Skip to main content
Log in

Catecholamine innervation of the intestine of flying foxes (Pteropus spp.): a substantial supply from enteric neurons

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The distribution of catecholamines in the small and large intestine of flying foxes (Pteropus spp.) was investigated using glyoxylic-acid-induced fluorescence and immunohistochemical staining of tyrosine hydroxylase and dopamine-β-hydroxylase. Dense networks of varicose axons stained by each of these methods supplied blood vessels, the mucosa and both submucous and myenteric ganglia, but were scarce in the circular and longitudinal muscle. The majority (>90%) of submucous neuronal perikarya contained both enzymes and most of these also exhibited catecholamine fluorescence. Somata of similar staining characteristics were less common in the myenteric plexus, where single cells were found in only the minority of ganglia. All of the stained submucosal somata and mucosal axons contained vasoactive intestinal peptide, whereas catecholamine-containing axons that supplied the ganglia, external muscle and blood vessels did not. It is concluded that (1) there is dense catecholamine innervation of most tissues in the flyingfox intestine, similar to many other mammals, (2) mucosal axons originate from enteric catecholamine neurons, not found in other mammals, and (3) axons supplying the blood vessels and enteric ganglia are probably of sympathetic origin and can be distinguished from the intrinsic catecholamine-containing axons by their lack of vasoactive intestinal peptide. The roles and interactions of these two types of catecholamine innervation in the control of secretion and motility remain to be identified.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bennett MR, Burnstock G, Holman ME (1966) Transmission from perivascular inhibitory nerves to the smooth muscle of the guinea-pig taenia coli. J Physiol (Lond) 182:527–540

    Google Scholar 

  • Bornstein JC, Furness JB (1988) Correlated electrophysiological and histochemical studies of submucous neurons and their contribution to understanding enteric neural circuits. J Auton Nerv Syst 25:1–13

    Google Scholar 

  • Cooke HJ (1986) Neurobiology of the intestinal mucosa. Gastroenterology 90:57–81

    Google Scholar 

  • Costa M, Gabella G (1971) Adrenergic innervation of the alimentary canal. Z Zellforsch 122:357–377

    Google Scholar 

  • Costa M, Furness JB, Gabella G (1971) Catecholamine containing nerve cells in the mammalian myenteric plexus. Histochemie 25:103–106

    Google Scholar 

  • Furness JB, Costa M (1971) Morphology and distribution of intrinsic adrenergic neurones in the proximal colon of the guinea-pig. Z Zellforsch 120:346–363

    Google Scholar 

  • Furness JB, Costa M (1974) The adrenergic innervation of the gastrointestinal tract. Ergeb Physiol 69:1–51

    Google Scholar 

  • Furness JB, Costa M (1987) The enteric nervous system. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Gillespie JS (1962) Spontaneous mechanical and electrical activity of stretched and unstretched intestinal smooth muscle cells and their response to sympathetic nerve stimulation. J Physiol (Lond) 162:54–75

    Google Scholar 

  • Keast JR (1987) Mucosal innervation and control of water and ion transport in the intestine. Rev Physiol Biochem Pharmacol 109:1–60

    Google Scholar 

  • Keast JR (1991) Patterns of co-existence of peptides and differences of nerve fibre types associated with noradrenergic and non-noradrenergic (putative cholinergic) neurons in the major pelvic ganglion of the male rat. Cell Tissue Res 266:405–415

    Google Scholar 

  • Kitahama K, Luppi P-H, Berod A, Goldstein M, Jouvet M (1987) Localization of tyrosine hydroxylase-immunoreactive neurons in the cata hypothalamus, with special reference to fluorescence histochemistry. J Comp Neurol 262:578–593

    Google Scholar 

  • Llewellyn-Smith IJ, Furness JB, O'Brien PE, Costa M (1984) Noradrenergic nerves in human small intestine. Distribution and ultrastructure. Gastroenterology 87:513–529

    Google Scholar 

  • Morris JL, Gibbins IL (1987) Neuronal colocalization of peptides, catecholamines, and catecholamine-synthesizing enzymes in guinea pig paracervical ganglia. J Neurosci 7:3117–3130

    Google Scholar 

  • Skagerberg G, Meister B, Hökfelt T, Lindvall O, Goldstein M, Joh T, Cuello AC (1988) Studies on dopamine-, tyrosine hydroxylase-and aromatic L-amino acid decarboxylase-containing cells in the rat diencephalon: comparison between formaldehyde-induced histofluorescence and immunofluorescence. Neuroscience 24:605–620

    Google Scholar 

  • Tedman RA, Hall LS (1985a) The absorptive surface area of the small intestine of Pteropus poliocephalus (Megachiroptera: Pteropodidae): an important factor in rapid food transit? Aust Mamm 8:271–278

    Google Scholar 

  • Tedman RA, Hall LS (1985b) The morphology of the gastrointestinal tract and food transit in the fruit bats Pteropus alecto and P. poliocephalus (Megachiroptera). Aust J Zool 33:625–640

    Google Scholar 

  • Torre JC de la (1980) An improved approach to histofluorescence using the SPG method for tissue monoamines. J Neurosci Methods 3:1–5

    Google Scholar 

  • Vizi ES, Knoll J (1971) The effects of sympathetic nerve stimulation and guanethidine on parasympathetic neuroeffector transmission: the inhibition of acetylcholine release. J Pharm Pharmacol 23:918–925

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Keast, J.R. Catecholamine innervation of the intestine of flying foxes (Pteropus spp.): a substantial supply from enteric neurons. Cell Tissue Res 276, 403–410 (1994). https://doi.org/10.1007/BF00306126

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00306126

Key words

Navigation