The role of oxytocin and the paraventricular nucleus in the sexual behaviour of male mammals

Physiology and Behavior

Volumn 83, Issue 2, 2004, Pages 309-317

  Argiolas, Antonio ^a   Melis, Maria Rosaria ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Copulatory behaviour; Dopamine; Excitatory amino acids; GABA; Hexarelin analogue peptides; Nitric oxide; Noncontact erection; Opiates; Opioid peptides; Oxytocin; Paraventricular nucleus; Penile erection

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; DOPAMINE; EXCITATORY AMINO ACID; HEXARELIN; NEUROPEPTIDE; NEUROTRANSMITTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OPIATE; OPIATE PEPTIDE; OXYTOCIN; OXYTOCIN RECEPTOR; PEPTIDE DERIVATIVE;

BRAIN NERVE CELL; BRAIN REGION; CELL ACTIVATION; COPULATION; FEMALE; GENDER; HUMAN; HYPOTHALAMUS; MALE; MAMMAL; NONHUMAN; PENIS ERECTION; PHYSIOLOGY; PRIORITY JOURNAL; PSYCHOGENIC IMPOTENCE; RAT; REVIEW; SEXUAL BEHAVIOR; SPINAL CORD; THALAMUS MIDLINE NUCLEUS;

EID: 5444260639     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2004.08.019     Document Type: Article

References (81)

1. R.L. Meisel, and B.D. Sachs The physiology of male sexual behaviour E. Knobil J. Neil second edition The Physiology of Reproduction vol. 2 1994 Raven Press New York 3 96
2. J.E. Andersson, and G. Wagner Physiology of erection Physiol. Rev. 75 1995 191 236
3. A. Argiolas, and M.R. Melis Neuromodulation of penile erection: an overview of the role of neurotransmitters and neuropeptides Prog. Neurobiol. 47 1995 235 255
4. K.E. McKenna Some proposals regarding the organization of the central nervous system control of penile erection Neurosci. Biobehav. Rev. 24 2000 535 540
5. F. Giuliano, and O. Rampin Central control of penile erection Neurosci. Biobehav. Rev. 24 2000 517 533
6. E.M. Hull, J. K Du, D.S. Lorrain, and L. Matuszewich Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation J. Neurosci. 15 1995 7465 7471
7. M.R. Melis, and A. Argiolas Dopamine and sexual behavior Neurosci. Biobehav. Rev. 19 1995 19 38
8. A. Argiolas Neuropeptides and sexual behaviour Neurosci. Biobehav. Rev. 23 1999 1127 1142
9. M.R. Melis, and A. Argiolas Central oxytocinergic neurotransmission: a drug target for the therapy of psychogenic erectile dysfunction Curr. Drugs Target 4 2003 55 66
10. L.J. Ignarro Biosynthesis and metabolism of endothelium-derived nitric oxide Annu. Rev. Pharmacol. Toxicol. 30 1990 535 560
11. M.R. Melis, S. Succu, A. Mauri, and A. Argiolas Nitric oxide production is increased in the paraventricular nucleus of the hypothalamus of male rats during non-contact penile erections and copulation Eur. J. Neurosci. 10 1998 1968 1974
12. R.M. Buijs Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat Cell Tissue Res. 192 1978 423 435
13. M.W. Sofroniew Vasopressin and oxytocin in the mammalian brain and spinal cord Trends Neurosci. 6 1983 467 472
14. Y. Tang, O. Rampin, A. Calas, P. Facchinetti, and F. Giuliano Oxytocinergic and serotoninergic innervation of identified lumbosacral nuclei controlling penile erection in the male rat Neuroscience 82 1998 241 254
15. F. Veronneau-Longueville, O. Rampin, M.-J. Freund-Mercier, Y. Tang, A. Calas, and L. Marson Oxytocinergic innervation of autonomic nuclei controlling penile erection in the rat Neuroscience 93 1999 1437 1447
16. C.K. Wagner, and L.G. Clemens Neurophysin-containing pathway from the paraventricular nucleus of the hypothalamus to a sexually dimorphic motor nucleus in lumbar spinal cord J. Comp. Neurol. 336 1993 106 116
17. A. Argiolas, and G.L. Gessa Central functions of oxytocin Neurosci. Biobehav. Rev. 15 1991 217 231
18. C.S. Carter Oxytocin and sexual behavior Neurosci. Biobehav. Rev. 16 1992 131 144
19. C.A. Pedersen, J.D. Caldwell, G.F. Jirikowski, and T.R. Insel Oxytocin in Maternal, Sexual and Social Behaviors vol. 652 1992 The New York Academy of Sciences New York
20. M.S. Carmichael, R. Humbert, J. Dixen, G. Palmisano, W. Greeleaf, and J.M. Davidson Plasma oxytocin increases in human sexual response J. Clin. Endocrinol. Metab. 64 1987 27 31
21. M.R. Murphy, J.R. Seckl, S. Burton, S.A. Checkley, and S.L. Lightman Changes in oxytocin and vasopressin secretion during sexual activity in men J. Clin. Endocrinol. Metab. 65 1987 738 741
22. J.S. Tindall Stimuli that cause the release of oxytocin S.R. Geiger E. Knobil W.H. Sawyer R. Greef E.B. Astwood Handbook of physiology Endocrinology vol. IV 1974 American Physiology Society Washington D.C. 257 267 Sect. 7
23. P. Melin, and J.E. Kihlstrom Influence of oxytocin on sexual behaviour in male rabbits Endocrinology 73 1963 433 435
24. A. Argiolas, M.R. Melis, and G.L. Gessa Intraventricular oxytocin induces yawning and penile erection in rats Eur. J. Pharmacol. 117 1985 395 396
25. R. Arletti, C. Bazzani, M. Castelli, and A. Bertolini Oxytocin improves male copulatory performance in rats Horm. Behav. 19 1985 14 20
26. R. Arletti, and A. Bertolini Oxytocin stimulates lordosis behavior in female rats Neuropeptides 6 1985 247 255
27. J.D. Caldwell, A.J. Prange Jr., and C.A. Pedersen Oxytocin facilitates the sexual receptivity of estrogen-treated female rats Neuropeptides 7 1986 175 189
28. M.R. Melis, A. Argiolas, and G.L. Gessa Oxytocin-induced yawning and penile erection: site of action in the brain Brain Res. 398 1986 259 265
29. M.J. Freund-Mercier, and M.E. Stoeckel Somatodendritic autoreceptors on oxytocin neurons R. Ivell J.A Russel Oxytocin, cellular and molecular approaches in medicine and research Adv. Exp. Med. Biol. vol. 365 1995 Plenum Press New York 185 194
30. M.J. Freund-Mercier, and P. Richard Excitatory effects of intraventricular injections of oxytocin on the milk ejection reflex in the rat Neurosci. Lett. 23 1981 193 198
31. M.J. Freund-Mercier, and Ph. Richard Electrophysiological evidence for facilitatory control of oxytocin neurons by oxytocin during suckling in the rat J. Physiol. (London) 352 1984 447 466
32. F. Moos, M.J. Freund-Mercier, Y. Guerne, J.M. Guerne, M.E. Stoeckel, and P. Richard Release of oxytocin and vasopressin by magnocellular nuclei in vitro: specific facilitatory effect of oxytocin on its own release J. Endocrinol. 102 1984 63 72
33. H. Yamashita, O. Shigeru, K. Inenaga, M. Kasai, S. Uesugi, and H. Kannan Oxytocin predominantly excites putative oxytocin neurons in the rat supraoptic nucleus in vitro Brain Res. 416 1987 364 368
34. D.T. Theodosis Oxytocin-immunoreactive terminals synapse on oxytocin neurones in the supraoptic nuclei Nature (London) 313 1985 682 684
35. A. Argiolas, M.R. Melis, A. Mauri, and G.L. Gessa Paraventricular nucleus lesion prevents yawning and penile erection induced by apomorphine and oxytocin, but not by ACTH in rats Brain Res. 421 1987 349 352
36. Y.-C. Liu, J.D. Salamone, and B.D. Sachs Impaired sexual response after lesions of the paraventricular nucleus of the hypothalamus in male rats Behav. Neurosci. 111 1997 1361 1367
37. B.D. Sachs Erection evoked in male rats by airborne scent from estrous females Physiol. Behav. 62 1997 921 924
38. D.A. Edwards, and A.B. Davis Deafferentation of the olfactory bulbs of male rat reduces erection to remote cues from females Physiol. Behav. 62 1997 145 149
39. 8-vasotocin reduces non-contact erections in male rats Neurosci. Lett. 265 1999 171 174
40. 8-vasotocin inhibits male copulatory behaviour in rats Eur. J. Pharmacol. 149 1988 389 392
41. R. Arletti, A. Benelli, and A. Bertolini Oxytocin involvement in male and female sexual behaviour Ann. N.Y. Acad. Sci. 652 1992 180 193
42. A.M. Hughes, B.J. Everitt, S.L. Lightman, and K. Todd Oxytocin in the central nervous system and sexual behavior in male rats Brain Res. 414 1987 133 137
43. M.D. Stoneham, B.J. Everitt, S. Hansen, S.L. Lightman, and K. Todd Oxytocin and sexual behaviour in the male rat and rabbit J. Endocrinol. 107 1985 97 106
44. R. Arletti, C. Bazzani, M. Castelli, and A. Bertolini Oxytocin improves male copulatory performance in rats Horm. Behav. 19 1985 14 20
45. R. Arletti, A. Benelli, and A. Bertolini Sexual behavior of aging male rats is stimulated by oxytocin Eur. J. Pharmacol. 179 1990 377 382
46. J.T. Winslow, and T.R. Insel Social status in pairs of male squirrel monkeys determines the behavioral response to central oxytocin administration J. Neurosci. 11 1991 2032 2038
47. D.M. Witt, and T.R. Insel Male sexual behavior activates c-fos-like protein in oxytocin neurons in the paraventricular nucleus of the hypothalamus J. Neuroendocrinol. 6 1994 13 18
48. A. Arletti, L. Calzà, L. Giardino, A. Benelli, E. Cavazzuti, and A. Bertolini Sexual impotence is associated with a reduced production of oxytocin and an increased production of opioid peptides in the paraventricular nucleus of the hypothalamus Neurosci. Lett. 233 1997 65 68
49. E.W. McCleskey, A.P. Fox, D.H. Feldman, L.J. Cruz, B.M. Olivera, and R.W. Tsien ω-Conotoxin: direct and persistent blockade of specific types of calcium channels in neurons but not muscle Proc. Natl. Acad. Sci. U. S. A. 84 1987 4327 4331
50. S.R. Vincent, and H. Kimura Histochemical mapping of nitric oxide synthase in the rat brain Neuroscience 46 1992 755 784
51. S.H. Snyder Nitric oxide: first in a new class of neurotransmitters? Science 257 1992 494 496
52. F. Sanchez, J.R. Alonso, R. Arevalo, E. Blanco, J. Aijon, and R. Vazquez Coexistence of NADPH-diaphorase with vasopressin and oxytocin in the hypothalamic magnocellular neurosecretory nuclei of the rat Cell Tissue Res. 276 1994 31 34
53. G. Torres, Soon Lee, and C. Rivier Ontogeny of the rat hypothalamic nitric oxide synthase and colocalization with neuropeptides Mol. Cell. Neurosci. 4 1993 155 163
54. M.R. Melis, and A. Argiolas Role of central nitric oxide in the control of penile erection and yawning Prog. Neuro-Psychopharmacol. Biol. Psychiatry 21 1997 899 922
55. M.R. Melis, S. Succu, U. Iannucci, and A. Argiolas Oxytocin increases nitric oxide production in the paraventricular nucleus of the hypothalamus of male rats: correlation with penile erection and yawning Regul. Pept. 69 1997 105 111
56. E.M. Schuman, and D.V. Madison Nitric oxide and synaptic function Annu. Rev. Neurosci. 17 1994 153 183
57. E. Southam, and J. Garthwaite The nitric oxide-cyclic GMP signalling pathway in rat brain Neuropharmacology 32 1993 1267 1277
58. C.M. Vacher, H. Hardin-Ponzet, H.W. Steinbusch, A. Calas, and J. De Vente The effects of nitric oxide on magnocellular neurons could involve multiple indirect cyclic GMP-dependent pathways Eur. J. Neurosci. 17 2003 455 466
59. A. Benelli, A. Bertolini, R. Poggioli, E. Cavazzuti, L.M. Calzà, and L. Giardino Nitric oxide is involved in male sexual behaviour of rats Eur. J. Pharmacol. 294 1995 505 510
60. A. Dahlstrom, and K. Fuxe Evidence for the existence of monoamine-containing neurons in the central nervous system: I. Demonstration of monoamines in the cell bodies of brainstem neurons Acta Physiol. Scand. 62 Suppl. 232 1964 1 55
61. R.M. Buijs, M. Geffard, C.W. Pool, and E.M.D. Hoorneman The dopaminergic innervation of the supraoptic and paraventricular nucleus. A light and electron microspical study Brain Res. 323 1984 65 74
62. O. Lindvall, A. Bjorklund, and G. Skagerberg Selective istochemical demonstration of dopamine terminal systems in rat di- and telencephalon: new evidence for dopaminergic innervation of hypothalamic neurosecretory nuclei Brain Res. 306 1984 19 30
63. M.R. Melis, A. Argiolas, R. Stancampiano, and G.L. Gessa Effect of apomorphine on oxytocin concentrations in different brain areas and plasma of male rats Eur. J. Pharmacol. 182 1990 101 107
64. J.L. Cameron, S.M. Pomerantz, L.M. Layden, and J.A. Amico Dopaminergic stimulation of oxytocin concentrations in the plasma of male and female monkeys by apomorphine and a D2 receptor agonist J. Clin. Endocrinol. Metab. 75 1992 855 860
65. 8-vasotocin in rats Pharmacol. Biochem. Behav. 33 1989 81 83
66. M.R. Melis, S. Succu, M.S. Mascia, L. Cortis, and A. Argiolas Extra-cellular dopamine increases in the paraventricular nucleus of male rats during sexual activity Eur. J. Neurosci. 17 2003 1266 1272
67. M.R. Melis, S. Succu, and A. Argiolas Dopamine agonists increase nitric oxide production in the paraventricular nucleus of the hypothalamus: correlation with penile erection and yawning Eur. J. Neurosci. 8 1996 2056 2063
68. M.R. Melis, S. Succu, M.S. Spano, and A. Argiolas Effect of excitatory amino acid, dopamine, and oxytocin receptor antagonists on noncontact penile erections and paraventricular nitric oxide production in male rats Behav. Neurosci. 114 2000 849 857
69. A. van den Pol Glutamate and aspartate immunoreactivity in hypothalamic presynaptic axons J. Neurosci. 11 1991 2087 2101
70. K.-K. Chen, J.Y.H. Chan, L.S. Chang, M.-T. Chen, and S.H.H. Chan Elicitation of penile erection following activation of the hippocampal formation in the rat Neurosci. Lett. 141 1992 218 222
71. D. Saphier, and S. Feldman Effects of septal and hippocampal stimuli on paraventricular nucleus neurons Neuroscience 20 1987 749 755
72. M.R. Melis, S. Succu, M.S. Spano, A. Torsello, V. Locatelli, and E.E. Muller EP 60761- and EP 50885-induced penile erection: structure†"activity studies and comparison with apomorphine, oxytocin and N-methyl-d-aspartic acid Int. J. Impot. Res. 12 2000 255 262
73. M.S. Melis, S. Succu, M.S. Spano, R. Deghenghi, and A. Argiolas EP 91073 prevents EP 80661-induced penile erection: new evidence for the existence of specific EP peptide receptors mediating penile erection Neuropharmacology 41 2001 254 262
74. M. Kojima, H. Hosoda, Y. Date, M. Nakazato, H. Matsuo, and K. Kangawa Ghrelin is a growth hormone-releasing acylated peptide from stomach Nature 402 1999 656 660
75. H. Hosoda, M. Kojima, H. Matsuo, and K. Kangawa Purification and characterization of rat des-Gln-14-ghrelin, a second endogenous ligand for growth hormone secretagogue receptor J. Biol. Chem. 275 2000 21995 22000
76. M.R. Melis, M.S. Mascia, S. Succu, A. Torsello, E.E. Muller, and R. Deghenghi Ghrelin injected into the paraventricular nucleus of male rats induces feeling but not penile erection Neurosci. Lett. 329 2002 339 343
77. A receptors in the paraventricular nucleus: involvement of nitric oxide Eur. J. Neurosci. 15 2002 852 860
78. C. Boubada, K. Szabò, and G. Tasker Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus J. Neurosci. 15 1996 7151 7160
79. P. Jourdain, B. Dupouy, R. Bonhomme, D.A. Poulain, J.M. Israel, and D.T. Theodosis Visualization of local afferent inputs to magnocellular oxytocin neurons in vitro Eur. J. Neurosci. 11 1999 1960 1972
80. M.R. Melis, S. Succu, M.S. Spano, and A. Argiolas Morphine injected into the paraventricular nucleus of the hypothalamus prevents non-contact erections and impairs copulation: Involvement of nitric oxide Eur. J. Neurosci. 11 1999 1857 1864
81. M. Muhlethaler, B.H. Gahwiler, and J.J. Dreifuss Enkephalin-induced inhibition of hypothalamic paraventricular neurons Brain Res. 197 1980 264 268