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Catecholaminergic projections onto spinal neurons destined to the pelvis including the penis in rat

International Journal of Impotence Research volume 14, pages 151–166 (2002)Cite this article

Abstract

In rats, the spinal cord contains proerectile autonomic motoneurons destined to the penile tissue and its vasculature, and somatic motoneurons destined to the perineal striated muscles. It receives dense catecholaminergic projections issued from the medulla and pons. In adult male rats, we evidenced the catecholaminergic innervation of spinal neurons controlling lower urogenital tissues and regulating penile erection. We combined retrograde tracing techniques and immunohistochemistry against synthetic enzymes of noradrenaline and adrenaline. Both sympathetic and parasympathetic preganglionic neurons, labeled from the major pelvic ganglion or from the corpus cavernosum, were apposed by catecholaminergic immunoreactive fibers. Motoneurons, retrogradely labeled from the striated muscles, were also apposed by catecholaminergic immunoreactive fibers. Synapses between these motoneurons and fibers were suggested by confocal microscopy and confirmed by electron microscopy in some cases. The results reinforce the hypothesis of a catecholaminergic control of autonomic and somatic motoneurons regulating penile erection at the spinal level.

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References

  1. DeGroat WC, Booth AM . Neural control of penile erection In: Maggi CA (ed) The autonomic nervous system, nervous control of the urogenital system Vol 3: Harwood Academic Publishers: London 1993 467–524

    Google Scholar 

  2. Hancock MB, Peveto CA . Preganglionic neurons in the sacral spinal cord of the rat: an HRP study Neurosci Lett 1979 11: 1–5

    Article  CAS  Google Scholar 

  3. Nadelhaft I, Booth AM . The location and morphology of preganglionic neurons and the distribution of visceral afferents from the rat pelvic nerve: a horseradish peroxidase study J Comp Neurol 1984 226: 238–245

    Article  CAS  Google Scholar 

  4. Giuliano F et al. Evidence of sympathetic fibers in the male rat pelvic nerve by gross anatomy, retrograde labeling and high resolution autoradiographic study Int J Impot Res 1997 9: 179–185

    Article  CAS  Google Scholar 

  5. Hancock MB, Peveto CA . A preganglionic autonomic nucleus in the dorsal gray commissure of the lumbar spinal cord of the rat J Comp Neurol 1979 183: 65–72

    Article  CAS  Google Scholar 

  6. McKenna KE, Nadelhaft I . Pudendal nerve reflexes in the male and female rat Soc Neurosci Abstr 1985 11: 701

    Google Scholar 

  7. Langworthy OR . Innervation of the pelvic organs of the rat Invest Urol 1965 2: 491

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  9. McKenna KE, Nadelhaft I . The organization of the pudendal nerve in the male and female rat J Comp Neurol 1986 248: 532–549

    Article  CAS  Google Scholar 

  10. Schroder HD . Organization of the motoneurons innervating the pelvic muscles of the male rat J Comp Neurol 1980 192: 567–587

    Article  CAS  Google Scholar 

  11. Glazer EJ, Ross LL . Localization of noradrenergic terminals in sympathetic preganglionic nuclei of the rat: demonstration by immunocytochemical localization of dopamine-beta-hydroxylase Brain Res 1980 185: 39–49

    Article  CAS  Google Scholar 

  12. Westlund KN, Bowker RM, Ziegler MG, Coulter JD . Noradrenergic projections to the spinal cord of the rat Brain Res 1983 263: 15–31

    Article  CAS  Google Scholar 

  13. Kojima M et al. Characteristic distribution of noradrenergic terminals on the anterior horn motoneurons innervating the perineal striated muscles in the rat. An immuno-electromicroscopic study Anat Embryol (Berl) 1985 171: 267–273

    Article  CAS  Google Scholar 

  14. Ross CA et al. Adrenaline neurons in the rostral ventrolateral medulla innervate thoracic spinal cord: a combined immunocytochemical and retrograde transport demonstration Neurosci Lett 1981 25: 257–262

    Article  CAS  Google Scholar 

  15. Hökfelt T, Fuxe K, Goldstein M, Johansson O . Immunohistochemical evidence for the existence of adrenaline neurons in the rat brain Brain Res 1974 66: 235–251

    Article  Google Scholar 

  16. Kohno J et al. Interaction between adrenergic fibers and intermediate cholinergic neurons in the rat spinal cord: a new double-immunostaining method for correlated light and electron microscopic observations Neuroscience 1988 25: 113–121

    Article  CAS  Google Scholar 

  17. Ross CA et al. Rostral ventrolateral medulla: selective projections to the thoracic autonomic cell column from the region containing C1 adrenaline neurons J Comp Neurol 1984 228: 168–185

    Article  CAS  Google Scholar 

  18. Kohno J et al. Direct adrenergic inputs to sacral autonomic neurons: using a double-immunostaining method at the light and electron microscopic levels Brain Res 1988 461: 1581–1562

    Article  Google Scholar 

  19. Molander C, Xu Q, Grant G . The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord J Comp Neurol 1984 230: 133–141

    Article  CAS  Google Scholar 

  20. Dail WG, 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 224: 94–101

    Article  CAS  Google Scholar 

  21. Nadelhaft I, McKenna KE . Sexual dimorphism in sympathetic preganglionic neurons of the rat hypogastric nerve J Comp Neurol 1987 256: 308–315

    Article  CAS  Google Scholar 

  22. Neuhuber W . The central projections of visceral primary afferent neurons of the inferior mesenteric plexus and hypogastric nerve and the location of the related sensory and preganglionic sympathetic cell bodies in the rat Anat Embryol 1982 164: 413–425

    Article  CAS  Google Scholar 

  23. Marson L, Platt KB, McKenna KE . Central nervous system innervation of the penis as revealed by the transneuronal transport of pseudorabies virus Neuroscience 1993 55: 263–280

    Article  CAS  Google Scholar 

  24. Veronneau-Longueville F et al. Oxytocinergic innervation of autonomic nuclei controlling penile erection in the rat Neuroscience 1999 93: 1437–1447

    Article  CAS  Google Scholar 

  25. Carlsson A, Falck B, Fuxe K, Hillarp NA . Cellular localisation of monoamines in the spinal cord Acta Physiol Scand 1964 60: 112–119

    Article  CAS  Google Scholar 

  26. Westlund KN, Bowker RM, Ziegler MG, Coulter JD . Descending noradrenergic projections and their spinal terminations Prog Brain Res 1982 57: 219–238

    Article  CAS  Google Scholar 

  27. Fritschy JM et al. Distribution of locus coeruleus axons in the rat spinal cord: a combined anterograde transport and immunohistochemical study Brain Res 1987 437: 176–180

    Article  CAS  Google Scholar 

  28. Fritschy JM, Grzanna R . Demonstration of two separate descending noradrenergic pathways to the rat spinal cord: evidence for an intragriseal trajectory of locus coeruleus axons in the superficial layers of the dorsal horn J Comp Neurol 1990 291: 553–582

    Article  CAS  Google Scholar 

  29. Tillet Y, Thibault J, Dubois MP . Immunocytochemical demonstration of the presence of catecholamine and serotonin neurons in the sheep olfactory bulb Neuroscience 1987 20: 1011–1022

    Article  CAS  Google Scholar 

  30. Anderson CR, McLachlan EM, Srb-Christie O . Distribution of sympathetic preganglionic neurons and monoaminergic nerve terminals in the spinal cord of the rat J Comp Neurol 1989 283: 269–284

    Article  CAS  Google Scholar 

  31. Rajaofetra N et al. Immunocytochemical mapping of noradrenergic projections to the rat spinal cord with an antiserum against noradrenaline J Neurocytol 1992 21: 481–494

    Article  CAS  Google Scholar 

  32. Rajaofetra N et al. Serotoninergic, noradrenergic, and peptidergic innervation of Onuf's nucleus of normal and transected spinal cords of baboons (Papio papio) J Comp Neurol 1992 318: 1–17

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  34. Giuliano F, Rampin O, Bernabe J, Rousseau JP . Neural control of penile erection in the rat J Auton Nerv Syst 1995 55: 36–44

    Article  CAS  Google Scholar 

  35. Clark JT, Smith ER, Davidson JM . Evidence for the modulation of sexual behavior by alpha-adrenoceptors in male rats Neuroendocrinology 1985 41: 43

    Article  Google Scholar 

  36. Clark JT . Suppression of copulatory behavior in male rats following central administration of clonidine Neuropharmacology 1991 30: 373–382

    Article  CAS  Google Scholar 

  37. Clark JT, Smith ER, Davidson JM . Enhancement of sexual moti-vation in male rats by yohimbine Science 1984 225: 847–849

    Article  CAS  Google Scholar 

  38. Hemandez Gonzalez M et al. Effects of intrathecal administration of adrenergic agonists on the frequency of copulatory pelvic thrusting of the male rat Arch Med Res 1994 25: 419–425

    Google Scholar 

  39. Clark JT, Smith ER . Clonidine suppresses copulatory behavior and erectile reflexes in male rats: lack of effect of naloxone pretreatment Neuroendocrinology 1990 51: 357–364

    Article  CAS  Google Scholar 

  40. Smith ER, Lee RL, Schnur SL, Davidson JM . Alpha 2-adrenoceptor antagonists and male sexual behavior: II. Erectile and ejaculatory reflexes Physiol Behav 1987 41: 15–19

    Article  CAS  Google Scholar 

  41. Smith ER et al. The inhibitory effects of propranolol on genital reflexes in male rats Pharmacol Biochem Behav 1995 52: 541–546

    Article  CAS  Google Scholar 

  42. McIntosh TK, Barfield RJ . Brain monoaminergic control of male reproductive behavior: III. Norepinephrine and the post-ejaculatory refractory period Behav Brain Res 1984 12: 275–281

    Article  CAS  Google Scholar 

  43. Stefanick ML, Smith ER, Szumowski DA, Davidson JM . Reproductive physiology and behavior in the male rat following acute and chronic peripheral adrenergic depletion by guanethidine Pharmacol Biochem Behav 1985 23: 55–63

    Article  CAS  Google Scholar 

  44. Roussel B, Pujol JF, Jouvet M . Effects of lesions in the pontine tegmentum on the sleep stages in the rat Arch Ital Biol 1976 114: 188–209

    CAS  PubMed  Google Scholar 

  45. Gajewski J, Downie JW, Awad SA . Experimental evidence for a central nervous system site of action in the effect of alpha-adrenergic blockers on the external urinary sphincter J Urol 1984 132: 403–409

    Article  CAS  Google Scholar 

  46. Downie JW, Bialik GJ . Evidence for a spinal site of action of clonidine on somatic and viscerosomatic reflex activity evoked on the pudendal nerve in cats J Pharmacol Exp Ther 1988 246: 352–358

    CAS  PubMed  Google Scholar 

  47. Danuser H, Thor KB . Inhibition of central sympathetic and somatic outflow to the lower urinary tract of the cat by the alpha 1 adrenergic receptor antagonist prazosin J Urol 1995 153: 1308–1312

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The contribution of the Institut Cochin de Génétique Moléculaire for providing confocal laser scanning microscope assistance is gratefully acknowledged. This work was supported in part by a grant from Association Française d'Urologie (AFU) 1997–1998 to FG.

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Authors and Affiliations

  1. Groupe de Recherche en Urologie, UPRES EA 1602, Faculté de Médecine Paris-Sud, Le Kremlin-Bicêtre, France

    E D Yaïci, Y Tang, G Benoit & F Giuliano

  2. Laboratoire de Neurobiologie des Fonctions Végétatives, Bâtiment 325, Institut National de la Recherche Agronomique, Jouy-en-Josas Cedex, France

    O Rampin

  3. Laboratoire de Neurobiologie des Signaux Intercellulaires, Institut des Neurosciences, CNRS UMR 7624, Université Pierre et Marie Curie, Paris, France

    A Calas

  4. Laboratoire de Biologie Moléculaire, Agence Française de Sécurité Sanitaire des Aliments, Ploufragan, France

    A Jestin

  5. IFR INSERM, CHU de Bicêtre, Le Kremlin-Bicêtre, France

    P Leclerc

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  1. E D Yaïci
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Correspondence to F Giuliano.

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Yaïci, E., Rampin, O., Tang, Y. et al. Catecholaminergic projections onto spinal neurons destined to the pelvis including the penis in rat. Int J Impot Res 14, 151–166 (2002). https://doi.org/10.1038/sj.ijir.3900809

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