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. 1991 Jun;176:197–210.

Specific patterns of immunoreactivity in neuronal elements of the anterior major pelvic ganglion of the male guinea-pig.

D Dhami 1, B S Mitchell 1
PMCID: PMC1260325  PMID: 1680842

Abstract

The anterior major pelvic ganglion (AMPG) of the male guinea-pig has been found to consist of three principal components. The presence of a cholinergic component was determined by the demonstration of cytoplasmic and nerve fibre acetylcholinesterase activity. A noradrenergic component was demonstrated by immunoreactivity (IR) of the catecholamine-synthesising enzymes tyrosine hydroxylase (TH) and dopamine-beta-hydroxylase (DBH) in neuronal perikarya. The AMPG also had a peptidergic component which may or may not sub-classify the cholinergic and noradrenergic components. Neuropeptide Y (NPY)-, vasoactive intestinal peptide (VIP)-, and atrial natriuretic factor (ANF)-immunoreactivities were seen in neuronal perikarya, nerve fibres and nerve terminals/varicosities, while somatostatin (SOM)-IR was restricted to neuronal perikarya. Substance P (SP)-IR was present in a dense network of varicose nerve fibres. However, on a rare occasion SP-IR was observed in neuronal perikarya. Enkephalin (ENK)-IR occurred in a sparsely distributed plexus of varicose nerve fibres. The analysis of adjacent serial sections demonstrated distinct patterns of neuropeptide coexistence in AMPG neurons. NPY-IR was colocalised to a subpopulation of TH-IR neuronal perikarya. NPY-IR was also colocalised with VIP-IR in non-TH-IR neuronal perikarya. VIP-IR occurred together with AChE in particular neuronal perikarya. The relationship between immunoreactive neuronal perikarya and immunoreactive nerve terminals was investigated. SP-IR nerve terminals were closely related to neuronal perikarya exhibiting VIP-, NPY-, or TH-IR. TH-IR neuronal perikarya were also abutted by ENK-IR nerve terminals. VIP- and NPY-immunoreactive neuronal perikarya were abutted by two nerve terminal types: one immunoreactive for VIP, the other for NPY. DBH-IR neuronal perikarya received AChE-positive varicosities while AChE-positive neurons were abutted by DBH-IR varicose nerve fibres. AChE-positive varicosities were also closely related to neuronal perikarya possessing VIP-IR and AChE activity.

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  1. Allen J. M., Gjörstrup P., Björkman J. A., Ek L., Abrahamsson T., Bloom S. R. Studies on cardiac distribution and function of neuropeptide Y. Acta Physiol Scand. 1986 Mar;126(3):405–411. doi: 10.1111/j.1748-1716.1986.tb07834.x. [DOI] [PubMed] [Google Scholar]
  2. Alm P., Alumets J., Håkanson R., Sundler F. Peptidergic (vasoactive intestinal peptide) nerves in the genito-urinary tract. Neuroscience. 1977;2(5):751–754. doi: 10.1016/0306-4522(77)90028-8. [DOI] [PubMed] [Google Scholar]
  3. Baumgarten H. G., Holstein A. F., Owman C. Auerbach's plexus of mammals and man: electron microscopic identification of three different types of neuronal processes in myenteric ganglia of the large intestine from rhesus monkeys, guinea-pigs and man. Z Zellforsch Mikrosk Anat. 1970;106(3):376–397. doi: 10.1007/BF00335780. [DOI] [PubMed] [Google Scholar]
  4. Bell C., McLean J. R. Localization of norepinephrine and acetylcholinesterase in separate neurons supplying the guinea-pig vas deferens. J Pharmacol Exp Ther. 1967 Jul;157(1):69–73. [PubMed] [Google Scholar]
  5. Birmingham A. T. The potentiation by anticholinesterase drugs of the responses of the guinea-pig isolated vas deferens to alternate preganglionic and postganglionic stimulation. Br J Pharmacol Chemother. 1966 May;27(1):145–156. doi: 10.1111/j.1476-5381.1966.tb01650.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Burnstock G. Autonomic neuromuscular junctions: current developments and future directions. J Anat. 1986 Jun;146:1–30. [PMC free article] [PubMed] [Google Scholar]
  7. Burnstock G., Cocks T., Crowe R., Kasakov L. Purinergic innervation of the guinea-pig urinary bladder. Br J Pharmacol. 1978 May;63(1):125–138. doi: 10.1111/j.1476-5381.1978.tb07782.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chesher G. B., Thorp R. H. The atropine-resistance of the response to intrinsic nerve stimulation of the guinea-pig bladder. Br J Pharmacol Chemother. 1965 Oct;25(2):288–294. doi: 10.1111/j.1476-5381.1965.tb02049.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Costa M., Funess J. B. 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 Entwicklungsgesch. 1973 May 30;140(1):85–108. doi: 10.1007/BF00520720. [DOI] [PubMed] [Google Scholar]
  10. Crowcroft P. J., Szurszewski J. H. A study of the inferior mesenteric and pelvic ganglia of guinea-pigs with intracellular electrodes. J Physiol. 1971 Dec;219(2):421–441. doi: 10.1113/jphysiol.1971.sp009670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dail W. G., Dziurzynski R. Substance P immunoreactivity in the major pelvic ganglion of the rat. Anat Rec. 1985 May;212(1):103–109. doi: 10.1002/ar.1092120115. [DOI] [PubMed] [Google Scholar]
  12. Dail W. G., Evan A. P., Eason H. R. The major ganglion in the pelvic plexus of the male rat: a histochemical and ultrastructural study. Cell Tissue Res. 1975 May 27;159(1):49–62. doi: 10.1007/BF00231994. [DOI] [PubMed] [Google Scholar]
  13. Dail W. G., Trujillo D., de la Rosa D., Walton G. Autonomic innervation of reproductive organs: analysis of the neurons whose axons project in the main penile nerve in the pelvic plexus of the rat. Anat Rec. 1989 May;224(1):94–101. doi: 10.1002/ar.1092240112. [DOI] [PubMed] [Google Scholar]
  14. Ekblad E., Edvinsson L., Wahlestedt C., Uddman R., Håkanson R., Sundler F. Neuropeptide Y co-exists and co-operates with noradrenaline in perivascular nerve fibers. Regul Pept. 1984 Apr;8(3):225–235. doi: 10.1016/0167-0115(84)90064-8. [DOI] [PubMed] [Google Scholar]
  15. Furness J. B., Costa M., Keast J. R. Choline acetyltransferase- and peptide immunoreactivity of submucous neurons in the small intestine of the guinea-pig. Cell Tissue Res. 1984;237(2):329–336. doi: 10.1007/BF00217152. [DOI] [PubMed] [Google Scholar]
  16. Furness J. B., Costa M. Types of nerves in the enteric nervous system. Neuroscience. 1980;5(1):1–20. doi: 10.1016/0306-4522(80)90067-6. [DOI] [PubMed] [Google Scholar]
  17. Gamse R., Wax A., Zigmond R. E., Leeman S. E. Immunoreactive substance P in sympathetic ganglia: distribution and sensitivity towards capsaicin. Neuroscience. 1981;6(3):437–441. doi: 10.1016/0306-4522(81)90136-6. [DOI] [PubMed] [Google Scholar]
  18. Grube D. Immunoreactivities of gastrin (G-) cells. II. Non-specific binding of immunoglobulins to G-cells by ionic interactions. Histochemistry. 1980;66(2):149–167. doi: 10.1007/BF00494642. [DOI] [PubMed] [Google Scholar]
  19. Grunditz T., Ekman R., Håkanson R., Sundler F., Uddman R. Neuropeptide Y and vasoactive intestinal peptide coexist in rat thyroid nerve fibers emanating from the thyroid ganglion. Regul Pept. 1988 Nov;23(2):193–208. doi: 10.1016/0167-0115(88)90027-4. [DOI] [PubMed] [Google Scholar]
  20. Heym C., Reinecke M., Weihe E., Forssmann W. G. Dopamine-beta-hydroxylase-, neurotensin-, substance P-, vasoactive intestinal polypeptide- and enkephalin-immunohistochemistry of paravertebral and prevertebral ganglia in the cat. Cell Tissue Res. 1984;235(2):411–418. doi: 10.1007/BF00217867. [DOI] [PubMed] [Google Scholar]
  21. Hill C. E., Hendry I. A. Development of neurons synthesizing noradrenaline and acetylcholine in the superior cervical ganglion of the rat in vivo and in vitro. Neuroscience. 1977;2(5):741–749. doi: 10.1016/0306-4522(77)90027-6. [DOI] [PubMed] [Google Scholar]
  22. Hökfelt T., Elfvin L. G., Elde R., Schultzberg M., Goldstein M., Luft R. Occurrence of somatostatin-like immunoreactivity in some peripheral sympathetic noradrenergic neurons. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3587–3591. doi: 10.1073/pnas.74.8.3587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hökfelt T., Johansson O., Ljungdahl A., Lundberg J. M., Schultzberg M. Peptidergic neurones. Nature. 1980 Apr 10;284(5756):515–521. doi: 10.1038/284515a0. [DOI] [PubMed] [Google Scholar]
  24. Hökfelt T., Millhorn D., Seroogy K., Tsuruo Y., Ceccatelli S., Lindh B., Meister B., Melander T., Schalling M., Bartfai T. Coexistence of peptides with classical neurotransmitters. Experientia. 1987 Jul 15;43(7):768–780. doi: 10.1007/BF01945354. [DOI] [PubMed] [Google Scholar]
  25. Inyama C. O., Hacker G. W., Gu J., Dahl D., Bloom S. R., Polak J. M. Cytochemical relationships in the paracervical ganglion (Frankenhäuser) of rat studied by immunocytochemistry. Neurosci Lett. 1985 Apr 19;55(3):311–316. doi: 10.1016/0304-3940(85)90454-9. [DOI] [PubMed] [Google Scholar]
  26. Jacobowitz D., Woodward J. K. Adrenergic neurons in the cat superior cervical ganglion and cervical sympathetic nerve trunk. A histochemical study. J Pharmacol Exp Ther. 1968 Aug;162(2):213–226. [PubMed] [Google Scholar]
  27. KARNOVSKY M. J., ROOTS L. A "DIRECT-COLORING" THIOCHOLINE METHOD FOR CHOLINESTERASES. J Histochem Cytochem. 1964 Mar;12:219–221. doi: 10.1177/12.3.219. [DOI] [PubMed] [Google Scholar]
  28. Kawatani M., Lowe I. P., Booth A. M., Backes M. G., Erdman S. L., De Groat W. C. The presence of leucine-enkephalin in the sacral preganglionic pathway to the urinary bladder of the cat. Neurosci Lett. 1983 Aug 29;39(2):143–148. doi: 10.1016/0304-3940(83)90067-8. [DOI] [PubMed] [Google Scholar]
  29. Keast J. R., Booth A. M., de Groat W. C. Distribution of neurons in the major pelvic ganglion of the rat which supply the bladder, colon or penis. Cell Tissue Res. 1989 Apr;256(1):105–112. doi: 10.1007/BF00224723. [DOI] [PubMed] [Google Scholar]
  30. Keast J. R., de Groat W. C. Immunohistochemical characterization of pelvic neurons which project to the bladder, colon, or penis in rats. J Comp Neurol. 1989 Oct 15;288(3):387–400. doi: 10.1002/cne.902880303. [DOI] [PubMed] [Google Scholar]
  31. Lundberg J. M., Terenius L., Hökfelt T., Martling C. R., Tatemoto K., Mutt V., Polak J., Bloom S., Goldstein M. Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects of NPY on sympathetic function. Acta Physiol Scand. 1982 Dec;116(4):477–480. doi: 10.1111/j.1748-1716.1982.tb07171.x. [DOI] [PubMed] [Google Scholar]
  32. MERRILLEES N. C., BURNSTOCK G., HOLMAN M. E. CORRELATION OF FINE STRUCTURE AND PHYSIOLOGY OF THE INNERVATION OF SMOOTH MUSCLE IN THE GUINEA PIG VAS DEFERENS. J Cell Biol. 1963 Dec;19:529–550. doi: 10.1083/jcb.19.3.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Macrae I. M., Furness J. B., Costa M. Distribution of subgroups of noradrenaline neurons in the coeliac ganglion of the guinea-pig. Cell Tissue Res. 1986;244(1):173–180. doi: 10.1007/BF00218395. [DOI] [PubMed] [Google Scholar]
  34. Matthews M. R., Cuello A. C. Substance P-immunoreactive peripheral branches of sensory neurons innervate guinea pig sympathetic neurons. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1668–1672. doi: 10.1073/pnas.79.5.1668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mitchell B. S., Stauber V. V. Morphological, histochemical and immunohistological studies of the paracervical ganglion in prepubertal, pregnant and adult, non-pregnant guinea-pigs. J Anat. 1990 Oct;172:177–189. [PMC free article] [PubMed] [Google Scholar]
  36. Morris J. L., Gibbins I. L., Campbell G., Murphy R., Furness J. B., Costa M. Innervation of the large arteries and heart of the toad (Bufo marinus) by adrenergic and peptide-containing neurons. Cell Tissue Res. 1986;243(1):171–184. doi: 10.1007/BF00221866. [DOI] [PubMed] [Google Scholar]
  37. Morris J. L., Gibbins I. L. Neuronal colocalization of peptides, catecholamines, and catecholamine-synthesizing enzymes in guinea pig paracervical ganglia. J Neurosci. 1987 Oct;7(10):3117–3130. doi: 10.1523/JNEUROSCI.07-10-03117.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Ottesen B., Fahrenkrug J. Effect of vasoactive intestinal polypeptide (VIP) upon myometrial blood flow in non-pregnant rabbit. Acta Physiol Scand. 1981 Jun;112(2):195–201. doi: 10.1111/j.1748-1716.1981.tb06804.x. [DOI] [PubMed] [Google Scholar]
  39. Papka R. E., Traurig H. H., Wekstein M. Localization of peptides in nerve terminals in the paracervical ganglion of the rat by light and electron microscopic immunohistochemistry: enkephalin and atrial natriuretic factor. Neurosci Lett. 1985 Nov 11;61(3):285–290. doi: 10.1016/0304-3940(85)90478-1. [DOI] [PubMed] [Google Scholar]
  40. Schultzberg M., Hökfelt T., Terenius L., Elfvin L. G., Lundberg J. M., Brandt J., Elde R. P., Goldstein M. Enkephalin immunoreactive nerve fibres and cell bodies in sympathetic ganglia of the guinea-pig and rat. Neuroscience. 1979;4(2):249–270. doi: 10.1016/0306-4522(79)90087-3. [DOI] [PubMed] [Google Scholar]
  41. Snyder S. H., Innis R. B. Peptide neurotransmitters. Annu Rev Biochem. 1979;48:755–782. doi: 10.1146/annurev.bi.48.070179.003543. [DOI] [PubMed] [Google Scholar]
  42. Tenmoku S., Ottesen B., O'Hare M. M., Sheikh S., Bardrum B., Hansen B., Walker B., Murphy R. F., Schwartz T. W. Interaction of NPY and VIP in regulation of myometrial blood flow and mechanical activity. Peptides. 1988 Mar-Apr;9(2):269–275. doi: 10.1016/0196-9781(88)90259-8. [DOI] [PubMed] [Google Scholar]
  43. Wakade A. R., Kirpekar S. M. Chemical and histochemical studies on the sympathetic innervation of the vas deferens and seminal vesicle of the guinea pig. J Pharmacol Exp Ther. 1971 Sep;178(3):432–441. [PubMed] [Google Scholar]
  44. Watanabe H. Adrenergic nerve elements in the hypogastric ganglion of the guinea pig. Am J Anat. 1971 Mar;130(3):305–313. doi: 10.1002/aja.1001300305. [DOI] [PubMed] [Google Scholar]
  45. Yokota R., Burnstock G. Synaptic organisation of the pelvic ganglion in the guinea-pig. Cell Tissue Res. 1983;232(2):379–397. doi: 10.1007/BF00213794. [DOI] [PubMed] [Google Scholar]

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