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Human sexuality
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Psychosexual behavior
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Sexual function disturbances
Sexuality

Sexual orientation refers to an individual’s personal and social identity involving behaviors and/or emotions concerning homosexuality, heterosexuality, and bisexuality. The ultimate causes and mechanisms of sexual orientation development in humans remain unclear and many theories are speculative and controversial. However, advances in the sciences of the brain (neuroscience) are providing evidence, support, and explanation of these ideas and are illustrating characteristics linked to sexual orientation.[How to reference and link to summary or text] StudiesTemplate:Which? have explored structural neural-correlates, functional and/or cognitive relationships, and developmental theories relating to sexual orientation in humans.

Developmental neurobiology

Many theories concerning the development of sexual orientation involve fetal neural development, with proposed models illustrating prenatal hormone exposure, maternal immunity, and developmental instability. Other proposed factors include genetic control of sexual orientation. No conclusive evidence has been shown that environmental or learned effects are responsible for the development of non-typical sexual orientation.[1]

Prenatal androgen model

Sexual dimorphisms in the brain and behavior among vertebrates are accounted for the by the influence of gonadal steroidal androgens as demonstrated in animal models over the past few decades. The prenatal androgen model of homosexuality describes the neuro-developmental effects of fetal exposure to these hormones.[1] In 1985, Geschwind and Galaburda proposed that homosexual men are exposed to high androgen levels early in development, explaining their tendency to be less right-handed and by extension the hyper-masculinized traits observed in this population. [1] It is currently argued[attribution needed] that temporal and local variations in androgen exposure to a fetus’s developing brain is a factor in the pathways determining homosexuality. Recent researchTemplate:Which? has been performed to find somatic markers for prenatal hormonal exposure which have been found to show variation based on sexual orientation in healthy adult individuals.

Other evidence supporting the role of testosterone and prenatal hormones in sexual orientation development include observations of male subjects with cloacal exstrophy who were sex-assigned as female during birth only later to declare themselves male. This supports the theory that the prenatal testosterone surge is crucial for gender identity development. Additionally, females whose mothers were exposed to diethylstilbestrol (DES) during pregnancy show higher rates of bi- and homosexuality.[2]

2D:4D digit ratio

The best, non-invasive, marker of prenatal hormone exposure is the digit ratio of the second and fourth finger lengths (2D:4D ratio), a known sexually dimorphic measure (males showing lower ratios than females). Patients with androgen over-exposure (such as in congenital adrenal hyperplasia) show lower 2D:4D ratios,[3][4] providing evidence linking prenatal androgen exposure as key to this feature. XY individuals with androgen insensitivity syndrome due to a dysfunctional gene for the androgen receptor present as women and have feminine digit ratios, as would be predicted if androgenic hormones affect digit ratios. This finding also demonstrates that the sex difference in digit ratio is unrelated to the Y chromosome per se.[5] Additionally, the 2D:4D ratio has been shown to be affected by variation in the androgen receptor gene in men.[6] The ratio of testosterone to estrogen in amniotic fluid has also been found to be negatively correlated with the 2D:4D ratio.[1]

Independent studies indicate that homosexual women have masculinized (lower) digit ratios,[7][8][9][10][11][12][13][14][15][16] and homosexual men show either hyper-masculinized or feminized ratios. These findings reinforce the prenatal androgen model - abnormal prenatal hormone exposure is related to the development of human homosexuality.[1]

Auditory evoked potentials

Studies of the central nervous system processing of auditory sensation, aspects of which has been linked to prenatal androgen exposure, to click-stimuli have shown that homosexual women have masculinized responses while homosexual men have hyper-masculinized responses.[1]

Fraternal birth order effect

Studies show that homosexual men have higher numbers of older male siblings.[17] This finding led to the development of the fraternal birth order effect theory of homosexuality, stating that a mother becomes progressively immunized to successive male children, leading to increased chances of homosexuality in later male children. The mechanism involves the mother producing increasing anti-male antibodies to male-specific antigens expressed in male fetuses. These antibodies are thought to block the full masculinization of the fetal brain by “binding to and inactivating male-specific molecules located on the surface of fetal brain cells”[18] thus preventing the morphogenesis of masculinized sexual preferences.[18] Estimations indicate that there is a 33% increase in chances of homosexuality in a male child with each older male sibling.[1] A BBC study reported that the fraternal birth order effect does not apply to left-handed homosexual males. Support for this theory is given by data indicating that the effect holds true only for biological brothers and the chances of male homosexuality is not increased by the number of older stepbrothers or adoptive siblings. This theory does not apply to the development of female homosexuality.[18]

Developmental instability and handedness

The chances of being left-handed are increased in homosexual populations. Homosexual men have an approximate 34% odds ratio of being non-right-handed while lesbian women have 91% odds of being so, both compared to heterosexual populations.[1] It has been proposed that non-right-handedness (including ambidexterity) is related to homosexuality through developmental instability.[18] Developmental instability refers to the level of vulnerability to environmental and genetic stresses and perturbations during development.

Structural differences

Postmortem and imaging studies over the past two decades have revealed structural differences in both global structures and sexually-related brain structures between heterosexual and homosexual subjects.

Hypothalamus

The hypothalamus is known to be involved in sex differences in reproductive behavior, mediating responses in menstrual cycles in women and specifically the anterior hypothalamus of the brain helps regulate male-typical sexual behavior. Recently, the hypothalamus has been linked to gender identity and sexual orientation.[19]

A seminal paper by Simon LeVay found that the an interstitial nucleus of the hypothalamus INAH3 was found to be dimorphic according to sexual orientation not gender. These results were obtained from postmortem analysis of hypothalamic nuclei of known homosexual subjects compared to heterosexual patients.[20]

The hypothalamus is also linked to sexual orientation through findings that show that activity of aromatase, an important enzyme converting androgens to estrogens, is high in the preoptic hypothalamic region of mammals during the pre- and neonatal periods. This activity is linked to sexual differentiation and may be a basis in structural and functional sexual differences playing a role in mediating the sexual orientation development due to prenatal hormonal exposure.[19]

The suprachiasmatic nucleus (SCN) of the anterior hypothalamus has also been found to relate to sexual orientation, with homosexual men having twice as large of a vasopressin-containing subnucleus of the SCN than heterosexuals. This might be a neurological explanation for the finding that homosexual men arise and retire earlier each day than heterosexuals, as it is known that the SCN is involved in modulating human circadian rhythms.[19] Analogously, in a rat model study, it was found that male rats treated with an aromatase inhibitor showed a partner preference for females when tested in the late dark phase but showed homosexual mating preferences when tested in the early dark phase, implicating the involvement of the SCN in sexual orientation in other species.[19]

Cerebral asymmetry

The size of the brain’s hemispheres is a sexually dimorphic trait in which men tend to show asymmetry in the volumes of their hemispheres while women show volumetric symmetry. A recent volumetric MRI study indicated that homosexuals showed sex-atypical symmetry: homosexual men showed hemispheric volumes to be symmetric similar to heterosexual women and homosexual women showed asymmetry in hemispheric volumes as heterosexual men do. These findings demonstrate a global neurological difference in brain structures showing sex-atypical characteristics associated with sexual orientation.[21]

Anterior commissure

The anterior commissure, a bundle of white matter fibers connecting the two cerebral hemispheres, was found by Allen and Gorski to be larger in homosexual men and heterosexual women than in heterosexual men.[19] This finding provides a possible anatomical basis for higher inter-hemispheric functional connections in homosexuals explaining why homosexual men and heterosexual women show language circuit functional symmetry in out performing heterosexual men in verbal tests.[21]

Functional differences

Recent studiesTemplate:Which? have begun exploring the functional and cognitive substrates of sexual orientation, ultimately a behavioral manifestation. Neural processing in response to specific stimuli and sexually-biased cognitive tasks have been found to be correlated with an individual’s sexual orientation.

Response to pheromones

Two proposed human pheromones – the progesterone derivative 4,16-androstadien-3-one (AND) and an estrogen-like steroid estra-1,3-5(10),16-tetraen-3-ol (EST) – have been shown to have sexual orientation specific responses in activating the neural circuits of the anterior hypothalamus in homosexual and heterosexual subjects. The anterior hypothalamus is involved in processing reproductive functions and recent evidence suggests it helps integrate hormonal and sensory cues involved in sexual behavior and sexual preference.[22]

Recent functional neuro-imaging experiments have shown that the presentation of AND, found in male sweat, as a olfactory stimuli produced normal olfactory responses in heterosexual men and homosexual women, while activating the anterior hypothalamus in homosexual men and heterosexual women.[23] The proposed pheromone EST, found in the urine of pregnant women, produces normal olfactory activation in homosexual men and heterosexual women while homosexual women and heterosexual men demonstrated sexually-related hypothalamic responses.[22]

Homosexual men showed the same sexually-related functional responses to these stimuli as heterosexual women and homosexual women responded like heterosexual men. This research conducted by Berglund and Savic indicates overall that AND and EST induce “sex-specific effects on the autonomic nervous system” and that the stimuli elicited a response pathway that was dependent on the subject’s sexual orientation rather than phenotypic sex.[23]

Functional cerebral asymmetry

Differences in neural processing and cognitive tasks have been found in relation to sexual orientation. In a 1987 review on cognition, cerebral lateralization, and sexual orientation, Sandes and Ross-Field suggested that prenatal hormonal events would lead to functional cerebral asymmetries related to sexual orientation.[24]

Certain cognitive tasks are known to be sexually dimorphic. The better verbal ability of women is associated with reduced lateralization of language tasks while the male advantage in spatial reasoning corresponds to marked cerebral lateralization. Sexual orientation effects in some of these tasks have been found in recent studies.

In the Vincent Mechanical Diagrams test, a dot detection divided field measure of functional cerebral asymmetry, homosexual men performed the same as heterosexual women with both scoring lower than heterosexual men displaying less asymmetry. Additionally, homosexual men display higher verbal performance IQ scores on subtests of the Wecshler Adult Intelligence Scale, in concordance with female testing patterns.[24] On several other tests,Template:Which? including a male-biased targeted throwing task and a female-biased Purdue pegboard test, the performance of homosexual men and heterosexual women showed no statistical difference from each other, while both significantly differed from heterosexual men.

Additionally, reduced asymmetry was found in a magnetoencephelographic study in which MEG-based source location estimates of an auditory evoked signal is found to be hemispherically symmetric in heterosexual women and homosexual men, while asymmetric in heterosexual men.[24]

Response to visual sexual stimuli

A recent functional magnetic resonance imaging study has demonstrated that upon viewing of both heterosexual and homosexual erotic visual stimuli, only those images corresponding to the subject’s sexual orientation produced hypothalamic activation patterns associated with sexual arousal.[25] The response of heterosexuals viewing heterosexual adult videos showed the same pattern of sexual arousing neural processing as homosexuals viewing same-sex adult videos, while the viewing of the opposite orientation’s images did not elicit the same response.

Related studies

Various animal and insect models have been used to explore sexual orientation and brain characteristics. One experiment involved genetically altering male Drosophila causing them to have feminized brain structures involved in processing sexually dimorphic contact pheromones. Transformed males showed increase homosexual courtship behaviors to wild-type male flies, and there a correlation was found between the courtship behavior and the expression of the altered gene in the sexually related brain regions.[26]

A 2004 study exploring the difference in brain metabolism between heterosexual and homosexual males found that homosexuals had a significant reduction in hypothalamic glucose metabolism compared to that of heterosexuals with other brain regions including the prefrontal association cortex and portions of the cingulate cortex showing differences in the measured activation.[27]

Future studies

The development of sexual orientation is a far from complete subject. While neuroscience has made advancements shedding light on the mechanisms and relationships between the human brain and sexual orientation, much more further research should be conducted.

Areas for future research include:[1]

  • finding markers for sex steroid levels in the brains of fetuses that highlight features of early neuro-development leading to certain sexual orientations
  • determine the precise neural circuitry underlying direction of sexual preference
  • use animal models to explore genetic and developmental factors that influence sexual orientation
  • further population studies, genetic studies, and serological markers to clarify and definitively determine the effect of maternal immunity
  • neuroimaging studies to quantify sexual-orientation-related differences in structure and function in vivo
  • neurochemical studies to investigate the roles of sex steroids upon neural circuitry involved in sexual attraction

References

  1. 1.0 1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.8 (2005). The neurodevelopment of human sexual orientation. Neuroscience & Biobehavioral Reviews 29: 1057.
  2. Swaab DF (December 2004). Sexual differentiation of the human brain: relevance for gender identity, transsexualism and sexual orientation. Gynecological Endocrinology 19 (6): 301–12.
  3. [http://msu.edu/~breedsm/pdf/CAHFingersFinal.pdf Brown et al. 2002
  4. Okten et al. 2002
  5. Berenbaum SA, Bryk KK, Nowak N, Quigley CA, Moffat S (November 2009). Fingers as a marker of prenatal androgen exposure. Endocrinology 150 (11): 5119–24.
  6. (2003). The second to fourth digit ratio and variation in the androgen receptor gene. Evolution and Human Behavior 24: 399–405.
  7. Williams, T.J. et al. (2000). Finger-length ratios and sexual orientation.
  8. Tortorice, J.L. (2002). Written on the body: butch/femme lesbian gender identity and biological correlates. Rutgers Ph.D. Dissertation.
  9. McFadden D, Shubel E (December 2002). Relative lengths of fingers and toes in human males and females. Hormones and Behavior 42 (4): 492–500.
  10. Hall LS, Love CT (February 2003). Finger-length ratios in female monozygotic twins discordant for sexual orientation. Archives of Sexual Behavior 32 (1): 23–8.
  11. Rahman Q, Wilson GD (April 2003). Sexual orientation and the 2nd to 4th finger length ratio: evidence for organising effects of sex hormones or developmental instability?. Psychoneuroendocrinology 28 (3): 288–303.
  12. Csathó A, Osváth A, Bicsák E, Karádi K, Manning J, Kállai J (February 2003). Sex role identity related to the ratio of second to fourth digit length in women. Biological Psychology 62 (2): 147–56.
  13. (2004). Sex hormones and finger lengthWhat does 2D:4D indicate?. Evolution and Human Behavior 25: 182.
  14. Rahman Q (May 2005). Fluctuating asymmetry, second to fourth finger length ratios and human sexual orientation. Psychoneuroendocrinology 30 (4): 382–91.
  15. Kraemer B, Noll T, Delsignore A, Milos G, Schnyder U, Hepp U (2006). Finger length ratio (2D:4D) and dimensions of sexual orientation. Neuropsychobiology 53 (4): 210–4.
  16. Wallien MS, Zucker KJ, Steensma TD, Cohen-Kettenis PT (August 2008). 2D:4D finger-length ratios in children and adults with gender identity disorder. Hormones and Behavior 54 (3): 450–4.
  17. Bogaert AF (July 2006). Biological versus nonbiological older brothers and men's sexual orientation. Proceedings of the National Academy of Sciences of the United States of America 103 (28): 10771–4.
  18. 18.0 18.1 18.2 18.3 Blanchard R, Lippa RA (April 2007). Birth order, sibling sex ratio, handedness, and sexual orientation of male and female participants in a BBC internet research project. Archives of Sexual Behavior 36 (2): 163–76.
  19. 19.0 19.1 19.2 19.3 19.4 Swaab DF, Hofman MA (June 1995). Sexual differentiation of the human hypothalamus in relation to gender and sexual orientation. Trends in Neurosciences 18 (6): 264–70.
  20. LeVay S (August 1991). A difference in hypothalamic structure between heterosexual and homosexual men. Science 253 (5023): 1034–7.
  21. 21.0 21.1 Savic I, Lindström P (July 2008). PET and MRI show differences in cerebral asymmetry and functional connectivity between homo- and heterosexual subjects. Proceedings of the National Academy of Sciences of the United States of America 105 (27): 9403–8.
  22. 22.0 22.1 Berglund H, Lindström P, Savic I (May 2006). Brain response to putative pheromones in lesbian women. Proceedings of the National Academy of Sciences of the United States of America 103 (21): 8269–74.
  23. 23.0 23.1 Savic I, Berglund H, Lindström P (May 2005). Brain response to putative pheromones in homosexual men. Proceedings of the National Academy of Sciences of the United States of America 102 (20): 7356–61.
  24. 24.0 24.1 24.2 Sanders G, Wright M (October 1997). Sexual orientation differences in cerebral asymmetry and in the performance of sexually dimorphic cognitive and motor tasks. Archives of Sexual Behavior 26 (5): 463–80.
  25. Paul T, Schiffer B, Zwarg T, et al. (June 2008). Brain response to visual sexual stimuli in heterosexual and homosexual males. Human Brain Mapping 29 (6): 726–35.
  26. Ferveur JF, Störtkuhl KF, Stocker RF, Greenspan RJ (February 1995). Genetic feminization of brain structures and changed sexual orientation in male Drosophila. Science 267 (5199): 902–5.
  27. Kinnunen LH, Moltz H, Metz J, Cooper M (October 2004). Differential brain activation in exclusively homosexual and heterosexual men produced by the selective serotonin reuptake inhibitor, fluoxetine. Brain Research 1024 (1-2): 251–4.

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