Jennifer I. Downey, MD

In this article we discuss psychoneuroendocrine influences on sexual orientation and the psychodynamics of internalized homophobia. Because of space limitations, we focus on homosexual orientation, although research in this area sheds light on heterosexual and bisexual orientation as well.

Research that has been conducted on the relationships between hormones and behavior suggests that prenatal hormones might influence sexual orientation in some persons. Although this hypothesis still requires definitive proof, accumulating evidence has ever-increasing clinical significance.

It has long been recognized that male sex-stereotypical behavior in many animals-mounting, penile insertion, pelvic thrusting-is controlled by the medial preoptic area of the hypothalamus. Female sex-stereotypical behavior-lordosis (arching of the back)-is controlled by the ventromedial nucleus. These hypothalamic nuclei are organized by sex steroid hormones. During a critical period of prenatal or (depending on the species) perinatal life, the male fetal testis secretes androgen, which alters the structure of the hypothalamus, increasing male sex-stereotypical behavior later in development and diminishing female sex-stereotypical behavior. In humans, a testosterone surge occurs between the 8th and 24th week of pregnancy. If no testosterone surge occurs, the brain differentiates as female, and the sex-stereotypical behavior that develops is also typically female-organized around the lordosis response.

It is possible to experimentally manipulate prenatal sex steroid hormones to influence animals to demonstrate both female and male sex-stereotypical responses (lordosis and mounting).

 Based on this research, a number of investigators have speculated that human sexual orientation might be influenced by prenatal hormones.

This theory of hypothalamic influence on human sexual orientation has found some support; for example, some girls who are exposed to increased prenatal androgens because of congenital adrenal hyperplasia (CAH) have increased homosexual interest and diminished heterosexual interest later in life. Even though these findings are not robust and most such girls grow up to become heterosexual women, they point in a direction predicted by the prenatal androgen hypothesis.

 undertook a study that increased attention to this line of thinking. He observed that a particular hypothalamic nucleus (the third interstitial nucleus of the anterior hypothalamus [INAH 3]) in roughly the same location in humans as the sexual dimorphic nucleus (SDN) of rats was much smaller in homosexual than heterosexual men and, in fact, similar in size to that of women. Because this nucleus is prenatally influenced by androgens, he speculated that the object of sexual interest of rats and humans might be controlled by similar hormone-brain interactions. LeVay studied brain structure, not function, however, and a subsequent attempt to replicate his research by Byne and colleagues

 studied sheep, an animal species in which a small number of males prefer mounting other males to females. These male-oriented rams were shown to differ from female-oriented rams in one particular hypothalamic nucleus. This hypothalamic nucleus was located in roughly the same place as the rat SDN and INAH 3 in humans. However, the researchers emphasized that there was no way of knowing whether these hypothalamic nuclei are homologous across species. They called the sheep nucleus ovine (o)SDN.

However, ancillary evidence was found to strengthen the argument that this hypothalamic nucleus might influence the sexual object of sheep. In the brain, androgens are converted to estrogens, which then act on estrogen receptors to masculinize sexual behavior. The enzyme responsible for this steroid conversion is aromatase. The Roselli group found that messenger RNA levels for aromatase were higher in the oSDN in males than in females, and higher in those rams sexually oriented toward females than those sexually oriented toward males.

Among men motivated to have sex with other men, some might simply be expressing behavior prenatally determined by hypothalamic structures formed under the influence of sex steroid hormones whose ebbs and flows happened to differ from those of the mainstream. Although scant, some data do exist to support this theory in humans and to suggest that a similar line of reasoning may be applied to some women.

On the one hand, persons who have same-sex partners are quite diverse, and no psychobiological generalizations about their motivation can possibly be applied to all. On the other hand, the psychoneuroendocrine research only briefly outlined here is undeniably intriguing and, at the very least, indicates that psychiatrists must be cognizant of prenatal hormonal influences on brain structure and function in order to understand sexual behavior.

Prenatal androgen and gender-role behavior

Prenatal androgen also influences gender-role behavior. This is evident from the play patterns of girls with early corrected CAH. These children tend to play more like boys than unaffected girls do. They tend to be tomboys, for example, and enjoy rough-and-tumble activities more frequently than their sisters. Although their childhood gender-role behavior is somewhat boy-like, most of these girls see themselves as female and are not uncertain about their gender identity. Gender identity formation usually is the product of many interacting biological, psychological, and social influences, including intrafamilial relationships.

The play behavior of toddlers is also shaped by prenatal androgens.

 As children grow and acquire ever greater social experience and cognitive sophistication, their childhood play patterns become incorporated into gender-stereotypical play. During the juvenile phase of development, when gender-segregated play is the norm, the different play styles of the children of different sexes influence their peer relationships. Boys tend to form peer groups that are hierarchical, exclusive of adults, and frequently organized around team sports. Boys' groups are also likely to be intolerant of gender-atypical behavior in other boys and may stigmatize those drawn to such behavior as "sissies." In keeping with play styles present since toddlerhood, peer groups of girls tend to be less aggressive and walled off from adults and more tolerant of gender-atypical behavior. This is not to suggest that girls are somehow "nicer" than boys. Both sexes may be equally friendly or mean. They tend to differ in their attitudes toward gender-role behavior, however.

Boys and girls on a nonheterosexual developmental pathway are more likely than those on a heterosexual path to be drawn toward nonstereotypical gender-role activities. This developmental phenomenon occurs for reasons that have not been definitively determined, but it has been taken by some investigators as additional indirect evidence of prena- tal neuroendocrine influence on brain embryogenesis.

As noted above, there seems to be a tendency for boys with atypical gender-role interests to be penalized by other males in a way that is less common among girls. Such penalty comes in the form of bullying, threats of violence, or ostracism often beginning by the juvenile phase of development.

 Although the tolerance of girls for cross-gender behavior is greater than that of boys, it is not boundless. For example, a now famous case report discusses the development of a boy who was raised as a girl after an accidental penile amputation in early childhood.

 As a juvenile, she was tormented by female peers and was called "gorilla" because of extremely masculine gender-role behavior, which was incongruent with a female name and gender of her rearing. Such behavior appeared to be an innate attribute of the child's temperament (presumably due to masculinazation of the hypothalamus) and resisted attempts to modify it psychosocially.

 This case illustrates the response of female peers to a girl with extremely boy-like gender-role behavior. Many other instances of prenatal androgenization of girls have been discussed in which complex nature-nurture interactions have been described.

Peers are not the only source of difficulties for boys, however. Often older males-even fathers and other relatives-are also intolerant of atypical gender-role behavior. An important reason for difficulties between boys on a homosexual developmental track and their fathers is temperamental incompatibility in gender-role behavior. The son's innate temperamental proclivity toward nonstereotypical gender-role activities provokes anxiety and defensive responses in the father whose attitudes and values about masculinity are likely to be influenced by his own sex-stereotypical gender-role temperament.

Childhood difficulties with same-sex peers and with his father may have additive effects in diminishing a child's self-regard and contributing to his sense of being "different."

 The feeling of not belonging to the mainstream may also be influenced by awareness of romantic and sexual feelings toward those of the same sex.

The term "homophobia" was introduced almost half a century ago to indicate irrational aversion to nonheterosexual persons and has now become part of everyday parlance.

 Arguably, its most distressing manifestation is violence, almost always perpetrated by males, and directed against males more frequently than females.

Homophobic violence is perhaps best understood as being a special type of male aggression. Worldwide, some men and boys have a tendency to be violent, and their victims include other men, women, and children.

 This tendency, however, is not simply due to the effects of testosterone, either prenatal or postnatal. Most men are not violent, and androgenized females are not any more prone to violence than ordinary ones. We speculate that the antecedent history of childhood neglect/abuse with disruption of secure bonding increases the likelihood of male violence later in life. We do view the tendency of some males toward violence, however, as a pathological distortion of the tendency of most to engage in a certain type of male-bonding behavior whose earliest manifestation is rough-and-tumble play.

 Prenatal testosterone effects most likely interact with postnatal psychosocial influences to shape behavior, either in a prosocial or antisocial direction.

Many clinicians and investigators have documented an increased prevalence of psychopathology among homosexual  men and women compared with heterosexual individuals and have generally attributed this to minority stress and stigmatization.

Psychodynamic psychiatry offers an additional conceptual model for understanding the phenomenon of internalized homophobia. Children internalize the attitudes, values, and moral precepts of significant others. These internalizations all influence the conscience structure of the child. Violation of internal taboos triggers guilt, and failure to live up to internal standards leads to shame. Guilt and shame are the affects associated with "internalized homophobia"-a term introduced in the 1980s.

Clinical experience indicates that negative internalizations from different phases of development and including different significant others can become condensed into a unitary negative self-label. Internalized homophobia is not a specific psychopathological syndrome. Rather, it is a psychological dynamic found across all syndromes and may influence severity and treatment outcome in varying degrees, depending on clinical context.

There are many influences on internalized homophobia; in this article only those commonly associated with gender-role difficulties-due to innate temperamental incompatibilities between a boy, his family members, and peers, are addressed.

Bill W., a homosexual man, sought treatment for depression. Although most of his symptoms rapidly improved with appropriate pharmacological intervention, he had persistent low self-esteem that required psychotherapy. Painful experiences at varying stages of development influenced a negative self-image about being homosexual. This self-condemnatory stance had persisted, despite the fact that he was a highly regarded member of the homosexual community-openly homosexual at work and with all significant others.

As a child, Bill avoided team sports, preferred girl to boy playmates, and was drawn to art and drama. His father, an enthusiastic weekend athlete, withdrew from him in favor of his older brother-a star hockey player. In middle school, Bill had been bullied and ostracized by male peers. During adolescence he had been menaced and beaten on more than one occasion and called "fag." For years-until late adolescence, when he went to college-he felt so anxious around groups of men that he became nauseated. As an adult, much of his low self-esteem was related to self-destructive behavior motivated by the mental mechanism of identification with the aggressor.

This negative self-label was based on childhood internalizations, primarily of his father and peers. In psychotherapy, significant attention was devoted to the influence of his temperament on the development of his personality-particularly in the area of gender-role behavior. The ongoing therapeutic effort was directed to reframing the interests determined by his innate temperament so that they could be positively valued by him. As the work progressed, his chronic feelings of shame, present since childhood, diminished.

Although many patients who experience internalized homophobia respond positively to an affirmative supportive stance about being homosexual, others require psychotherapy. In psychotherapy, improvement is not only associated with efforts to help the patient overcome present life stress but also to better understand childhood determinants of negative self-esteem.

The factors contributing to the genesis of internalized homophobia must be assessed on a case-by-case basis. In addition, the same types of variables that influence treatment outcome in psychotherapy generally are relevant here. These include the presence of psychiatric disorder(s), a past history of trauma, the genetically influenced tendency toward psychopathology versus adaptive coping, and the quality of the therapeutic relationship.

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Jennifer I. Downey, MD

Articles

Sexual Orientation: Neuroendocrine and Psychodynamic Influences