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
18
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: binggen.zhu@tongji.edu.cn
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.
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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.
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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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