Skip to main content
Log in

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

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

Summary

The pelvic ganglia supply cholinergic and noradrenergic nerve pathways to many organs. Other possible transmitters are also present in these nerves, including peptides. Multiple labelling immunofluorescence techniques were used in this study of the male rat major pelvic ganglion (MPG) to examine: (1) the peptides present in noradrenergic (tyrosine hydroxylase (TH)-positive) and non-noradrenergic (putative cholinergic) neurons, and (2) the types of peptide-containing nerve fibres closely associated with these two groups of neurons. The distribution of the peptide galanin (GAL) within the MPG was also investigated. All of the TH-neurons contained neuropeptide Y (NPY), but none of the other tested peptides. However, many NPY neurons did not contain TH and may have been cholinergic. TH-negative neurons also displayed vasoactive intestinal peptide (VIP), enkephalin (ENK) or GAL. VIP and NPY formed the most common types of putative cholinergic pelvic neurons, but few cells contained both peptides. Many ENK neurons exhibited VIP, NPY or GAL. Varicose nerve terminals surrounding ganglion cells contained ENK, GAL, somatostatin (SOM) and cholecystokinin (CCK). These peptide-immunoreactive fibres were more often associated with the non-noradrenergic (putative cholinergic) than the noradrenergic neurons; two types (SOM and CCK) were preferentially associated with the non-noradrenergic NPY neurons. GAL was distributed throughout the MPG, in small neurons, scattered small, intensely fluorescent (SIF) cells, and both varicose and non-varicose nerve fibres. The nerve fibres were concentrated near the pelvic and penile nerves; most of the varicose fibres formed “baskets” surrounding individual GAL-negative somata.

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

  • Akasu T, Gallagher JP, Hirai K, Shinnick-Gallagher P (1986) Vasoactive intestinal polypeptide depolarizations in cat bladder parasympathetic ganglia. J Physiol 374:457–473

    Google Scholar 

  • Alm P, Alumets J, Håkanson R, Sundler F (1977) Peptidergic (vasoactive intestinal peptide) nerves in the genito-urinary tract. Neuroscience 2:751–754

    Google Scholar 

  • Ambache N, Zar AN (1970) Non-cholinergic transmission by postganglionic motor neurones in the mammalian bladder. J Physiol 210:761–783

    Google Scholar 

  • Andersson P-O, Bloom SR, Järhult J (1983) Colonic motor and vascular responses to pelvic nerve stimulation and their relation to local peptide release in the cat. J Physiol 334:293–307

    Google Scholar 

  • Blackman JG, Crowcroft PJ, Devine CE, Holman ME, Yonemura K (1969) Transmission from preganglionic fibres in the hypogastric nerve to peripheral ganglia of male guinea-pigs. J Physiol 201:723–743

    Google Scholar 

  • Blessing WW, Howe PRC, Joh TH, Oliver JR, Willoughby JO (1986) Distribution of tyrosine hydroxylase and neuropeptide Y-like immunoreactive neurons in rabbit medulla oblongata, with attention to colocalization studies, presumptive adrenaline-synthesizing perikarya, and vagal preganglionic cells. J Comp Neurol 248:285–300

    Google Scholar 

  • Brading AF, Mostwin JL (1989) Electrical and mechanical responses of guinea-pig bladder muscle to nerve stimulation. Br J Pharmacol 98:1083–1090

    Google Scholar 

  • Buchan AMJ, Sikora LKJ, Levy JG, McIntosh CHS, Dyck I, Brown JC (1985) An immunocytochemical investigation with monoclonal antibodies to somatostatin. Histochemistry 83:175–180

    Google Scholar 

  • Campbell G (1987) Cotransmission. Annu Rev Pharmacol Toxicol 27:51–70

    Google Scholar 

  • Costa M, Furness JB (1973) Observations on the anatomy and amine histochemistry of the nerves and ganglia which supply the pelvic viscera and on the associated chromaffin tissue in the guinea-pig. Z Anat Entwickl-Gesch 40:88–108

    Google Scholar 

  • Costa M, Furness JB, Gibbins IL (1986) Chemical coding of enteric neurons. Prog Brain Res 68:217–238

    Google Scholar 

  • Crowcroft PJ, Szurszewski JH (1971) A study of the inferior mesenteric and pelvic ganglia of guinea-pigs with intracellular electrodes. J Physiol 219:421–441

    Google Scholar 

  • Cuello AC, Milstein C, Couture R, Wright B, Priestley JV, Jarvis J (1984) Characterization and immunochemical application of monoclonal antibodies against enkephalins. J Histochem Cytochem 32:947–957

    Google Scholar 

  • Dail WG, Dziurzynski R (1985) Substance P immunoreactivity in the major pelvic ganglion of the rat. Anat Rec 212:103–108

    Google Scholar 

  • Dail WG, Hamill RW (1989) Parasympathetic nerves in penile erectile tissue of the rat contain choline acetyltransferase. Brain Res 487:165–170

    Google Scholar 

  • Dail WG, Evan AP, Eason HR (1975) The major pelvic ganglion in the pelvic plexus of the male rat: a histochemical and ultrastructural study. Cell Tissue Res 159:49–62

    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 

  • Dail WG, Manzanares K, Moll MA, Minorsky N (1985) The hypogastric nerve innervates a population of penile neurons in the pelvic plexus. Neuroscience 16:1014–1046

    Google Scholar 

  • Ekblad E, Håkanson R, Sundler F, Wahlestedt C (1985) Galanin: neuromodulatory and direct contractile effects on smooth muscle preparations. Br J Pharmacol 86:241–246

    Google Scholar 

  • Gillespie JS, Sheng H (1990) The effects of pyrogallol and hydroquinone on the response to NANC nerve stimulation in the rat anococcygeus and the bovine retractor penis muscles. Br J Pharmacol 99:194–196

    Google Scholar 

  • Gonella J, Bouvier M, Blanquet F (1987) Extrinsic nervous control of motility of small and large intestines and related sphincters. Physiol Rev 67:902–961

    Google Scholar 

  • Groat WC de, Booth AM (1980) Inhibition and facilitation in parasympathetic ganglia of the urinary bladder. Fed Proc 39:2990–2996

    Google Scholar 

  • Groat WC de, Kawatani M (1989) Enkephalinergic inhibition in parasympathetic ganglia of the urinary bladder of the cat. J Physiol 413:13–29

    Google Scholar 

  • Groat WC de, Saum WR (1972) Sympathetic inhibition of the urinary bladder and of pelvic ganglionic transmission in the cat. J Physiol 220:297–314

    Google Scholar 

  • Groat WC de, Steers WD (1988) Neural control of the urinary bladder and sexual organs: experimental studies in animals. In: Bannister R (ed) Autonomic failure. A textbook of clinical disorders of the autonomic nervous system, 2nd edn. Oxford University Press, Oxford, pp 196–222

    Google Scholar 

  • Hedlund H, Fandriks L, Delbro D, Fasth S (1985) On the transmission of sacral parasympathetic nervous influence on distal colonic and rectal motility in the cat. Acta Physiol Scand 125:225–234

    Google Scholar 

  • Hökfelt T, Schultzberg M, Elde R, Nilsson G, Terenius L, Said S, Goldstein M (1978) Peptide neurons in peripheral tissues including the urinary tract: immunohistochemical studies. Acta Pharmacol Toxicol 43:79–89

    Google Scholar 

  • Inyama CO, Hacker GW, Gu J, Dahl D, Bloom SR, Polak JM (1987) Cytochemical relationships in the paracervical ganglion (Frankenhauser) of rat studied by immunocytochemistry. Neurosci Lett 55:311–316

    Google Scholar 

  • Jänig W, McLachlan EM (1987) Organization of lumbar spinal outflow to distal colon and pelvic organs. Physiol Rev 67:1332–1404

    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, Lowe I, Booth AM, Groat WC de (1983) The presence of leucine-enkephalin in the sacral preganglionic pathways to the urinary bladder of the cat. Neurosci Lett 39:143–148

    Google Scholar 

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

    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 

  • Keast JR, Booth AM, Groat WC de (1989) Distribution of neurons in the major pelvic ganglion of the rat which supply the bladder, colon or penis. Cell Tissue Res 256:105–112

    Google Scholar 

  • Kumamoto E (1989) Synaptic potentials induced by postganglionic stimulation in cat bladder parasympathetic neurones. Pflügers Arch 414:235–244

    Google Scholar 

  • Langley JN, Anderson HK (1896) The innervation of the pelvic and adjoining viscera. J Physiol 20:372–406

    Google Scholar 

  • Langworthy OR (1965) Innervation of the pelvic organs of the rat. Invest Urol 2:491–511

    Google Scholar 

  • Li CG, Rand MJ (1989) Evidence for a role of nitric oxide in the neurotransmitter system mediating relaxation of the rat anococcygeus muscle. Clin Exp Physiol Pharmacol 16:933–938

    Google Scholar 

  • Mattiasson A, Ekblad E, Sundler F, Uvelius B (1985) Origin and distribution of neuropeptideY-, vasoactive intestinal polypeptide-and substance P-containing nerve fibres in the urinary bladder of the rat. Cell Tissue Res 239:141–146

    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 

  • Morris JL, Gibbins IL (1989) Co-localization and plasticity of transmitters in peripheral autonomic and sensory neurons. Int J Dev Neurosci 7:521–531

    Google Scholar 

  • Papka RE, Traurig HH (1989) Galanin-immunoreactive nerves in the female rat paracervical ganglion and uterine cervix: distribution and reaction to capsaicin. Cell Tissue Res 257:41–51

    Google Scholar 

  • Papka RE, Cotton JP, Traurig HH (1985) Comparative distribution of neuropeptide tyrosine, vasoactive intestinal polypeptide-, substance P-IR, acetylcholinesterase-positive and noradrenergic nerves in the reproductive tract of the female rat. Cell Tissue Res 242:475–490

    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 179:243–252

    Google Scholar 

  • Partanen M, Hervonen A (1979) The formaldehyde-induced fluorescence of the developing hypogastric (main pelvic) ganglion of the rat. Short adrenergic neurons and the effect of testosterone. Histochemistry 62:249–258

    Google Scholar 

  • Purinton PT, Fletcher TF, Bradley WE (1973) Gross and light microscopic features of the pelvic plexus in the rat. Anat Rec 175:697–706

    Google Scholar 

  • Schultzberg M, Hökfelt T, Nilsson G, Terenius L, Rehfeld JF, Brown M, Elfvin LG, Elde R, Goldstein M, Said S (1980) Distribution of peptide- and catecholamine-containing neurons in the gastro-intestinal tract of rat and guinea-pig: immunohistochemical studies with antisera to substance P, vasoactive intestinal polypeptide, enkephalins, somatostatin, gastrin/cholecystokinin, neurotensin and dopamine-β-hydroxylase. Neuroscience 5:689–744

    Google Scholar 

  • Senba E, Tohyama M (1988) Calcitonin gene-related peptide containing autonomic efferent pathways to the pelvic ganglia of the rat. Brain Res 449:386–390

    Google Scholar 

  • Senba E, Yanaihara C, Yanaihara N, Tohyama M (1989) Proenkephalin opioid peptide product in the sensory ganglia of the rat: a developmental immunohistochemical study. Dev Brain Res 48:263–271

    Google Scholar 

  • Tabatabai M, Booth AM, Groat WC de (1986) Morphological and electrophysiological properties of pelvic ganglion cells in the rat. Brain Res 283:61–70

    Google Scholar 

  • Wang B-R, Senba E, Tohyama M (1990) Met5-enkephalin-Arg6-Gly7-Leu8-like immunoreactivity in the pelvic ganglion of the male rat: a light and electron microscopic study. J Comp Neurol 293:26–36

    Google Scholar 

  • Wessendorf MW, Appel NM, Molitor TW, Elde RP (1990) A method for immunofluorescent demonstration of three coexisting neurotransmitters in rat brain and spinal cord, using the fluorophores fluorescein, lissamine rhodamine, and 7-amino-4-methylcoumarin-3-acetic acid. J Histochem Cytochem 38:1859–1877

    Google Scholar 

  • Wozniak W, Skowronska U (1967) Comparative anatomy of pelvic plexus in cat, dog, rabbit, macaque and man. Anat Anz 120:457–473

    Google Scholar 

  • Yuri K (1990) Immunohistochemical and enzyme histochemical localization of peptidergic, aminergic and cholinergic nerve fibres in the rat seminal vesicle. J Urol 143:194–198

    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. 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 (1991). https://doi.org/10.1007/BF00318197

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00318197

Key words

Navigation