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. 1985 Jul;364:301–312. doi: 10.1113/jphysiol.1985.sp015746

Submucosal plexus and electrolyte transport across rat colonic mucosa.

H Andres, R Rock, R J Bridges, W Rummel, J Schreiner
PMCID: PMC1192971  PMID: 2411917

Abstract

Electrolyte transport across two preparations of mucosa from rat colon descendens was compared to determine what influence the submucosal plexus has on electrolyte transport. One preparation consisted of the mucosa, muscularis mucosae, and the submucosal tissue and is referred to as the mucosa-submucosa preparation. The second preparation obtained by further blunt dissection of the mucosa-submucosa preparation consisted of only the mucosa and the circular muscle layer of muscularis mucosae and is referred to as the mucosa preparation. Histological studies showed that the submucosal tissue and the longitudinal layer of muscularis mucosae could be removed leaving only the mucosa and the circular layer of muscularis mucosae. The extensive neuronal network of the submucosa was shown when the submucosal tissue and longitudinal muscle layer of muscularis mucosae, which were removed, were stained histochemically for acetylcholinesterase activity. Both the mucosa-submucosa and mucosa preparations absorbed Na+ and Cl- when short-circuited. However, Na+ and Cl- absorption were significantly higher in the mucosa preparation. The increase in Na+ and Cl- transport in the mucosa preparation was accompanied with a decrease in the short-circuit current (Isc), the open-circuit potential difference (p.d.) and the transmural tissue conductance (Gt) when compared to the mucosa-submucosa preparation. Tetrodotoxin (TTX), a neurotoxin which blocks specifically the propagation of action potentials in excitable tissues, dose-dependently decreased Isc and p.d. in the mucosa-submucosa preparation when added to the serosal solution. The half-maximal effective concentration of TTX was 5 nM and maximal effective concentration 100 nM. TTX (1 microM) had no effect on Isc or p.d. when added to the mucosal solution. The decrease in Isc and p.d. caused by TTX in the mucosa-submucosa preparation was accompanied with an increase in Na+ and Cl- absorption. TTX caused only a small decrease in Isc and p.d. in the mucosa preparation. However, there was no measurable change in Na+ and Cl- transport in the mucosa preparation. The results suggest that spontaneously active neurones from the submucosal plexus have an inhibitory influence on the mucosa. Physical removal of the submucosal plexus or pharmacological blockade of the neurones within the mucosa-submucosa preparation by TTX led to enhanced absorption, suggesting that the set point of the mucosa for electrolyte transport is at or near a maximal absorptive state. Regulation or modulation of the mucosa may therefore occur by mechanisms that lower this set point, causing an inhibition of absorption of electrolytes.

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Selected References

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

  1. Bock R., Mühlen K aus der Beiträge zur funktionellen Morphologie der Neurohypophyse. I. Uber ein "gomoripostitive" Substanz in der Zona extrtna infundibuli beidseitig adrenalektomierter weisser Mäuse. Z Zellforsch Mikrosk Anat. 1968;92(1):130–148. [PubMed] [Google Scholar]
  2. Bridges R. J., Rummel W., Simon B. Forskolin induced chloride secretion across the isolated mucosa of rat colon descendens. Naunyn Schmiedebergs Arch Pharmacol. 1983 Aug;323(4):355–360. doi: 10.1007/BF00512476. [DOI] [PubMed] [Google Scholar]
  3. Catterall W. A. Neurotoxins that act on voltage-sensitive sodium channels in excitable membranes. Annu Rev Pharmacol Toxicol. 1980;20:15–43. doi: 10.1146/annurev.pa.20.040180.000311. [DOI] [PubMed] [Google Scholar]
  4. Cooke H. J., Shonnard K., Highison G., Wood J. D. Effects of neurotransmitter release on mucosal transport in guinea pig ileum. Am J Physiol. 1983 Dec;245(6):G745–G750. doi: 10.1152/ajpgi.1983.245.6.G745. [DOI] [PubMed] [Google Scholar]
  5. Cooke H. J., Shonnard K., Wood J. D. Effects of neuronal stimulation on mucosal transport in guinea pig ileum. Am J Physiol. 1983 Aug;245(2):G290–G296. doi: 10.1152/ajpgi.1983.245.2.G290. [DOI] [PubMed] [Google Scholar]
  6. Furness J. B., Costa M. Types of nerves in the enteric nervous system. Neuroscience. 1980;5(1):1–20. doi: 10.1016/0306-4522(80)90067-6. [DOI] [PubMed] [Google Scholar]
  7. Gershon M. D. The enteric nervous system. Annu Rev Neurosci. 1981;4:227–272. doi: 10.1146/annurev.ne.04.030181.001303. [DOI] [PubMed] [Google Scholar]
  8. Hubel K. A. Effects of scorpion venom on electrolyte transport by rabbit ileum. Am J Physiol. 1983 May;244(5):G501–G506. doi: 10.1152/ajpgi.1983.244.5.G501. [DOI] [PubMed] [Google Scholar]
  9. Hubel K. A., Shirazi S. Human ileal ion transport in vitro: changes with electrical field stimulation and tetrodotoxin. Gastroenterology. 1982 Jul;83(1 Pt 1):63–68. [PubMed] [Google Scholar]
  10. Hubel K. A. The effects of electrical field stimulation and tetrodotoxin on ion transport by the isolated rabbit ileum. J Clin Invest. 1978 Nov;62(5):1039–1047. doi: 10.1172/JCI109208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. KARNOVSKY M. J., ROOTS L. A "DIRECT-COLORING" THIOCHOLINE METHOD FOR CHOLINESTERASES. J Histochem Cytochem. 1964 Mar;12:219–221. doi: 10.1177/12.3.219. [DOI] [PubMed] [Google Scholar]
  12. Narahashi T. Chemicals as tools in the study of excitable membranes. Physiol Rev. 1974 Oct;54(4):813–889. doi: 10.1152/physrev.1974.54.4.813. [DOI] [PubMed] [Google Scholar]
  13. PARSONS D. S., PATERSON C. R. FLUID AND SOLUTE TRANSPORT ACROSS FAT COLONIC MUCOSA. Q J Exp Physiol Cogn Med Sci. 1965 Apr;50:220–231. doi: 10.1113/expphysiol.1965.sp001784. [DOI] [PubMed] [Google Scholar]
  14. Schultzberg M., Hökfelt T., Nilsson G., Terenius L., Rehfeld J. F., Brown M., Elde R., Goldstein M., Said S. Distribution of peptide- and catecholamine-containing neurons in the gastro-intestinal tract of rat and guinea-pig: immunohistochemical studies with antisera to substance P, vasoactive intestinal polypeptide, enkephalins, somatostatin, gastrin/cholecystokinin, neurotensin and dopamine beta-hydroxylase. Neuroscience. 1980;5(4):689–744. doi: 10.1016/0306-4522(80)90166-9. [DOI] [PubMed] [Google Scholar]
  15. Sjövall H. Sympathetic control of jejunal fluid and electrolyte transport. An experimental study in cats and rats. Acta Physiol Scand Suppl. 1984;535:1–63. [PubMed] [Google Scholar]
  16. Tapper E. J. Local modulation of intestinal ion transport by enteric neurons. Am J Physiol. 1983 May;244(5):G457–G468. doi: 10.1152/ajpgi.1983.244.5.G457. [DOI] [PubMed] [Google Scholar]
  17. Welsh M. J., Smith P. L., Fromm M., Frizzell R. A. Crypts are the site of intestinal fluid and electrolyte secretion. Science. 1982 Dec 17;218(4578):1219–1221. doi: 10.1126/science.6293054. [DOI] [PubMed] [Google Scholar]

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