Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1994 Feb 1;474(3):539–546. doi: 10.1113/jphysiol.1994.sp020043

Accommodation mediated by enteric inhibitory reflexes in the isolated guinea-pig small intestine.

S A Waterman 1, M Costa 1, M Tonini 1
PMCID: PMC1160343  PMID: 7912284

Abstract

1. The aim of the present study was to investigate whether the guinea-pig small intestine shows accommodation to infused fluid, similarly to other regions of the gastrointestinal tract. Tetrodotoxin, papaverine and transmitter antagonists were used to establish the existence of reflex pathways and the nature of the neurotransmitters involved. 2. Compliance, measured as the change in volume of infused fluid divided by the intraluminal pressure change, was reduced by tetrodotoxin (0.6 microM), indicating that there is an overall neurally mediated relaxation of the circular muscle in response to low rates of distension. Papaverine (10 microM) did not have any significant effect on compliance at the low rates of distension, suggesting that the circular muscle is fully relaxed. 3. At each rate of distension, 400 microM N omega-nitro-L-arginine methyl ester (L-NAME, a nitric oxide synthase inhibitor) significantly decreased the compliance of the intestinal wall, indicating that the circular muscle was relaxed by a nitric oxide-mediated mechanism. Apamin (0.5 microM), which blocks a component of inhibitory transmission, did not have a significant effect. 4. In control preparations, the intestinal wall was less compliant when distended by fluid at a fast rate, compared with the lower rates of distension. This was not due to changes in passive components of the intestinal wall or a myogenic response to rapid stretch. 5. When the intestine was distended rapidly, 1 microM hyoscine and 100 microM hexamethonium increased intestinal compliance. However, they had no detectable effect on compliance with low rates of distension.(ABSTRACT TRUNCATED AT 250 WORDS)

Full text

PDF
539

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BULBRING E. Correlation between membrane potential, spike discharge and tension in smooth muscle. J Physiol. 1955 Apr 28;128(1):200–221. doi: 10.1113/jphysiol.1955.sp005299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BURNSTOCK G., PROSSER C. L. Responses of smooth muscles to quick stretch: relation of stretch to conduction. Am J Physiol. 1960 May;198:921–925. doi: 10.1152/ajplegacy.1960.198.5.921. [DOI] [PubMed] [Google Scholar]
  3. Banks B. E., Brown C., Burgess G. M., Burnstock G., Claret M., Cocks T. M., Jenkinson D. H. Apamin blocks certain neurotransmitter-induced increases in potassium permeability. Nature. 1979 Nov 22;282(5737):415–417. doi: 10.1038/282415a0. [DOI] [PubMed] [Google Scholar]
  4. Barthó L., Holzer P., Donnerer J., Lembeck F. Evidence for the involvement of substance P in the atropine-resistant peristalsis of the guinea-pig ileum. Neurosci Lett. 1982 Sep 20;32(1):69–74. doi: 10.1016/0304-3940(82)90231-2. [DOI] [PubMed] [Google Scholar]
  5. Bornstein J. C., Costa M., Furness J. B., Lang R. J. Electrophysiological analysis of projections of enteric inhibitory motoneurones in the guinea-pig small intestine. J Physiol. 1986 Jan;370:61–74. doi: 10.1113/jphysiol.1986.sp015922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brookes S. J., Steele P. A., Costa M. Identification and immunohistochemistry of cholinergic and non-cholinergic circular muscle motor neurons in the guinea-pig small intestine. Neuroscience. 1991;42(3):863–878. doi: 10.1016/0306-4522(91)90050-x. [DOI] [PubMed] [Google Scholar]
  7. Costa M., Furness J. B., Humphreys C. M. Apamin distinguishes two types of relaxation mediated by enteric nerves in the guinea-pig gastrointestinal tract. Naunyn Schmiedebergs Arch Pharmacol. 1986 Jan;332(1):79–88. doi: 10.1007/BF00633202. [DOI] [PubMed] [Google Scholar]
  8. Costa M., Furness J. B., Pompolo S., Brookes S. J., Bornstein J. C., Bredt D. S., Snyder S. H. Projections and chemical coding of neurons with immunoreactivity for nitric oxide synthase in the guinea-pig small intestine. Neurosci Lett. 1992 Dec 14;148(1-2):121–125. doi: 10.1016/0304-3940(92)90819-s. [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. Davison J. S., Pearson G. T. The role of intrinsic, non-adrenergic, non-cholinergic inhibitory nerves in the regulation of distensibility of the guinea-pig colon. Pflugers Arch. 1979 Jul;381(1):75–77. doi: 10.1007/BF00582335. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Furness J. B., Costa M. The participation of enteric inhibitory nerves in accommodation of the intestine to distension. Clin Exp Pharmacol Physiol. 1977 Jan-Feb;4(1):37–41. doi: 10.1111/j.1440-1681.1977.tb02375.x. [DOI] [PubMed] [Google Scholar]
  13. Furness J. B., Trussell D. C., Pompolo S., Bornstein J. C., Smith T. K. Calbindin neurons of the guinea-pig small intestine: quantitative analysis of their numbers and projections. Cell Tissue Res. 1990 May;260(2):261–272. doi: 10.1007/BF00318629. [DOI] [PubMed] [Google Scholar]
  14. Hirst G. D., Holman M. E., McKirdy H. C. Two descending nerve pathways activated by distension of guinea-pig small intestine. J Physiol. 1975 Jan;244(1):113–127. doi: 10.1113/jphysiol.1975.sp010786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Holzer P. Ascending enteric reflex: multiple neurotransmitter systems and interactions. Am J Physiol. 1989 Mar;256(3 Pt 1):G540–G545. doi: 10.1152/ajpgi.1989.256.3.G540. [DOI] [PubMed] [Google Scholar]
  16. Holzer P., Schluet W., Maggi C. A. Ascending enteric reflex contraction: roles of acetylcholine and tachykinins in relation to distension and propagation of excitation. J Pharmacol Exp Ther. 1993 Jan;264(1):391–396. [PubMed] [Google Scholar]
  17. Hoyle C. H., Knight G. E., Burnstock G. Suramin antagonizes responses to P2-purinoceptor agonists and purinergic nerve stimulation in the guinea-pig urinary bladder and taenia coli. Br J Pharmacol. 1990 Mar;99(3):617–621. doi: 10.1111/j.1476-5381.1990.tb12979.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. KOSTERLITZ H. W., LEES G. M. PHARMACOLOGICAL ANALYSIS OF INTRINSIC INTESTINAL REFLEXES. Pharmacol Rev. 1964 Sep;16:301–339. [PubMed] [Google Scholar]
  19. KOSTERLITZ H. W., ROBINSON J. A. Reflex contractions of the longitudinal muscle coat of the isolated guinea-pig ileum. J Physiol. 1959 May 19;146(2):369–379. doi: 10.1113/jphysiol.1959.sp006198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Knowles R. G., Palacios M., Palmer R. M., Moncada S. Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proc Natl Acad Sci U S A. 1989 Jul;86(13):5159–5162. doi: 10.1073/pnas.86.13.5159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kottegoda S. R. An analysis of possible nervous mechanisms involved in the peristaltic reflex. J Physiol. 1969 Feb;200(3):687–712. doi: 10.1113/jphysiol.1969.sp008717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Llewellyn-Smith I. J., Song Z. M., Costa M., Bredt D. S., Snyder S. H. Ultrastructural localization of nitric oxide synthase immunoreactivity in guinea-pig enteric neurons. Brain Res. 1992 Apr 17;577(2):337–342. doi: 10.1016/0006-8993(92)90294-j. [DOI] [PubMed] [Google Scholar]
  23. Lyster D. J., Bywater R. A., Taylor G. S., Watson M. J. Effects of a nitric oxide synthase inhibitor on non-cholinergic junction potentials in the circular muscle of the guinea pig ileum. J Auton Nerv Syst. 1992 Dec;41(3):187–196. doi: 10.1016/0165-1838(92)90058-o. [DOI] [PubMed] [Google Scholar]
  24. Maas A. J., Den Hertog A., Ras R., Van den Akker J. The action of apamin on guinea-pig taenia caeci. Eur J Pharmacol. 1980 Oct 17;67(2-3):265–274. doi: 10.1016/0014-2999(80)90507-5. [DOI] [PubMed] [Google Scholar]
  25. Niel J. P., Bywater R. A., Taylor G. S. Apamin-resistant post-stimulus hyperpolarization in the circular muscle of the guinea-pig ileum. J Auton Nerv Syst. 1983 Nov;9(2-3):565–569. doi: 10.1016/0165-1838(83)90014-0. [DOI] [PubMed] [Google Scholar]
  26. Rees D. D., Palmer R. M., Schulz R., Hodson H. F., Moncada S. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol. 1990 Nov;101(3):746–752. doi: 10.1111/j.1476-5381.1990.tb14151.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schulze-Delrieu K., Brown B. P., Custer-Hagen T. Contraction and accommodation of guinea pig duodenum in vitro. Am J Physiol. 1991 Aug;261(2 Pt 1):G364–G372. doi: 10.1152/ajpgi.1991.261.2.G364. [DOI] [PubMed] [Google Scholar]
  28. Smith T. K., Bornstein J. C., Furness J. B. Distension-evoked ascending and descending reflexes in the circular muscle of guinea-pig ileum: an intracellular study. J Auton Nerv Syst. 1990 Mar;29(3):203–217. doi: 10.1016/0165-1838(90)90146-a. [DOI] [PubMed] [Google Scholar]
  29. Steele P. A., Brookes S. J., Costa M. Immunohistochemical identification of cholinergic neurons in the myenteric plexus of guinea-pig small intestine. Neuroscience. 1991;45(1):227–239. doi: 10.1016/0306-4522(91)90119-9. [DOI] [PubMed] [Google Scholar]
  30. Tonini M., Costa M. A pharmacological analysis of the neuronal circuitry involved in distension-evoked enteric excitatory reflex. Neuroscience. 1990;38(3):787–795. doi: 10.1016/0306-4522(90)90071-b. [DOI] [PubMed] [Google Scholar]
  31. Tonini M., Frigo G., Lecchini S., D'Angelo L., Crema A. Hyoscine-resistant peristalsis in guinea-pig ileum. Eur J Pharmacol. 1981 May 22;71(4):375–381. doi: 10.1016/0014-2999(81)90181-3. [DOI] [PubMed] [Google Scholar]
  32. Waterman S. A., Costa M., Tonini M. Modulation of peristalsis in the guinea-pig isolated small intestine by exogenous and endogenous opioids. Br J Pharmacol. 1992 Aug;106(4):1004–1010. doi: 10.1111/j.1476-5381.1992.tb14448.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES