Skip to main content
Log in

Projection pathways, co-existence of peptides and synaptic organization of nerve fibers in the inferior mesenteric ganglion of the guinea-pig

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

Summary

The presence of immunoreactive enkephalin, dynorphin, vasoactive intestinal polypeptide, cholecystokinin, substance P and neuropeptide Y in nerve fibers that project to the guinea-pig inferior mesenteric ganglion was analysed, after different denervation and ligation procedures. A quantitative analysis demonstrates that enkephalin- and substance P fibers reach the ganglion mainly via lumbar splanchnic and partly via intermesenteric nerves. Dynorphin-, vasoactive intestinal polypeptide- and cholecystokinin fibers reach the ganglion mainly via colonic and partly via hypogastric or intermesenteric nerves. Neuropeptide Y fibers enter via intermesenteric, lumbar splanchnic and hypogastric nerves and pass through the ganglion. Analysis of serial 0.5 μm sections tends to confirm co-existence: of dynorphin, vasoactive intestinal polypeptide and cholecystokinin in fibers projecting from the colon; of dynorphin with substance P in the lumbar splanchnic nerves; and of neuropeptide Y with substance P in the hypogastric and colonic fibers. Synaptic contacts, predominantly axodendritic, onto the ganglion cells from enkephalin-, vasoactive intestinal polypeptide-, and substance P-containing terminals were revealed by electron microscopy. Enkephalin-immunoreactive axon varicosities are filled with small, clear vesicles with a few large, cored vesicles and form asymmetric synapses; dynorphin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive axon varicosities are rich in large, dense-cored vesicles and form symmetric synapses.

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

  • Baker SC, Cuello AC, Matthews MR (1980) Substance P-containing synapses in a sympathetic ganglion, and their possible origin as collaterals from sensory nerve fibers. J Physiol Lond 308:76–77

    Google Scholar 

  • Coleman HA (1987) Multiple sites for the initiation of action potentials in neurons of the inferior mesenteric ganglion of the guinea-pig. Neuroscience 20:357–363

    Google Scholar 

  • Connaughton M, Cuello AC, Matthews MR (1983) Synaptic networks formed by substance P-immunoreactive sensory nerve fibers in guinea-pig prevertebral ganglia. J Physiol Lond 334:96

    Google Scholar 

  • Costa M, Furness JB (1983) The origins, pathway and terminations of neurons with VIP-like immunoreactivity in the guinea-pig small intestine. Neuroscience 8:665–676

    Google Scholar 

  • Costa M, Furness JB (1984) Somatostatin is present in a subpopulation of noradrenergic nerve fibers supplying the intestine. Neuroscience 13:911–919

    Google Scholar 

  • Costa M, Furness JB, Yanaihara N, Yanaihara C, Moody TW (1984) Distribution and projections of neurons with immunoreactivity for both gastrin-releasing peptide and bombesin in the guinea-pig small intestine. Cell Tissue Res 235:285–293

    Google Scholar 

  • Costa M, Furness JB, Gibbins IL (1986) Chemical coding of enteric neurons. Prog Brain Res 68:217–239

    Google Scholar 

  • Crowcroft PJ, Holman ME, Szurszewski IH (1971) Excitatory imput from the distal colon to the inferior mesenteric ganglion in the guinea-pig. J Physiol Lond 19:443–461

    Google Scholar 

  • Dalsgaard C-J, Elfvin L-G (1979) Spinal origin of preganglionic fibers projecting onto the superior cervical ganglion and inferior mesenteric ganglion of the guinea-pig, as demonstrated by the horseradish peroxidase technique. Brain Res 172:139–143

    Google Scholar 

  • Dalsgaard C-J, Elfvin L-G (1982) Structural studies on the connectivity of the inferior mesenteric ganglion of the guinea-pig. J Auton Nerv Syst 5:265–278

    Google Scholar 

  • Dalsgaard C-J, Hökfelt T, Elfvin L-G, Skirboll L, Emson P (1982a) Substance P-containing primary sensory neurons projecting to the inferior mesenteric ganglion: evidence from combined retrograde tracing and immunohistochemistry. Neuroscience 7:647–654

    Google Scholar 

  • Dalsgaard C-J, Hökfelt T, Elfvin L-G, Terenius L (1982b) Enkephalin-containing sympathetic preganglionic neurons projecting to the inferior mesenteric ganglion: evidence from combined retrograde tracing and immunohistochemistry. Neuroscience 7:2309–2050

    Google Scholar 

  • Dalsgaard C-J, Hökfelt T, Schultzberg M (1983a) Origin of peptide-containing fibers in the inferior mesenteric ganglion of the guinea-pig: immunohistochemical studies with antisera to substance P, enkephalin, vasoactive intestinal polypeptide, cholecystokinin and bombesin. Neuroscience 9:191–211

    Google Scholar 

  • Dalsgaard C-J, Vincent SR, Hökfelt T, Christensson I, Terenius L (1983 b) Separate origin for the dynorphin and enkephalin immunoreactive fibers in the inferior mesenteric ganglion of the guinea pig. J Comp Neurol 221:482–489

    Google Scholar 

  • Dun NJ, Jiang ZG (1982) Non-cholinergic excitatory transmission in inferior mesenteric ganglia of the guinea-pig: possible mediation by substance P. J Physiol Lond 325:145–159

    Google Scholar 

  • Elfvin L-G (1971) Ultrastructural studies on the synaptology of the inferior mesenteric ganglion of the cat. III. The structure and distribution of the axodendritic and dendrodendritic contacts. J Ultrastruct Res 37:432–448

    Google Scholar 

  • Elfvin L-G, Dalsgaard C-J (1977) Retrograde axonal transport of horseradish peroxidase in afferent fibers of the inferior mesenteric ganglion of the guinea pig. Identification of the cells of origin in dorsal root ganglia. Brain Res 126:149–153

    Google Scholar 

  • Gibbins IL, Furness JB, Costa M (1987) Pathway-specific patterns of the co-existence of substance P, calcitonin gene-related peptide, cholecystokinin and dynorphin in neurons of the dorsal root ganglia of the guinea-pig. Cell Tissue Res 248:417–437

    Google Scholar 

  • Hatanaka H, Amano T (1981) A mouse neuroblastoma x rat glioma hybrid cell produces immunoreactive substance P-like material. Brain Res 215:305–316

    Google Scholar 

  • Jiang ZG, Simmons MA, Dun NJ (1982) Enkephalinergic modulation of non-cholinergic transmission in mammalian prevertebral ganglia. Brain Res 235:185–191

    Google Scholar 

  • Job C, Lundberg A (1952) Reflex excitation of cells in the inferior mesenteric ganglion on stimulation of the hypogastric nerve. Acta Physiol Scand 26:366–382

    Google Scholar 

  • Kobayashi S, Uchida T, Ohashi T, Fujita T, Imura H, Mochizuki T, Yanaihara C, Yanaihara N (1983) Met-enkephalin-Arg-GlyLeu-like immunoreactivity in adrenal chromaffin cells and carotid body chief cells of the dog and monkey. Biomed Res 4:201–210

    Google Scholar 

  • Kondo H, Dun NJ, Pappas GD (1980) A light and electron microscopic study of the rat superior cervical ganglion cells by intracellular HRP-labeling. Brain Res 197:193–199

    Google Scholar 

  • Konishi S, Tsunoo A, Otsuka M (1979) Enkephalins presynaptically inhibit cholinergic transmission in sympathetic ganglia. Nature 282:515–516

    Google Scholar 

  • Konishi S, Tsunoo A, Yanaihara N, Otsuka M (1980) Peptidergic excitatory and inhibitory synapses in mammalian sympathetic ganglia: roles of substance P and enkephalin. Biomed Res 1:528–536

    Google Scholar 

  • Kosaka T, Nagatsu I, Wu J-Y, Hama K (1986) Use of high concentrations of glutaraldehyde for immunocytochemistry of transmitter-synthesizing enzymes in the central nervous system. Neuroscience 18:975–990

    Google Scholar 

  • Kreulen DL, Szurszewski JH (1979) Reflex pathways in abdominal prevertebral ganglia: evidence of a colo-colonic inhibitory reflex. J Physiol Lond 295:21–32

    Google Scholar 

  • Kummer W, Heym Ch (1986) Correlation of neuronal size and peptide immunoreactivity in the guinea-pig trigeminal ganglion. Cell Tissue Res 245:657–665

    Google Scholar 

  • Kuntz A, Saccomanno G (1944) Reflex inhibition of intestinal motility mediated through decentralized prevertebral ganglia. J Neurophysiol 7:163–170

    Google Scholar 

  • Lindh B, Hökfelt T, Elfvin L-G, Terenius L, Fahrenkrug J, Elde R, Goldstein M (1986) Topography of NPY-, somatostatin-, and VIP-immunoreactive neuronal subpopulations in the guinea pig celiac-superior mesenteric ganglion and their projection to the pylorus. J Neurosci 6:2371–2383

    Google Scholar 

  • Lundberg JM, Hökfelt T, Schultzberg M, Uvnäs-Wallensten K, Köhler C, Said SIB (1979) Occurrence of vasoactive intestinal polypeptide (VIP)-like immunoreactivity in certain cholinergic neurons of the cat. Evidence from combined immunohistochemistry and acetylcholinesterase staining. Neuroscience 4:1539–1559

    Article  CAS  PubMed  Google Scholar 

  • Macrae IM, Furness JB, Costa M (1986) Distribution of subgroups of noradrenaline neurons in the coeliac ganglion of the guinea-pig. Cell Tissue Res 244:173–180

    Google Scholar 

  • Masuko S, Chiba T (1987) Electron microscopic studies on the organization of peptide nerve terminals in the inferior mesenteric ganglion. In: Heym C (ed) Histochemistry and cell biology of autonomic neurons and paraganglia. Exp Brain Res, Series 16, Springer, Berlin Heidelberg New York, pp 174–179

    Google Scholar 

  • Matthews MR, Cuello AC (1982) Subatance P-immunoreactive peripheral branches of sensory neurons innervate guinea-pig sympathetic neurons. Proc Natl Acad Sci USA 79:1668–1672

    Google Scholar 

  • Matthews MR, McConnell P (1984) Evidence from double retrograde labelling that peripheral processes of visceral sensory neurons give synaptic collaterals in the guinea-pig inferior mesenteric ganglion. J Anat 138:562

    Google Scholar 

  • Matthews MR, Connaughton M, Cuello AC (1987) Ultrastructure and distribution of substance P-immunoreactive sensory collaterals in the guinea pig prevertebral sympathetic ganglia. J Comp Neurol 258:28–51

    Google Scholar 

  • Mayor HD, Hampton JC, Rosario B (1961) A simple method for removing the resin from epoxy-embedded tissue. J Biophys Biochem Cytol 9:909–910

    Article  CAS  PubMed  Google Scholar 

  • Mo N, Dun NJ (1984) Vasoactive intestinal polypeptide facilitates muscarinic transmission in mammalian sympathetic ganglia. Neurosci Lett 52:19–23

    Google Scholar 

  • Mo N, Dun NJ (1986) Cholecystokinin octapeptide depolarizes guinea pig inferior mesenteric ganglion cells and facilitates nicotinic transmission. Neurosci Lett 64:263–268

    Google Scholar 

  • Peters S, Kreulen DL (1986) Fast and slow synaptic potentials produced in a mammalian sympathetic ganglion by colon distension. Proc Natl Acad Sci USA 83:1941–1944

    Google Scholar 

  • Sternberger LA (1979) Immunohistochemistry. 2nd edn. John Wiley and Sons Inc. New York, pp 104–169

    Google Scholar 

  • Szurszewski JH, Weems WA (1976) A study of peripheral input to and its control by postganglionic neurons of the inferior mesenteric ganglion. J Physiol Lond 256:541–556

    Google Scholar 

  • Tsunoo A, Konishi S, Otsuka M (1982) Substance P as an excitatory transmitter of primary afferent neurons in guinea-pig sympathetic ganglia. Neuroscience 7:2025–2037

    Google Scholar 

  • Ungvary G, Leranth C (1970) Termination in the prevertebral abdominal sympathetic ganglia of axons arising from the local (terminal) vegetative plexus of visceral organs. Z Zellforsch Mikrosk Anat 110:185–191

    Google Scholar 

  • Zamboni L, DeMartino C (1967) Buffered picric-acid formaldehyde; a new rapid fixative for electron microscopy. J Cell Biol 35:148a

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Masuko, S., Chiba, T. Projection pathways, co-existence of peptides and synaptic organization of nerve fibers in the inferior mesenteric ganglion of the guinea-pig. Cell Tissue Res. 253, 507–516 (1988). https://doi.org/10.1007/BF00219741

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00219741

Key words

Navigation