Summary
Double-labelling immunohistochemistry and retrograde transport of the carbocyanine dye, DiI, were used to establish the pathways of submucous neurons to the mucosa of the guinea-pig small intestine. Following the application of DiI to a villus, DiI-labelled nerve cell bodies were found in the submucous plexus up to 8.3 mm circumferentially and 3.8 mm longitudinally. The size of each of the four characterised classes of submucous neurons was determined and their distributions and projections mapped. Cells characterised by vasoactive intestinal polypeptide immunoreactivity accounted for 52% of DiI-labelled cells and had the longest projections. Cells characterised by neuropeptide Y (19%) or by calretinin immunoreactivity (13% of all DiI-labelled neurons) had relatively short projections and cells with substance P immunoreactivity (20%) had intermediate lengths of projection. When DiI was applied directly to the submucous plexus, filled neurons of all classes had significantly shorter projections, indicating that they must run for considerable distances in other pathways to the mucosa, probably via the non-ganglionated plexus. On average, each villus is innervated by at least 70 submucous neurons. From quantitative estimates there are 9 submucous neurons per villus. Thus, each submucous neuron is likely to supply about 8 villi. This demonstrates a high degree of convergence and divergence in the innervation of the mucosa.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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
Bornstein JC, Costa M, Furness JB (1986) Synaptic inputs to immunohistochemically identified neurons in the submucous plexus of the guinea-pig small intestine. J Physiol 381:465–482
Brookes SJH, Costa M (1990) Identification of enteric motor neurons which innervate the circular muscle of the guinea-pig small intestine. Neurosci Lett 118:227–230
Brookes SJH, Steele PA, Costa M (1991) Calretinin immunoreactivity in cholinergic motor neurones, interneurones and vasomotor neurones in the guinea-pig small intestine. Cell Tissue Res 263:471–481
Costa M, Buffa R, Furness JB, Solcia E (1980) Immunohistochemical localization of peptides in peripheral autonomic nerves using whole mount preparations. Histochemistry 65:157–165
Costa M, Furness JB, Llewellyn-Smith IJ, Cuello AC (1981) Projections of substance P-containing neurons within the guinea-pig small intestine. Neuroscience 6:411–424
Costa M, Furness JB, Llewellyn-Smith IJ (1987) Histochemistry of the enteric nervous system. In: Johnson LR (ed) Physiology of the gastrointestinal tract, 2nd edn. Raven Press, New York, pp 1–40
Cuello AC, Galfre G, Milstein C (1979) Detection of substance P in the central nervous system by a monoclonal antibody. Proc Natl Acad Sci USA 67:3532–3536
Furness JB, Costa M (1987) The enteric nervous system. Churchill Livingstone, Edinburgh
Furness JB, Costa M, Walsh JH (1981) Evidence for and significance of the projections of VIP neurons from the myenteric plexus to the tacnia coli in the guinea-pig. Gastroenterology 80:1557–1561
Furness JB, Costa M, Keast JR (1984) Choline acetyltransferase-and peptide immunoreactivity of submucous neurons in the small intestine of the guinea-pig. Cell Tissue Res 237:329–336
Furness JB, Costa M, Gibbins IL, Llewellyn-Smith IJ, Oliver JR (1985) Neurochemically similar myenteric and submucous neurons directly traced to the mucosa of the small intestine. Cell Tissue Res 241:155–163
Furness JB, Costa M, Rökaeus Å, McDonald TJ, Brooks B (1987) Galanin-immunoreactive neurons in the guinea-pig small intestine: their projections and relationships to other enteric neurons. Cell Tissue Res 250:607–615
Furness JB, Llewellyn-Smith IJ, Bornstein JC, Costa M (1988) Chemical neuroanatomy and the analysis of neuronal circuitry in the enteric nervous system. In: Björklund A, Hökfelt T, Owman C (eds) The peripheral nervous system. Handbook of chemical neuroanatomy, vol 6. Elsevier, Amsterdam, pp 161–218
Furness JB, Trussell DC, Pompolo S, Bornstein JC, Smith TK (1990) Calbindin neurons of the guinea-pig small intestine: quantitative analysis of their numbers and projections. Cell Tissue Res 260:261–272
Gallacher M, Mackenna BR, McKirdy HC (1973) Effects of drugs and of electrical stimulation on the muscularis mucosae of rabbit large intestine. Br J Pharmac 47:760–764
Grube D (1980) Immunoreactivities of gastrin (G-) cells. II. Nonspecific binding of immunoglobulins to G-cells by ionic interactions. Histochemistry 66:149–167
Gulbenkian S, Wharton J, Polak JM (1987) The visualisation of cardiovascular innervation in the guinea-pig using an antiserum to protein gene product 9.5 (PGP 9.5). J Auton Nerv Syst 18:235–247
Keast JR (1987) Mucosal innervation and control of water and ion transport in the intestine. Rev Physiol Biochem Pharmacol 109:1–59
Morris JL, Gibbins IL, Furness JB, Costa M, Murphy R (1985) Co-localization of NPY, VIP and dynorphin in non-noradrenergic axons of the guinea-pig uterine artery. Neurosci Lett 62:31–37
Morris JL, Gibbins IL, Murphy R (1986) Neuropeptide Y-like immunoreactivity is absent from most of the perivascular noradrenergic axons in a marsupial, the brush-tailed possum. Neurosci Lett 71:264–270
Onori L, Friedmann CA, Frigo GM, Tonini M (1971) Effects of catecholamines, nicotine, acetylcholine and potassium on the mechanical activity of the colonic muscularis mucosae in the cat. Am J Dig Dis 16:689–692
Rogers JH (1989) Immunoreactivity for calretinin and other calcium-binding proteins in the cerebellum. Neuroscience 31:711–721
Song Z-M, Brookes SJH, Costa M (1991) Identification of myenteric neurons which project to the mucosa of the guinea-pig small intestine. Neurosci Lett 129:294–298
Steele PA, Costa M (1990) Opioid-like immunoreactive neurons in secretomotor pathways of the guinea-pig ileum. Neuroscience 38:771–786
Steele PA, Brookes SJH, Costa M (1991) Immunohistochemical identification of cholinergic neurons in the myenteric plexus of guinea-pig small intestine. Neuroscience 45:227–239
Wilson AJ, Furness JB, Costa M (1981) The fine structure of the submucous plexus of the guinea-pig ileum. I. The ganglia, neurons, Schwann cells and neuropil. J Neurocytol 10:759–784
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Song, Z.M., Brookes, S.J.H., Steele, P.A. et al. Projections and pathways of submucous neurons to the mucosa of the guinea-pig small intestine. Cell Tissue Res 269, 87–98 (1992). https://doi.org/10.1007/BF00384729
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00384729