The Change of Heterosexual Preference in Adolescents: Implications of Stress and Cognitive Regulation on Sexual Orientation

doi:10.4236/jss.2013.16004

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Open Journal of Social Sciences

2013. Vol.1, No.6, 18-22

Published Online November 2013 in SciRes (http://www.scirp.org/journal/jss) http://dx.doi.org/10.4236/jss.2013.16004

Open Access

The Change of Heterosexual Preference in Adolescents:

Implications of Stress and Cognitive Regulation on Sexual

Orientation

Binggen Zhu1,2*, Xiaodan Ren1*, Jing Cao1, Yujie Wu1, Rongshen Zhu1

1The Department of Psychiatry at Shanghai Tenth People’s Hospital,

Tongji University School of Medicine, Shanghai, China

2Departmet of Physiology, Tongji University School of Medicine, Shanghai, China

Email: [email protected]

Received October 2013

Sexual orientation is a complex area. It is unclear to date how people precisely establish their preferred

sexual objects. This paper presents two cases, whose heterosexual preference were changed in late ado-

lescent age after a severe psychological event, to draw attention to the study of the possible underlying

mechanism. Case 1, one identical male twin, was seriously punished at age 12 years, as he loved a girl in

his classroom. Afterwards, he feared to contact with girls, and became attracted to young men at age 17

years, and kept same-sex sexual behaviors since then. However, his twin brother is always heterosexual.

Case 2, a girl at age 16 years, was unexpectedly betrayed by her boyfriend, she bore great pain and dis-

tress in the beginning. Since then, she had a definite opinion that men were unbelievable, and gradually

turned her heterosexual preference and had same-sex sexual behaviors with a girl classmate more than 3

years. Our case presentation indicates that severe frustration of primary heterosexual desires or behaviors

and the successive cognitive regulation might lead susceptible adolescents into reorienting their sexual

preference. The role of prefrontal cortex and related neurom odul at or y pat hways were discussed.

Keywords: Adolescents; Sexual Orient at i on; Sexual Prefer ence; Stress; Cognitive Regulation

Introduction

Sexual orientation is a complex area (Rubio-Aurioles & Wy-

lie, 2008). It is unclear to date how people precisely establish

their preferred sexual objects, although many researchers sig-

nify the contributions of sex steroid hormones, sex chromo-

some genes, and environment and socialization factors (Arnold,

2009; Corsello et al., 2011; Garcia-Falgueras & Swaab, 2010;

Hines, 2011). The differentiation of sex-specific gonads deter-

mined by the function of sex chromosone genes is a primary

step in the physiological development of sex (Blecher & Erick-

son, 2007; DiNapoli & Capel, 2008). Then, sex-specific traits

(including structures and functions) in nongonadal tissues are

determined by sex steroids (e.g. testosterone and estrogen) se-

creted from the developing gonads, according to an absolute

hormonal determinism (Arnold, 2009; Garcia-Falgueras &

Swaab, 2010). Fetal exposure to sex steroids particularly plays

a major organizing influence on the expression of later sexual

dimorphism (Arnold, 2009). But the hypothesis of hormonal

determinism has been challenged. There are good evidences

suggesting that the cell-autonomous information directly pro-

vided by sex chromosome genes, but unrelated to gonadal hor-

mones, participates in the establishment of tissue sex differen-

tiation (Arnold, 2009; Bocklandt & Vilain, 2007). Moreover,

after birth, in addition that the early and pubertal surges of tes-

tosterone or estrogen continue to play organizing/activating

roles in sex-specific body and behavioral development (Beren-

baum & Beltz, 2011), environment and socialization factors

gain importance (Corsello et al., 2011; Hines, 2011; Joel, 2011).

Parents/caregivers and then peers usually encourage children to

develop in their physiological gender-type way, guiding by the

widely -recognized psychological characteristics of sexual di-

morphism.

Some of brain structures are found to exhibit sexual dimor-

phism, which is presumably related to sexual orientation (Her-

bert, 2008; Savic & Lindstrom, 2008). Many researchers

pointed to the third interstitial nucleus of the anterior hypotha-

lamus, because it is 2.5 times larger in men than in women, and

this volume difference in other mammals results from prenatal

testosterone exposure (Herbert, 2008; Savic, Garcia-Falgueras,

& Swaab, 2010). Moreover, patterns of cerebral asymmetry and

functional brain connectivity/network are also linked to sexual

orientation in men and women (Savic & Lindstrom, 2008; Cor-

sello et al., 2011). Some studies indicate that the right hemis-

phere is larger in men and the connection between left and right

hemisphere is more extensive in women, whereas cerebral

asymmetry is not pronounced in homosexual men, as well as

women (Savic & Lindstrom, 2008; Hines, 2011). Homosexual

men and heterosexual women displayed more pronounced be-

tween-amygdala connections and greater connections with the

anterior cingula te, the subcallo sum, and the hyp othalamu s. How-

ever, the sensorimotor cortex and striatum displayed stronger

connections in homosexual women and heterosexual men

(Savic & Lindstrom, 2008). The sex differences in the adoles-

cent brain were already recognized clearly, implying the orga-

nizational effect of sex hormones and genes (Lenroot & Giedd,

2010). It is not known whether social and environmental factors

engage the same neural circuitry as underlie the effects of sex

hormones and genes (Hines, 2011).

*Binggen Zhu and Xiaodan Ren contributed equally t o t his work.

B. G. ZHU ET AL.

Open Access

There are several types of sexual orientation, such as hetero-

sexual, homosexual, bisexual (Rubio-Aurioles & Wyl ie , 2008).

Studies and clinical practices disclosed that sexual orientation,

at least in some people, is not unchangeable (Davis et al., 1996;

Friedman & Downey, 2002, 2010; Jones & Yarhouse, 2011).

Some persons who had a heterosexual or homosexual life for

more than ten years became bisexual when they had to deal

with tough life events at middle age (Friedman & Downey,

2010). Here, we present two cases, whose heterosexual prefe-

rence were changed in late adolescent age after a severe psy-

chological event and successive cognitive regulation, to draw

attention to the study of the possible underlying mechanism.

Case Presentation

Two cases were assessed according to the clinic practice

guidelines, follow-up studies were made in case 1 for nearly 4

years by phone calls and two interviews. The study was ap-

proved by the institutional research ethics committee of the

Tenth People’s Hospital affiliated to Tongji University School

of Medicine, and written informed consent was obtained from

each subject.

Case 1: A young male, at age 24 years. He is the older iden-

tical twin of two. His mother forced him to take treatments in

order to return his sexual orientation from homosexual to hete-

rosexual, as his twin brother was heterosexual, and he had been

interested in girls during his early adolescent period. At age 12

years, he fell in love with an attractive girl in his classroom. He

sought any chances to contact with this girl, and wrote letters to

her. But the girl did not love him, and passed his letters on to

their advisor. The female advisor criticized him seriously, and

slapped him across the face, and read his letters in the class-

room before all of his classmates. He was astonished and re-

pressed, and felt ashamed of being treated like thi s. He became

timid, and realized that girls were untouchable. He gradually

lost interest in girls. Meanwhile, his sexual preference changed.

At age 17 years, he acknowledged that he failed to grow at-

tracted to any girl. In contrast, he had interests in young men,

although his twin brother dated a girl at that time. Since then,

he has been dating several male partners, being high on same-

sexual activities, and his sexual preference to men has not been

altered after referral to our clinic for nearly 4 years of follow-up

observation. There is neither family history of psychiatric dis-

eases, nor Axis I and Axis II diagnosis for him, in the descrip-

tive terminology of the DSM-IV (American Psychiatric Asso-

ciation, 1994).

Case 2: A young female, at age 21 years. She, as a high

school second-year student at age 16 years, dated a young man

for 3 months, and had sexual intercourse with him. She was

very sad and angry after she occasionally realized that the man

had other female sexual partners. She hated his disloyal be-

havior, and instantly determined to end their relationship.

Meanwhile, she had a definite opinion that men were un- be-

lievable. One of her girl classmate, whose parents divorced,

was attracted to her at that time. She gradually became a sexual

partner of the girl with various sexual activities, such as oral

sex and mutual masturbation, and was satisfied with her homo-

sexual life more than 3 years. But she felt upset and depressed,

and had poor sleep in recent two months, as the relationship

between her and the girl was almost broken, and she felt totally

wronged by saying that she had male sex partners. She came to

our clinic for relieving her depressed mood. There is neither

family history of psychiatric diseases, nor DSM-IV Axis II

diagnosis for her.

Discussion

Our case 1, a male identical twin, changed his heterosexual

preference from girls to young men, since being suffered a

serious psychological distress at age 12 years, while his twin

brother maintained the heterosexuality without any change. Pre-

vious data showed familial clustering of same-sex sexual beha-

vior (Bailey , Dunne, & Mar tin, 2000; Kendler, Thornton, Gil-

man, & Kessler, 2000; Sant tila, Sandnabba, Harlaar, Varjonen,

Alanko, & von der Pahlen, 2008), but a new population-based

study of twins, analyzed by the biometric modeling, revealed

that the genetic effects were moderate or mild (0.34 - 0.39 in

men and 0.18 - 0.19 in women), unique environmental factors

contributed much more (0.61 - 0.66 in men and 0.64 - 0.66 in

women) (Langstrom, Rahman, Carlstrom, & Lichtenstein,

2010). The experience of our case 1 is concordant with this

recent finding. But, it is, to some extent, different from the

reports in the literature, particularly of the famous “Joan/John

(one of identical male twins) case”, that supported that ultimate

male or female assignment decisions mainly depend upon the

action of sex chromosome genes and the imprinting of prenatal

testosterone (Bostwick & Martin, 2007; Friedman, 2001).

Our two cases were young man and woman, but they chang-

ed the heterosexual preference during the adolescent period,

because their primary sex desires were severely frustrated.

They lost their dignity, meanwhile, had to endure the unexpec-

tedly stressful situation. They bore great pain and distress, since

the adolescent brain is very sensitive to stress (Casey , Jones, &

Somerville, 2011; Sebastian, Tan, Roiser, Viding, Dumontheil,

& Blakemore, 2011). The sexual preference was altered in the

background of the psychological stress and sufferings and after

a series of behavioral/cognitive reactions, such as behavioral

withdrawal, reappraisal and cognitive regulation.

Many studies have demonstrated that strong acute stress and

mild repeated stress cause functional and structural changes in

some brain regions, such as the hippocampus, prefrontal cortex

(PFC), and amygdala, that are parts of a neural circuit that plays

a central role in fear conditioning and stress responsivity

(McEwen, 2010). According to animal experiments, the stress

caused dendritic shortening in medial prefrontal cortex and hip-

pocampus, but produced dendritic growth in neurons in amyg-

dala, as well as in orbitofrontal cortex (McEwen, 2010). These

structure changes induced by the strong psychological stress

might compromise the development of regional sexual dimor-

phism in the brain/sexually dimorphic brain connectivity

guided by sex chromosone and sex hormones, resulting in the

conversion of heterosexual orientation in some susceptible

adolescents.

As the PFC, which is responsible for the higher-order cogni-

tive regulation (Coutlee & Huettel, 2012), is continuing to de-

velop during adolescence and throughout the third decades of

life before stabilizing at the adult level (Petanjek, Judas, Rasin,

Uylings, Rakic, & Kostovic, 2011). This results in use-depen-

dent patterns of connectivity, and has implications for under-

standing the effect of environmental impact (including the psy-

chological stress) on the development of human cognitive and

emotional capacities as well as the onset of age-related beha-

vioral manifestations (Lee & Hoaken, 2007). The orbital PFC is

primed to detect negative effect, and plays important role in the

B. G. ZHU ET AL.

Open Access

reappraisal (Kalisch, 2009; Kanske, Heissler, Schonfelder, Bon-

gers, & Wessa, 2011). The previous clinical data revealed that

the operations of immature PFC in adolescents is prone to get a

distorted cognitive regulation (Casey, Jones, & Somerville,

2011; Ernst & Korelitz, 2009; Sebastian, Tan, Roiser, Viding,

Dumontheil, & Blakemore, 2011; Sturman DA & Moghaddam

B, 2011). The distorted recognition and reappraisal which pos-

sibly produced a latently converse regulation might lead sus-

ceptible adolescents changing their sexual preference against

his or her physiological sex gender and primary heterosexual

desires or behaviors.

In both male and female rodents, the vomeronasal system

which receives pheromonal inputs was found tonically to inhi-

bit the expression of social and reproductive innate responses

typically shown by the opposite sex (Dulac & Kimchi, 2007).

Male or female mice in which the vomeronasal organ (VNO)

had been surgically or genetically (TRPC2−/−) ablated were

found to indiscriminate courtship, or do in a complete reversal

of sex-specific behavior (Dulac & Kimchi, 2007). The mount-

ing behavior of TRPC2−/− male mice was towards both males

and females (Stowers, Holy, Meister, Dulac, & Koentges,

2002), and VNO-deficient female mice attempted to copulate

with other mice in a male-specific manner (Kimchi, Xu, &

Dulac, 2007). It is worth pointing out that elimination of this

pheromone-mediated sensory repression during development or

adulthood results in the rapid reversal of sex-specific behavioral

responses, independently from the organizational action of

gonadal hormones during development (Dulac & Kimchi,

2007). However, there is no reported evidence that human be-

ings have active sensory neurons like those in working vome-

ronasal systems of other animals (Dulac & Kimchi, 2007; Witt

& Hummel, 2006). In addition to gonadal hormones and con-

stitutive chemosensory information, monoamine signaling is

also involved in the neuromodulation. A recent study has

shown that adult male mice defective in serotonin signaling

lose their normal mating preference for females over males, and

attempt to mate with male mice (Liu, Jiang, Si, Kim, Chen, &

Rao Y, 2011). As the strong cognitive regulation has been de-

veloped in human being, following the enlargement of newer

brain areas (prefrontal cortex) (Meeks & Jeste, 2009), some

conservative neuromodulatory pathways in animals, such as

vomeronasal chemosensory system, might be evolutionarily

eliminated through competition, and be given place to a new

mate recognition mechanism. We suppose that the PFC and

related neuromodulatory factors/systems, such as gonadal hor-

mones, adrenal stress hormones, and serotonin systems, play an

important role in the development of the mate recognition me-

chanism, and is mainly responsible for the targeting process in

human sexual orientation. The mate recognition systems which

gradually built up along with the development of PFC and re-

lated neuromodulatory pathways might be vulnerable and

changeable in some susceptible adolescents.

Our hypothesis is consistent with a consensus that the top-

down neuromodulatory pathways play a crucial role in human

in regulating behavioral decision-making (Meeks & Jeste, 2009;

Heatherton & Wagner, 2011). The PFC and related neuromo-

dulatory approaches let humans to effectively handle complexi-

ties and uncertainties in the environment and predict future

events and make appropriate decisions (Coutlee & Huettel,

2012; Mushtaq, Bland, & Schaefer, 2011). Some researchers

focused on the organizing effect of prenatal sex steroid hor-

mones and the key role of hypothalamus. They insisted that

sexual orientation is determined during early development, as

well as the physiological gender, and left little room for learn-

ing models of sexual orientation (Garcia-Falgueras & Swaab,

2010; Rahman, 2005; Savic, Garcia-Falgueras, & Swaab, 2010;

Swaab, 2004). However, their hypothesis is not compatible

with the clinical data and genetic research findings (Davis et al.,

1996; Friedman & Downey, 2010; Joel, 2011; Langstrom,

Rahman, Carlstrom, & Lichtenstein, 2010), and our case pres-

entation. According to the recent phylogenetic studies, there is

mounting evidence that supports the roles of social learning and

social recognition in determining and shaping mate choice and

preferences (Kavaliers & Choleris, 2013; Verzijden, Cate, Ser-

vedio, Kozak, Boughman, & Svensson, 2012). Males and fe-

males of many species learn their mate preferences, and learn-

ing can take place throughout life, although sexual imprinting,

which occurs at early stage of life, affecting pair formation at a

much later stage in life, is seen in some birds and mammals

(Verzijden, Cate, Servedio, Kozak, Boughman, & Svensson,

2012). Human being should not be an exception. An absolute

prenatal hormonal determinism is not accepted widely, but it is

maintained that the hormonal prenatal milieu simply changes

the threshold for the development of an appropriate psycho-

sexuality, interacting in any case with a series of postnatal va-

riables (Corsello et al., 2011).

Our case presentation has some limitations. First, because

both patients disagreed with further examination, such as sexual

and adrenal hormone test, brain imaging, and personality as-

sessment did not carry out, corresponding data was lacking.

Second, the stress and successive cognitive regulation in two

adolescent cases documented retrospectively took place several

years ago and no concrete data detailed the degree and the

course. Third, in addition to stress and cognitive regulation, the

susceptibility is also essential. Personal history, personality,

executive function, fami ly function, brain image, etc. should be

studied simultaneously. All of these disadvantages have to be

overcame in the future research.

In conclusion, our case presentation suggests that severe fru-

stration of primary heterosexual desires and successive cogni-

tive regulation might lead to reorientation of sexual preference

in susceptible adolescents. The PFC and related neuromodula-

tory pathways may play an important role in a human mate

recognition mechanism. The operations of immature PFC and

related neuromodulatory pathways which are vulnerable to

stress may underlie a converse regulation in these susceptible

adolescents, resulting in the conversion of heterosexual orienta-

tion.

Acknowledgemen ts

We thank Prof. Friedman at Weil Medical College, Cornell

Univrsity Medical School, for providing relative literatures

which are not available for us.

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