Neural Bases of Hypoactive Sexual Desire Disorder in Women: An Event-Related fMRI Study

Journal of Sexual Medicine

Volumn 8, Issue 9, 2011, Pages 2546-2559

  Bianchi Demicheli, Francesco ^a,b   Cojan, Yann ^c   Waber, Lakshmi ^a   Recordon, Nathalie ^a   Vuilleumier, Patrik ^c   Ortigue, Stephanie ^b,d  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c Centre Medicale Universitaire   (Switzerland)

^d SYRACUSE UNIVERSITY   (United States)

Author keywords

FMRI; Self Representation; Sexual Desire; Sexual Medicine; Social Neuroscience; Top Down

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; BEHAVIOR; BOLD SIGNAL; BRAIN BLOOD FLOW; BRAIN MAPPING; BRAIN REGION; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; EROTISM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HYPOACTIVE SEXUAL DESIRE DISORDER; INFERIOR FRONTAL GYRUS; INFERIOR PARIETAL LOBULE; INFORMATION PROCESSING; INTRAPARIETAL SULCUS; NERVE CELL NETWORK; NEURAL BASE; NEUROIMAGING; OCCIPITAL GYRUS; PERIRHINAL CORTEX; PRIORITY JOURNAL; RIGHT HANDEDNESS; SEXUAL FUNCTION; SEXUALITY; SOCIAL STATUS;

EID: 80052488379     PISSN: 17436095     EISSN: 17436109     Source Type: Journal    
DOI: 10.1111/j.1743-6109.2011.02376.x     Document Type: Article

References (99)

1. Laumann EO, Nicolosi A, Glasser DB, Paik A, Gingell C, Moreira E, Wang T; GSSAB Investigators' Group. Sexual problems among women and men aged 40-80 y: Prevalence and correlates identified in the Global Study of Sexual Attitudes and Behaviors. Int J Impot Res 2005;17:39-57.
2. Segraves KB, Segraves RT. Hypoactive sexual desire disorder: Prevalence and comorbidity in 906 subjects. J Sex Marital Ther 1991;17:55-8.
3. Basson R, Berman J, Burnett A, Derogatis L, Ferguson D, Fourcroy J, Goldstein I, Graziottin A, Heiman J, Laan E, Leiblum S, Padma-Nathan H, Rosen R, Segraves K, Segraves RT, Shabsigh R, Sipski M, Wagner G, Whipple B. Report of the international consensus development conference on female sexual dysfunction: Definitions and classifications. J Urol 2000;163:888-93.
4. Hatfield E, Rapson RL. Love and sex. Cross-cultural perspectives. Boston, MA: Allyn and Bacon; 1996.
5. Brotto LA, Bitzer J, Laan E, Leiblum S, Luria M. Women's sexual desire and arousal disorders. J Sex Med 2010;7:586-614.
6. Bancroft J. Human sexuality and its problems. 3rd edition. New York: Elsevier; 2009.
7. Levine SB. The nature of sexual desire: A clinician's perspective. Arch Sex Behav 2003;32:279-85.
8. Ortigue S, Bianchi-Demicheli F. [Interactions between human sexual arousal and sexual desire: A challenge for social neuroscience]. Rev Med Suisse 2007;3:809-13.
9. Ortigue S, Bianchi-Demicheli F. [A socio-cognitive approach of human sexual desire]. Rev Med Suisse 2008;4:768-71.
10. Ortigue S, Bianchi-Demicheli F. [Unconscious sexual desire: fMRI and EEG evidences from self-expansion theory to mirror neurons]. Rev Med Suisse 2010;6:620-2, 24.
11. Basson R, Leiblum S, Brotto L, Derogatis L, Fourcroy J, Fugl-Meyer K, Graziottin A, Heiman JR, Laan E, Meston C, Schover L, van Lankveld J, Schultz WW. Revised definitions of women's sexual dysfunction. J Sex Med 2004;1:40-8.
12. Barton I, Koochaki P, Leiblum S, Rodenberg C, Rosen R. Hypoactive sexual desire disorder in postmenopausal women: U.S. results from the women's international study of health and sexuality (WISHeS). Menopause 2006;13:46-56.
13. Gingell C, Glasser D, Laumann E, Moreira E, Nicolosi A, Wang T. Sexual problems among women and men aged 40-80y: Prevalence and correlates identified in the global study of sexual attitudes and behaviors. Int J Impot Res 2005;17:39-57.
14. Nicolosi A, Laumann EO, Glasser DB, Moreira ED Jr, Paik A, Gingell C. Sexual behavior and sexual dysfunctions after age 40: The global study of sexual attitudes and behaviors. Urology 2004;64:991-7.
15. Ishak IH, Low WY, Othman S. Prevalence, risk factors and predictors of female sexual dysfunction in a primary care setting: A survey finding. J Sex Med 2010;7:3080-7.
16. McCall K, Meston C. Differences between pre- and postmenopausal women in cues for sexual desire. J Sex Med 2007;4:364-71.
17. McCall K, Meston C. Cues resulting in desire for sexual activity in women. J Sex Med 2006;3:838-52.
18. Clayton AH, Segraves RT, Leiblum S, Basson R, Pyke R, Cotton D, Lewis-D'Agostino D, Evans KR, Sills TL, Wunderlich GR. Reliability and validity of the Sexual Interest and Desire Inventory-Female (SIDI-F), a scale designed to measure severity of female hypoactive sexual desire disorder. J Sex Marital Ther 2006;32:115-35.
19. Esposito K, Ciotola M, Giugliano F, Bisogni C, Schisano B, Autorino R, Cobellis L, De Sio M, Colacurci N, Giugliano D. Association of body weight with sexual function in women. Int J Impot Res 2007;19:353-7.
20. Maserejian NN, Shifren JL, Parish SJ, Braunstein GD, Gerstenberger EP, Rosen RC. The presentation of hypoactive sexual desire disorder in premenopausal women. J Sex Med 2010;7:3439-48.
21. Panzer C, Wise S, Kang D, Munarriz R, Guay A, Goldstein I. Impact of oral contraceptives on sex hormone-binding globulin and androgen levels: A retrospective study in women with sexual dysfunction. J Sex Med 2006;3:104-13.
22. Meston CM, Frohlich PF. The neurobiology of sexual function. Arch Gen Psychiatry 2000;57:1012-30.
23. Gerstenberger EP, Rosen RC, Brewer JV, Meston CM, Brotto LA, Wiegel M, Sand M. Sexual desire and the Female Sexual Function Index (FSFI): A sexual desire cutpoint for clinical interpretation of the FSFI in women with and without hypoactive sexual desire disorder. J Sex Med 2010;7:3096-103.
24. Basson R. Women's sexual function and dysfunction: Current uncertainties, future directions. Int J Impot Res 2008;20:466-78.
25. Giles J. The nature of sexual desire. Westport, CT: Praeger; 1958.
26. Kaplan HS. Disorders of sexual desire and other new concepts and techniques in sex therapy. New York: Brunner/Hazel; 1979.
27. Pfaus JG. Pathways of sexual desire. J Sex Med 2009;6:1506-33.
28. Rosen R, Brown C, Heiman J, Leiblum S, Meston C, Shabsigh R, Ferguson D, D'Agostino R Jr. The Female Sexual Function Index (FSFI): A multidimensional self-report instrument for the assessment of female sexual function. J Sex Marital Ther 2000;26:191-208.
29. Regan PC, Atkins L. Sex differences and similarities in frequency and intensity of sexual desire. Soc Behav Pers 2006;34:95-102.
30. Basson R. Are our definitions of women's desire, arousal and sexual pain disorders too broad and our definition of orgasmic disorder too narrow? J Sex Marital Ther 2002;28:289-300.
31. Basson R. Recent advances in women's sexual function and dysfunction. Menopause 2004;11:714-25.
32. Buss DM. The evolution of desire. New York: Basic Books; 2003.
33. Rosen RC, Connor MK, Maserejian NN. The HSDD registry for women: A novel patient registry for women with generalized acquired hypoactive sexual desire disorder. J Sex Med 2010;7:1747-56.
34. Kaplan HS. The sexual desire disorders. New York: Brunner-Routlege; 1995.
35. Regan PC, Berscheid E. Lust: What we know about human sexual desire. Thousand Oaks, CA: Sage series on Close Relationships; 1999.
36. Hatfield E, Rapson RL. Passionate love/sexual desire: Can the same paradigm explain both? Arch Sex Behav 1987;16:259-78.
37. Pfaus JG. Neurobiology of sexual behavior. Curr Opin Neurobiol 1999;9:751-8.
38. Basson R. Women's sexual desire-Disordered or misunderstood? J Sex Marital Ther 2002;28(1 suppl):17-28.
39. Bancroft J. Sexual desire and the brain. Sex Relat Ther 1988;3:11-27.
40. Buhler M, Vollstadt-Klein S, Klemen J, Smolka MN. Does erotic stimulus presentation design affect brain activation patterns? Event-related vs. blocked fMRI designs. Behav Brain Funct 2008;4:30.
41. Karama S, Lecours AR, Leroux JM, Bourgouin P, Beaudoin G, Joubert S, Beauregard M. Areas of brain activation in males and females during viewing of erotic film excerpts. Hum Brain Mapp 2002;16:1-13.
42. Gizewski ER, Krause E, Karama S, Baars A, Senf W, Forsting M. There are differences in cerebral activation between females in distinct menstrual phases during viewing of erotic stimuli: A fMRI study. Exp Brain Res 2006;174:101-8.
43. Kim SW, Sohn DW, Cho YH, Yang WS, Lee KU, Juh R, Ahn KJ, Chung YA, Han SI, Lee KH, Lee CU, Chae JH. Brain activation by visual erotic stimuli in healthy middle aged males. Int J Impot Res 2006;18:452-7.
44. Mouras H, Stoleru S, Bittoun J, Glutron D, Pélégrini-Issac M, Paradis AL, Burnod Y. Brain processing of visual sexual stimuli in healthy men: A functional magnetic resonance imaging study. Neuroimage 2003;20:855-69.
45. Moulier V, Mouras H, Pelegrini-Issac M, Glutron D, Rouxel R, Grandjean B, Bittoun J, Stoléru S. Neuroanatomical correlates of penile erection evoked by photographic stimuli in human males. Neuroimage 2006;33:689-99.
46. Mouras H, Stoleru S, Moulier V, Pélégrini-Issac M, Rouxel R, Grandjean B, Glutron D, Bittoun J. Activation of mirror-neuron system by erotic video clips predicts degree of induced erection: An fMRI study. Neuroimage 2008;42:1142-50.
47. Walter M, Bermpohl F, Mouras H, Schiltz K, Tempelmann C, Rotte M, Heinze HJ, Bogerts B, Northoff G. Distinguishing specific sexual and general emotional effects in fMRI-subcortical and cortical arousal during erotic picture viewing. Neuroimage 2008;40:1482-94.
48. Stark R, Schienle A, Girod C, Walter B, Kirsch P, Blecker C, Ott U, Schäfer A, Sammer G, Zimmermann M, Vaitl D. Erotic and disgust-inducing pictures-Differences in the hemodynamic responses of the brain. Biol Psychol 2005;70:19-29.
49. Stoleru S, Gregoire MC, Gerard D, Decety J, Lafarge E, Cinotti L, Lavenne F, Le Bars D, Vernet-Maury E, Rada H, Collet C, Mazoyer B, Forest MG, Magnin F, Spira A, Comar D. Neuroanatomical correlates of visually evoked sexual arousal in human males. Arch Sex Behav 1999;28:1-21.
50. Stoleru S, Redoute J, Costes N, Lavenne F, Bars DL, Dechaud H, Forest MG, Pugeat M, Cinotti L, Pujol JF. Brain processing of visual sexual stimuli in men with hypoactive sexual desire disorder. Psychiatry Res 2003;124:67-86.
51. Redoute J, Stoleru S, Pugeat M, Costes N, Lavenne F, Le Bars D, Dechaud H, Cinotti L, Pujol JF. Brain processing of visual sexual stimuli in treated and untreated hypogonadal patients. Psychoneuroendocrinology 2005;30:461-82.
52. Ferretti A, Caulo M, Del Gratta C, Di Matteo R, Merla A, Montorsi F, Pizzella V, Pompa P, Rigatti P, Rossini PM, Salonia A, Tartaro A, Romani GL. Dynamics of male sexual arousal: Distinct components of brain activation revealed by fMRI. Neuroimage 2005;26:1086-96.
53. Arnow BA, Millheiser L, Garrett A, Lake Polan M, Glover GH, Hill KR, Lightbody A, Watson C, Banner L, Smart T, Buchanan T, Desmond JE. Women with hypoactive sexual desire disorder compared to normal females: A functional magnetic resonance imaging study. Neuroscience 2009;158:484-502.
54. Kawabata H, Zeki S. The neural correlates of desire. PLoS ONE 2008;3:e3027.
55. Jeong GW, Park K, Youn G, Kang HK, Kim HJ, Seo JJ, Ryu SB. Assessment of cerebrocortical regions associated with sexual arousal in premenopausal and menopausal women by using BOLD-based functional MRI. J Sex Med 2005;2:645-51.
56. Park K, Seo JJ, Kang HK, Ryu SB, Kim HJ, Jeong GW. 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.
57. Hamann S, Herman RA, Nolan CL, Wallen K. Men and women differ in amygdala response to visual sexual stimuli. Nat Neurosci 2004;7:411-6.
58. Ortigue S, Bianchi-Demicheli F. The chronoarchitecture of human sexual desire: A high-density electrical mapping study. Neuroimage 2008;43:337-45.
59. Gastaut H, Collomb H. Etude du comportement sexuel chez les epileptiques psychomoteurs. Ann Med Psychol 1954;112:657-96.
60. Freemon FR, Nevis AH. Temporal lobe sexual seizures. Neurology 1969;19:87-90.
61. Oldfield RC. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 1971;9:97-113.
62. Ventura MA, Green MF, Shaner A, Liberman RP. Training and quality assurance with the brief psychiatric rating scale: "The drift buster". Int J Methods Psychiatr Res 1993;3:221-44.
63. Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand 1983;67:361-70.
64. Association AP, ed. Diagnostic and statistical manual of mental disorders. 4th edition. Washington, DC: DSM-IV; 2000.
65. Meston CM. Validation of the Female Sexual Function Index (FSFI) in women with female orgasmic disorder and in women with hypoactive sexual desire disorder. J Sex Marital Ther 2003;29:39-46.
66. Rupp HA, James TW, Ketterson ED, Sengelaub DR, Janssen E, Heiman JR. Neural activation in the orbitofrontal cortex in response to male faces increases during the follicular phase. Horm Behav 2009;56:66-72.
67. Heister G, Landis T, Regard M, Schroeder-Heister P. Shift of functional cerebral asymmetry during the menstrual cycle. Neuropsychologia 1989;27:871-80.
68. Altemus M, Wexler BE, Boulis N. Changes in perceptual asymmetry with the menstrual cycle. Neuropsychologia 1989;27:233-40.
69. Kimura D. Sex and cognition. Cambridge, Mass: A Bradford Book: MIT Press; 1999.
70. Broverman DM, Vogel W, Klaiber EL, Majcher D, Shea D, Paul V. Changes in cognitive task performance across the menstrual cycle. J Comp Physiol Psychol 1981;95:646-54.
71. Rode C, Wagner M, Gunturkun O. Menstrual cycle affects functional cerebral asymmetries. Neuropsychologia 1995;33:855-65.
72. Hausmann M, Becker C, Gather U, Gunturkun O. Functional cerebral asymmetries during the menstrual cycle: A cross-sectional and longitudinal analysis. Neuropsychologia 2002;40:808-16.
73. Hausmann M, Gunturkun O. Steroid fluctuations modify functional cerebral asymmetries: The hypothesis of progesterone-mediated interhemispheric decoupling. Neuropsychologia 2000;38:1362-74.
74. Hausmann M, Slabbekoorn D, Van Goozen SH, Cohen-Kettenis PT, Gunturkun O. Sex hormones affect spatial abilities during the menstrual cycle. Behav Neurosci 2000;114:1245-50.
75. Hausmann M, Tegenthoff M, Sanger J, Janssen F, Gunturkun O, Schwenkreis P. Transcallosal inhibition across the menstrual cycle: A TMS study. Clin Neurophysiol 2006;117:26-32.
76. Shattuck DW, Mirza M, Adisetiyo V, Hojatkashani C, Salamon G, Narr KL, Poldrack RA, Bilder RM, Toga AW. Construction of a 3D probabilistic atlas of human cortical structures. Neuroimage 2008;39:1064-80.
77. Peelen MV, Glaser B, Vuilleumier P, Eliez S. Differential development of selectivity for faces and bodies in the fusiform gyrus. Dev Sci 2009;12:F16-25.
78. Peelen MV, Atkinson AP, Andersson F, Vuilleumier P. Emotional modulation of body-selective visual areas. Soc Cogn Affect Neurosci 2007;2:274-83.
79. Ortigue S, Patel N, Bianchi-Demicheli F. New electroencephalogram (EEG) neuroimaging methods of analyzing brain activity applicable to the study of human sexual response. J Sex Med 2009;6:1830-45.
80. Redoute J, Stoleru S, Gregoire MC, Costes N, Cinotti L, Lavenne F, Le Bars D, Forest MG, Pujol JF. Brain processing of visual sexual stimuli in human males. Hum Brain Mapp 2000;11:162-77.
81. Vuilleumier P. How brains beware: Neural mechanisms of emotional attention. Trends Cogn Sci 2005;9:585-94.
82. LeDoux JE. Emotion circuits in the brain. Annu Rev Neurosci 2000;23:155-84.
83. Cabeza R, Prince SE, Daselaar SM, Greenberg DL, Budde M, Dolcos F, LaBar KS, Rubin DC. Brain activity during episodic retrieval of autobiographical and laboratory events: An fMRI study using a novel photo paradigm. J Cogn Neurosci 2004;16:1583-94.
84. Spiering M, Everaerd W, Elzinga B. Conscious processing of sexual information: Interference caused by sexual primes. Arch Sex Behav 2002;31:159-64.
85. Pizzagalli DA, Lehmann D, Hendrick AM, Regard M, Pascual-Marqui RD, Davidson RJ. Affective judgments of faces modulate early activity (approximately 160 ms) within the fusiform gyri. Neuroimage 2002;16:663-77.
86. Peelen MV, Lucas N, Mayer E, Vuilleumier P. Emotional attention in acquired prosopagnosia. Soc Cogn Affect Neurosci 2009;4:268-77.
87. Laan E, Both S. What makes women experience desire. Fem Psychol 2008;18:505-14.
88. Meston CM, Buss DM. Why humans have sex? Arch Sex Behav 2007;36:477-507.
89. Toates F. An integrative theoretical framework for understanding sexual motivation, arousal, and behavior. J Sex Res 2009;46:168-93.
90. Oya H, Kawasaki H, Howard MA 3rd, Adolphs R. Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli. J Neurosci 2002;22:9502-12.
91. Ochsner KN. Current directions in social cognitive neuroscience. Curr Opin Neurobiol 2004;14:254-8.
92. Frith U, Frith CD. Development and neurophysiology of mentalizing. Philos Trans R Soc Lond B Biol Sci 2003;358:459-73.
93. Masters WH, Johnson VE. Human sexual inadequacy. Boston, MA: Little, Brown; 1970.
94. Kaplan HS. The new sex therapy: Active treatment of sexual dysfunctions. New York: Brunner/Mazel; 1974.
95. Barlow DH. Causes of sexual dysfunction: The role of anxiety and cognitive inference. J Consult Clin Psychol 1986;54:140-48.
96. Rupp A, Wallen K. Sex differences in response to visual sexual stimuli: A review. Arch Sex Behav 2008;37:206-18.
97. Soulieres I, Dawson M, Samson F, Barbeau EB, Sahyoun CP, Strangman GE, Zeffiro TA, Mottron L. Enhanced visual processing contributes to matrix reasoning in autism. Hum Brain Mapp 2009;30:4082-107.
98. Basson R, Brotto LA, Laan E, Redmond G, Utian WH. Assessment and management of women's sexual dysfunctions: Problematic desire and arousal. J Sex Med 2005;2:291-300.
99. Basson R. Clinical practice. Sexual desire and arousal disorders in women. N Engl J Med 2006;354:1497-506.