Neuroscience and sexual orientation

Sexual orientation is an enduring pattern of romantic or sexual attraction (or a combination of these) to persons of the opposite sex or gender, the same sex or gender, or to both sexes or more than one gender.[1][2] The ultimate causes and mechanisms of sexual orientation development in humans remain unclear and many theories are speculative and controversial. However, advances in neuroscience explain and illustrate characteristics linked to sexual orientation. Studies 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-heterosexual orientation.[3]

Prenatal androgen model

Sexual dimorphisms in the brain and behavior among vertebrates are accounted for 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.[3] 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.[3] It is currently argued that temporal and local variations in androgen exposure to a fetus’s developing brain is a factor in the pathways determining homosexuality. Recent research 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.[4]

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,[5][6] 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.[7] Additionally, the 2D:4D ratio has been shown to be affected by variation in the androgen receptor gene in men.[8] The ratio of testosterone to estrogen in amniotic fluid has also been found to be negatively correlated with the 2D:4D ratio.[3]

Independent studies indicate that homosexual women have masculinized (lower) digit ratios,[9][10][11][12][13][14][15][16][17][18] and homosexual men show either hyper-masculinized or feminized ratios. These findings reinforce the prenatal androgen model that atypical prenatal hormone exposure is related to the development of human homosexuality.[3]

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.[3]

Fraternal birth order effect

Studies show that homosexual men have higher numbers of older male siblings.[19] This finding led to the discovery of the fraternal birth order effect, according to which the more older brothers a man has from the same mother, the greater the probability is that he will have a homosexual orientation. Estimations indicate that there is a 33% increase in chances of homosexuality in a male child with each older male sibling.[3] The fraternal birth order effect only applies to right-handed homosexual males; it does not increase the likelihood of homosexuality in left-handed or ambidextrous males. As the effect is contingent on handedness and handedness is a prenatally determined trait, the fraternal birth order effect is understood to be biological, rather than psychosocial, in nature and is known to operate prenatally.[20] The biological mechanism by which it is believed to operate prenatally states 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”[21] thus preventing the morphogenesis of masculinized sexual preferences.[21] Support for this mechanism 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. The effect does not apply to the development of female homosexuality.[21]

Developmental instability and handedness

The chances of being left-handed may be increased in homosexual populations. In comparison with a heterosexual sample, a 2000 meta-analysis of earlier studies [22] showed that homosexual men have approximately one-third (34%) higher odds of being left-handed while homosexual women have almost twice (91%) higher odds of being so.[22] It has been proposed that non-right-handedness (including ambidexterity) is related to homosexuality through developmental instability.[21]

However, as the effect is not particularly strong, the results remain disputed, even though several studies appear to show a relationship.[23][24]

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 a portion of the brain that contains a number of 'nuclei' (discrete groups of cell bodies of neurons).[note 1] 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.[27]

A seminal paper by Simon LeVay found that an interstitial nucleus of the hypothalamus, INAH3, was dimorphic according to sexual orientation not gender. Specifically, the INAH3 of homosexual men was found to be smaller in volume than that of heterosexual men. These results were obtained from postmortem analysis of hypothalamic nuclei of known homosexual subjects compared to heterosexual patients.[28] Further research has found that the INAH3 is of smaller volume in homosexual men than in heterosexual men because homosexual men have a higher neuronal density in the INAH3 than heterosexual men; there is no difference in the number or cross-sectional area of neurons in the INAH3 of homosexual versus heterosexual men.[29] It has also been found that there is no effect of HIV infection on the size of INAH3, that is, HIV infection does not account for the observed difference in INAH3 volume between homosexual and heterosexual men.[29]

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.[27]

The suprachiasmatic nucleus (SCN) of the anterior hypothalamus has also been found to relate to sexual orientation, as it is larger in size and more elongated in shape in homosexual males than in heterosexual males and females. The vasopressin-containing subnucleus of the SCN of homosexual men is twice as large and has 2.1 times as many cells than the vasopressin-containing subnucleus of the SCN in heterosexual men.[30][27] This may 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.[27] 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.[27]

Bed nucleus of the stria terminalis

The bed nucleus of the stria terminalis (BNST) is a forebrain limbic area that is involved in control of mating behaviour. It receives neuronal inputs from the medial amygdala and the accessory olfactory bulb and sends projections to both the medial preoptic area and the ventromedial nucleus of the hypothalamus.[31][32] The central part of the BNST (BNSTc) is 44% larger in heterosexual men than heterosexual women and 62% larger in homosexual men than heterosexual women.[33] The BNSTc is larger in homosexual men than heterosexual men, though the difference in size is not statistically significant.[33] The BNSTc of homosexual men appears to be ‘hypermasculinised’ as it is larger than the BNSTc of both heterosexual men and women.[32]

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.[27] 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.[34]

The narrow region between the body and splenium of the corpus callosum is called the isthmus. It is larger in size in homosexual versus heterosexual men.[35]

Corpus callosum

The corpus callosum (CC), like the anterior commissure, is a major neuronal link connecting the two cerebral hemispheres. However, unlike the anterior commissure (which is present in all vertebrates), the CC is only present in placental animals (including humans).[36] An MRI study comparing the CC of right-handed homosexual and heterosexual men found that all parts of the CC are larger in homosexual men.[37] In particular, the isthmus (a part of the CC between the callosal body and the splenium) is significantly larger in size in homosexual than heterosexual men.[35][36] The size of the CC has a strong genetic basis, with heritability rates between 82–94%.[35] This association of sexual orientation with a brain structure having high heritability supports a genetic and neurobiological basis in the origin of sexual orientation.[35]

Gray matter

Gray matter is a major part of the central nervous system that is composed mostly of neuronal cell bodies. While men generally have greater amounts of grey and white matter than women (due to men’s larger body mass and consequently larger brain size), women generally possess a greater grey matter-to-white matter ratio and thicker layers of grey matter in specific cortical areas compared to men.[38][39] It has been found that homosexual women have relatively less gray matter than heterosexual women in the ventral cerebellum, left ventral premotor cortex, temporo-basal cortex, and most significantly, in the left perirhinal cortex. No difference in amount of gray matter was found between heterosexual and homosexual men.[38]

These findings are important because the perirhinal cortex is located near brain regions (entorhinal cortex, hippocampus, parahippocampal gyrus, and amygdala) involved in olfactory and spatial processing, which have been shown to exhibit differences in sexual orientation — specifically, homosexual women are known to perform higher than heterosexual women in spatial processing tests.[38][40] The perirhinal cortex itself is involved in functions related to the processing of sexual stimuli such as olfactory processing, memory encoding and spatial processing. It is also involved in detection of object identity. Olfactory processing is known to modify sexual attraction in humans and the olfactory system is able to differentiate pheromone-like compounds according to sexual orientation.[38]

The finding that homosexual women have a “male-like” GM pattern but homosexual men do not have a “female-like” pattern indicates that male and female homosexuality do not manifest the same way at a structural level in the brain. In addition, other findings of sexually dimorphic features that are more male-like in homosexual women, but not female-like in homosexual men, include otoacoustic emissions, the 2D:4D finger ratio, and body build. Altogether, these findings suggest that sex-atypical levels of prenatal androgen action may be involved in the origin of female homosexuality but not in the origin of male homosexuality.[38]

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.[34] It was also found that that both homosexual men and homosexual women show different amygdala connections than do heterosexual men and women.[34][40]

Functional differences

Recent studies 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.[41]

Recent functional neuro-imaging experiments have shown that the presentation of AND, found in male sweat, as an olfactory stimuli produced normal olfactory responses in heterosexual men and homosexual women, while activating the anterior hypothalamus in homosexual men and heterosexual women.[42] 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.[41]

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.[42]

Response to visual sexual stimuli

Sexual arousal is a highly coordinated process that prepares a person for reproductive behavior. Widespread changes occur in the person’s neurophysiological state during arousal to achieve adaptive responses. The person’s attentive, affective, and motivational systems are optimized so that successful selection and engagement of sexual stimuli may occur. In response to visual sexual stimuli, men exhibit category-specific genital and self-reported subjective sexual arousal. Their greatest sexual arousal is to the categories of people with whom they prefer to have sex — homosexual men experience higher genital and subjective arousal to men than to women (and thus prefer male sexual stimuli) whereas heterosexual men experience higher genital and subjective arousal to women than to men (and thus prefer female sexual stimuli). Hormones are believed to prenatally influence the development of neural structures that regulate sexual behavior. Hence, it is thought that certain aspects of neurohormonal development in homosexuals proceed in a manner different from heterosexuals, resulting in psychological differences such as distinct triggers (or 'stimuli') for sexual arousal.[43]

A 2007 functional magnetic resonance imaging (fMRI) study exploring the neural mechanisms of sexual arousal in homosexual and heterosexual men showed their subjects male–male and female–female sexual interactions. They demonstrated that homosexual and heterosexual men activate the same brain regions after each one is exposed to a sexual stimulus concordant with the subject’s sexual orientation (i.e., male–male sexual interactions for homosexual men and female–female sexual interactions for heterosexual men).[43]

Another fMRI study demonstrated that upon viewing of both male–female and male–male erotic visual stimuli, only those videos corresponding to the subject’s sexual orientation produced activation patterns in brain areas associated with sexual arousal. The response of heterosexuals viewing male–female adult videos showed the same pattern of sexual arousing neural processing as homosexuals viewing male–male adult videos, while the viewing of the opposite orientation’s images did not elicit the same response. Significant correlation was found between sexual arousal and neural activation in the hypothalamus, a key brain region in sexual function. Self-reported sexual arousal ratings were also equal in both groups. However, the magnitude of hypothalamic activation was lower in homosexual men than heterosexual men, a characteristic that is shared by women who are attracted to men.[44]

Another fMRI study determined the patterns of brain activation in homosexual and heterosexual subjects while exposing them to male–male, male–female and female–female sexual visual stimuli. They found that brain regions such as the left angular gyrus, right pallidum and left caudate nucleus were exclusively activated in homosexual men whereas the bilateral lingual gyrus, the right parahippocampal gyrus and the right hippocampus were exclusively activated in heterosexual men. These findings indicate that the neural circuits (related to the processing of visual sexual stimuli) that are active during sexual arousal in homosexual and heterosexual men are different.[45]

Another fMRI study showed heterosexual and homosexual men and women photographs of aroused male and female genitals. By limiting the visual sexual stimulus to photographs of genitals, the authors minimized neuronal activity related to neuronal processing of various stimuli such as faces, voices, body movements, and sexually arousing body parts other than genitals. They found that the ventral striatum, centromedian thalamus and bilateral ventral premotor cortex showed a stronger response to photographs of aroused genitals of the preferred sex relative to corresponding photographs of the non-preferred sex. As the ventral striatum and centromedian thalamus are known to be activated by innate preferences, the selective responsiveness of these regions to preferred sexual stimuli appears to reflect a predetermined response pattern. This notion is supported by evidence that sexual orientation is biological in origin.[46]

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, Sanders and Ross-Field suggested that prenatal hormonal events would lead to functional cerebral asymmetries related to sexual orientation.[47]

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 tasks 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 Wechsler Adult Intelligence Scale, in concordance with female testing patterns.[47] On several other tests, 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.[47]

A flat oval object is surrounded by blue. The object is largely green-yellow, but contains a dark red patch at one end and a number of blue patches.
PET image of the human brain showing energy consumption

Response to serotonin

Serotonin is a neurotransmitter found in the central nervous system that has various roles in the regulation of sexual behavior. Serotonin agonists and antagonists have activational or inhibitory effects depending on their concentration and the brain area involved. Fluoxetine is a selective serotonin reuptake inhibitor that prolongs the effect of serotonin on neurons.[48] Kinnunen et al. (2004) administered fluoxetine to their study subjects to see if the brain is differentially activated in homosexual and heterosexual men through the action of serotonin.[49][48] After fluorexine administration, they measured glucose metabolism in the brain by using fluorodeoxyglucose positron emission tomography (FDG-PET). They found that the brain response to fluoxetine differs between homosexual and heterosexual men, that is, homosexual men show a smaller reduction of glucose metabolism in the hypothalamus than heterosexual men. In addition, other areas of the brain were differentially activated: the prefrontal association cortex of homosexual men exhibited increased activity after fluoxetine administration while the prefrontal association cortex of heterosexual men did not show any change. The cunate gyrus, lateral anterior cingulate and bilateral hippocampus/ parahippocampal gyrus of heterosexual men exhibited increased activity while decreased activity was seen in portions of their cingulate cortex.[49] These findings suggest that homosexuals and heterosexuals may not only differ in the total number of neurons in various areas of their central nervous systems, but also may differ in the distribution of certain kinds of neurons, such as serotonergic and dopaminergic neurons.[48]

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.[50]

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:[3]

Notes

  1. ↑ The term nucleus in neuroanatomy must not be confused with the term nucleus in cytology. In cytology, the term nucleus refers to the organelle found in eukaryotic cells that contains the cell's genetic material. In neuroanatomy, the term nucleus refers to discrete groups of densely packed neuronal cell bodies in the central nervous system.[25][26] In anatomical sections, a nucleus appears as a region of gray matter surrounded by white matter.

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