Skip to main content
Log in

Selective association of nerve fibres immunoreactive for substance P or bombesin with putative cholinergic neurons of the male rat major pelvic ganglion

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

Abstract

The male rat major pelvic ganglion contains both sympathetic and parasympathetic neurons that supply the lower urinary and digestive tracts, and the reproductive organs. The aim of this study was to describe the distribution and identify potential targets of sensory and intestinofugal axons in this ganglion. Two putative markers of these projections were chosen, substance P for primary sensory axons and bombesin for myenteric intestinofugal projections. Varicose substance P-immunoreactive axons were associated only with non-noradrenergic (putative cholinergic) somata, and most commonly with those that contained vasoactive intestinal peptide. Immunoreactivity for substance P was also present in a small group of non-noradrenergic somata, many of which were immunoreactive for enkephalins, neuropeptide Y or vasoactive intestinal peptide. Bombesin immunoreactivity was found only in preterminal and terminal (varicose) axons, the latter of which were exclusively associated with non-noradrenergic somata that contain neuropeptide Y-immunoreactivity. Some varicose axons containing either substance P-or bombesin-immunoreactivity were intermingled with clumps of small, intensely fluorescent cells. These studies indicate that substance P-and bombesin-immunoreactive axons are likely to connect with numerically small, but discrete, populations of pelvic neurons.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Cameron AA, Leah JD, Snow PJ (1988) The coexistence of neuropeptides in feline sensory neurones. Neuroscience 27:969–979

    Google Scholar 

  • Dail WG, Dziurzynski R (1985) Substance P immunoreactivity in the major pelvic ganglion of the rat. Anat Rec 212:103–109

    Google Scholar 

  • Dail WG, Moll MA, Weber K (1983) Localization of vasoactive intestinal polypeptide in penile erectile tissue and in the major pelvic ganglion of the rat. Neuroscience 10:1379–1386

    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 7:2039–2050

    Google Scholar 

  • Dalsgaard C-J, Hökfelt T, Schultzberg M, Lundberg JM, Terenius L, Dockray GJ, Goldstein M (1983) 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 

  • Dhami D, Mitchell BS (1992) The effects of decentralization on substance P-immunoreactivity in the anterior major pelvic ganglion of the male guinea pig. J Auton Nerv Syst 38:167–176

    Google Scholar 

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

    Google Scholar 

  • Furness JB, Costa M (1987) The enteric nervous system, 1st edn. Churchill Livingstone, Edinburg

    Google Scholar 

  • Gamse R, Wax A, Zigmond RE, Leeman SE (1981) Immunoreactive substance P in sympathetic ganglia: distribution and sensitivity towards capsaicin. Neuroscience 6:437–441

    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 ganglion of the guinea-pig. Cell Tissue Res 248:417–437

    Google Scholar 

  • Hankins MW, Dray A (1988) Non-cholinergic synaptic potentials mediated by lumbar colonic nerve in the guinea-pig inferior mesenteric ganglion in vitro. Neuroscience 26:1073–1081

    Google Scholar 

  • Helén P, Panula P, Yang H-YT, Rapoport SI (1984) Bombesin/gastrin-releasing peptide (GRP)-and Met5-enkephalin-Arg6-Gly7-Leu8-like immunoreactivities in small intensely fluorescent (SIF) cells and nerve fibers of rat sympathetic ganglia. J Histochem Cytochem 32:1131–1138

    Google Scholar 

  • Hökfelt T, Elde R, Johanssen O, Luft R, Nilsson G, Arimura A (1976) Immunohistochemical evidence for separate populations of somatostatin-containing and substance P-containing primary afferent neurons in the rat. Neuroscience 1:131–136

    Google Scholar 

  • Hökfelt T, Elfvin L-G, Schultzberg M, Goldstein M, Nilsson G (1977) On the occurrence of substance P-containing fibers in sympathetic ganglia: immunohistochemical evidence. Brain Res 132:29–41

    Google Scholar 

  • Ju G, Hökfelt T, Brodin E, Fahrenkrug J, Fischer JA, Frey P, Elde RP, Brown JC (1987) Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide-and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res 247:417–431

    Google Scholar 

  • Kawatani M, Whitney T, Booth AM, Groat de WC (1989) Excitatory effect of substance P in parasympathetic ganglia of cat urinary bladder. Am J Physiol 257:R1450-R1456

    Google Scholar 

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

    Google Scholar 

  • Keast JR (1992) Location and peptide content of pelvic neurons supplying the muscle and lamina propria of the rat vas deferens. J Auton Nerv Syst 40:1–12

    Google Scholar 

  • Keast JR, Groat WC de (1989) Immunohistochemical characterization of pelvic neurons which project to the bladder, colon, or penis in rats. J Comp Neurol 288:387–400

    Google Scholar 

  • Kondo H, Kuramoto H, Wainer BH, Yanaihara N (1985) Evidence for the coexistence of acetylcholine and enkephalin in the sympathetic preganglionic neurons of rats. Brain Res 335:309–314

    Google Scholar 

  • Konishi S, Song S-Y, Ogawa T, Kanazawa I (1989) Tachykinins produce fast and slow depolarizations in sympathetic neurons of rat coeliac-superior mesenteric ganglia. Brain Res 490:162–165

    Google Scholar 

  • Kreulen DL, Peters S (1986) Non-cholinergic transmission in a sympathetic ganglion of the guinea-pig elicited by colon distension. J Physiol 374:315–334

    Google Scholar 

  • Lindh B, Hökfelt T, Elfvin L-G (1988) Distribution and origin of peptide-containing nerve fibers in the celiac superior mesenteric ganglion of the guinea-pig. Neuroscience 26:1037–1071

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Panula P, Hadjiconstantinou M, Yang H-YT, Costa E (1983) Immunohistochemical localisation of bombesin/gastrin-releasing peptide and substance P in primary sensory neurons. J Neurosci 3:2021–2029

    Google Scholar 

  • Papka RE, Traurig HH, Klenn P (1987) Paracervical ganglia of the female rat: histochemistry and immunohistochemistry of neurons, SIF cells, and nerve terminals. Am J Anat 179:243–257

    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 

  • Senba E, Yanaihara C, Yanaihara N, Tohyama M (1988) Co-localization of substance P and Met-enkephalin-Arg6-Glu7-Leu8 in the intraspinal neurons of the rat, with special reference to the neurons in the substantia gelatinosa. Brain Res 453:110–116

    Google Scholar 

  • Yaksh TL, Michener SR, Bailey JE, Harty GJ, Lucas DL, Nelson DK, Roddy DR, Go VLW (1988) Survey of distribution of substance P, vasoactive intestinal polypeptide, cholecystokinin, neurotensin, met-enkephalin, bombesin and PHI in the spinal cord of cat, dog, sloth and monkey. Peptides 9:357–372

    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., Chiam, H.C. Selective association of nerve fibres immunoreactive for substance P or bombesin with putative cholinergic neurons of the male rat major pelvic ganglion. Cell Tissue Res 278, 589–594 (1994). https://doi.org/10.1007/BF00331378

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00331378

Key words

Navigation