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Rôle des androgènes dans la motivation sexuelle masculine: approche par la neuroanatomie cérébrale fonctionnelle

Role of androgens in male sexual motivation: approach with functional brain imaging techniques

Resume

Le système nerveux central joue un rôle à toutes les étapes du comportement sexuel, notamment en ce qui concerne le traitement des stimuli externes. Une étape clé consiste en l’attribution à ces signaux externes d’une valeur dite de «récompense» qui conditionnera la mise en place des différentes étapes de l’excitation sexuelle. Ces étapes font intervenir des processus cognitifs complexes, interagissant avec des composantes émotionnelles et physiologiques. Les androgènes, et notamment la testostérone, par leur action au sein du système nerveux central, jouent un rôle fondamental dans la régulation et le maintien du comportement sexuel. Ceci est en particulier mis en évidence dans le cadre de pathologies entraînant un déficit androgénique, tel que l’hypogonadisme, pathologies caractérisées par une diminution significative de la motivation et de l’activité sexuelles.

Les techniques récentes d’imagerie cérébrale fonctionnelle (Tomographie par Emission de Positons, Imagerie par Résonance Magnétique fonctionnelle) ont permis de mettre en évidence un réseau de structures cérébrales impliquées dans le développement et le contrôle de la motivation sexuelle chez l’homme. Ces techniques, associées à l’étude de patients hypogonadiques, peuvent permettre de mieux comprendre la spécificité de ces structures cérébrales dans la fonction sexuelle, ainsi que de préciser les mécanismes d’action des androgènes dans la régulation de la motivation sexuelle.

Abstract

The central nervous system plays a crucial role in all of the successive stages of sexual behaviour, particularly for the processing of external stimuli. One important step consists of the evaluation of these stimuli and the assessment of their potential reward value, which will determine the development of the sexual response. These different stages involve complex cognitive processes interacting with emotional and physiological components.

Androgens, and particularly testosterone, are closely related to the regulation of sexual behaviour. Many of the various effects of testosterone on sexual behaviour have been thought to result from its effects on the central nervous system. Several studies have demonstrated that a minimum concentration of plasma testosterone is necessary to maintain a normal level of sexual desire in human males. Consequently, in normal men, acute and profound androgen deficiency induced by an experimental pharmacological treatment results in decreased sexual desire and fantasies. This reduced sexual desire is also one of the major symptoms observed in male hypogonadism. Conversely, in hypogonadal men, androgen substitution therapy results in increased sexual interest and activity.

Over recent years, the development of brain functional imaging techniques (Positron Emission Tomography, functional Magnetic Resonance Imaging) has demonstrated the brain regions participating in a neural network that controls and regulates sexual arousal. We have proposed a four component neurobehavioural model, comprising cognitive (e.g. orbitofrontal cortex), motivational (e.g. anterior cingulate gyrus), emotional (e.g. somatosensory cortex, insula) and physiological (e.g. hypothalamus) processes, to describe this cerebral control of sexual motivation in human males. This network comprises activating and inhibiting structures that interact with each other.

As testosterone can modulate sexual desire via its action on cerebral function, we decided to perform a brain imaging study in hypogonadal patients (both when they were untreated and when they received hormone replacement therapy), to obtain e better understanding of the specificity of these brain regions in sexual arousal processes. This study could also help describe the brain regions via which testosterone acts to modulate sexual behaviour.

References

  1. 1.

    ABDELGADIR S.E., ROSELLI C.E., CHOATE J.V., RESKO J.A.: Androgen receptor messenger ribonucleic acid in brains and pituitaries of male rhesus monkeys: studies on distribution, hormonal control, and relationship to luteinizing hormone secretion. Biol. Reprod., 1999, 60: 1251–1256.

    PubMed  Article  CAS  Google Scholar 

  2. 2.

    ABRAHAM G., MARRAMA P., CARANI C., GAILLARD J.M.: Psycho-neuroendocrinologie du plaisir. Villeurbanne, SIMEP, 1985.

    Google Scholar 

  3. 3.

    ALEXANDER G.M., PACKARD M.G., HINES M.: Testosterone has rewarding affective properties in male rats: implications for the biological basis of sexual motivation. Behav. Neurosci., 1994, 108: 424–428.

    PubMed  Article  CAS  Google Scholar 

  4. 4.

    ARNOW B.A., DESMOND J.E., BANNER L.L. et al.: Brain activation and sexual arousal in healthy, heterosexual males. Brain, 2002, 125: 1014–1023.

    PubMed  Article  Google Scholar 

  5. 5.

    BAGATELL C.J., HEIMAN J.R., RIVIER J.E., BREMNER W.J.: Effects of endogenous testosterone and estradiol on sexualbehavior in normal young men. J. Clin. Endocrinol. Metab., 1994, 78: 711–7166.

    PubMed  Article  CAS  Google Scholar 

  6. 6.

    BALTHAZART J., REID J., ABSIL P., FOIDART A., BALL G.F.: Appetitive as well as consummatory aspects of male sexual behavior in quail are activated by androgens and estrogens. Behav. Neurosci., 1995, 109: 485–501.

    PubMed  Article  CAS  Google Scholar 

  7. 7.

    BANCROFT J.: Hormones and human sexual behavior. J. Sex. Marital Ther., 1984, 10: 3–21.

    PubMed  CAS  Google Scholar 

  8. 8.

    BANCROFT J.: Human sexuality and its problems. London, Churchill Livingstone, 1989.

    Google Scholar 

  9. 9.

    BANCROFT J.: Sexual desire and the brain. Sexual and Marital Therapy, 1988, 3: 11–27.

    Google Scholar 

  10. 10.

    BANCROFT J., WU F.C.: Changes in erectile responsiveness during androgen replacement therapy. Arch. Sex. Behav., 1983, 12: 59–66.

    PubMed  Article  CAS  Google Scholar 

  11. 11.

    BAUM M.J., EVERITT B.J., HERBERT J., KEVERNE E.B.: Hormonal basis of proceptivity and receptivity in female primates. Arch. Sex. Behav., 1977, 6: 173–192.

    PubMed  Article  CAS  Google Scholar 

  12. 12.

    BEAUREGARD M., KARAMA S., LEROUX J.M. et al.: The functional neuroanatomy of amusement, disgust and sexual arousal. 4th International Conference on Functional Mapping of the Human Brain, 1998.

  13. 13.

    BERTHOLD A.D.: Transplantation der Hoden. 1849, 16: 42–46.

    Google Scholar 

  14. 14.

    BEUMONT P.J., BANCROFT J.H., BEARDWOOD C.J., RUSSELL G.F.: Behavioural changes after treatment with testosterone: case report. Psychol. Med., 1972, 2: 70–72.

    PubMed  CAS  Google Scholar 

  15. 15.

    BIELERT C., VAN DER WALT L.A.: Male chacma baboon (Papio ursinus) sexual arousal: mediation by visual cues from female conspecifics. Psychoneuroendocrinology, 1982, 7: 31–48.

    PubMed  Article  CAS  Google Scholar 

  16. 16.

    BOCHER M., CHISIN R., PARAG Y. et al.: Cerebral activation associated with sexual arousal in response to a pornographic clip: A 15O−H2O PET study in heterosexual men. Neuroimage, 2001, 14: 105–117.

    PubMed  Article  CAS  Google Scholar 

  17. 17.

    BROWN W.A., MONTI P.M., CORRIVEAU D.P.: Serum testosterone and sexual activity and interest in men. Arch. Sex. Behav., 1978, 7: 97–103.

    PubMed  Article  CAS  Google Scholar 

  18. 18.

    BURRIS A.S., BANKS S.M., CARTER C.S., DAVIDSON J.M., SHERINS R.J.: A long-term, prospective study of the physiologic and behavioral effects of hormone replacement in untreated hypogonadal men. J. Androl., 1992, 13: 297–304.

    PubMed  CAS  Google Scholar 

  19. 19.

    BUSH G., LUU P., POSNER M.I.: Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci., 2000, 4: 215–222.

    PubMed  Article  Google Scholar 

  20. 20.

    BUSS D.M.: Sex differences in human mate preferences: evolutionary hypotheses tested in 37 cultures. Behav Brain Sci, 1989, 12: 1–14.

    Google Scholar 

  21. 21.

    BUVAT J.: Hormones et comportement sexuel de l’homme: données physiologiques et physiopathologiques. Contracept. Fertil. Sex., 1996, 24: 767–778.

    PubMed  CAS  Google Scholar 

  22. 22.

    CARANI C., BANCROFT J., GRANATA A., DEL RIO G., MARRAMA P.: Testosterone and erectile function, nocturnal penile tumescence and rigidity, and erectile response to visual erotic stimuli in hypogonadal and eugonadal men. Psychoneuroendocrinology, 1992, 17: 647–654.

    PubMed  Article  CAS  Google Scholar 

  23. 23.

    DAVIDSON J.M., KWAN M., GREENLEAF W.J.: Hormonal replacement and sexuality in men. Clin. Endocrinol. Metab., 1982, 11: 599–623.

    PubMed  Article  CAS  Google Scholar 

  24. 24.

    DE ROUX N., MILGROM E.: Inherited disorders of GnRH and gonadotropin receptors. Mol. Cell. Endocrinol., 2001, 179: 83–87.

    PubMed  Article  Google Scholar 

  25. 25.

    DELEMARRE-VAN DE WAAL H.A.: Induction of testicular growth and spermatogenesis by pulsatile, intravenous administration of gonadotrophin-releasing hormone in patients with hypogonadotrophic hypogonadism. Clin. Endocrinol. (Oxf), 1993, 38: 473–480.

    Article  CAS  Google Scholar 

  26. 26.

    DENTON D., SHADE R., ZAMARIPPA F. et al.: Neuroimaging of genesis and satiation of thirst and an interoceptor-driven theory of origins of primary consciousness. Proc. Natl Acad. Sci. (USA), 1999, 96: 5304–5309.

    Article  CAS  Google Scholar 

  27. 27.

    DEVINSKY O., MORRELL M.J., VOGT B.A.: Contributions of anterior cingulate cortex to behaviour. Brain, 1995, 118: 279–306.

    PubMed  Article  Google Scholar 

  28. 28.

    DUA S., MACLEAN P.D.: Localisation for penile erection in medial frontal lobe. Am. J. Physiol., 1964, 207: 1425–1434.

    PubMed  CAS  Google Scholar 

  29. 29.

    EVERITT B.J., STACEY P.: Studies of instrumental behavior with sexual reinforcement in male rats (Rattus norvegicus): II. Effects of preoptic area lesions, castration, and testosterone. J. Comp. Psychol., 1987, 101: 407–419.

    PubMed  Article  CAS  Google Scholar 

  30. 30.

    FERNANDEZ-GUASTI A., KRUIJVER F.P., FODOR M., SWAAB D.F.: Sex differences in the distribution of androgen receptors in the human hypothalamus. J. Comp. Neurol., 2000, 425: 422–435.

    PubMed  Article  CAS  Google Scholar 

  31. 31.

    FERRIS C.F., SNOWDON C.T., KING J.A. et al.: Functional imaging of brain activity in conscious monkeys responding to sexually arousing cues. Neuroreport, 2001, 12: 2231–2236.

    PubMed  Article  CAS  Google Scholar 

  32. 32.

    FINKEL D.M., PHILLIPS J.L., SNYDER P.J.: Stimulation of spermatogenesis by gonadotropins in men with hypogonadotropic hypogonadism. N. Engl. J. Med., 1985, 313: 651–655.

    PubMed  CAS  Article  Google Scholar 

  33. 33.

    FINLEY S.K., KRITZER M.F.: Immunoreactivity for intracellular androgen receptors in identified subpopulations of neurons, astrocytes and oligodendrocytes in primate prefrontal cortex. J. Neurobiol., 1999, 40: 446–457.

    PubMed  Article  CAS  Google Scholar 

  34. 34.

    GOOREN L.J.: Androgen levels and sex functions in testosterone-treated hypogonadal men. Arch. Sex. Behav., 1987, 16: 463–473.

    PubMed  Article  CAS  Google Scholar 

  35. 35.

    GOOREN L.J.: Human male sexual functions do not require aromatization of testosterone: a study using tamoxifen, testolactone, and dihydrotestosterone. Arch. Sex. Behav., 1985, 14: 539–548.

    PubMed  Article  CAS  Google Scholar 

  36. 36.

    HAGEMANN J.H., BERDING G., BERGH S. et al.: Effects of visual sexual stimuli and apomorphine SL on cerebral activity in men with erectile dysfunction. Eur. Urol., 2003, 43: 412–420.

    PubMed  Article  CAS  Google Scholar 

  37. 37.

    HAYES F.J., SEMINARA S.B., CROWLEY W.F. Jr.: Hypogonadotropic hypogonadism. Endocrinol. Metab. Clin. North Am., 1998, 27: 739–763, vii.

    PubMed  Article  CAS  Google Scholar 

  38. 38.

    HOLSTEGE G., GEORGIADIS J.R., PAANS A.M. et al.: Brain activation during human male ejaculation. J. Neurosci., 2003, 23: 9185–9193.

    PubMed  CAS  Google Scholar 

  39. 39.

    KARAMA S., LECOURS A.R., LEROUX J.M. et al.: Areas of brain activation in males and females during viewing of erotic film excerpts. Hum. Brain Mapp., 2002, 16: 1–13.

    PubMed  Article  Google Scholar 

  40. 40.

    LANGE J.D., BROWN W.A., WINCZE J.P., ZWICK W.: Serum testosterone concentration and penile tumescence changes in men. Horm. Behav., 1980, 14: 267–270.

    PubMed  Article  CAS  Google Scholar 

  41. 41.

    LEJEUNE H.: Hypogonadismes testiculaires. Rev. Prat., 1999, 49: 1303–1308.

    PubMed  CAS  Google Scholar 

  42. 42.

    LUISI M., FRANCHI F.: Double-blind group comparative study of testosterone undecanoate and mesterolone in hypogonadal male patients. J. Endocrinol. Invest., 1980, 3: 305–308.

    Google Scholar 

  43. 43.

    MATOCHIK J.A., SIPOS M.L., NYBY J.G., BARFIELD R.J.: Intracranial androgenic activation of male-typical behaviors in house mice: motivation versus performance. Behav. Brain Res., 1994, 60: 141–149.

    PubMed  Article  CAS  Google Scholar 

  44. 44.

    MATSUMOTO A.M.: Hormonal therapy of male hypogonadism. Endocrinol. Metab. Clin. North Am., 1994, 23: 857–875.

    PubMed  CAS  Google Scholar 

  45. 45.

    MATSUMOTO A.M.: The testis and male sexual function. In: Wyngaarden J.B., Smith L.H., Bennett J.C. eds. Textbook of Medicine. Philadelphia, Saunders, W.B., 1992.

    Google Scholar 

  46. 46.

    MATSUMOTO A.M., GROSS K.M., BREMNER W.J.: The physiological significance of pulsatile LHRH secretion in man: gonadotrophin responses to physiological doses of pulsatile versus continuous LHRH administration. Int. J. Androl., 1991, 14: 23–32.

    PubMed  Article  CAS  Google Scholar 

  47. 47.

    MEISEL R.L., SACHS B.D.: The physiology of male sexual behavior. In: Knobil E., Neill J.D. eds. The Physiology of Reproduction. New York, Raven Press, 1994: 3–105.

    Google Scholar 

  48. 48.

    MONEY J.: Components of eroticism in man: the hormones in relation to sexual morphology and sexual desire. J. Nerv. Ment. Dis., 1961, 132: 229–238.

    Google Scholar 

  49. 49.

    MONTORSI F., PERANI D., ANCHISI D. et al.: Apomorphine-induce brain modulation during sexual stimulation: a new look at central phenomena related to erectile dysfunction. Int. J. Impot. Res., 2003, 15: 203–209.

    PubMed  Article  CAS  Google Scholar 

  50. 50.

    MORALI G., HERNANDEZ G., BEYER C.: Restoration of the copulatory pelvic thrusting pattern in castrated male rats by the intracerebral implantation of androgen. Physiol. Behav., 1986, 36: 495–499.

    PubMed  Article  CAS  Google Scholar 

  51. 51.

    MOURAS H., STOLERU S., BITTOUN J. et al.: Brain processing of visual sexual stimuli in healthy men: a functional magnetic resonance imaging study. Neuroimage, 2003, 20: 855–869.

    PubMed  Article  Google Scholar 

  52. 52.

    OOMURA Y., YOSHIMATSU H., AOU S.: Medial preoptic and hypothalamic neuronal activity during sexual behavior of the male monkey. Brain Res., 1983, 266: 340–343.

    PubMed  Article  CAS  Google Scholar 

  53. 53.

    PARK K., SEO J.J., KANG H.K. et al.: A new potential of blood oxygenation level dependent (BOLD) functional MRI for evaluating cerebral centers of penile erection. Int. J. Impot. Res., 2001, 13: 73–81.

    PubMed  Article  CAS  Google Scholar 

  54. 54.

    PUY L., MACLUSKY N.J., BECKER L. et al.: Immunocytochemical detection of androgen receptor in human temporal cortex characterization and application of polyclonal androgen receptor antibodies in frozen and paraffin-embedded tissues. J. Ster. Bioch. Mol. Biol., 1995, 55: 197–209.

    Article  CAS  Google Scholar 

  55. 55.

    RAUCH S.L., SHIN L.M., DOUGHERTY D.D. et al.: Neural activation during sexual and competitive arousal in healthy men. Psychiatry Res., 1999, 91: 1–10.

    PubMed  Article  CAS  Google Scholar 

  56. 56.

    REDOUTÉ J., STOLÉRU S., GRÉGOIRE M.C. et al.: Brain processing of visual sexual stimuli in human males. Hum. Brain Mapp., 2000, 11: 162–177.

    PubMed  Article  Google Scholar 

  57. 57.

    ROBINSON B.W., MISHKIN M.: Penile erection evoked from forebrain structures in Macaca mulatta. Arch. Neurol., 1968, 19: 184–198.

    PubMed  CAS  Google Scholar 

  58. 58.

    ROLLS E.T.: The brain and emotion. New-York, Oxford University Press, 1999: 367.

    Google Scholar 

  59. 59.

    ROSELLI C.E., CHAMBERS K.: Sex differences in male-typical copulatory behaviors in response to androgen and estrogen treatment in rats. Neuroendocrinology, 1999, 69: 290–298.

    PubMed  Article  CAS  Google Scholar 

  60. 60.

    ROSELLI C.E., KLOSTERMAN S., RESKO J.A.: Anatomic relationships between aromatase and androgen receptor mRNA expression in the hypothalamus and amygdala of adult male cynomolgus monkeys. J. Comp. Neurol., 2001, 439: 208–223.

    PubMed  Article  CAS  Google Scholar 

  61. 61.

    SALMIMIES P., KOCKOTT G., PIRKE K.M., VOGT H.J., SCHILL W.B.: Effects of testosterone replacement on sexual behavior in hypogonadal men. Arch. Sex. Behav., 1982, 11: 345–353.

    PubMed  Article  CAS  Google Scholar 

  62. 62.

    SANTEN R.J.: The testis: Function and Dysfunction. In: Yen S.S.C., Jaffe R.B., Barbieri R.L. eds. Reproductive Endocrinology: Physiology, Pathophysiology and Clinical Management. Philadelphia, W.B. Saunders Company, 1999: 632–668.

    Google Scholar 

  63. 63.

    SARRIEAU A., MITCHELL J.B., LAL S. et al.: Androgen binding sites in human temporal cortex. Neuroendocrinology, 1990, 51: 713–716.

    PubMed  Article  CAS  Google Scholar 

  64. 64.

    SIMERLY R.B., CHANG C., MURAMATSU M., SWANSON L.W.: Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J. Comp. Neurol., 1990, 294: 76–95.

    PubMed  Article  CAS  Google Scholar 

  65. 65.

    SKAKKEBAEK N.E., BANCROFT J., DAVIDSON D.W., WARNER P.: Androgen replacement with oral testosterone undercanoate in hypogonadal men: a double blind controlled study. Clin. Endocrinol. (Oxf), 1981, 14: 49–61.

    Article  CAS  Google Scholar 

  66. 66.

    SNYDER P.J., LAWRENCE D.A.: Treatment of male hypogonadism with testosterone enanthate. J. Clin. Endocrinol. Metab., 1980, 51: 1335–1339.

    PubMed  CAS  Article  Google Scholar 

  67. 67.

    STOLÉRU S., GREGOIRE M.C., GERARD D. et al.: Neuroanatomical correlates of visually evoked sexual arousal in human males. Arch. Sex. Behav., 1999, 28: 1–21.

    PubMed  Article  Google Scholar 

  68. 68.

    STOLÉRU S., REDOUTÉ J., COSTES N. et al.: Brain processing of visual sexual stimuli in men with hypoactive sexual desire disorder. Psychiatry Res., 2003, 124: 67–86.

    PubMed  Article  Google Scholar 

  69. 69.

    STOLÉRU S.G., ENNAJI A., COURNOT A., SPIRA A.: LH pulsatile secretion and testosterone blood levels are influenced by sexual arousal in human males. Psychoneuroendocrinology, 1993, 18: 205–218.

    PubMed  Article  Google Scholar 

  70. 70.

    VAGELL M.E., MCGINNIS M.Y.: The role of aromatization in the restoration of male rat reproductive behavior. J. Neuroendocrinol., 1997, 9: 415–421.

    PubMed  Article  CAS  Google Scholar 

  71. 71.

    YEN S.C.C.: Neuroendocrinology of reproduction. In: Yen S.C.C., Jaffe R.B. Barbieri R.L. eds. Reproductive Endocrinology: Physiology, Pathophysiology and Clinical Management. Philadelphia, W.B. Saunders Company, 1999: 30–80.

    Google Scholar 

  72. 72.

    ZINI D., CARANI C., BALDINI A., GHIZZANI A., MARRAMA P.: Sexual behavior of men with isolated hypogonadotropic hypogonadism or prepubertal anterior panhypopituitarism. Horm. Behav., 1990, 24: 174–185.

    PubMed  Article  CAS  Google Scholar 

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Correspondence to Jérôme Redouté.

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Bourse SALF 2003

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Redouté, J., Stoléru, S. Rôle des androgènes dans la motivation sexuelle masculine: approche par la neuroanatomie cérébrale fonctionnelle. Androl. 14, 324–335 (2004). https://doi.org/10.1007/BF03034921

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Mots clés

  • testostérone
  • motivation sexuelle
  • cerveau
  • hypogonadisme
  • imagerie fonctionnelle

Key words

  • testosterone
  • sexual motivation
  • brain Imaging
  • hypogonadism