Dopamine-oxytocin interactions in penile erection

European Journal of Neuroscience

Volumn 30, Issue 11, 2009, Pages 2151-2164

  Baskerville, T A ^a,c   Allard, J ^b   Wayman, C ^b   Douglas, A J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b PFIZER GLOBAL RESEARCH AND DEVELOPMENT   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Fos expression; Intracavernous pressure; Magnocellular neurons; Medial preoptic area; Paraventricular nucleus; Supraoptic nucleus

Indexed keywords

APOMORPHINE; DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; DOPAMINE 4 RECEPTOR; NAFADOTRIDE; OXYTOCIN; OXYTOCIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MALE; MASCULINITY; MEDIAL PREOPTIC AREA; NONHUMAN; PENIS ERECTION; PRIORITY JOURNAL; RAT; SEXUAL BEHAVIOR; SUPRAOPTIC NUCLEUS; THALAMUS MIDLINE NUCLEUS;

ANIMALS; APOMORPHINE; BLOOD PRESSURE; DOPAMINE; DOPAMINE AGONISTS; DOPAMINE ANTAGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; HORMONE ANTAGONISTS; INJECTIONS, INTRAVENTRICULAR; MALE; OXYTOCIN; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PENILE ERECTION; PREOPTIC AREA; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE; RECEPTORS, OXYTOCIN; SEXUAL BEHAVIOR, ANIMAL; SPINAL CORD; STATISTICS, NONPARAMETRIC;

EID: 71249131311     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.06999.x     Document Type: Article

References (55)

1. Allard, J. Giuliano, F. (2001) Central nervous system agents in the treatment of erectile dysfunction: how do they work?. Curr Urol Rep., 2, 488 494.
2. 2 receptor agonist. Life Sci., 52, 1301 1309.
3. Argiolas, A. Melis, M.R. (2004) The role of oxytocin and the paraventricular nucleus in the sexual behaviour of male mammals. Physiol. Behav., 83, 309 317.
4. Argiolas, A. Melis, M.R. (2005) Central control of penile erection: role of the paraventricular nucleus of the hypothalamus. Prog. Neurobiol., 76, 1 21.
5. Argiolas, A., Collu, M., D'Aquila, P., Gessa, G.L., Melis, M.R. Serra, G. (1989) Apomorphine stimulation of male copulatory behavior is prevented by the oxytocin antagonist d(CH2)5 Tyr(Me)-Orn8-vasotocin in rats. Pharmacol. Biochem. Behav., 33, 81 83.
6. 4 receptor-mediated presynaptic inhibition of GABAergic transmission in the rat supraoptic nucleus. J. Neurophysiol., 90, 559 565. (Pubitemid 37092541)
7. Baskerville, T.A. Douglas, A.J. (2008) Interactions between dopamine and oxytocin in the control of sexual behaviour. Prog. Brain Res., 170, 277 290.
8. 4 receptor signaling in the rat paraventricular hypothalamic nucleus: evidence of natural coupling involving immediate early gene induction and mitogen activated protein kinase phosphorylation. Neuropharmacology, 50, 521 531.
9. Bjorklund, A., Lindvall, O. Nobin, A. (1975) Evidence of an incerto-hypothalamic dopamine neurone system in the rat. Brain Res., 89, 29 42.
10. Bloch, G.J., Eckersell, C. Mills, R. (1993) Distribution of galanin-immunoreactive cells within sexually dimorphic components of the medial preoptic area of the male and female rat. Brain Res., 620, 259 268.
11. Bloch, G.J., Butler, P.C., Eckersell, C.B. Mills, R.H. (1998) Gonadal steroid-dependent GAL-IR cells within the medial preoptic nucleus (MPN) and the stimulatory effects of GAL within the MPN on sexual behaviors. Ann. N Y Acad. Sci., 863, 188 205.
12. Brioni, J.D., Moreland, R.B., Cowart, M., Hsieh, G.C., Stewart, A.O., Hedlund, P., Donnelly-Roberts, D.L., Nakane, M., Lynch, J.J., Kolasa, T., Polakowski, J.S., Osinski, M.A., Marsh, K., Andersson, K.E. Sullivan, J.P. (2004) Activation of dopamine D-4 receptors by ABT-724 induces penile erection in rats. Proc. Natl Acad. Sci. USA, 101, 6758 6763.
13. Brunton, P.J., Bales, J. Russell, J.A. (2006) Neuroendoctrine stress but not feeding responses to centrally administered neuropeptide Y are suppressed in pregnant rats. Endocrinology, 148, 3737 3745.
14. Buller, K.M., Crane, J.W., Spencer, S.J. Day, T.A. (2003) Systemic apomorphine alters HPA axis responses to interleukin-1 beta administration but not sound stress. Psychoneuroendocrinology, 28, 715 732.
15. 2 receptor agonist. J. Clin. Endocrinol. Metab., 75, 855 860.
16. Caquineau, C., Leng, G., Guan, X.M.M., Jiang, M., Van der Ploeg, L. Douglas, A.J. (2006) Effects of alpha-melanocyte-stimulating hormone on magnocellular oxytocin neurones and their activation at intromission in male rats. J. Neuroendocrinol., 18, 685 691.
17. Carmichael, M.S., Humbert, R., Dixen, J., Palmisano, G., Greenleaf, W. Davidson, J.M. (1987) Plasma oxytocin increases in the human sexual-response. J. Clin. Endocrinol. Metab., 64, 27 31.
18. Chen, K.K., Chan, J.Y.H. Chang, L.S. (1999) Dopaminergic neurotransmission at the paraventricular nucleus of hypothalamus in central regulation of penile erection in the rat. J. Urol., 162, 237 242.
19. Clément, P., Bernabé, J., Denys, P., Alexandre, L. Giuliano, F. (2007) Ejaculation induced by i.c.v. injection of the preferential dopamine D(3) receptor agonist 7-hydroxy-2-(di-N-propylamino)tetralin in anesthetized rats. Neuroscience, 145, 605 610.
20. Clément, P., Peeters, M., Bernabé, J., Denys, P., Alexandre, L. Giuliano, F. (2008) Brain oxytocin receptors mediate ejaculation elicited by 7-hydroxy-2-(di-N-propylamino) tetralin (7-OH-DPAT) in anaesthetized rats. Br. J. Pharmacol., 154, 1150 1159.
21. Decavel, C., Geffard, M. Calas, A. (1987) Comparative study of dopamine- and noradrenaline-immunoreactive terminals in the paraventricular and supraoptic nuclei of the rat. Neurosci. Lett., 77, 149 154.
22. Dennison, E., Bain, P.A., Bartke, A. Meliska, C.J. (1996) Systemically administered gonadotrophin-releasing hormone enhances copulatory behaviour in castrated, testosterone-treated hyperprolactinaemic male rats. Int. J. Androl., 19, 253 259.
23. 2 receptors in the paraventricular nucleus regulate genital responses and copulation in male-rats. Pharmacol. Biochem. Behav., 39, 177 181.
24. Giuliano, F., Bernabé, J., Rampin, O., Courtois, F., Benoit, G. Rousseau, J.P. (1994) Telemetric monitoring of intracavernous pressure in freely moving rats during copulation. J. Urol., 152, 271 274.
25. Giuliano, F., Bernabe, J., McKenna, K., Longueville, F. Rampin, O. (2001) Spinal proerectile effect of oxytocin in anesthetized rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 280, 1870 1877.
26. Hallbeck, M., Larhammar, D. Blomqvist, A. (2001) Neuropeptide expression in rat paraventricular hypothalamic neurons that project to the spinal cord. J. Comp. Neurol., 433, 222 238.
27. Heaton, J.P. (2000) Central neuropharmacological agents and mechanisms in erectile dysfunction: role of dopamine. Neurosci. Biobehav. Rev., 24, 561 569.
28. Hillegaart, V., Alster, P., Uvnäs-Moberg, K. Ahlenius, S. (1998) Sexual motivation promotes oxytocin secretion in male rats. Peptides, 19, 39 45.
29. Honda, K., Yanagimoto, M., Negoro, H., Narita, K., Murata, T. Higuchi, T. (1999) Excitation of oxytocin cells in the hypothalamic supraoptic nucleus by electrical stimulation of the dorsal penile nerve and tactile stimulation of the penis in the rat. Brain Res. Bull., 48, 309 313.
30. Hull, E.M. Dominguez, J.M. (2006) Getting his act together: roles of glutamate, nitric oxide and dopamine in the medial preoptic area. Brain Res., 1126, 66 75.
31. 3 agonist 7-hydroxy-N,N-di-n-propylaminotetralin hydrobromide into the hypothalamic medial preoptic area induced ejaculation in anesthetized rats. Neuroscience, 149, 636 641.
32. Liu, Y.C., Salamone, J.D. Sachs, B.D. (1997b) Lesions in medial preoptic area and bed nucleus of stria terminalis: differential effects on copulatory behavior and noncontact erection in male rats. J. Neurosci., 17, 5245 5253.
33. Martino, B., Hsieh, G.C., Hollingsworth, P.R., Mikusa, J.P., Moreland, R.B. Bitner, R.S. (2005) Central oxytocinergic and dopaminergic mechanisms regulating penile erection in conscious rats. Pharmacol. Biochem. Behav., 81, 797 804.
34. Mason, W.T. (1983) Excitation by dopamine of putative oxytocinergic neurones in the rat supraoptic nucleus in vitro: evidence for two classes of continuously firing neurones. Brain Res., 267, 113 121.
35. Melis, M.R., Argiolas, A. Gessa, G.L. (1987) Apomorphine-induced penile erection and yawning - site of action in brain. Brain Res., 415, 98 104.
36. Melis, M.R., Argiolas, A., Stancampiano, R. Gessa, G.L. (1990) Effect of apomorphine on oxytocin concentrations in different brain areas and plasma of male rats. Eur. J. Pharmacol., 182, 101 107.
37. Melis, M.R., Succu, S., Iannucci, U. Argiolas, A. (1997) Oxytocin increases nitric oxide production in the paraventricular nucleus of the hypothalamus of male rats: correlation with penile erection and yawning. Regul. Pept., 69, 105 111.
38. Melis, M.R., Succu, S., Mascia, M.S., Cortis, L. Argiolas, A. (2003) Extra-cellular dopamine increases in the paraventricular nucleus of male rats during sexual activity. Eur. J. Neurosci., 17, 1266 1272.
39. Melis, M.R., Succu, S., Mascia, M.S. Argiolas, A. (2005) PD-168077, a selective dopamine D-4 receptor agonist, induces penile erection when injected into the paraventricular nucleus of male rats. Neurosci. Lett., 379, 59 62.
40. 4 receptor agonists, induce penile erection in male rats: site and mechanism of action in the brain. Eur. J. Neurosci., 24, 2021 2030.
41. Moreland, R.B., Nakane, M., Donnelly-Roberts, D.L., Miller, L.N., Chang, R., Uchic, M.E., Terranova, M.A., Gubbins, E.J., Helfrich, R.J., Namovic, M.T., El-Kouhen, O.F., Masters, J.N. Brioni, J.D. (2004) Comparative pharmacology of human dopamine D(2)-like receptor stable cell lines coupled to calcium flux through Galpha(qo5). Biochem. Pharmacol., 68, 761 772.
42. Nishitani, S., Moriya, T., Kondo, Y., Sakuma, Y. Shinohara, K. (2004) Induction of Fos immunoreactivity in oxytocin neurons in the paraventricular nucleus after female odor exposure in male rats: effects of sexual experience. Cell. Mol. Neurobiol., 24, 283 291.
43. Paredes, R.G. Agmo, A. (2004) Has dopamine a physiological role in the control of sexual behavior?. A critical review of the evidence Prog. Neurobiol., 73, 179 226.
44. Pattij, T., de Jong, T.R., Uitterdijk, A., Waldinger, M.D., Veening, J.G., Cools, A.R., van der Graaf, P.H. Olivier, B. (2005) Individual differences in male rat ejaculatory behaviour: searching for models to study ejaculation disorders. Eur. J. Neurosci., 22, 724 734.
45. Phillips-Farfan, B.V. Fernandez-Guasti, A. (2007) c-Fos expression related to sexual satiety in the male rat forebrain. Physiol. Behav., 91, 609 619.
46. 4 receptor activation inhibits presynaptically glutamatergic neurotransmission in the rat supraoptic nucleus. J. Neurophysiol., 86, 1149 1155.
47. Sabatier, N. Leng, G. (2006) Presynaptic actions of endocannabinoids mediate alpha-MSH-induced inhibition of oxytocin cells. Am. J. Physiol. Regul. Integr. Comp. Physiol., 290, 577 584.
48. Sabatier, N., Caquineau, C., Dayanithi, G., Bull, P., Douglas, A.J., Guan, XMM., Jiang, M., van der Ploeg, L Leng, G. (2003) αMSH stimulates oxytocin release from the dendrites of hypothalamic neurons while inhibiting oxytocin release from their terminals in the neurohypophysis. J. Neurosci., 23, 10351 10358.
49. Sachs, B.D. (2000) Contextual approaches to the physiology and classification of erectile function, erectile dysfunction, and sexual arousal. Neurosci. Biobehav. Rev., 24, 541 560.
50. Swanson, L.W. Sawchenko, P.E. (1980) Paraventricular nucleus: a site for the integration of neuroendocrine and autonomic mechanisms. Neuroendocrinology, 31, 410 417.
51. Tang, Y., Rampin, O., Calas, A., Facchinetti, P. Giuliano, F. (1998) Oxytocinergic and serotonergic innervation of identified lumbosacral nuclei controlling penile erection in the male rat. Neuroscience, 82, 241 254.
52. Uckert, S., Becker, A.J., Ness, B.O., Stief, C.G., Scheller, F., Knapp, W.H. Jonas, U. (2003) Oxytocin plasma levels in the systemic and cavernous blood of healthy males during different penile conditions. World J. Urol., 20, 323 326. (Pubitemid 44175299)
53. Veronneau-Longueville, F., Rampin, O., Freund-Mercier, M.J., Tang, Y., Calas, A., Marson, L., McKenna, K.E., Stoeckel, M.E., Benoit, G. Giuliano, F. (1999) Oxytocinergic innervation of autonomic nuclei controlling penile erection in the rat. Neuroscience, 93, 1437 1447. (Pubitemid 29397573)
54. Waldherr, M. Neumann, I.D. (2007) Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc. Natl Acad. Sci. USA, 104, 16681 16684.
55. Wessells, H., Hruby, V.J., Hackett, J., Han, G.X., Balse-Srinivasan, P. Vanderah, T.W. (2003) MT-II induces penile erection via brain and spinal mechanisms. Ann. N Y Acad. Sci., 994, 90 95.