mikrosk Anat Forsch 85:245–272, 1972

    Google Scholar 

  15. Berezin I, Huizinga JD, Daniel EE: Interstitial cells of Cajal in the canine colon: A special communication network at the inner border of the circular muscle. J Comp Neurol 273:42–51, 1988

    Google Scholar 

  16. Christensen J, Williams TW, Jew J, O'Dorisio TM: Distribution of vasoactive intestinal polypeptide-immunoreactive structures in the opossum esophagus. Gastroenterology 92:1007–1018, 1987

    Google Scholar 

  17. Jew J, Fountain N: An evaluation of procedures for ultrastructural immunocytochemistry. Anat Rec 211:92A, 1985

    Google Scholar 

  18. Hsu SM, Raine L, Fanger H: The use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577–580, 1981

    Google Scholar 

  19. Maillet M: Modification de la technique de Champy au tetraoxyde d'osmium-iodure de potassium. Resultats de son application d'etude des fibres nerveuses. CR Soc Biol 153:939–941, 1959

    Google Scholar 

  20. Schultzberg M, Hokfelt T, Nilsson G, Terenius L, Rehfeld JF, Brown M, Elde R, Goldstein M, Said S: Distribution of peptide- and catecholamine containing neurons in the gastrointestinal tract of rat and guinea-pig: Immunohistochemical studies with antisera to substance P, enkephalins, somatostatin, gastrin/cholecystokinin, neurotensin and dopamine B-hydroxylase. Neuroscience 5:689–744, 1980

    Google Scholar 

  21. Costa M, Furness JB, Buffa R, Said SI: Distribution of enteric nerve cell bodies and axons showing immunoreactivity for vasoactive intestinal polypeptide in the guinea-pig intestine. Neuroscience 5:587–596, 1980

    Google Scholar 

  22. Tange A: Distribution of peptide-containing endocrine cells and neurons in the gastrointestinal tract of the dog: Immunohistochemical studies using antisera to somatostatin, substance P, vasoactive intestinal polypeptide, met-enkephalin, and neurotensin. Biomed Res 4:9–24, 1983

    Google Scholar 

  23. Grider JR, Rivier J: Vasoactive intestinal peptide (VIP) as transmitter of inhibitory motor neurons of the gut: Evidence from the use of selective VIP antagonists and VIP antiserum. J Pharmacol Exp Ther 253:738, 1990

    Google Scholar 

  24. Gonda T, Daniel EE, McDonald TJ, Fox JET, Brooks BD, Oki M: Distribution and function of enteric GAL-IR nerves in dogs: Comparison with VIP. Am J Physiol 256:G884-G896, 1989

    Google Scholar 

  25. Belai A, Lincoln J, Burnstock G: Lack of release of vasoactive intestinal polypeptide and calcitonin gene-related peptide during electrical stimulation of enteric nerves in streptozotocin-diabetic rats. Gastroenterology 93:1034–1040, 1987

    Google Scholar 

  26. Chijiiwa Y, Misawa T, Idayashi H: Evidence of local mechanism involvement in vasoactive intestinal polypeptide release from canine small intestine. Gastroenterology 90:1877–1881, 1986

    Google Scholar 

  27. Edin R, Lundberg JM, Ahlman H, Dahlstrom A, Fahrenkrug J, Hokfelt T, Kewenter J: On the VIPergic innervation of the feline pylorus. Acta Physiol Scand 107:185–187, 1979

    Google Scholar 

  28. Eklund S, Fahrenkrug J, Jodal M, Lundgren O, Schaffalitzky De Muckadell OB, Sjoqvist A: Vasoactive intestinal polypeptide, 5-hydroxytryptamine and reflex hyperaemiain in the small intestine of the cat. J Physiol (London) 302:549–557, 1989

    Google Scholar 

  29. Gaginella TS, O'Dorisio TM, Hubel KA: Release of vasoactive intestinal polypeptide by electrical field stimulation of rabbit ileum. Regul Pept 2:165–174, 1981

    Google Scholar 

  30. Grider JR, Cable MB, Bitar HN, Said SI, Makhlouf GM: Vasoactive intestinal peptide: Relaxant neurotransmitter in taenia coli of the guinea pig. Gastroenterology 89:36–42, 1985

    Google Scholar 

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Authors and Affiliations

  1. Department of Internal Medicine, University of Iowa College of Medicine, 52242, Iowa City, Iowa

    Chuang Du PhD,  Jeffrey L. Conklin MD & Glenn Hammer MD

  2. Veterans Administration Medical Center, 52242, Iowa City, Iowa

    Chuang Du PhD,  Jeffrey L. Conklin MD & Glenn Hammer MD

Authors
  1. Chuang Du PhD
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  2. Jeffrey L. Conklin MD
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  3. Glenn Hammer MD
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Additional information

This work was supported by NIH grants DK 1750 and Digestive Diseases Core Center grant AM 34986 and a grant from the Veterans Administration.

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Du, C., Conklin, J.L. & Hammer, G. Enteric neural modulation of slow-wave activity in cat colon. Digest Dis Sci 36, 719–726 (1991). https://doi.org/10.1007/BF01311227

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  • DOI: https://doi.org/10.1007/BF01311227

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