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. 1997 Oct 15;504(Pt 2):479–488. doi: 10.1111/j.1469-7793.1997.479be.x

Characterization of vagal pathways mediating gastric accommodation reflex in rats.

T Takahashi 1, C Owyang 1
PMCID: PMC1159925  PMID: 9365919

Abstract

1. We investigated the vagal pathways mediating the gastric accommodation reflex in the rat stomach. 2. Gastric distension (6 ml) evoked an increase of 9.0 +/- 1.0 cmH2O of intragastric pressure in vivo. Pretreatment with tetrodotoxin (TTX) caused a significant pressure increase by gastric distension, reaching 17.0 +/- 1.7 cmH2O, suggesting mediation by neural pathways. 3. The pressure increase evoked by gastric distension was significantly enhanced in vivo by acute truncal vagotomy (TV), hexamethonium (C6), and NG-nitro-L-arginine methyl ester (L-NAME), but not by vasoactive intestinal polypeptide (VIP) antiserum, guanethidine, or splanchnicotomy. 4. Gastric distension (6 ml) evoked a much larger intragastric pressure in the denervated, vascularly isolated, perfused rat stomach in vitro. Intra-arterial application of TTX and L-NAME did not cause further pressure increases evoked by gastric distension. 5. The pressure increase evoked by gastric distension remained high 2 weeks after TV in vivo. However, the accommodation reflex was fully restored 4 weeks after TV in vivo. This reflex was antagonized by TTX, C6 and L-NAME, but not by VIP antiserum, guanethidine and splanchnicotomy. 6. Similar to in vivo studies, gastric distension caused a smaller increase in intragastric pressure in response to gastric distension in the denervated, vascularly isolated, perfused stomach obtained from rats 4 weeks after vagotomies in vitro. The pressure increase evoked by gastric distension was significantly enhanced by L-NAME, hexamethonium and TTX. 7. It is suggested that the vago-vagal reflex plays an important role in mediating the accommodation reflex. This involves a vagal efferent pathway that uses nitric oxide as a final neurotransmitter mediating gastric relaxation in intact rats. It is also suggested that the adaptive mechanism mediating the accommodation reflex following vagotomy occurs in the gastric myenteric plexus.

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Selected References

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  1. Abrahamsson H., Jansson G. Elicitation of reflex vagal relaxation of the stomach from pharynx and esophagus in the cat. Acta Physiol Scand. 1969 Sep-Oct;77(1):172–178. doi: 10.1111/j.1748-1716.1969.tb04561.x. [DOI] [PubMed] [Google Scholar]
  2. Agoston D. V., Conlon J. M., Whittaker V. P. Selective depletion of the acetylcholine and vasoactive intestinal polypeptide of the guinea-pig myenteric plexus by differential mobilization of distinct transmitter pools. Exp Brain Res. 1988;72(3):535–542. doi: 10.1007/BF00250599. [DOI] [PubMed] [Google Scholar]
  3. Aimi Y., Kimura H., Kinoshita T., Minami Y., Fujimura M., Vincent S. R. Histochemical localization of nitric oxide synthase in rat enteric nervous system. Neuroscience. 1993 Mar;53(2):553–560. doi: 10.1016/0306-4522(93)90220-a. [DOI] [PubMed] [Google Scholar]
  4. Andrews P. L., Grundy D., Lawes I. N. The role of the vagus and splanchnic nerves in the regulation of intragastric pressure in the ferret. J Physiol. 1980 Oct;307:401–411. doi: 10.1113/jphysiol.1980.sp013442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boeckxstaens G. E., Pelckmans P. A., Bogers J. J., Bult H., De Man J. G., Oosterbosch L., Herman A. G., Van Maercke Y. M. Release of nitric oxide upon stimulation of nonadrenergic noncholinergic nerves in the rat gastric fundus. J Pharmacol Exp Ther. 1991 Feb;256(2):441–447. [PubMed] [Google Scholar]
  6. Bojö L., Lefebvre R. A., Nellgård P., Cassuto J. Involvement of vasoactive intestinal polypeptide in gastric reflex relaxation. Eur J Pharmacol. 1993 Jun 4;236(3):443–448. doi: 10.1016/0014-2999(93)90483-x. [DOI] [PubMed] [Google Scholar]
  7. Bredt D. S., Hwang P. M., Snyder S. H. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature. 1990 Oct 25;347(6295):768–770. doi: 10.1038/347768a0. [DOI] [PubMed] [Google Scholar]
  8. Bult H., Boeckxstaens G. E., Pelckmans P. A., Jordaens F. H., Van Maercke Y. M., Herman A. G. Nitric oxide as an inhibitory non-adrenergic non-cholinergic neurotransmitter. Nature. 1990 May 24;345(6273):346–347. doi: 10.1038/345346a0. [DOI] [PubMed] [Google Scholar]
  9. Crist J. R., He X. D., Goyal R. K. Both ATP and the peptide VIP are inhibitory neurotransmitters in guinea-pig ileum circular muscle. J Physiol. 1992 Feb;447:119–131. doi: 10.1113/jphysiol.1992.sp018994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. D'Amato M., Currò D., Montuschi P. Evidence for dual components in the non-adrenergic non-cholinergic relaxation in the rat gastric fundus: role of endogenous nitric oxide and vasoactive intestinal polypeptide. J Auton Nerv Syst. 1992 Mar;37(3):175–186. doi: 10.1016/0165-1838(92)90039-j. [DOI] [PubMed] [Google Scholar]
  11. D'Amato M., De Beurme F. A., Lefebvre R. A. Comparison of the effect of vasoactive intestinal polypeptide and non-adrenergic non-cholinergic neurone stimulation in the cat gastric fundus. Eur J Pharmacol. 1988 Jul 26;152(1-2):71–82. doi: 10.1016/0014-2999(88)90837-0. [DOI] [PubMed] [Google Scholar]
  12. Desai K. M., Sessa W. C., Vane J. R. Involvement of nitric oxide in the reflex relaxation of the stomach to accommodate food or fluid. Nature. 1991 Jun 6;351(6326):477–479. doi: 10.1038/351477a0. [DOI] [PubMed] [Google Scholar]
  13. Grundy D., Gharib-Naseri M. K., Hutson D. Effect of immunisation against vasoactive intestinal polypeptide on gastric corpus tone and motility in the ferret. Gut. 1992 Nov;33(11):1473–1476. doi: 10.1136/gut.33.11.1473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grundy D., Gharib-Naseri M. K., Hutson D. Plasticity in the gastric inhibitory innervation after immunization against VIP and vagotomy in the ferret. Am J Physiol. 1993 Sep;265(3 Pt 1):G432–G439. doi: 10.1152/ajpgi.1993.265.3.G432. [DOI] [PubMed] [Google Scholar]
  15. Hartley M. N., Mackie C. R. Gastric adaptive relaxation and symptoms after vagotomy. Br J Surg. 1991 Jan;78(1):24–27. doi: 10.1002/bjs.1800780109. [DOI] [PubMed] [Google Scholar]
  16. Jahnberg T., Abrahamsson H., Jansson G., Martinson J. Vagal gastric relaxation in the dog. Scand J Gastroenterol. 1977;12(2):221–224. doi: 10.1203/00006450-199404000-00022. [DOI] [PubMed] [Google Scholar]
  17. Keef K. D., Du C., Ward S. M., McGregor B., Sanders K. M. Enteric inhibitory neural regulation of human colonic circular muscle: role of nitric oxide. Gastroenterology. 1993 Oct;105(4):1009–1016. doi: 10.1016/0016-5085(93)90943-7. [DOI] [PubMed] [Google Scholar]
  18. Kreulen D. L., Muir T. C., Szurszewski J. H. Peripheral sympathetic pathways to gastroduodenal region of the guinea pig. Am J Physiol. 1983 Sep;245(3):G369–G375. doi: 10.1152/ajpgi.1983.245.3.G369. [DOI] [PubMed] [Google Scholar]
  19. Larsson L. I., Fahrenkrug J., Schaffalitzky De Muckadell O., Sundler F., Håkanson R., Rehfeld J. R. Localization of vasoactive intestinal polypeptide (VIP) to central and peripheral neurons. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3197–3200. doi: 10.1073/pnas.73.9.3197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lefebvre R. A., De Vriese A., Smits G. J. Influence of vasoactive intestinal polypeptide and NG-nitro-L-arginine methyl ester on cholinergic neurotransmission in the rat gastric fundus. Eur J Pharmacol. 1992 Oct 20;221(2-3):235–242. doi: 10.1016/0014-2999(92)90707-b. [DOI] [PubMed] [Google Scholar]
  21. Li Y., Owyang C. Pancreatic secretion evoked by cholecystokinin and non-cholecystokinin-dependent duodenal stimuli via vagal afferent fibres in the rat. J Physiol. 1996 Aug 1;494(Pt 3):773–782. doi: 10.1113/jphysiol.1996.sp021531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Li Y., Owyang C. Vagal afferent pathway mediates physiological action of cholecystokinin on pancreatic enzyme secretion. J Clin Invest. 1993 Jul;92(1):418–424. doi: 10.1172/JCI116583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Osthaus L. E., Galligan J. J. Antagonists of nitric oxide synthesis inhibit nerve-mediated relaxations of longitudinal muscle in guinea pig ileum. J Pharmacol Exp Ther. 1992 Jan;260(1):140–145. [PubMed] [Google Scholar]
  24. Price L. M., El-Sharkawy T. Y., Mui H. Y., Diamant N. E. Effect of bilateral cervical vagotomy on balloon-induced lower esophageal sphincter relaxation in the dog. Gastroenterology. 1979 Aug;77(2):324–329. [PubMed] [Google Scholar]
  25. Raybould H. E., Roberts M. E., Dockray G. J. Reflex decreases in intragastric pressure in response to cholecystokinin in rats. Am J Physiol. 1987 Aug;253(2 Pt 1):G165–G170. doi: 10.1152/ajpgi.1987.253.2.G165. [DOI] [PubMed] [Google Scholar]
  26. Raybould H. E., Taché Y. Cholecystokinin inhibits gastric motility and emptying via a capsaicin-sensitive vagal pathway in rats. Am J Physiol. 1988 Aug;255(2 Pt 1):G242–G246. doi: 10.1152/ajpgi.1988.255.2.G242. [DOI] [PubMed] [Google Scholar]
  27. Reid A. M., Shulkes A., Titchen D. A. Effects of the vagus nerves on gastric motility and release of vasoactive intestinal polypeptide in the anaesthetized lamb. J Physiol. 1988 Feb;396:11–24. doi: 10.1113/jphysiol.1988.sp016946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shimamura K., Fujisawa A., Toda N., Sunano S. Effects of NG-nitro-L-arginine on electrical and mechanical responses to stimulation of non-adrenergic, non-cholinergic inhibitory nerves in circular muscle of the rat gastric fundus. Eur J Pharmacol. 1993 Jan 26;231(1):103–109. doi: 10.1016/0014-2999(93)90690-j. [DOI] [PubMed] [Google Scholar]
  29. Takahashi T., Owyang C. Vagal control of nitric oxide and vasoactive intestinal polypeptide release in the regulation of gastric relaxation in rat. J Physiol. 1995 Apr 15;484(Pt 2):481–492. doi: 10.1113/jphysiol.1995.sp020680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Takasugi S., Ueda T., Kurata Y., Kodama M., Ezaki H., Fujii K. Neural and humoral factors influence gastric receptive relaxation in dogs. Jpn J Surg. 1982;12(3):208–213. doi: 10.1007/BF02469589. [DOI] [PubMed] [Google Scholar]
  31. Wilbur B. G., Kelly K. A. Effect of proximal gastric, complete gastric, and truncal vagotomy on canine gastric electric activity, motility, and emptying. Ann Surg. 1973 Sep;178(3):295–303. doi: 10.1097/00000658-197309000-00009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Yokotani K., Okuma Y., Nakamura K., Osumi Y. Release of endogenous acetylcholine from a vascularly perfused rat stomach in vitro; inhibition by M3 muscarinic autoreceptors and alpha-2 adrenoceptors. J Pharmacol Exp Ther. 1993 Sep;266(3):1190–1195. [PubMed] [Google Scholar]

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