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Gonadal Hormone Influences on Human Neurobehavioral Development: Outcomes and Mechanisms

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Part of the book series: Research and Perspectives in Endocrine Interactions ((RPEI))

Abstract

Testosterone exposure during early development has enduring influences on mammalian behavior, increasing male-typical characteristics and decreasing female-typical characteristics. Research in non-human mammals indicates that testosterone also influences development of the mammalian brain, affecting programmed cell death, anatomical connectivity and neurochemical specification, and these neural changes, which occur during early development, are thought to explain the subsequent behavioral changes. The strongest evidence linking prenatal testosterone exposure to human behavioral sexual differentiation has come from studies of children’s sex-typed play. There also is substantial evidence linking early testosterone exposure to sexual orientation and to core gender identity and some evidence linking such hormone exposure to physically aggressive behavior and to empathy. However, for most, perhaps all, human behaviors that show sex differences, other factors, including socialization, also play a role, and the magnitude of this role appears to vary across behavioral outcomes. In addition, in contrast to other species, the acquisition of sex-typical behavior in humans involves social-cognitive mechanisms related to gender identification. This chapter will suggest that these social-cognitive mechanisms could be involved in the developmental cascade of processes linking early testosterone exposure to sexual differentiation of human behavior.

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References

  • Abramovich DR (1974) Human sexual differentiation – in utero influences. J Obstet Gynaecol Brit Commonwealth 81:448–453

    Article  CAS  Google Scholar 

  • Abramovich DR, Rowe P (1973) Foetal plasma testosterone levels at mid-pregnancy and at term: relationship to foetal sex. J Endocrinol 56:621–622

    Article  PubMed  CAS  Google Scholar 

  • Alexander GM (2003) An evolutionary perspective of sex-typed toy preferences: pink, blue, and the brain. Arch Sex Behav 32:7–14

    Article  PubMed  Google Scholar 

  • Alexander GM, Hines M (2002) Sex differences in response to children’s toys in nonhuman primates (cercopithecus aethiops sabaeus). Evol Hum Behav 23:467–479

    Article  Google Scholar 

  • Arnold AP (2009) The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Horm Behav 55:570–578

    Article  PubMed  CAS  Google Scholar 

  • Auyeung B, Baron-Cohen S, Chapman E, Knickmeyer R, Taylor K, Hackett G, Hines M (2009) Fetal testosterone predicts sexually differentiated childhood behavior in girls and in boys. Psychol Sci 20:144–148

    Article  PubMed  Google Scholar 

  • Berenbaum SA, Hines M (1992) Early androgens are related to childhood sex-typed toy preferences. Psychol Sci 3:203–206

    Article  Google Scholar 

  • Berenbaum SA, Resnick SM (1997) Early androgen effects on aggression in children and adults with congenital adrenal hyperplasia. Psychoneuroendocrinology 22:505–515

    Article  PubMed  CAS  Google Scholar 

  • Campbell A, Shirley L, Heywood C (2000) Infants’ visual preference for sex-congruent babies, children, toys, and activities: a longitudinal study. Brit J Dev Psychol 18:479–498

    Article  Google Scholar 

  • Carson DJ, Okuno A, Lee PA, Stetten G, Didolkar SM, Migeon CJ (1982) Amniotic fluid steroid levels: fetuses with adrenal hyperplasia, 46, XXY fetuses, and normal fetuses. Am J Dis Child 136:218–222

    PubMed  CAS  Google Scholar 

  • Chapman E, Baron-Cohen S, Auyeung B, Knickmeyer R, Taylor K, Hackett G (2006) Fetal testosterone and empathy: evidence from the Empathy Quotient (EQ) and the “Reading the mind in the eyes” test. Soc Neurosci 1:135–148

    Article  PubMed  Google Scholar 

  • Cohen-Bendahan CCC, van de Beek C, Berenbaum SA (2005) Prenatal sex hormone effects on child and adult sex-typed behavior: methods and findings. Neurosci Biobehav Rev 29:353–384

    Article  PubMed  CAS  Google Scholar 

  • Cohen-Kettenis PT (2005) Gender change in 46, XY persons with 5alpha-reductase-2 deficiency and 17beta-hydroxysteroid dehydrogenase-3 deficiency. Arch Sex Behav 34:399–410

    Article  PubMed  Google Scholar 

  • Dessens AB, Slijper FME, Drop SLS (2005) Gender dysphoria and gender change in chromosomal females with congenital adrenal hyperplasia. Arch Sex Behav 34:389–397

    Article  PubMed  Google Scholar 

  • Dittmann RW, Kappes MH, Kappes ME, Börger D, Stegner H, Willig RH, Wallis H (1990) Congenital adrenal hyperplasia I: gender-related behavior and attitudes in female patients and sisters. Psychoneuroendocrinology 15:401–420

    Article  PubMed  CAS  Google Scholar 

  • Dittmann RW, Kappes ME, Kappes MH (1992) Sexual behavior in adolescent and adult females with congenital adrenal hyperplasia. Psychoneuroendocrinology 17:153–170

    Article  PubMed  CAS  Google Scholar 

  • Ehrhardt AA, Baker SW (1974) Fetal androgens, human central nervous system differentiation, and behavior sex differences. In: Friedman RC, Richart RM, van de Wiele RL (eds) Sex differences in behavior. Wiley, New York, pp 33–52

    Google Scholar 

  • Ehrhardt AA, Epstein R, Money J (1968) Fetal androgens and female gender identity in the early-treated adrenogenital syndrome. Johns Hopkins Med J 122:160–167

    PubMed  CAS  Google Scholar 

  • Fagot BI (1977) Consequences of moderate cross-gender behavior in preschool children. Child Dev 48:902–907

    Article  Google Scholar 

  • Fagot BI (1978) The influence of sex of child on parental reactions to toddler children. Child Dev 49:459–465

    Article  Google Scholar 

  • Fagot BI, Patterson GR (1969) An in vivo analysis of reinforcing contingencies for sex-role behaviors in the preschool child. Dev Psychol 5:563–568

    Article  Google Scholar 

  • Fausto-Sterling A (1992) Myths of gender. Basic Books, New York

    Google Scholar 

  • Frisén J, Nordenstrom A, Falhammar H, Filipsson H, Holmdahl G, Janson PO, Thoren M, Hagenfeldt K, Moller A, Nordenskjold A (2009) Gender role behavior, sexuality, and psychosocial adaptation in women with congenital adrenal hyperplasia due to CYP21A2 deficiency. J Clin Endocrinol Metab 94:3432–3439

    Article  PubMed  Google Scholar 

  • Golombok S, Rust J, Zervoulis K, Croudace T, Golding J, Hines M (2008) Developmental trajectories of sex-typed behavior in boys and girls: a longitudinal general population study of children aged 2.5–8 years. Child Dev 79:1583–1593

    Article  PubMed  Google Scholar 

  • Goy RW, McEwen BS (1980) Sexual differentiation of the brain. MIT Press, Cambridge, MA

    Google Scholar 

  • Hassett JM, Siebert ER, Wallen K (2008) Sex differences in rhesus monkey toy preferences parallel those of children. Horm Behav 54:359–364

    Article  PubMed  Google Scholar 

  • Hines M (2004) Brain gender. Oxford University Press, New York

    Google Scholar 

  • Hines M (2009) Gonadal hormones and sexual differentiation of human brain and behavior. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, brain and behavior. Academic, San Diego, pp 1869–1909

    Chapter  Google Scholar 

  • Hines M (2011) Gender development and the human brain. Ann Rev Neurosci 34:67–86

    Article  Google Scholar 

  • Hines M, Golombok S, Rust J, Johnston K, Golding J, The ALSPAC Study Team (2002) Testosterone during pregnancy and childhood gender role behavior: a longitudinal population study. Child Dev 73:1678–1687

    Article  PubMed  Google Scholar 

  • Hines M, Brook C, Conway GS (2004) Androgen and psychosexual development: core gender identity, sexual orientation and recalled childhood gender role behavior in women and men with congenital adrenal hyperplasia (CAH). J Sex Res 41:75–81

    Article  PubMed  Google Scholar 

  • Jadva V, Golombok S, Hines M (2010) Infants’ preferences for toys, colors and shapes. Arch Sex Behav 39:1261–1273

    Article  PubMed  Google Scholar 

  • Jordan-Young RM (2010) Brainstorm: the flaws in the science of sex differences. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Leinbach MD, Fagot BI (1986) Acquisition of gender labels: a test for toddlers. Sex Roles 15:655–666

    Article  Google Scholar 

  • Lo Bue V, De Loache JS (2011) Pretty in pink: the early development of gender-stereotyped colour preferences. Brit J Dev Psychol 29:656–667

    Article  Google Scholar 

  • Lytton H, Romney DM (1991) Parents’ differential socialization of boys and girls: a meta-analysis. Psychol Bull 109:267–296

    Article  Google Scholar 

  • Maccoby EE (1998) The two sexes: growing up apart, coming together. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Maccoby EE, Jacklin CN (1974) The psychology of sex differences. Stanford University Press, Stanford

    Google Scholar 

  • Maccoby EE, Jacklin CN (1987) Gender segregation in children. In: Reece HW (ed) Advances in child development and behavior. Academic, New York, pp 239–287

    Chapter  Google Scholar 

  • Masters JC, Ford ME, Arend R, Grotevant HD, Clark LV (1979) Modeling and labelling as integrated determinants of children’s sex-typed imitative behavior. Child Dev 50:364–371

    Article  Google Scholar 

  • Mathews GA, Fane BA, Conway GS, Brook C, Hines M (2009) Personality and congenital adrenal hyperplasia: possible effects of prenatal androgen exposure. Horm Behav 55:285–291

    Article  PubMed  CAS  Google Scholar 

  • McCarthy MM, De Vries GJ, Forger NG (2009) Sexual differentiation of the brain: mode, mechanisms, and meaning. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, brain and behavior. Academic, San Diego, pp 1707–1744

    Chapter  Google Scholar 

  • Meyer-Bahlburg HFL (2005) Gender identity outcome in female-raised 46, XY persons with penile agenesis, cloacal exstrophy of the bladder, or penile ablation. Archiv Sex Behav 34:423–438

    Article  Google Scholar 

  • Meyer-Bahlburg HFL, Gruen RS, New MI, Bell JJ, Morishima A, Shimshi M, Bueno Y, Vargas I, Baker SW (1996) Gender change from female to male in classical congenital adrenal hyperplasia. Horm Behav 30:319–332

    Article  PubMed  CAS  Google Scholar 

  • Meyer-Bahlburg HFL, Dolezal C, Baker SW, New MI (2008) Sexual orientation in women with classical or non-classical congenital adrenal hyperplasia as a function of degree of prenatal androgen excess. Arch Sex Behav 37:85–99

    Article  PubMed  Google Scholar 

  • Money J, Schwartz M, Lewis V (1984) Adult erotosexual status and fetal hormonal masculinization and demasculinization: 46 XX congenital virilizing adrenal hyperplasia and 46 XY androgen-insensitivity syndrome compared. Psychoneuroendocrinology 9:405–414

    Article  PubMed  CAS  Google Scholar 

  • Nagamani M, McDonough PG, Ellegood JO, Mahesh VB (1979) Maternal and amniotic fluid steroids throughout human pregnancy. Am J Obstet Gynecol 134:674–680

    PubMed  CAS  Google Scholar 

  • New M (1998) Diagnosis and management of congenital adrenal hyperplasia. Ann Rev Med 49:311–328

    Article  PubMed  CAS  Google Scholar 

  • Nordenstrom A, Servin A, Bohlin G, Larsson A, Wedell A (2002) Sex-typed toy play behavior correlates with the degree of prenatal androgen exposure assessed by CYP21 genotype in girls with congenital adrenal hyperplasia. J Clin Endocrinol Metab 87:5119–5124

    Article  PubMed  CAS  Google Scholar 

  • Pang S, Levine LS, Cederqvist LL, Fuentes M, Riccardi VM, Holcombe JH, Nitowsky HM, Sachs G, Anderson CE, Duchon MA, Owens R, Merkatz I, New MI (1980) Amniotic fluid concentrations of delta 5 and delta 4 steroids in fetuses with congenital adrenal hyperplasia due to 21-hydroxylase deficiency and in anencephalic fetuses. J Clin Endocrinol Metabol 51:223–229

    Article  CAS  Google Scholar 

  • Pasterski VL, Geffner ME, Brain C, Hindmarsh P, Brook C, Hines M (2005) Prenatal hormones and postnatal socialization by parents as determinants of male-typical toy play in girls with congenital adrenal hyperplasia. Child Dev 76:264–278

    Article  PubMed  Google Scholar 

  • Pasterski VL, Hindmarsh P, Geffner M, Brook C, Brain C, Hines M (2007) Increased aggression and activity level in 3- to 11-year-old girls with congenital adrenal hyperplasia (CAH). Horm Behav 52:368–374

    Article  PubMed  CAS  Google Scholar 

  • Pasterski VL, Geffner ME, Brain C, Hindmarsh PC, Brook C, Hines M (2011) Prenatal hormones and childhood sex segregation: playmate and play style preferences in girls with congenital adrenal hyperplasia. Horm Behav 59:549–555

    Article  PubMed  CAS  Google Scholar 

  • Perry DG, Bussey K (1979) The social learning theory of sex difference: imitation is alive and well. J Personal Soc Psychol 37:1699–1712

    Article  Google Scholar 

  • Reinisch JM (1981) Prenatal exposure to synthetic progestins increases potential for aggression in humans. Science 211:1171–1173

    Article  PubMed  CAS  Google Scholar 

  • Reyes FI, Winter JSD, Faiman C (1973) Studies on human sexual development. I. Fetal gonadal and adrenal sex steroids. J Clin Endocrinol Metabol 37:74–78

    Article  CAS  Google Scholar 

  • Rheingold HL, Cook KV (1975) The content of boys’ and girls’ room as an index of parents’ behavior. Child Dev 46:459–463

    Article  Google Scholar 

  • Robinson J, Judd H, Young P, Jones D, Yen S (1977) Amniotic fluid androgens and estrogens in midgestation. J Clin Endocrinol Metab 45:755–761

    Article  PubMed  CAS  Google Scholar 

  • Rodeck CH, Gill D, Rosenberg DA, Collins WP (1985) Testosterone levels in midtrimester maternal and fetal plasma and amniotic fluid. Prenatal Diagn 5:175–181

    Article  CAS  Google Scholar 

  • Seavey AA, Katz PA, Zalk SR (1975) Baby X: the effect of gender labels on adult responses to infants. Sex Roles 1:103–109

    Article  Google Scholar 

  • Serbin LA, Poulin-Dubois D, Colbourne KA, Sen MG, Eichstedt JA (2001) Gender stereotyping in infancy: visual preferences for and knowledge of gender-stereotyped toys in the second year. Intl J Behav Dev 25:7–15

    Article  Google Scholar 

  • Slaby RG, Frey KS (1975) Development of gender constancy and selective. Child Dev 46:849–856

    Article  PubMed  CAS  Google Scholar 

  • Slijper FME (1984) Androgens and gender role behaviour in girls with congenital adrenal hyperplasia (CAH). In: De Vries GJ, De Bruin JPC, Uylings HBM, Corner MA (eds) Progress in brain research. Elsevier, Amsterdam, pp 417–422

    Google Scholar 

  • Slijper FME, Drop SLS, Molenaar JC, de Muinck K-SSMPF (1998) Long-term psychological evaluation of intersex children. Arch Sex Behav 27:125–144

    Article  PubMed  CAS  Google Scholar 

  • Stagnor C, Ruble DN (1987) Development of gender role knowledge and gender constancy. In: Liben LS, Signorella ML (eds) Children’s gender schemata: new directions for child development. Jossey-Bass, San Francisco, pp 5–22

    Google Scholar 

  • Stern M, Karraker KH (1989) Sex stereotyping of infants: a review of gender labeling studies. Sex Roles 20:501–522

    Article  Google Scholar 

  • Wilson JD, George FW, Griffin JE (1981) The hormonal control of sexual development. Science 211:1278–1284

    Article  PubMed  CAS  Google Scholar 

  • Wudy SA, Dörr HG, Solleder C, Djalali M, Homoki J (1999) Profiling steroid hormones in amniotic fluid of midpregnancy by routine stable isotope dilution/ gas chromatography–mass spectrometry: reference values and concentrations in fetuses at risk for 21-hydroxylase deficiency. J Clin Endocrinol Metab 84:2724–2728

    Article  PubMed  CAS  Google Scholar 

  • Zucker KJ, Bradley SJ, Oliver G, Blake J, Fleming S, Hood J (1996) Psychosexual development of women with congenital adrenal hyperplasia. Horm Behav 30:300–318

    Article  PubMed  CAS  Google Scholar 

  • Zucker KJ, Bradley SJ, Kuksis M, Pecore K, Birkenfeld-Adams A, Doering RW, Mitchell JN, Wild J (1999) Gender constancy judgements in children with gender identity disorder: evidence for a developmental lag. Arch Sex Behav 28:475–502

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Melissa Hines .

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Hines, M. (2013). Gonadal Hormone Influences on Human Neurobehavioral Development: Outcomes and Mechanisms. In: Pfaff, D., Christen, Y. (eds) Multiple Origins of Sex Differences in Brain. Research and Perspectives in Endocrine Interactions. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-33721-5_5

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