Neurobiological characteristics associated with gender identity: Findings from neuroimaging studies in the Amsterdam cohort of children and adolescents experiencing gender incongruence.

Bakker, Julie

doi:10.1016/j.yhbeh.2024.105601

Article (Scientific journals)

Neurobiological characteristics associated with gender identity: Findings from neuroimaging studies in the Amsterdam cohort of children and adolescents experiencing gender incongruence.

Bakker, Julie

2024 • In Hormones and Behavior, 164, p. 105601

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/323552

DOI
10.1016/j.yhbeh.2024.105601

PubMed
39029340

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Review HB SBN 2024.pdf

Author postprint (563.59 kB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Cognition; Gender identity; Hormones; Hypothalamus; Puberty; Humans; Adolescent; Child; Male; Female; Netherlands; Cohort Studies; Puberty/physiology; Transgender Persons; Neuroimaging/methods; Brain/diagnostic imaging; Brain/growth & development; Gender Identity; Gender Dysphoria/diagnostic imaging; Brain; Gender Dysphoria; Neuroimaging; Endocrinology; Endocrine and Autonomic Systems; Behavioral Neuroscience

Abstract :

[en] This review has been based on my invited lecture at the annual meeting of the Society for Behavioral Neuroendocrinology in 2023. Gender incongruence is defined as a marked and persistent incongruence between an individual's experienced gender and the sex assigned at birth. A prominent hypothesis on the etiology of gender incongruence proposes that it is related to an altered or less pronounced sexual differentiation of the brain. This hypothesis has primarily been based on postmortem studies of the hypothalamus in transgender individuals. To further address this hypothesis, a series of structural and functional neuroimaging studies were conducted in the Amsterdam cohort of children and adolescents experiencing gender incongruence. Additional research objectives were to determine whether any sex and gender differences are established before or after puberty, as well as whether gender affirming hormone treatment would affect brain development and function. We found some evidence in favor of the sexual differentiation hypothesis at the functional level, but this was less evident at the structural level. We also observed some specific transgender neural signatures, suggesting that they might present a unique brain phenotype rather than being shifted towards either end of the male-female spectrum. Our results further suggest that the years between childhood and mid-adolescence represent an important period in which puberty-related factors influence several neural characteristics, such as white matter development and functional connectivity patterns, in both a sex and gender identity specific way. These latter observations thus lead to the important question about the possible negative consequences of delaying puberty on neurodevelopment. To further address this question, larger-scale, longitudinal studies are required to increase our understanding of the possible neurodevelopmental impacts of delaying puberty in transgender youth.

Disciplines :

Neurosciences & behavior

Author, co-author :

Bakker, Julie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau

Language :

English

Title :

Neurobiological characteristics associated with gender identity: Findings from neuroimaging studies in the Amsterdam cohort of children and adolescents experiencing gender incongruence.

Publication date :

August 2024

Journal title :

Hormones and Behavior

ISSN :

0018-506X

eISSN :

1095-6867

Publisher :

Academic Press Inc., United States

Volume :

164

Pages :

105601

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S0018506X24001260?httpAccept=text/xml

Funding text :

Julie Bakker is a research director of the Belgian Fonds National de la Recherche. All MRI studies were financed through a VICI grant ( 453-08-003 ) from the Dutch Science Foundation (Nederlandse Organisatie voor Wetenschappelijk Onderzoek) to Julie Bakker. I would like to thank all the participants and their parents. Finally, I would like to thank Dr. Margaret McCarthy for commenting on an earlier version of this paper.

Available on ORBi :

since 17 October 2024

Statistics

Number of views

7 (0 by ULiège)

Number of downloads

10 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Asato, M.R., Sweeney, J.A., Luna, B., Cognitive processes in the development of TOL performance. Neuropsychologia 44 (2006), 2259–2269.
Bakker, J., The sexual differentiation of the human brain: role of sex hormones versus sex chromosomes. Curr. Top. Behav. Neurosci. 43 (2019), 45–67.
Bava, S., Boucquey, V., Goldenberg, D., Thayer, R.E., Ward, M., Jacobus, J., Tapert, S.F., Sex differences in adolescent white matter architecture. Brain Res. 1375 (2011), 41–48.
Beking, T., Burke, S.M., Geuze, R.H., Staphorsius, A.S., Bakker, J., Groothuis, A.G.G., Kreukels, B.P.C., Testosterone effects on functional amygdala lateralization: a study in adolescent transgender boys and cisgender boys and girls. Psychoneuroendocrinology, 111, 2020, 104461.
Beltz, A.M., Berenbaum, S.A., Cognitive effects of variations in pubertal timing: is puberty a period of brain organization for human sex-typed cognition?. Horm. Behav. 63 (2013), 823–828.
Berglund, H., Lindström, P., Savic, I., Brain response to putative pheromones in lesbian women. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 8269–8274.
Brooksbank, B.W., Cunningham, A.E., Wilson, D.A., The detection of androsta-4,16-dien-3-one in peripheral plasma of adult men. Steroids 13 (1969), 29–50.
Brooksbank, B.W., Wilson, D.A., Macsweeney, D.A., Fate of androsta-4,16-dien-3-one and the origin of 3-hydroxy-5-androst-16-ene in man. J. Endocrinol. 52 (1972), 239–251.
Brunner, F., Fliegner, M., Krupp, K., Rall, K., Brucker, S., Richter-Appelt, H., Gender role, gender identity and sexual orientation in CAIS (“XY-women”) compared with subfertile and infertile 46. XX Women. J Sex Res. 53 (2016), 109–124.
Burke, S.M., Veltman, D.J., Gerber, J., Hummel, T., Bakker, J., Heterosexual men and women both show a hypothalamic response to the chemo-signal androstadienone. PloS One, 7, 2012, e40993.
Burke, S.M., Cohen-Kettenis, P.T., Veltman, D.J., Klink, D.T., Bakker: hypothalamic response to the chemo-signal androstadienone in gender-dysphoric children and adolescents. Front. Endocrinol., 5, 2014, 60.
Burke, S.M., Kreukels, B.P., Cohen-Kettenis, P.T., Veltman, D.J., Klink, D.T., Bakker, J., Male-typical visuospatial functioning in gynephilic girls with gender dysphoria – organizational and activational effects of testosterone. J. Psychiatry Neurosci. 41 (2016), 395–404.
Burke, S.M., Manzouri, A.H., Savic, I., Structural connections in the brain in relation to gender identity and sexual orientation. Sci. Rep., 7, 2017, 17954.
Burke, S.M., Manzouri, A.H., Dhejne, C., Bergström, K., Arver, S., Feusner, J.D., Savic, I., Testosterone effects on the brain in transgender men. Cereb. Cortex 28 (2018), 1582–1596.
Burke, S.M., Majid, D.S.A., Manzouri, A.H., Moody, T., Feusner, J.D., Savic, I., Sex differences in own and other body perception. Hum. Brain Mapp. 40 (2019), 474–488.
Butler, T., Imperato-McGinley, J., Pan, H., Voyer, D., Cordero, J., Zhu, Y.-S., Stern, E., Silbersweig, D., Sex differences in mental rotation: top-down versus bottom-up processing. Neuroimage 32 (2006), 445–456.
Cahill, L., Uncapher, M., Kilpatrick, L., Alkire, M.T., Turner, J., Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: an fMRI investigation. Learn. Mem. 11 (2004), 261–266.
Carlin, D., Bonerba, J., Phipps, M., Alexander, G., Shapiro, M., Grafman, J., Planning impairments in frontal lobe dementia and frontal lobe lesion patients. Neuropsychologia 38 (2000), 655–665.
Carrillo, B., Gómez-Gil, E., Rametti, G., Junque, C., Gomez, A., Karadi, K., Segovia, S., Guillamon, A., Cortical activation during mental rotation in male-to-female and female-to-male transsexuals under hormonal treatment. Psychoneuroendocrinology 35 (2010), 1213–1222.
Casey, B.J., Tottenham, N., Fossella, J., Clinical, imaging, lesion, and genetic approaches toward a model of cognitive control. Dev. Psychobiol. 40 (2002), 237–254.
Chahal, R., Vilgis, V., Grimm, K.J., Hipwell, A.E., Forbes, E.E., Keenan, K., Guyer, A.E., Girls’ pubertal development is associated with white matter microstructure in late adolescence. Neuroimage 181 (2018), 659–669.
Chen, D., Strang, J.F., Kolbuck, V.D., et al. Consensus parameter: research methodologies to evaluate neurodevelopmental effects of pubertal suppression in transgender youth. Transgender Health 5 (2020), 246–257.
Cohen-Kettenis, P.T., van Goozen, S.H., Doorn, C.D., Gooren, L.J., Cognitive ability and cerebral lateralisation in transsexuals. Psychoneuroendocrinology 23 (1998), 631–641.
Coleman, J.C., Hendry, L., The nature of adolescence. 2nd edition 1990. London, Routledge. Hines M, Ahmed SF, Hughes IA: psychological outcomes and gender-related development in complete androgen insensitivity syndrome. Arch. Sex. Behav. 32 (2003), 93–101.
Collaer, M.L., Hines, M., No evidence for enhancement of spatial ability with elevated prenatal androgen exposure in congenital adrenal hyperplasia: a meta-analysis. Arch. Sex. Behav. 49 (2020), 395–411.
Cox, S.R., Ritchie, S.J., Tucker-Drob, E.M., Liewald, D.C., Hagenaars, D.P., Davies, G., et al. Ageing and brain white matter microstructure in 3513 UK biobank participants. Nat. Commun. 7 (2016), 1–13.
David, S.P., Ware, J.J., Chu, I.M., Loftus, P.D., Fusar-Poli, P., Radua, J., Munafò, M.R., Ioannidis, J.P., Potential reporting bias in fMRI studies of the brain. PloS One, 8, 2013, e70104.
David, S.P., Naudet, F., Laude, J., Fusar-Poli, P., Chu, I., Stefanick, M.L., Ioannidis, J.P., Potential reporting bias in neuroimaging studies of sex differences. Sci. Rep., 8, 2018, 6082.
De Luca, C.R., Wood, S.J., Anderson, V., et al. Normative data from the CANTAB. I. Development of executive function over the lifespan. J. Clin. Exp. Neuropsychol. 25 (2003), 242–254.
Dessens, A.B., Slijper, F.M.E., Drop, S.L.S., Gender dysphoria and gender change in chromosomal females with congenital adrenal hyperplasia. Arch. Sex. Behav. 34 (2005), 389–397.
Epting, L.K., Overman, W.H., Sex-sensitive tasks in men and women: a search for performance fluctuations across the menstrual cycle. Behav. Neurosci. 112 (1998), 1304–1317.
Fernandez, R., Guillamon, A., Cortés-Cortés, J., et al. Molecular basis of gender dysphoria: androgen and estrogen receptor interaction. Psychoneuroendocrinology 98 (2018), 161–167.
Feusner, J.D., Dervisic, J., Kosidou, K., Dhejne, C., Bookheimer, S., Savic, I., Female-to-male transsexual individuals demonstrate different own body identification. Arch. Sex. Behav. 45 (2016), 525–536.
Garcia-Falgueras, A., Swaab, D.F., A sex difference in the hypothalamic uncinate nucleus: relationship to gender identity. Brain 131 (2008), 3132–3146.
Gizewski, E.R., Krause, E., Wanke, I., Forsting, M., Senf, W., Gender-specific cerebral activation during cognitive tasks using functional MRI: comparison of women in mid-luteal phase and men. Neuroradiology 48 (2006), 14–20.
Gower, D.B., Ruparelia, B.A., Olfaction in humans with special reference to odorous 16-androstenes: their occurrence, perception and possible social, psychological and sexual impact. J. Endocrinol. 137 (1993), 167–187.
Guadalupe, T., et al. Human subcortical brain asymmetries in 15,847 people worldwide reveal effects of age and sex. Brain Imaging Behav., 1–18, 2016.
Guillamon, A., Junque, C., Gómez-Gil, E., A review of the status of brain structure research in transsexualism. Arch. Sex. Behav. 45 (2016), 1615–1648.
Halari, R., Hines, M., Kumari, V., Mehrota, R., Wheeler, M., Ng, V., Sharma, T., Sex differences and individual differences in cognitive performance and their relationship to endogenous gonadal hormones and gonadotropins. Behav. Neurosci. 119 (2005), 104–117.
Hausmann, M., Slabbekoorn, D., Van Goozen, S.H., Cohen-Kettenis, P.T., Güntürkün, O., Sex hormones affect spatial abilities during the menstrual cycle. Behav. Neurosci. 114 (2000), 1245–1250.
Hembree, W.C., Cohen-Kettenis, P.T., Gooren, L., Hannema, S.E., Meyer, W.J., et al. Endocrine treatment of gender dysphoric/gender incongruent persons: an Endocrine Society clinical practice guideline. J. Clin. Endocrinol. Metab. 102 (2017), 3869–3903.
Herting, M.M., Maxwell, E.C., Irvine, C., Nagel, B.J., The impact of sex, puberty, and hormones on white matter microstructure in adolescents. Cereb. Cortex 22 (2012), 1979–1992.
Herting, M.M., Kim, R., Uban, K.A., Kan, E., Binley, A., Sowell, E.R., Longitudinal changes in pubertal maturation and white matter microstructure. Psychoneuroendocrinology 81 (2017), 70–79.
Hines, M., Ahmed, S.F., Hughes, I.A., Psychological outcomes and gender-related development in complete androgen insensitivity syndrome. Arch. Sex. Behav. 32 (2003), 93–101.
Hirnstein, M., Hugdahl, K., Hausmann, M., Cognitive sex differences and hemispheric asymmetry: a critical review of 40 years of research. Laterality Asymmetries Body. Brain Cogn., 2018, 1–49.
Ho, T.C., Colich, N.L., Sisk, L.M., Oskirko, K., Jo, B., Gotlib, I.H., Sex differences in the effects of gonadal hormones on white matter microstructure development in adolescence. Dev. Cogn. Neurosci., 42, 2020, 100773.
Hoekzema, E., Schagen, S., Kreukels, B.P., Veltman, D.J., Cohen-Kettenis, P.T., Delemarre-van de Waal H, Bakker J: regional volumes and spatial volumetric distribution of gray matter in the gender dysphoric brain. Psychoneuroendocrinology 55 (2015), 59–71.
Hoppe, C., Fliessbach, K., Stausberg, S., Stojanovic, J., Trautner, P., Elger, C.E., Weber, B., A key role for experimental task performance: effects of math talent, gender and performance on the neural correlates of mental rotation. Brain Cognition 78 (2012), 14–27.
Hughes, I.A., Davies, J.D., Bunch, T.I., Pasterski, V., Mastroyannopoulou, K., MacDougall, J., Androgen insensitivity syndrome. Lancet, 2012, 1419–1428.
Huizinga, M., Dolan, C.V., van der Molen, M.W., Age-related change in executive function: developmental trends and a latent variable analysis. Neuropsychologia 44 (2006), 2017–2036.
Huttenlocher, P.R., Synaptic density in human frontal cortex – developmental changes and effects of aging. Brain Res. 163 (1979), 195–205.
Janowsky, J.S., Chavez, B., Zamboni, B.D., Orwoll, E., The cognitive neuropsychology of sex hormones in men and women. Dev. Neuropsychol. 14 (1998), 421–440.
Jordan, K., Würstenberg, T., Jochen Heinze, H., Peters, M., Jäncke, L., Women and men exhibit different cortical activation patterns during mental rotations tasks. Neuropsychologia 40 (2002), 2397–2408.
Jorgensen, S.C.J., Transition regret and detransition: meanings and uncertainties. Arch. Sex. Behav. 52 (2023), 2173–2184.
Kohlberg, L.A., A cognitive-developmental analysis of children's sex role concepts and attitudes. Maccoby, E.E., (eds.) The Development of Sex Differences, 1966, 82–173 Stanford University.
Korte, A., Lehmkuhl, U., Goecker, D., Beier, K.M., Krude, H., Grüters-Kieslich, A., Gender identity disorders in childhood and adolescence: currently debated concepts and treatment strategies. Dtsch. Arztebl. Int. 105 (2008), 834–841.
Kranz, G.S., Han, A., Kaufmann, U., Küblböck, M., Hummer, A., Ganger, S., et al. White matter microstructure in transsexuals and controls investigated by diffusion tensor imaging. J. Neurosci. 34 (2014), 15466–15475.
Kreukels, B.P., Guillamon, A., Neuroimaging studies in people with gender incongruence. Int. Rev. Psychiatry 28 (2016), 120–128.
Kreukels, B.P.C., Cohen-Kettenis, P.T., Puberty suppression in gender identity disorder: the Amsterdam experience. Nat. Rev. Endocrinol. 7 (2011), 466–472.
Kreukels, B.P.C., Köhler, B., Nordenström, A., Roehle, R., Thyen, U., Bouvattier, C., de Vries, A.L.C., Cohen-Kettenis, P.T., Dsd-LIFE group: gender dysphoria and gender change in disorders of sex development/intersex conditions: results from the dsd-LIFE study. J. Sex. Med. 15 (2018), 777–785.
Kruijver, F.P., Zhou, J.N., Pool, C.W., Hofman, M.A., Gooren, L.J., Swaab, D.F., Male-to-female transsexuals have female neuron numbers in a limbic nucleus. J. Clin. Endocrinol. Metab. 85 (2000), 2034–2041.
Kuyper, E., Wijsen, C., Gender identities and gender dysphoria in the Netherlands. Arch. Sex. Behav. 43 (2014), 377–385.
Kwan, T.K., Trafford, D.J., Makin, H.L., Mallet, A.I., Gower, D.B., GC-MS studies of 16-androstenes and other C19 steroids in human semen. J. Steroid Biochem. Mol. Biol. 43 (1992), 549–556.
Kwan, T.K., Kraevskaya, M.A., Makin, H.L., Trafford, D.J., Gower, D.B., Use of gas chromatographic-mass spectrometric techniques in studies of androst-16-ene and androgen biosynthesis in human testis; cytosolic specific binding of 5alpha-androst-16-en-3-one. J. Steroid Biochem. Mol. Biol. 60 (1997), 137–146.
Lin, C.-S., Ku, H.-L., Chao, H.-T., Tu, P.-C., Li-T, Cheng, C.-M., Su, T.-P., Lee, Y.-C., Hsieh, J.C., Neural network of body representation differs between transsexuals and cissexuals. PloS One, 9, 2014, e85914.
Linn, M.C., Petersen, A.C., Emergence and characterization of sex differences in spatial ability: a meta-analysis. Child Dev. 56 (1985), 1479–1498.
Lombardo, M.V., Ashwin, E., Auyeung, B., Chakrabarti, B., Taylor, K., Hackett, G., Bullmore, E.T., Baron-Cohen, S., Fetal testosterone influences sexually dimorphic gray matter in the human brain. J. Neurosci. 32 (2012), 674–680.
Manzouri, A., Kosidou, K., Savic, I., Anatomical and functional findings in female-to-male transsexuals: testing a new hypothesis. Cereb. Cortex 27 (2017), 998–1010.
Masica, D.N., Money, J., Ehrhardt, A.A., Fetal feminization and female gender identity in the testicular feminizing syndrome of androgen insensitivity. Arch. Sex. Behav. 1 (1971), 131–142.
Maylor, E.A., Reimers, S., Choi, J., Collaer, M.L., Peters, M., Silverman, I., Gender and sexual orientation differences in cognition across adulthood: age is kinder to women than to men regardless of sexual orientation. Arch. Sex. Behav. 36 (2007), 235–249.
Merke, D., Kabbani, M., Congenital adrenal hyperplasia: epidemiology, management and practical drug treatment. Paediatr. Drugs 3 (2001), 599–611.
Meyenburg, B., Gender identity disorder in adolescence: outcomes of psychotherapy. Adolescence 34 (1999), 305–313.
Miles, C., Green, R., Hines, M., Estrogen and memory in a transsexual population. Horm. Behav. 34 (1998), 199–208.
Miles, C., Green, R., Hines, M., Estrogen treatment effects on cognition, memory and mood in male-to-female transsexuals. Horm. Behav. 50 (2006), 708–717.
Mueller, S.C., et al. The neuroanatomy of transgender identity: mega-analytic findings from the ENIGMA transgender persons working group. J. Sex. Med. 18 (2021), 1122–1129.
Nixon, A., Mallet, A.I., Gower, D.B., Simulateneous quantification of five odorous steroids (16-androstenes) in the axillary hair of men. J. Steroid Biochem. 29 (1988), 505–510.
Nota, N.M., Kreukels, B.P.C., den Heijer, M., Veltman, D.J., Cohen-Kettenis, P.T., Burke, S.M., Bakker: brain functional connectivity patterns in children and adolescents with gender dysphoria: sex-atypical or not?. Psychoneuroendocrinology 86 (2017), 187–195.
Pang, K.C., de Graaf, N.M., Chew, D., Hoq, M., Keith, D.R., Carmichael, P., Steensma, T.D., Association of media coverage of transgender and gender diverse issues with rates of referral of transgender children and adolescents to specialized gender clinics in the UK and Australia. JAMA Netwerk Open, 3, 2020, e2011161.
Peper, J.S., de Reus, M.A., van den Heuvel, M.P., Schutter, D.J.L.G., Short fused? Associations between white matter connections, sex steroids, and aggression across adolescence. Hum. Brain Mapp. 36 (2015), 1043–1052.
Peters, M., Manning, J.T., Reimers, S., The effects of sex, sexual orientation, and digit ratio (2D:4D) on mental rotation performance. Arch. Sex. Behav. 36 (2007), 251–260.
Pfannkuche, K.A., Bouma, A., Groothuis, T.G.G., Does testosterone affect lateralization of brain and behaviour? A meta-analysis in humans and other animal species. Philos. Trans. R. Soc. B Biol. Sci. 364 (2009), 929–942.
Pletzer, B., Bodenbach, H., Hoehn, M., Hajdari, L., Hausinger, T., Noachtar, I., Beltz, A.M., Reproducible stability of verbal and spatial functions along the menstrual cycle. Neuropsychopharmacology 49 (2024), 933–941 (PMID: 38267632).
Rametti, G., Carillo, B., Gomez-Gil, E., Junque, C., Segovia, S., Gomez, A., Guillamon, A., White matter microstructure in female to male transsexuals before cross-sex hormonal treatment. A diffusion tensor imaging study. J. Psychiatr. Res. 45 (2011), 199–204.
Rametti, G., Carillo, B., Gomez-Gil, E., Junque, C., Zubiarre-Elorza, L., Segovia, S., et al. The microstructure of white matter in male to female transsexuals before cross-sex hormonal treatment: a DTI study. J. Psychiatr. Res. 45 (2011), 949–954.
Ritchie, S.J., Cox, S.R., Shen, X., Lombardo, M.V., Reus, L.M., Alloza, C., Harris, M.A., Alderson, H.L., Hunter, S., Neilson, E., Liewald, D.C.M., Auyeung, B., Whalley, H.C., Lawrie, S.M., Gale, C.R., Bastin, M.E., McIntosh, A.M., Deary, I.J., Sex differences in the adult human brain: evidence from 5216 UK biobank participants. Cereb. Cortex 28 (2018), 2959–2975.
Rubia, K., Functional brain imaging across development. Eur. Child Adolesc. Psychiatry 22 (2013), 719–731.
Ruigrok, A.N.V., Salimi-Khorshidi, G., Lai, M.-C., Baron-Cohen, S., Lombardo, M.V., Tait, R.J., Suckling, J., A meta-analysis of sex differences in human brain structure. Neurosci. Biobehav. Rev. 39 (2014), 34–50.
Savic, I., Berglund, H., Gulyas, B., Roland, P., Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans. Neuron 31 (2001), 661–668.
Savic, I., Berglund, H., Lindström, P., Brain response to putative pheromones in homosexual men. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 7356–7361.
Scheinost, D., Finn, E.S., Tokoglu, F., Shen, X., Papademetris, X., Hampson, M., Constable, R.T., Sex differences in normal age trajectories of functional brain networks. Hum. Brain Mapp. 36 (2015), 1524–1535.
Schneider, M.A., Spritzer, P.M., Soll, B.M.B., Fontanari, A.M.V., Carneiro, M., Tovar-Moll, F., et al. Brain maturation, cognition and voice pattern in a gender dysphoric case under pubertal suppression. Front. Hum. Neurosci. 11 (2017), 1–9.
Schöning, S., Engelien, A., Kugel, H., Schäfer, S., Schiffbauer, H., Zwitserlood, P., Pletziger, E., Beizai, P., Kersting, A., Ohrann, P., Functional anatomy of visuo-spatial working memory during mental rotation is influenced by sex, menstrual cycle, and sex steroid hormones. Neuropsychologia 45 (2007), 3203–3214.
Schöning, S., Engelien, A., Bauer, C., Kugel, H., Kersting, A., Roestel, C., Zwitserlood, P., Pyka, M., Dannlowski, U., Lehmann, W., Heindel, W., Arolt, V., Konrad, C., Neuroimaging differences in spatial cognition between men and male-to-female transsexuals before and during hormone therapy. J. Sex. Med. 7 (2010), 1858–1867.
Schraa-Tam, C.K.L., Rietdijk, W.J.R., Verbeke, W.J.M.I., Dietvorst, R.C., van den Berg, W.E., Bagozzi, R.P., De Zeeuw, C.I., fMRI activities in the emotional cerebellum: a preference for negative stimuli and goal-directed behavior. Cerebellum 11 (2012), 233–245.
Schulz, K.M., Molenda-Figueira, H.A., Sisk, C.L., Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm. Behav. 55 (2009), 597–604.
Sisk, C.L., Schulz, K.M., Zehr, J.L., Puberty: a finishing school for male social behavior. Ann NY Acad Sci USA 1007 (2003), 189–198.
Slabbekoorn, D., Van Goozen, S.H., Megens, J., Gooren, L.J., Cohen-Kettenis, P.T., Activating effects of cross-sex hormones on cognitive functioning: a study of short-term and long-term hormone effects in transsexuals. Psychoneuroendocrinology 24 (1999), 423–447.
Spriggs, M.P., Ethics and the proposed treatment for a 13-year-old with atypical gender identity. Med. J. Aust. 181 (2004), 319–321.
Staphorsius, A.S., Kreukels, B.P.C., Cohen-Kettenis, P.T., et al. Puberty suppression and executive functioning: an fMRI study in adolescents with gender dysphoria. Psychoneuroendocrinology 56 (2015), 190–199.
Swaab, D.F., Sexual differentiation of the brain and behavior. Best Pract. Res. Clin. Endocrinol. Metab. 21 (2007), 431–444.
Taziaux, M., Swaab, D.F., Bakker, J., Sex differences in the neurokinin B system in the human infundibular nucleus. J. Clin. Endocrinol. Metab. 97 (2012), E2210–E2220.
Taziaux, M., Staphorsius, A.S., Ghatei, M.A., Bloom, S.R., Swaab, D.F., Bakker, J., Kisspeptin expression in the human infundibular nucleus in relation to sex, gender identity, and sexual orientation. J. Clin. Endocrinol. Metab. 10 (2016), 2380–2389.
Toffoletto, S., Lanzenberger, R., Gingnell, M., Sundström-Poromaa, I., Comasco, E., Emotional and cognitive functional imaging of estrogen and progesterone effects in the female human brain: a systematic review. Psychoneuroendocrinology 50 (2014), 28–52.
T'Sjoen, G., De Cuypere, G., Monstrey, S., et al. Male gender identity in complete androgen insensitivity syndrome. Arch. Sex. Behav. 40 (2011), 635–638.
Uematsu, A., Matsui, M., Tanaka, C., Takahashi, T., Noguchi, K., Suzuki, M., Nishijo, H., Developmental trajectories of amygdala and Hippocampus from infancy to early adulthood in healthy individuals. PloS One, 7, 2012, e46970.
Van der Loos, M.A.T.C., et al. Children and adolescents in the Amsterdam cohort of gender dysphoria: trends in diagnostic- and treatment trajectories during the first 20 years of the Dutch protocol. J. Sex. Med. 20 (2023), 398–409.
Van Goozen, S.H.M., Cohen-Kettenis, P.T., Gooren, L.J.G., Frijda, N.H., Van de Poll, N.E., Activating effects of androgens on cognitive performance: causal evidence in a group of female-to-male transsexuals. Neuropsychologia 32 (1994), 1153–1157.
Van Goozen, S.H.M., Cohen-Kettenis, P.T., Gooren, L.J.G., Frijda, N.H., Van de Poll, N.E., Gender differences in behaviour: activating effects of cross-sex hormones. Psychoneuroendocrinology 20 (1995), 343–363.
Van Goozen, S.H.M., Gooren, L.J.G., Sanders, G., Cohen-Kettenis, P.T., Slabbekoorn, D., Organizing and activating effects of sex hormones in homosexual transsexuals. Behav. Neurosci. 116 (2002), 982–988.
Van Heesewijk, J., Steenwijk, M.D., Kreukels, B.P.C., Veltman, D.J., Bakker, J., Burke, S.M., Alterations in the inferior fronto-occipital fasciculus – a specific neural correlate of gender incongruence?. Psychol. Med. 53:8 (2023), 3461–3470, 10.1017/S0033291721005547.
Van Hemmen, J., Veltman, D.J., Hoekzema, E., Cohen-Kettenis, P.T., Dessens, A.B., Bakker, J., Neural activation during mental rotation in complete androgen insensitivity syndrome: the influence of sex hormones and sex chromosomes. Cereb. Cortex 26 (2016), 1036–1045.
Wallien, M.S.C., Cohen-Kettenis, P.T., Psychosexual outcome of gender dysphoric children. J. Am. Acad. Child Adolesc. Psychiatry 47 (2008), 1413–1423.
Weiss, E., Siedentopf, C.M., Hofer, A., Deisenhammer, E.A., Hoptman, M.J., Kremser, C., Golaszewski, S., Felber, S., Fleischhacker, W.W., Delazer, M., Sex differences in brain activation pattern during a visuospatial cognitive task: a functional magnetic resonance imaging study in healthy volunteers. Neurosci. Lett. 344 (2003), 169–172.
Wiepjes, C.M., Nota, N.M., de Blok, C.J.M., Klaver, M., de Vries, A.L.C., Wensing-Kruger, S.A., de Jongh, R.T., Bouman, M.B., Steensma, T.D., Cohen-Kettenis, P., Gooren, L.J.G., Kreukels, B.P.C., den Heijer, M., The Amsterdam cohort of gender dysphoria study (1972–2015): trends in prevalence, treatment, and regrets. Journal of Sexual Medicine 15 (2018), 582–590.
Wisniewski, A.B., Migeon, C.J., Meyer-Bahlburg, H.F., Gearhart, J.P., Berkovitz, G.D., Brown, T.R., Money, J., Complete androgen insensitivity syndrome: long-term medical, surgical, and psychosexual outcome. J. Clin. Endocrinol. Metab. 85 (2000), 2664–2669.
Zhou, J.N., Hofman, M.A., Gooren, L.J., Swaab, D.F., A sex difference in the human brain and its relation to transsexuality. Nature 378 (1995), 68–70.
Zitzman, M., Testosterone and the brain. Aging Male 9 (2006), 195–199.
Zucker, K.J., Bradley, S.J., Gender Identity Disorder and Psychosexual Problems in Children and Adolescents. 1995, The Guilford Press, New York.
Zucker, K.J., vander Laan, D.P., Aitken, M., The contemporary sex ratio of transgender youth that favors assigned females at birth is a robust phenomenon: a response to the letter to the editor re: “shifts in assigned sex ratios at gender identity clinics likely reflect change in referral patterns”. J. Sex. Med. 16 (2019), 949–950.