Brain response to putative pheromones in lesbian women.

The progesterone derivative 4,16-androstadien-3-one (AND) and the estrogen-like steroid estra-1,3,5(10),16-tetraen-3-ol (EST) are candidate compounds for human pheromones. In previous positron emission tomography studies, we found that smelling AND and EST activated regions primarily incorporating the sexually dimorphic nuclei of the anterior hypothalamus, that this activation was differentiated with respect to sex and compound, and that homosexual men processed AND congruently with heterosexual women rather than heterosexual men. These observations indicate involvement of the anterior hypothalamus in physiological processes related to sexual orientation in humans. We expand the information on this issue in the present study by performing identical positron emission tomography experiments on 12 lesbian women. In contrast to heterosexual women, lesbian women processed AND stimuli by the olfactory networks and not the anterior hypothalamus. Furthermore, when smelling EST, they partly shared activation of the anterior hypothalamus with heterosexual men. These data support our previous results about differentiated processing of pheromone-like stimuli in humans and further strengthen the notion of a coupling between hypothalamic neuronal circuits and sexual preferences.

[1]  B. Hart,et al.  Female and male sexual responses in female cats with ventromedial hypothalamic lesions. , 1985, Behavioral neuroscience.

[2]  R. Paredes,et al.  Lesions of the medial preoptic area/anterior hypothalamus (MPOA/AH) modify partner preference in male rats , 1998, Brain Research.

[3]  S. Faraone,et al.  A Twin Study of Sexual Behavior in Men , 2004, Archives of sexual behavior.

[4]  Cathryn M. Lewis,et al.  Psychoneuroendocrinology , 1979, Pharmacology Biochemistry and Behavior.

[5]  W. Portillo,et al.  Facilitation of male-like coital behavior in female rats by kindling , 2003, Behavioural Brain Research.

[6]  Ivanka Savic,et al.  Imaging of brain activation by odorants in humans , 2002, Current Opinion in Neurobiology.

[7]  D. Wegesin,et al.  A Neuropsychologic Profile of Homosexual and Heterosexual Men and Women , 1998, Archives of sexual behavior.

[8]  M. Bensafi,et al.  Light microscopy (communication arising): Beyond the diffraction limit , 2002, Nature.

[9]  Sven Joubert,et al.  Areas of brain activation in males and females during viewing of erotic film excerpts , 2002, Human brain mapping.

[10]  B. Gulyás,et al.  Olfactory Functions Are Mediated by Parallel and Hierarchical Processing , 2000, Neuron.

[11]  K. Barnhart,et al.  Male Axillary Extracts Contain Pheromones that Affect Pulsatile Secretion of Luteinizing Hormone and Mood in Women Recipients1 , 2003, Biology of reproduction.

[12]  P. Dalton,et al.  Gender-specific induction of enhanced sensitivity to odors , 2002, Nature Neuroscience.

[13]  B. Dudas,et al.  Close juxtapositions between luteinizing hormone-releasing hormone-immunoreactive neurons and corticotropin-releasing factor-immunoreactive axons in the human diencephalon. , 2002, The Journal of clinical endocrinology and metabolism.

[14]  D F Swaab,et al.  A sexually dimorphic nucleus in the human brain. , 1985, Science.

[15]  C. Turner,et al.  Sex Differences in the Flexibility of Sexual Orientation: A Multidimensional Retrospective Assessment , 2005, Archives of sexual behavior.

[16]  S. Levay,et al.  A difference in hypothalamic structure between heterosexual and homosexual men , 1991, Science.

[17]  Ivanka Savic,et al.  Brain response to putative pheromones in homosexual men. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[18]  G. Dörner,et al.  Differential localization of a male and a female hypothalamic mating centre. , 1968, Journal of reproduction and fertility.

[19]  Alfred C. Kinsey,et al.  Sexual Behaviour in the Human Female , 1954, The Indian Medical Gazette.

[20]  J. Gabrieli,et al.  Imaging gender differences in sexual arousal , 2004, Nature Neuroscience.

[21]  W. H. Elliott,et al.  Identification of estra-1,3,5(10),16-tetraen-3-ol (estratetraenol) from the urine of pregnant women (1). , 1968, Steroids.

[22]  H Eichenbaum,et al.  Selective olfactory deficits in case H.M. , 1983, Brain : a journal of neurology.

[23]  M. Bensafi,et al.  Sniffing a human sex-steroid derived compound affects mood and autonomic arousal in a dose-dependent manner , 2004, Psychoneuroendocrinology.

[24]  R. Gorski,et al.  Two sexually dimorphic cell groups in the human brain , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  T. Hummel,et al.  Androstadienone odor thresholds in adolescents , 2005, Hormones and Behavior.

[26]  D. Pfaff,et al.  Luteinizing hormone-releasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome. , 1989, Brain research. Molecular brain research.

[27]  M. Schuster,et al.  Lesbians' sexual history with men: implications for taking a sexual history. , 1999, Archives of internal medicine.

[28]  B. Gulyás,et al.  Smelling of Odorous Sex Hormone-like Compounds Causes Sex-Differentiated Hypothalamic Activations in Humans , 2001, Neuron.

[29]  Alan C. Evans,et al.  Functional localization and lateralization of human olfactory cortex , 1992, Nature.

[30]  M. Bensafi,et al.  Sex-steroid derived compounds induce sex-specific effects on autonomic nervous system function in humans. , 2003, Behavioral neuroscience.

[31]  B. Gulyás,et al.  Brain activation during odor perception in males and females , 2001, Neuroreport.

[32]  R. Paredes,et al.  Altered sexual partner preference in male ferrets given excitotoxic lesions of the preoptic area/anterior hypothalamus , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  G. Wilson,et al.  Large sexual-orientation-related differences in performance on mental rotation and judgment of line orientation tasks. , 2003, Neuropsychology.

[34]  Gilles Sicard,et al.  Functional Anatomy of Perceptual and Semantic Processing for Odors , 1999, Journal of Cognitive Neuroscience.

[35]  W. Rohde,et al.  A neuroendocrine predisposition for homosexuality in men , 1975, Archives of sexual behavior.

[36]  J. Pardo,et al.  Functional neuroimaging of the olfactory system in humans. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[37]  D. F. Swaab,et al.  An enlarged suprachiasmatic nucleus in homosexual men , 1990, Brain Research.

[38]  D. Swaab,et al.  Gender and sexual orientation in relation to hypothalamic structures. , 1992, Hormone Research.

[39]  M. Kavaliers,et al.  Comparing immune activation (lipopolysaccharide) and toxin (lithium chloride)-induced gustatory conditioning: lipopolysaccharide produces conditioned taste avoidance but not aversion , 2004, Behavioural Brain Research.

[40]  M. Bensafi,et al.  Sniffing human sex-steroid derived compounds modulates mood, memory and autonomic nervous system function in specific behavioral contexts , 2003, Behavioural Brain Research.

[41]  L. Monti-Bloch,et al.  Behavioral and electrophysiological effects of androstadienone, a human pheromone , 2000, Psychoneuroendocrinology.

[42]  G. Engel,et al.  Neuropsychology , 1994, Schizophrenia Research.

[43]  M. McClintock,et al.  Psychological Effects of Musky Compounds: Comparison of Androstadienone with Androstenol and Muscone , 2002, Hormones and Behavior.

[44]  J. D. E. Gabrieli,et al.  Sniffing and smelling: separate subsystems in the human olfactory cortex , 1998, Nature.

[45]  M. McClintock,et al.  Context-dependent effects of steroid chemosignals on human physiology and mood , 2001, Physiology & Behavior.

[46]  Y. Chung,et al.  Assessment of sexual orientation in lesbian/gay/bisexual studies. , 1996, Journal of homosexuality.

[47]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[48]  A. Bogaert Birth order and sexual orientation in women. , 1997, Behavioral neuroscience.

[49]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[50]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[51]  G. Schaltenbrand,et al.  Einführung in die stereotaktischen Operationen : mit einem Atlas des menschlichen Gehirns = Introduction to stereotaxis, with an atlas of the human brain , 1959 .

[52]  Ralf Deichmann,et al.  Functional Heterogeneity in Human Olfactory Cortex: An Event-Related Functional Magnetic Resonance Imaging Study , 2002, The Journal of Neuroscience.

[53]  R. Spitzer Can Some Gay Men and Lesbians Change Their Sexual Orientation? 200 Participants Reporting a Change from Homosexual to Heterosexual Orientation , 2003, Archives of sexual behavior.