Prenatal and postnatal hormone effects on the human brain and cognition

Pflugers Archiv European Journal of Physiology

Volumn 465, Issue 5, 2013, Pages 557-571

  Auyeung, Bonnie ^a   Lombardo, Michael V ^a   Baron Cohen, Simon ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Amniocentesis; Amniotic fluid; Oxytocin; Postnatal testosterone; Prenatal testosterone; Puberty; Sex differences; Testosterone administration

Indexed keywords

HORMONE; OXYTOCIN; TESTOSTERONE;

AMNIOCENTESIS; AMNION FLUID ANALYSIS; AUTISM; BRAIN DEVELOPMENT; BRAIN FUNCTION; CHILD BEHAVIOR; COGNITION; CONGENITAL ADRENAL HYPERPLASIA; EMOTIONALITY; EMPATHY; EYE CONTACT; HORMONE ACTION; HORMONE BLOOD LEVEL; HORMONE DETERMINATION; HORMONE SYNTHESIS; HUMAN; LANGUAGE DEVELOPMENT; MENTAL FUNCTION; MIND READING; NONHUMAN; OVARY POLYCYSTIC DISEASE; PERINATAL PERIOD; PLAY; PRENATAL EXPOSURE; PRENATAL PERIOD; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SEX DIFFERENTIATION; SEX ROLE; SEXUAL FUNCTION; SOCIAL COGNITION; SOCIAL INTERACTION; VISUAL SYSTEM FUNCTION; VOCABULARY SIZE;

BRAIN; CHILD; CHILD DEVELOPMENT; COGNITION; FEMALE; HUMANS; MALE; OXYTOCIN; SEX CHARACTERISTICS; TESTOSTERONE; YOUNG ADULT;

EID: 84878017235     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-013-1268-2     Document Type: Review

References (145)

1. Abramovich DR (1974) Human sexual differentiation - in utero influences. J Obstet Gynecol 81:448-453
2. Abramovich DR, Rowe P (1973) Foetal plasma testosterone levels at mid-pregnancy and at term: relationship to foetal sex. J Endocrinol 56(3):621-622
3. Alexander GM, Hines M (1994) Gender labels and play styles: their relative contribution to children's selection of playmates. Child Dev 65:869-879
4. Allison C, Baron-Cohen S, Wheelwright S, Charman T, Richler J, Pasco G, Brayne C (2008) The Q-CHAT (Quantitative Checklist for Autism in Toddlers): a normally distributed quantitative measure of autistic traits at 18-24 months of age: preliminary report. J Autism Dev Disord 38:1414-1425
5. APA (1994) DSM-IV Diagnostic and statistical manual of mental disorders, 4th edn. American Psychiatric Association, Washington
6. Arnold AP, Gorski RA (1984) Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci 7:413-442
7. Auyeung B (2008) Foetal testosterone, cognitive sex differences and autistic traits. University of Cambridge, Cambridge
8. Auyeung B, Allison C, Wheelwright S, Baron-Cohen S (2012) Brief report: development of the adolescent empathy and systemizing quotients. J Autism Dev Disord 42(10):2225-2235. doi: 10.1007/s10803-012-1454-7
9. Auyeung B, Baron-Cohen S, Ashwin 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
10. Auyeung B, Baron-Cohen S, Chapman E, Knickmeyer R, Taylor K, Hackett G (2006) Foetal testosterone and the child systemizing quotient. Eur J Endocrinol 155(suppl 1):S123-S130
11. Auyeung B, Baron-Cohen S, Chapman E, Knickmeyer R, Taylor K, Hackett G (2009) Fetal testosterone and autistic traits. Brit J Psychol 100:1-22
12. Auyeung B, Baron-Cohen S, Wheelwright S, Allison C (2008) The Autism Spectrum Quotient: children's version (AQ-Child). J Autism Dev Disord 38:1230-1240
13. Auyeung B, Taylor K, Hackett G, Baron-Cohen S (2010) Foetal testosterone and autistic traits in 18 to 24-month-old children. Mol Autism 1(1):11
14. Baron-Cohen S (1999) The extreme male-brain theory of autism. In: Tager Flusberg H (ed) Neurodevelopmental disorders. MIT Press, Cambridge
15. Baron-Cohen S, Lutchmaya S, Knickmeyer R (2004) Prenatal testosterone in mind. MIT Press, Cambridge
16. Baron-Cohen S, Wheelwright S, Spong A, Scahill L, Lawson J (2001) Are intuitive physics and intuitive psychology independent? A test with children with Asperger syndrome. J Dev Learn Disord 5:47-78
17. Baum MJ, Erskine MS (1984) Effect of neonatal gonadectomy and administration of testosterone on coital masculinization in the ferret. Endocrinology 115(6):2440-2444
18. Baumgartner T, Heinrichs M, Vonlanthen A, Fischbacher U, Fehr E (2008) Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58(4):639-650. doi: 10.1016/j.neuron.2008.04.009
19. Beatty WW, Tröster AI (1987) Gender differences in geographical knowledge. Sex Roles 16(11-12):565-590
20. Beck-Peccoz P, Padmanabhan V, Baggiani AM, Cortelazzi D, Buscaglia M, Medri G, Marconi AM, Pardi G, Beitins IZ (1991) Maturation of hypothalamic-pituitary-gonadal function in normal human fetuses: circulating levels of gonadotropins, their common alpha-subunit and free testosterone, and discrepancy between immunological and biological activities of circulating follicle-stimulating hormone. J Clin Endocr Metab 73:525-532
21. Bem SL (1974) The measurement of psychological androgyny. J Consult Clin Psychol 42(2):155-162
22. Berenbaum SA, Hines M (1992) Early androgens are related to childhood sex-typed toy preferences. Psychol Sci 3:203-206
23. Berlin DF, Languis ML (1981) Hemispheric correlates of the rod-and-frame test. Percept Mot Ski 52(1):35-41
24. Bishop DVM (1998) Development of the children's communication checklist (CCC): a method for assessing qualitative aspects of communicative impairment in children. J Child Psychol Psychiatry 6:879-891
25. Bos PA, Hermans EJ, Montoya ER, Ramsey NF, van Honk J (2010) Testosterone administration modulates neural responses to crying infants in young females. Psychoneuroendocrinology 35(1):114-121. doi: 10.1016/j.psyneuen.2009.09.013
26. Bos PA, Hermans EJ, Ramsey NF, van Honk J (2012) The neural mechanisms by which testosterone acts on interpersonal trust. NeuroImage 61(3):730-737. doi: 10.1016/j.neuroimage.2012.04.002
27. Bos PA, Panksepp J, Bluthe RM, van Honk J (2012) Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: a review of single administration studies. Front Neuroendocrinol 33(1):17-35. doi: 10.1016/j.yfrne.2011.01.002
28. Bos PA, Terburg D, van Honk J (2010) Testosterone decreases trust in socially naive humans. Proc Natl Acad Sci U S A 107(22):9991-9995. doi: 10.1073/pnas.0911700107
29. Bramen JE, Hranilovich JA, Dahl RE, Chen J, Rosso C, Forbes EE, Dinov ID, Worthman CM, Sowell ER (2012) Sex matters during adolescence: testosterone-related cortical thickness maturation differs between boys and girls. PLoS One 7(3):e33850. doi: 10.1371/journal.pone.0033850
30. Breedlove SM (1994) Sexual differentiation of the human nervous system. Ann RevPsychol 45:389-418
31. Carter CS, Williams JR, Witt DM, Insel TR (1992) Oxytocin and social bonding. Ann N Y Acad Sci 652:204-211
32. Chakrabarti S, Fombonne E (2005) Pervasive developmental disorders in preschool children: confirmation of high prevalence. Am J Psychiatry 162(6):1133-1141
33. 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
34. Christensen LW, Gorski RA (1978) Independent masculinization of neuroendocrine systems by intracerebral implants of testosterone or estradiol in the neonatal female rat. Brain Res 146(2):325-340. doi: 10.1016/0006-8993(78) 90977-0
35. Chura LR, Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Bullmore ET, Baron-Cohen S (2010) Organizational effects of fetal testosterone on human corpus callosum size and asymmetry. Psychoneuroendocrinology 35:122-132
36. Clements JA, Reyes FI, Winter JS, Faiman C (1976) Studies on human sexual development. III. Fetal pituitary and serum, and amniotic fluid concentrations of LH, CG, and FSH. J Clin Endocrinol Metab 42(1):9-19
37. Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale
38. Cohen-Bendahan CCC, Buitelaar JK, van Goozen SHM, Orlebeke JF, Cohen-Kettenis PT (2005) Is there an effect of prenatal testosterone on aggression and other behavioral traits? A study comparing same-sex and opposite-sex twin girls. Horm Behav 47:230-237
39. Cohen-Bendahan CC, van de Beek C, Berenbaum SA (2005) Prenatal sex hormone effects on child and adult sex-typed behavior: methods and findings. Neurosci Biobehav R 29(2):353-384
40. Collaer ML, Hines M (1995) Human behavioural sex differences: a role for gonadal hormones during early development? Psychol Bull 118:55-107
41. Connellan J, Baron-Cohen S, Wheelwright S, Batki A, Ahluwalia J (2000) Sex differences in human neonatal social perception. Infant Behav Dev 23(1):113-118
42. d'Ercole C, Shojai R, Desbriere R, Chau C, Bretelle F, Piechon L, Boubli L (2003) Prenatal screening: invasive diagnostic approaches. Child's Nerv Syst 19(7-8):444-447
43. Derntl B, Kryspin-Exner I, Fernbach E, Moser E, Habel U (2008) Emotion recognition accuracy in healthy young females is associated with cycle phase. Horm Behav 53(1):90-95. doi: 10.1016/j.yhbeh.2007.09.006
44. Derntl B, Windischberger C, Robinson S, Lamplmayr E, Kryspin-Exner I, Gur RC, Moser E, Habel U (2008) Facial emotion recognition and amygdala activation are associated with menstrual cycle phase. Psychoneuroendocrinology 33(8):1031-1040. doi: 10.1016/j.psyneuen.2008.04.014
45. Di Martino A, Ross K, Uddin LQ, Sklar AB, Castellanos FX, Milham MP (2009) Functional brain correlates of social and nonsocial processes in autism spectrum disorders: an activation likelihood estimation meta-analysis. Biol Psychiatry 65(1):63-74. doi: 10.1016/j.biopsych.2008.09.022
46. Domes G, Heinrichs M, Glascher J, Buchel C, Braus DF, Herpertz SC (2007) Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol Psychiatry 62:1187-1190
47. Domes G, Lischke A, Berger C, Grossmann A, Hauenstein K, Heinrichs M, Herpertz SC (2010) Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 35(1):83-93. doi: 10.1016/j.psyneuen.2009.06. 016
48. Dumontheil I, Burgess PW, Blakemore SJ (2008) Development of rostral prefrontal cortex and cognitive and behavioural disorders. Dev Med Child Neurol 50(3):168-181. doi: 10.1111/j.1469-8749.2008.02026.x
49. Ehrhardt AA, Meyer-Bahlburg HF (1981) Effects of prenatal sex hormones on gender-related behavior. Science 211(4488):1312-1318
50. Eisenegger C, Naef M, Snozzi R, Heinrichs M, Fehr E (2010) Prejudice and truth about the effect of testosterone on human bargaining behaviour. Nature 463(7279):356-359. doi: 10.1038/nature08711
51. Fausto-Sterling A (1992) Myths of gender. Basic Books, New York
52. Finkelstein JW, Susman EJ, Chinchilli VM, Kunselman SJ, D'Arcangelo MR, Schwab J, Demers LM, Liben LS, Lookingbill G, Kulin HE (1997) Estrogen or testosterone increases self-reported aggressive behaviors in hypogonadal adolescents. J Clin Endocrinol Metab 82(8):2433-2438
53. Fleischman DS, Navarrete CD, Fessler DM (2010) Oral contraceptives suppress ovarian hormone production. Psychol Sci 21(5):750-752. doi: 10.1177/0956797610368062, author reply 753
54. Forbes EE, Dahl RE (2010) Pubertal development and behavior: hormonal activation of social and motivational tendencies. Brain Cogn 72(1):66-72. doi: 10.1016/j.bandc.2009.10.007
55. Frith U, Morton J, Leslie AM (1991) The cognitive basis of a biological disorder: autism. Trends Neurosci 14(10):433-438
56. Galea LA, Kimura D (1993) Sex differences in route-learning. Personal Individ Differ 14(1):53-65
57. Gamer M, Zurowski B, Buchel C (2010) Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proc Natl Acad Sci U S A 107(20):9400-9405. doi: 10.1073/pnas.1000985107
58. Gillberg C, Cederlund M, Lamberg K, Zeijlon L (2006) Brief report: "the autism epidemic". The registered prevalence of autism in a Swedish urban area. J Autism Dev Disord 36(3):429-435
59. Gotz F, Dorner G (1976) Sex hormone-dependent brain maturation and sexual behaviour in rats. Endokrinologie 68(3):275-282
60. Goy RW, Bercovitch FB, McBrair MC (1988) Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques. Horm Behav 22:552-571
61. Goy RW, McEwen BS (1980) Sexual differentiation of the brain. MIT Press, Cambridge
62. Guastella AJ, Mitchell PB, Dadds MR (2008) Oxytocin increases gaze to the eye region of human faces. Biol Psychiatry 63(1):3-5
63. Hamilton A, Plunkett K, Shafer G (2000) Infant vocabulary development assessed with a British communicative inventory: lower scores in the UK than the USA. J Child Lang 27(3):689-705
64. Hampson E, Rovet JF, Altmann D (1998) Spatial reasoning in children with congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Dev Neuropsychol 14(2):299-320
65. Harris JA, Vernon PA, Boomsma DI (1998) The heritability of testosterone: a study of Dutch adolescent twins and their parents. Behav Genet 28:165-171
66. Heinrichs M, von Dawans B, Domes G (2009) Oxytocin, vasopressin, and human social behavior. Front Neuroendocrinol 30(4):548-557. doi: 10.1016/j.yfrne.2009.05.005
67. Hermans EJ, Bos PA, Ossewaarde L, Ramsey NF, Fernandez G, van Honk J (2010) Effects of exogenous testosterone on the ventral striatal BOLD response during reward anticipation in healthy women. NeuroImage 52(1):277-283. doi: 10.1016/j.neuroimage.2010.04.019
68. Hermans EJ, Putman P, van Honk J (2006) Testosterone administration reduces empathetic behavior: a facial mimicry study. Psychoneuroendocrinology 31(7):859-866
69. Hermans EJ, Ramsey NF, van Honk J (2008) Exogenous testosterone enhances responsiveness to social threat in the neural circuitry of social aggression in humans. Biol Psychiatry 63(3):263-270. doi: 10.1016/j.biopsych.2007.05.013
70. Hines M (2003) Sex steroids and human behavior: prenatal androgen exposure and sex-typical play behavior in children. Ann N Y Acad Sci 1007:272-282
71. Hines M (2004) Brain gender. Oxford University Press, New York
72. 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(1):75-81
73. Hines M, Davis FC, Coquelin A, Goy RW, Gorski RA (1985) Sexually dimorphic regions in the medial preoptic area and the bed nucleus of the stria terminalis of the guinea pig brain: a description and an investigation of their relationship to gonadal steroids in adulthood. J Neurosci 5(1):40-47
74. Hines M, Fane BA, Pasterski VL, Matthews GA, Conway GS, Brook C (2003) Spatial abilities following prenatal androgen abnormality: targeting and mental rotations performance in individuals with congenital adrenal hyperplasia. Psychoneuroendocrinology 28:1010-1026
75. Hoekstra R, Bartels M, Boomsma DI (2006) Heritability of testosterone levels in 12-year-old twins and its relation to pubertal development. Twin Res Hum Genet 9:558-565
76. Hoffman ML (1977) Sex differences in empathy and related behaviors. Psychol Bull 84(4):712-722
77. Insel TR, Hulihan TJ (1995) A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behav Neurosci 109(4):782-789
78. Insel TR, Winslow JT, Wang ZX, Young L, Hulihan TJ (1995) Oxytocin and the molecular basis of monogamy. Adv Exp Med Biol 395:227-234
79. Insel TR, Winslow JT, Witt DM (1992) Homologous regulation of brain oxytocin receptors. Endocrinology 130(5):2602-2608
80. Johnson ES, Meade AC (1987) Developmental patterns of spatial ability: an early sex difference. Child Dev 58(3):725-740
81. Jost A (1970) Hormonal factors in the sex differentiation of the mammalian foetus. Philos Trans R Soc Lon: B Biol Sci 259(828):119-130
82. Kimura D (1999) Sex and cognition. MIT Press, Cambridge
83. Kirsch P, Esslinger C, Chen Q, Mier D, Lis S, Siddhanti S, Gruppe H, Mattay VS, Gallhofer B, Meyer-Lindenberg A (2005) Oxytocin modulates neural circuitry for social cognition and fear in humans. J Neurosci 25(49):11489-11493
84. Klin A, Jones W, Schultz R, Volkmar F, Cohen D (2002) Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Arch Gen Psychiatry 59(9):809-816
85. Knickmeyer RC, Baron-Cohen S (2006) Fetal testosterone and sex differences. Early Human Dev 82(12):755-760
86. Knickmeyer R, Baron-Cohen S, Raggatt P, Taylor K (2005) Foetal testosterone, social relationships, and restricted interests in children. J Child Psychol Psychiatry 46(2):198-210
87. Knickmeyer R, Baron-Cohen S, Raggatt P, Taylor K, Hackett G (2006) Fetal testosterone and empathy. Horm Behav 49:282-292
88. Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E (2005) Oxytocin increases trust in humans. Nature 435(7042):673-676
89. Labuschagne I, Phan KL, Wood A, Angstadt M, Chua P, Heinrichs M, Stout JC, Nathan PJ (2010) Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder. Neuropsychopharmacology 35(12):2403-2413
90. Larsen PR, Kronenberg HM, Melmed S, Polonsky KS (eds) (2002) Williams textbook of endocrinology, 10th edn. Philadelphia, Saunders
91. Leslie AM (1987) Pretence and representation: the origins of "theory of mind". Psychol Rev 94:412-426
92. Liss MB (1979) Variables influencing modeling and sex-typed play. Psychol Rep 44:1107-1115
93. Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Lai MC, Taylor K, Hackett G, Bullmore ET, Baron-Cohen S (2012) Fetal programming effects of testosterone on the reward system and behavioral approach tendencies in humans. Biol Psychiatry. doi: 10.1016/j.biopsych.2012.05.027
94. Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Taylor K, Hackett G, Bullmore ET, Baron-Cohen S (2012) Fetal testosterone influences sexually dimorphic gray matter in the human brain. J Neurosci 32(2):674-680. doi: 10.1523/JNEUROSCI.4389-11.2012
95. Lombardo MV, Baron-Cohen S, Belmonte MK, Chakrabarti B (2011) Neural endophenotypes of social behaviour in autism spectrum conditions. In: Decety J, Cacioppo J (eds) Oxford handbook of social neuroscience. Oxford University Press, Oxford
96. Lutchmaya S, Baron-Cohen S, Raggatt P (2002) Foetal testosterone and eye contact in 12 month old infants. Infant Behav Dev 25:327-335
97. Lutchmaya S, Baron-Cohen S, Raggatt P (2002) Foetal testosterone and vocabulary size in 18- and 24-month-old infants. Infant Behav Dev 24(4):418-424
98. MacLusky N, Naftolin F (1981) Sexual differentiation of the central nervous system. Science 211:1294-1303
99. Martin CA, Kelly TH, Rayens MK, Brogli BR, Brenzel A, Smith WJ, Omar HA (2002) Sensation seeking, puberty, and nicotine, alcohol, and marijuana use in adolescence. J Am Acad Child Adolesc Psychiatry 41(12):1495-1502. doi: 10.1097/00004583-200212000-00022
100. Masters MS, Sanders B (1993) Is the gender difference in mental rotation disappearing? Behav Genet 23(4):337-341
101. McCarthy MM, Arnold AP (2011) Reframing sexual differentiation of the brain. Nat Neurosci 14(6):677-683
102. McCarthy MM, Auger AP, Bale TL, De Vries GJ, Dunn GA, Forger NG, Murray EK, Nugent BM, Schwarz JM, Wilson ME (2009) The epigenetics of sex differences in the brain. J Neurosci 29(41):12815-12823
103. New MI (1998) Diagnosis and management of congenital adrenal hyperplasia. Ann Rev Med 49:311-328
104. Norman RJ, Dewailly D, Legro RS, Hickey TE (2007) Polycystic ovary syndrome. Lancet 370(9588):685-697
105. Palomba S, Marotta A, Di Cello A, Russo T, Falbo A, Orio F, Tolino A, Zullo F, Esposito R, La Sala GB (2012) Pervasive developmental disorders in children of hyperandrogenic women with polycystic ovary syndrome: a longitudinal case-control study. Clin Endocrinol (Oxf). doi: 10.1111/j.1365-2265.2012.04443. x
106. 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(1):264-278
107. Petersen AC, Crockett L, Richards M, Boxer A (1988) A self-report measure of pubertal status: reliability, validity, and initial norms. J Youth Adolesc 17:117-133
108. Petrovic P, Kalisch R, Singer T, Dolan RJ (2008) Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity. J Neurosci 28(26):6607-6615
109. Phoenix CH, Goy RW, Gerall AA, Young WC (1959) Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65:369-382
110. Pincus D, Kose S, Arana A, Johnson K, Morgan PS, Borckardt J, Herbsman T, Hardaway F, George MS, Panksepp J, Nahas Z (2010) Inverse effects of oxytocin on attributing mental activity to others in depressed and healthy subjects: a double-blind placebo controlled FMRI study. Front Psychiatry 1:134. doi: 10.3389/fpsyt.2010.00134
111. Popik P, Vos PE, Van Ree JM (1992) Neurohypophyseal hormone receptors in the septum are implicated in social recognition in the rat. Behav Pharmacol 3(4):351-358
112. Quadagno DM, Briscoe R, Quadagno JS (1977) Effects of perinatal gonadal hormones on selected nonsexual behavior patterns: a critical assessment of the nonhuman and human literature. Psychol Bull 84:62-80
113. Reinisch JM, Sanders SA (1986) A test of sex differences in aggressive response to hypothetical conflict situations. J Personal Soc Psychol 50(5):1045-1049
114. Resnick SM, Berenbaum SA, Gottesman II, Bouchard TJ (1986) Early hormonal influences on cognitive functioning in congenital adrenal hyperplasia. Dev Psychol 22(2):191-198
115. Reyes FI, Boroditsky RS, Winter JS, Faiman C (1974) Studies on human sexual development. II. Fetal and maternal serum gonadotropin and sex steroid concentrations. J Clin Endocrinol Metab 38(4):612-617
116. Reyes FI, Winter JS, Faiman C (1973) Studies on human sexual development. I. Fetal gonadal and adrenal sex steroids. J Clin Endocrinol Metab 37(1):74-78
117. Riem MM, Bakermans-Kranenburg MJ, Pieper S, Tops M, Boksem MA, Vermeiren RR, van Ijzendoorn MH, Rombouts SA (2011) Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biol Psychiatry. doi: 10.1016/j.biopsych.2011.02.006
118. Robinson J, Judd H, Young P, Jones D, Yen S (1977) Amniotic fluid androgens and estrogens in midgestation. J Clin Endocrinol 45:755-761
119. Romeo RD, Richardson HN, Sisk CL (2002) Puberty and the maturation of the male brain and sexual behavior: recasting a behavioral potential. Neurosci Biobehav Rev 26(3):381-391
120. Sangalli M, Langdana F, Thurlow C (2004) Pregnancy loss rate following routine genetic amniocentesis at Wellington Hospital. N Z Med J 117(1191):U818
121. Saxe R, Kanwisher N (2003) People thinking about thinking people. The role of the temporo-parietal junction in "theory of mind". NeuroImage 19(4):1835-1842
122. Schulz KM, Molenda-Figueira HA, Sisk CL (2009) Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm Behav 55(5):597-604. doi: 10.1016/j.yhbeh.2009.03.010
123. Scott FJ, Baron-Cohen S, Bolton P, Brayne C (2002) The CAST (Childhood Asperger Syndrome Test): preliminary development of a UK screen for mainstream primary-school-age children. Autism 6(1):9-13
124. Seron-Ferre M, Ducsay CA, Valenzuela GJ (1993) Circadian rhythms during pregnancy. Endocr Rev 14(5):594-609
125. Servin A, Bohlin G, Berlin D (1999) Sex differences in 1-, 3-, and 5-year-olds' toy-choice in a structured play session. Scand J Psychol 40:43-48
126. Smail PJ, Reyes FI, Winter JSD, Faiman C (1981) The fetal hormonal environment and its effect on the morphogenesis of the genital system. In: Kogan SJ, Hafez ESE (eds) Pediatric andrology. Martinus Nijhoff, Boston, pp 9-19
127. Stern M, Karraker KH (1989) Sex stereotyping of infants: a review of gender labeling studies. Sex Roles 20:501-522
128. Striepens N, Kendrick KM, Maier W, Hurlemann R (2011) Prosocial effects of oxytocin and clinical evidence for its therapeutic potential. Front Neuroendocrinol 32(4):426-450. doi: 10.1016/j.yfrne.2011.07.001
129. Swettenham J, Baron-Cohen S, Charman T, Cox A, Baird G, Drew A, Rees L, Wheelwright S (1998) The frequency and distribution of spontaneous attention shifts between social and non-social stimuli in autistic, typically developing, and non-autistic developmentally delayed infants. J Child Psychol Psychiatry 9:747-753
130. Tanner JM (1962) Growth at adolescence: with a general consideration of the effects of hereditary and environmental factors upon growth and maturity from birth to maturity, 2nd edn. Blackwell, Oxford
131. Terburg D, Aarts H, van Honk J (2012) Testosterone affects gaze aversion from angry faces outside of conscious awareness. Psychol Sci 23(5):459-463. doi: 10.1177/0956797611433336
132. van Honk J, Montoya ER, Bos PA, van Vugt M, Terburg D (2012) New evidence on testosterone and cooperation. Nature 485(7399):E4-E5. doi: 10.1038/nature11136, discussion E5-6
133. van Honk J, Schutter DJ (2007) Testosterone reduces conscious detection of signals serving social correction: implications for antisocial behavior. Psychol Sci 18(8):663-667. doi: 10.1111/j.1467-9280.2007.01955.x
134. van Honk J, Schutter DJ, Bos PA, Kruijt AW, Lentjes EG, Baron-Cohen S (2011) Testosterone administration impairs cognitive empathy in women depending on second-to-fourth digit ratio. Proc Natl Acad Sci U S A 108(8):3448-3452. doi: 10.1073/pnas.1011891108
135. van Honk J, Schutter DJ, Hermans EJ, Putman P, Tuiten A, Koppeschaar H (2004) Testosterone shifts the balance between sensitivity for punishment and reward in healthy young women. Psychoneuroendocrinology 29(7):937-943. doi: 10.1016/j.psyneuen.2003.08.007
136. van Wingen G, Mattern C, Verkes RJ, Buitelaar J, Fernandez G (2010) Testosterone reduces amygdala-orbitofrontal cortex coupling. Psychoneuroendocrinology 35(1):105-113. doi: 10.1016/j.psyneuen.2009.09.007
137. Walsh SW, Ducsay CA, Novy MJ (1984) Circadian hormonal interactions among the mother, fetus, and amniotic fluid. Am J Obstet Gynecol 150(6):745-753
138. Wheelwright S, Baron-Cohen S, Goldenfeld N, Delaney J, Fine D, Smith R, Weil L, Wakabayashi A (2006) Predicting Autism Spectrum Quotient (AQ) from the Systemizing Quotient-Revised (SQ-R) and Empathy Quotient (EQ). Brain Res 1079(1):47-56
139. Williams CL, Meck WH (1991) The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 16(1-3):155-176
140. Williams J, Scott F, Stott C, Allison C, Bolton P, Baron-Cohen S, Brayne C (2005) The CAST (Childhood Asperger Syndrome Test): test accuracy. Autism 9(1):45-68
141. Witkin HA, Dyk RB, Fattuson HF, Goodenough DR, Karp SA (1962) Psychological differentiation: studies of development. Wiley, Oxford, p 418
142. Witt DM, Winslow JT, Insel TR (1992) Enhanced social interactions in rats following chronic, centrally infused oxytocin. Pharmacol Biochem Behav 43(3):855-861
143. Wright ND, Bahrami B, Johnson E, Di Malta G, Rees G, Frith CD, Dolan RJ (2012) Testosterone disrupts human collaboration by increasing egocentric choices. Proc Biol Sci 279(1736):2275-2280. doi: 10.1098/rspb.2011.2523
144. Zak PJ, Kurzban R, Ahmadi S, Swerdloff RS, Park J, Efremidze L, Redwine K, Morgan K, Matzner W (2009) Testosterone administration decreases generosity in the ultimatum game. PLoS One 4(12):e8330. doi: 10.1371/journal.pone.0008330
145. Zuckerman M (1971) Dimensions of sensation seeking. J Consult Clin Psychol 36:45-52