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Similar to desired gender/different from assigned gender
Abbreviations: DTI = diffusion tensor imaging, FA = fractional anisotropy, SPECT = single photon emission tomography, rCBF = regional cerebral blood flow, PET = positron emission tomography, (f)MRI = (functional) magnetic resonance imaging, EEG = electroencephalogram, MR = magnetic resonance, FtM = female-to-male transsexuals, MtF = male-to-female transsexuals, SO = sexual orientation in relation to natal sex, OA = onset age, onset of cross-gender identification. a This group also tested an MtF group on hormone treatment evidence for feminization in their brains, whereas Rametti et al., 2011b only studied androphilic/homosexual (and early onset) MtF transsex- uals and found white matter microstructure patterns to be in between those of male and female controls, which could be explained as demasculization or incomplete masculinization. However, some of the other studies in non-androphilic/non-homosexual MtFs also observed similarities with female controls (see Table 1). FtMs constitute a rather homogeneous group with regard to sexual orientation and onset age and all studies in FtMs show differences compared to control women, which may be explained as a result of masculinization of their brains. Adolescent gender identity development and the brain Although adolescence seems to be a crucial period in gender vari- ant identity development, none of the aforementioned brain studies included gender dysphoric adolescent participants. Sex differences in the brain are present before adolescence, for example, sex differ- ences were observed at the age of 7 in total brain volume, gray and white matter volume (Giedd et al., 2012). However, puberty is the period in which male and female brains increasingly diverge (Lenroot and Giedd, 2010), and some brain sex differences may only be present after puberty. For example, Chung et al. (2002) showed that the sex dif- ference in the BSTc, the nucleus that was found to differ between trans- sexuals and non-transsexuals (Swaab and Garcia-Falgueras, 2009) became significant only in adulthood. Trajectories of brain development show sex differences as well: gray matter volumes seem to follow inverted U shaped trajectories with a peak size occurring earlier in females, whereas white matter volumes become increasingly divergent as men and women reach adulthood (Giedd et al., 2012). Pubertal sex hormones are associated with development of the brain: changes in cortical thickness are related to testosterone levels (Nguyen et al., 2012), increased levels of estradiol with gray matter development in girls (Peper et al., 2009), and functional polymor- phism of the androgen receptor moderates the effect of testosterone on relative white and gray matter volumes in boys (Paus et al., 2010). Recently, it has been postulated that puberty is an organizing period in itself, either as a separate period of sensitivity (Sisk and Zehr, 2005), or as a continuum of declining sensitivity from gestation until adulthood (Schulz et al., 2009), but separate from the prenatal sexual differentiation of the brain by organizing effects of gonadal hormones. One way to test this hypothesis suggested by Berenbaum and Beltz (2011) is to compare sex typed characteristics of adoles- cents with GID and having no hormonal interventions with those of adolescents with GID whose puberty was suppressed in a randomized clinical trial. The assumption would be that adolescents under gonad- al suppression would be less sex-typed than those who have a typical puberty, if sex hormones (testosterone and estradiol) organize the brain during puberty. They mention that this design is limited by the fact that it remains unclear to what extent the effects of pubertal hormones are influenced by the effects that have started during the prenatal period. There are also other problems related to such a study. It would not only be unethical to withhold supression of puber- ty in adolescents with GID, but one could also expect the willingness to participate in such a study to be nil. Puberty suppression by use of GnRH analogs is part of a careful clinical approach to gender dyspho- ria in adolescents that also comprises an extensive diagnostic proce- dure and psychological interventions, if necessary (Cohen-Kettenis et al., 2011). This fully reversible medical intervention provides ado- lescents with GID with time and rest before making definite decisions on gender reassignment without the distress of developing secondary sex characteristics. Withholding puberty suppression from an adoles- cent with GID might lead to depression, anxiety and arrests in social and cognitive development, and consequently hinder reliable mea- surement of gendered cognitive abilities and personality traits, as was suggested (Berenbaum and Beltz, 2011). Genetic studies Historically, studies into the biological roots of sex differences in brain and behavior focused on the role of prenatal exposure to gonadal hormones, but the interest in genetic factors in the development of sex differences is increasing (Ngun et al., 2011). This is also the case with regard to gender identity development. In a few studies in transsexuals associations were found between polymorphisms in genes related to sex steroid receptors or sex steroid metabolism and transsexualism, but results are very inconsistent (Ngun et al., 2011). Findings from twin studies show a more consistent picture: substantial heritability of gender dysphoria was estimated in children and adolescents (Coolidge et al., 2002), and a recent review of case reports on gender identity disorder in twins, showed that nearly 40% of the monozygotic twins were concordant for GID, whereas none of the dizygotic same- sex twins were (Heylens et al., 2012). These studies suggest that genetic factors certainly play a role in the development of gender dysphoria, but altogether, their role in gender identity development is far from clear and warrants further study. Conclusion Despite the current interest among professionals and lay people in gender non-conforming adolescents and the growing use of puberty suppression as an aid in the clinical management, there is a surprising lack of knowledge on adolescent gender identity development. While earlier studies mainly focused on the role of psychosocial factors on gen- der identity development in gender variant or gender dysphoric chil- dren, recent research has merely concentrated on its biological roots. Studies on individuals with DSD show that prenatal exposure to gonadal hormones affects gender role behavior, but its effects on gen- der identity are less straightforward. Although it is likely that prenatal hormone effects also affect gender identity development, the majori- ty of individuals with DSD who are prenatally exposed to elevated levels of androgens and are raised female, do not experience any gen- der identity problems. In brain imaging studies on individuals with gender dysphoria, evidence for a priori differences between individ- uals with GID and members of their natal sex prevails, although such differences have not been found on all measures, and the direc- tion of the differences is not always consistent with the sexual differ- entiation hypothesis. On several, but not all, investigated brain measures, individuals with GID resemble members of their experi- enced gender or score in-between males and females. Data from post-mortem, neuropsychological and imaging studies support the idea that biological factors are of importance in the development of gender dysphoria and may be seen as a DSD that is limited to the brain, but are as yet not sufficient to form a basis for a broad theory of GID (Meyer-Bahlburg, 2011). Despite the fact that the sexual differentiation hypothesis has been supported by quite a few studies, a number of points remain to be elucidated. One is the question of whether the brain differences between transsexuals and controls are a result of prenatal exposure to atypical levels of sex hormones only, need pubertal hormones to become manifest, are caused by other factors or need other factors to become manifest (Wallen, 1996). Another issue is to what extent the differences that have been found are directly related to gender identity or more indirectly related to aspects of functioning that influ- ence, but not determine, gender identity. Furthermore, brain struc- ture and functioning may alter as a result of certain behaviors, which complicates interpretation of the findings. The current evi- dence makes clear that there is no simple relationship between brain development and function on the one hand, and gender identity development on the other. Despite the acknowledgment that nature and nurture interact, researchers have so far not tried to integrate both aspects. Psychological and environmental factors have been studied separately, but to a lesser extent than biological ones. Although elevated levels of psychopathology in the parents, increased anxiety of the child, and a lack of parental limit setting have been put forward as possible determinants of atypical gender identity development, the evidence from these studies is, like in the brain studies, not unequivocal. Furthermore, it is unclear whether factors such as child anxiety and parental limit setting, are the cause of gen- der variant identity development or are a consequence of the gender variance. Of great relevance for the clinical management of gender non- conforming adolescents, is the question of whether gender identity is already consolidated before adolescence or only becomes fixed in early or late adolescence or even in adulthood. Follow-up studies on gender variant children and gender dysphoric adults designate ado- lescence as a crucial period for the consolidation of gender identity and persistence of gender dysphoria in early onset individuals and for the initiation of gender dysphoria in late onset individuals. More specifically, high rates of desistance of gender dysphoria in adoles- cence, its emergence in late onset gender dysphoric persons, with and without autogynephilia, and the high persistence of gender dys- phoria once it is established after puberty, all denote that adolescence may be vital for various developmental trajectories of gender variant identity. Although parents and medical professionals may not be very open to the requests of children with DSD for a gender change in childhood, the fact that most gender changes happen after puberty is also in line with a postpubertal consolidation of gender identity. There is, however, a wide variation in clinical presentations of youth with gender dysphoria. It is conceivable that in some, due to DSD or other factors, a (gender conforming, cross- or other) gender identity was not firmly established in childhood. For them, gender identity consolidation may be dependent on the hormonal and other, maybe psychosocial, changes that are associated with puberty. The study by McHale et al. (2009), designated the role of social context on gen- der development and gender interests during adolescence, and indi- cated a moderating role for testosterone for some of the aspects measured. Also from other studies so far, not one causal factor can be deter- mined and it is most likely that gender identity development is the result of a complex interplay between biological, environmental and psychological factors. Factors like hormones and genes cause differ- ences in morphology and physiology that in turn may lead to differ- ent interactions with the environment (McCarthy et al., 2012). In addition to this, the evidence is growing that the environment and experiences, for example stress (Hunter, 2012), can have permanent effects on the brain. It is also conceivable that sex-related experiences as experienced during adolescence shape the human brain. If biolog- ical, environmental and psychological factors are all in concordance with each other, gender identity seems to be fixed early in develop- ment and hardly susceptible to change over time. In case of discor- dance between or ambiguity of any of the factors, as in DSD and gender dysphoric individuals, the outcome may be more variable and the period in which gender identity becomes crystallized is less clear. As was indicated by Cadet (2011), gender identity has a cogni- tive component, also later in life. This implies that those who have been dissatisfied or confused about their gender identity (individuals with DSD and the children with less extreme gender dysphoria, or males who discover the association between dressing in female cloth- ing and intensely pleasant sexual sensations in early adolescence), may change gender identity more easily than those with a strongly established gender identity and associated interests. As for the clinical management of gender dysphoric adolescents, the introduction of puberty suppression has proven to relieve their acute suffering. However, despite its success one should realize that little is known as yet on what exactly happens around puberty concerning gender identity development, and that the role of gonadal hormones is largely unexplained. 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