Cell and Tissue Research

, Volume 278, Issue 2, pp 379–387 | Cite as

Projections of 5-hydroxytryptamine-immunoreactive neurons in guinea-pig distal colon

  • C. F. Wardell
  • J. C. Bornstein
  • J. B. Furness
Article

Abstract

The presence of 5-hydroxytryptamine in enteric neurons of the guinea-pig distal colon was demonstrated by immunohistochemistry and the projections of the neurons were determined. 5-Hydroxytryptamine-containing nerve cells were observed in the myenteric plexus but no reactive nerve cells were found in submucous ganglia. Varicose reactive nerve fibres were numerous in the ganglia of both the myenteric and submucous plexuses, but were infrequent in the longitudinal muscle, circular muscle, muscularis mucosae and mucosa. Reactivity also occurred in enterochromaffin cells. Lesion studies showed that the axons of myenteric neurons projected anally to provide innervation to the circular muscle and submucosa and to other more anally located myenteric ganglia. The results suggest that a major population of 5-hydroxytryptamine neurons in the colon is descending interneurons, most of which extend for 10 to 15 mm in the myenteric plexus and innervate both 5-hydroxytryptamine and non-5-hydroxytryptamine neurons.

Key words

Enteric nervous system Immunohistochemistry 5-Hydroxytryptamine Colon Guinea-pig 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bornstein JC, North RA, Costa M, Furness JB (1984) Excitatory synaptic potentials due to activation of neurons with short projections in the myenteric plexus. Neuroscience 11:723–731Google Scholar
  2. Bornstein JC, Furness JB, Smith TK, Trussell DC (1991) Synaptic responses evoked by mechanical stimulation of the mucosa in morphologically characterized myenteric neurons in the guineapig ileum. J Neurosci 11:505–518Google Scholar
  3. Bülbring E, Crema A (1958) Observations concerning the action of 5-hydroxytryptamine on the peristaltic reflex. Br J Pharmacol 13:444–457Google Scholar
  4. Bunce KT, Elswood CJ, Ball MT (1991) Investigation of the 5-hydroxytryptamine receptor mechanism mediating the short-circuit current response in rat colon. Br J Pharmacol 102:811–816Google Scholar
  5. Christensen J (1991) The motor functions of the colon. In: Yamada T (ed) Textbook of gastroenterology. Lippincott, Philadelphia, pp 180–195Google Scholar
  6. Costa M, Furness JB (1979) The sites of action of 5-hydroxytryptamine in nerve-muscle preparations from the guinea-pig small intestine and colon. Br J Pharmacol 65:237–248Google Scholar
  7. Costa M, Furness JB (1983) The origins, pathways and terminations of neurons with VIP-like immunoreactivity in the guinea-pig small intestine. Neuroscience 8:665–676Google Scholar
  8. Costa M, Gabella G (1971) Adrenergic innervation of the alimentary canal. Z Zellforsch 122:357–377Google Scholar
  9. Costa M, Furness JB, Cuello AC, Verhofstad, AAJ, Steinbusch HWM, Elde RP (1982) Neurons with 5-hydroxytryptamine-like immunoreactivity in the enteric nervous system: their visualization and reactions to drug treatment. Neuroscience 7:351–363Google Scholar
  10. Costa M, Brookes S, Waterman S, Mayo R (1992) Enteric neuronal circuitry and transmitters controlling intestinal motor function. In: Holle GE, Wood JD (eds) Advances in the innervation of the gastrointestinal tract. Elsevier, Amsterdam, pp 115–121Google Scholar
  11. Costall B, Naylor RJ (1990) 5-Hydroxytryptamine: new receptors and novel drugs for gastrointestinal motor disorders. Scand J Gastroenterol 25:769–787Google Scholar
  12. Craig DA, Clarke DE (1991) Peristalsis evoked by 5-HT and renzapride: evidence for putative 5-HT4 receptor activation. Br J Pharmacol 102:563–564Google Scholar
  13. Dahlström A, Ahlman H (1983) Immunocytochemical evidence for the presence of tryptaminergic nerves of blood vessels, smooth muscle and myenteric plexus in the rat small intestine. Acta Physiol Scand 117:589–591Google Scholar
  14. Dubois A, Jacobwitz DM (1974) Failure to demonstrate serotonergic neurons in the myenteric plexus of the rat. Cell Tissue Res 150:493–496Google Scholar
  15. Ekblad E, Håkanson R, Sundler F (1991) Microanatomy and chemical coding of peptide-containing neurons in the digestive tract. In: Daniel EE (ed) Neuropeptide function in the gastrointestinal tract. CRC Press, Boston, pp 131–179Google Scholar
  16. Elswood CJ, Bunce KT, Humphrey PPA (1991) Identification of putative 5-HT4 receptors in guinea-pig ascending colon. Eur J Pharmacol 196:149–155Google Scholar
  17. Frieling T, Cooke HJ, Wood JD (1991) Serotonin receptors on submucous neurons in guinea pig colon. Am J Physiol 261:G1017-G1023Google Scholar
  18. Furness JB, Costa M (1978) Distribution of intrinsic nerve cell bodies and axons which take up aromatic amines and their precursors in the small intestine of the guinea-pig. Cell Tissue Res 188:527–543Google Scholar
  19. Furness JB, Costa M (1982) Neurons with 5-hydroxytryptamine-like immunoreactivity in the enteric nervous system: their projections in the guinea-pig small intestine. Neuroscience 7:341–349Google Scholar
  20. Furness JB, Costa M (1987) The Enteric Nervous System. Churchill Livingstone, LondonGoogle Scholar
  21. Gershon MD, Sherman DL (1987) Noradrenergic innervation of serotominergic neurons in the myenteric plexus. J Comp Neurol 259:193–210Google Scholar
  22. Gershon MD, Wade PR, Kirchgessner AL, Tamir H (1990) 5-HT receptor subtypes outside the central nervous system: roles in the physiology of the gut. Neuropsychopharmacol 3:385–395Google Scholar
  23. Griffith SG, Burnstock G (1983) Serotoninergic neurons in human fetal intestine: an immunohistochemical study. Gastroenterology 85:929–937Google Scholar
  24. Hills JM, Jessen KR (1992) Transmission: γ-aminobutyric acid, 5-hydroxytryptamine and dopamine. In: Burnstock G, Hoyle CHV (eds) Autonomic Neuroeffector Mechanisms. Harwood, Reading, UK, pp 465–507Google Scholar
  25. Johnson SM, Katayama Y, North RA (1980) Multiple actions of 5-hydroxytryptamine on myenteric neurones of the guinea-pig ileum. J Physiol 304:459–470Google Scholar
  26. Jonakait GM, Tamir H, Gintzler AR, Gershon MD (1979) Release of [3H] serotonin and its binding protein from enteric neurons. Brain Res 174:55–69Google Scholar
  27. Kilbinger H, Wolf D (1992) Effects of 5-HT4 receptor stimulation on basal and electrically evoked release of acetylcholine from guinea-pig myenteric plexus. Naunyn-Schmiedeberg's Arch Pharmacol 345:270–275Google Scholar
  28. Kurian SS, Ferri GL, De Mey J, Polak JM (1983) Immunocytochemistry of serotonin-containing nerves in the human gut. histochemistry 78:523–529Google Scholar
  29. Landis SC, Jackson PC, Fredieu JR, Thibault J (1987) Catecholaminergic properties of cholinergie neurons and synapses in adult rat ciliary ganglion. Neurosci 7:3574–3587Google Scholar
  30. Legay C, Saffrey MJ, Burnstock G (1984) Coexistence of immunoreactive substance P and serotonin in neurones of the gut. Brain Res 302:379–382Google Scholar
  31. Mawe GM, Branchek TA, Gershon MD (1986) Peripheral neural serotonin receptors: Identification and characterization with specific antagonists and agonists. Proc Natl Acad Sci USA 83:9799–9803Google Scholar
  32. Messenger JP, Furness JB (1990) Projections of chemically-specified neurons in the guinea-pig colon. Arch Histol Cytol 53:467–495Google Scholar
  33. Nada O, Toyohara T (1987) An immunohistochemical study of serotonin-containing nerves in the colon of rats. Histochemistry 86:229–232Google Scholar
  34. North RA, Henderson G, Katayama Y, Johnson S (1980) Electrophysiological evidence for presynaptic inhibition of acetylcholine release by 5-hydroxytryptamine in the enteric nervous system. Neuroscience 5:581–586Google Scholar
  35. Pataky DM, Curtis SB, Buchan AMJ (1990) The co-localization of neuropeptides in the enteric nervous system of normal Wistar and non-diabetic BB rats. Neuroscience 36:247–254Google Scholar
  36. Robinson R, Gershon MD (1971) Synthesis and uptake of 5-hydroxytryptamine by the myenteric plexus of the small intestine of the guinea pig. J Pharmacol Exp Ther 179:29–41Google Scholar
  37. Scheuermann DW, Stach W, Timmermans JP, Adriaensen D, De Groodt-Lasseel MHA (1991) Calbindin D-28k in the enteric nervous system of the pig and its coexistence with 5-hydroxytryptamine. Anat Anz [Suppl] 178:369–370Google Scholar
  38. Steele PA, Brookes SJH, Costa M (1991) Immunohistochemical identification of cholinergic neurons in the myenteric plexus of guinea-pig small intestine. Neuroscience 45:227–239Google Scholar
  39. Surprenant A, Crist J (1988) Electrophysiological characterization of functionally distinct 5-hydroxytryptamine receptors on guinea-pig submucous plexus. Neurosience 24:283–295Google Scholar
  40. Thompson JH (1971) Serotonin and the alimentary tract Res Commun Chem Pathol Pharmacol 2:687–781Google Scholar
  41. Timmermans JP, Scheuermann DW, Stach W, Adriaensen D, De Groodt-Lasseel MHA (1990) Distinct distribution of CGRP-, enkephalin-, galanin-, VIP- and serotonin-containing neurons in the two submuoosal ganglionic neural networks of the porcine small intestine. Cell Tissue Res 260:367–379Google Scholar
  42. Timmermans JP, Scheuermann DW, Stach W, Barbiers M, Adriaensen D, Krammer HJ, De Groodt-Lasseel MHA (1991) Projections of serotonin-containing neurons in the enteric nerve plexus, an experimental study in the porcine small intestine. Anat Anz [Suppl] 170:89–90Google Scholar
  43. Timmermans JP, Scheuermann DW, Stach W, Adriaensen D, De Groodt-Lasseel MHA (1992) Functional morphology of the enteric nervous system with special reference to large mammals. Eur J Morphology 30:113–122Google Scholar
  44. Tonini M, Rizzi CA, Manzo L, Onori L (1991) Novel enteric 5-HT4 receptors and gastrointestinal prokinetic action. Pharmacol Res 24:5–14Google Scholar
  45. Vanner S, Surprenant A (1990) Effects of 5-HT3 receptor antagonists on 5-HT and nicotinic depolarizations in guinea-pig submucosal neurones. Br J Pharmacol 99:840–844Google Scholar
  46. Wood JD, Mayer CJ (1979) Serotonergic activation of tonic-type enteric neurons in guinea pig small bowel. J Neurophysiol 42:582–593Google Scholar
  47. Young HM, Furness JB, Bornstein JC, Pompolo S (1993a) Neuronal circuitry for enteric motility reflexes. In: Taché Y, Wingate D, Burks T (eds) Innervation of the gut: pathophysiological implications. CRC Press, Boston, pp 258–266Google Scholar
  48. Young HM, Furness JB, Sewell P, Burcher EF, Kandiah CJ (1993b) Total number of neurons in the myenteric plexus of the guineapig small intestine. Cell Tissue Res 272:197–200Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • C. F. Wardell
    • 1
  • J. C. Bornstein
    • 1
  • J. B. Furness
    • 2
  1. 1.Department of PhysiologyUniversity of MelbourneParkvilleAustralia
  2. 2.Department Anatomy and Cell BiologyUniversity of MelbourneParkvilleAustralia

Personalised recommendations