Sexual differentiation of the human brain: Relation to gender identity, sexual orientation and neuropsychiatric disorders

Frontiers in Neuroendocrinology

Volumn 32, Issue 2, 2011, Pages 214-226

  Bao, Ai Min ^a   Swaab, Dick F ^b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Aggression; Alzheimer's disease; Androgen receptor; Depression; Estrogen receptors; Gender identity; Sex hormones; Sexual differentiation; Sexual orientation

Indexed keywords

CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR; SEX HORMONE; VASOPRESSIN;

ALZHEIMER DISEASE; ANTERIOR HYPOTHALAMUS; BISEXUALITY; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN REGION; CONGENITAL ADRENAL HYPERPLASIA; COPING BEHAVIOR; DEPRESSION; GENDER IDENTITY; HETEROSEXUALITY; HOMOSEXUALITY; HORMONAL REGULATION; HORMONE RELEASE; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INCIDENCE; MENTAL DISEASE; NEUROLOGIC DISEASE; NEUROPSYCHIATRY; PERINATAL PERIOD; PREVALENCE; PRIORITY JOURNAL; PSYCHOSOCIAL ENVIRONMENT; REVIEW; RISK ASSESSMENT; SCHIZOPHRENIA; SEX DIFFERENTIATION; SEX HORMONE DETERMINATION; SEXUAL ORIENTATION; TRANSSEXUALISM; X CHROMOSOME;

BRAIN; GENDER IDENTITY; GONADAL STEROID HORMONES; HUMANS; MENTAL DISORDERS; NERVOUS SYSTEM DISEASES; PLAY AND PLAYTHINGS; SEX DIFFERENTIATION; SEXUAL BEHAVIOR; TESTOSTERONE; TRANSSEXUALISM;

EID: 79955484076     PISSN: 00913022     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yfrne.2011.02.007     Document Type: Review

References (148)

1. Alexander G.M., Hines M. Sex differences in response to children's toys in nonhuman primates (Cercopithecus aethiops sabaeus). Eval. Hum. Behav. 2002, 23:467-479.
2. Alexander G.M., Wilcox T., Woods R. Sex differences in infants' visual interest in toys. Arch. Sex Behav. 2009, 38:427-433.
3. Allen L.S., Gorski R.A. Sexual dimorphism of the anterior commissure and Massa intermedia of the human brain. J. Comp. Neurol. 1991, 312:97-104.
4. Allen L.S., Hines M., Shryne J.E., Gorski R.A. Two sexually dimorphic cell groups in the human brain. J. Neurosci. 1989, 9:497-506.
5. Asplund R., Aberg H. Diurnal variation in the levels of antidiuretic hormone in the elderly. J. Int. Med. 1991, 229:131-134.
6. Bailey J.M., Bell A.P. Familiarity of female and male homosexuality. Behav. Genet. 1993, 23:313-322.
7. Bangasser D.A., Curtis A., Reyes B.A., Bethea T.T., Parastatidis I., Ischiropoulos H., Van Bockstaele E.J., Valentino R.J. Sex differences in corticotropin-releasing factor receptor signaling and trafficking: potential role in female vulnerability to stress-related psychopathology. Mol. Psychiatry 2010, 15:877. 896-904.
8. Bao A.M., Swaab D.F. Gender difference in age-related number of corticotropin-releasing hormone-expressing neurons in the human hypothalamic paraventricular nucleus and the role of sex hormones. Neuroendocrinology 2007, 85:27-36.
9. Bao A.M., Ji Y.F., Van Someren E.J., Hofman M.A., Liu R.Y., Zhou J.N. Diurnal rhythms of free estradiol and cortisol during the normal menstrual cycle in women with major depression. Horm. Behav. 2004, 45:93-102.
10. Bao A.M., Hestiantoro A., Van Someren E.J., Swaab D.F., Zhou J.N. Colocalization of corticotropin-releasing hormone and oestrogen receptor-alpha in the paraventricular nucleus of the hypothalamus in mood disorders. Brain 2005, 128:1301-1313.
11. Bao A.M., Fischer D.F., Wu Y.H., Hol E.M., Balesar R., Unmehopa U.A., Zhou J.N., Swaab D.F. A direct androgenic involvement in the expression of human corticotropin-releasing hormone. Mol. Psychiatry 2006, 11:567-576.
12. Bao A.M., Meynen G., Swaab D.F. The stress system in depression and neurodegeneration: focus on the human hypothalamus. Brain Res. Rev. 2008, 57:531-553.
13. Bartanusz V., Muller D., Gaillard R.C., Streit P., Vutskits L., Kiss J.Z. Local gamma-aminobutyric acid and glutamate circuit control of hypophyseotrophic corticotropin-releasing factor neuron activity in the paraventricular nucleus of the hypothalamus. Eur. J. Neurosci. 2004, 19:777-782.
14. Berglund H., Lindstrom P., Dhejne-Helmy C., Savic I. Male-to-female transsexuals show sex-atypical hypothalamus activation when smelling odorous steroids. Cereb. Cortex 2008, 18:1900-1908.
15. Björkqvist K., Lagerspetz K., Kaukiainen A. Do girls manipulate and boys fight? Developmental trends in regard to direct and indirect aggression. Aggressive Behav. 1992, 18:117-127.
16. Björkqvist K., Österman K., Lagerspetz K.M.J. Sex differences in covert aggression among adults. Aggressive Behav. 1994, 20:27-33.
17. Blanchard R. Fraternal birth order and the maternal immune hypothesis of male homosexuality. Horm. Behav. 2001, 40:105-114.
18. Bocklandt S., Vilain E. Sex differences in brain and behavior: hormones versus genes. Adv. Genet. 2007, 59:245-266.
19. Bocklandt S., Horvath S., Vilain E., Hamer D.H. Extreme skewing of X chromosome inactivation in mothers of homosexual men. Hum. Genet. 2006, 118:691-694.
20. Bogaert A.F. Biological versus nonbiological older brothers and men's sexual orientation. Proc. Natl. Acad. Sci. USA 2006, 103:10771-10774.
21. Bouix S., Pruessner J.C., Louis Collins D., Siddiqi K. Hippocampal shape analysis using medial surfaces. Neuroimage 2005, 25:1077-1089.
22. Byne W., Lasco M.S., Kemether E., Shinwari A., Edgar M.A., Morgello S., Jones L.B., Tobet S. The interstitial nuclei of the human anterior hypothalamus: an investigation of sexual variation in volume and cell size, number and density. Brain Res. 2000, 856:254-258.
23. Byne W., Tobet S., Mattiace L.A., Lasco M.S., Kemether E., Edgar M.A., Morgello S., Buchsbaum M.S., Jones L.B. The interstitial nuclei of the human anterior hypothalamus: an investigation of variation with sex, sexual orientation, and HIV status. Horm. Behav. 2001, 40:86-92.
24. Campbell A. Staying alive: evolution, culture, and women's intrasexual aggression. Behav. Brain Sci. 1999, 22:203-214. (discussion 214-252).
25. Caseras X., Mataix-Cols D., An S.K., Lawrence N.S., Speckens A., Giampietro V., Brammer M.J., Phillips M.L. Sex differences in neural responses to disgusting visual stimuli: implications for disgust-related psychiatric disorders. Biol. Psychiatry 2007, 62:464-471.
26. Chen L.H., Baker S.P., Braver E.R., Li G. Carrying passengers as a risk factor for crashes fatal to 16- and 17-year-old drivers. JAMA 2000, 283:1578-1582.
27. Chung W.C., De Vries G.J., Swaab D.F. Sexual differentiation of the bed nucleus of the stria terminalis in humans may extend into adulthood. J. Neurosci. 2002, 22:1027-1033.
28. Cohen-Kettenis P.T., Gooren L.J. Transsexualism: a review of etiology, diagnosis and treatment. J. Psychosom. Res. 1999, 46:315-333.
29. Colapinto J. As Nature Made Him: The Boy Who Was Raised as a Girl 2000, HarperCollins.
30. Connelan J., Baron-Cohen S., Wheelwright S., Batki A., Ahluwalia J. Sex differences in human neonatal social perception. Infant Behav. Develop. 2000, 23:113-118.
31. Coolidge F.L., Thede L.L., Young S.E. The heritability of gender identity disorder in a child and adolescent twin sample. Behav. Genet. 2002, 32:251-257.
32. Crews D. Epigenetics and its implications for behavioral neuroendocrinology. Front Neuroendocrinol. 2008, 29:344-357.
33. de Zegher F., Devlieger H., Veldhuis J.D. Pulsatile and sexually dimorphic secretion of luteinizing hormone in the human infant on the day of birth. Pediatr. Res. 1992, 32:605-607.
34. Dessens A.B., Cohen-Kettenis P.T., Mellenbergh G.J., vd Poll N., Koppe J.G., Boer K. Prenatal exposure to anticonvulsants and psychosexual development. Arch. Sex Behav. 1999, 28:31-44.
35. Dewing P., Shi T., Horvath S., Vilain E. Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Brain Res. Mol. Brain Res. 2003, 118:82-90.
36. Diamond M., Sigmundson H.K. Sex reassignment at birth. Long-term review and clinical implications. Arch. Pediatr. Adolesc. Med. 1997, 151:298-304.
37. Ehrhardt A.A., Meyer-Bahlburg H.F., Rosen L.R., Feldman J.F., Veridiano N.P., Zimmerman I., McEwen B.S. Sexual orientation after prenatal exposure to exogenous estrogen. Arch. Sex Behav. 1985, 14:57-77.
38. Ellis L., Cole-Harding S. The effects of prenatal stress, and of prenatal alcohol and nicotine exposure, on human sexual orientation. Physiol. Behav. 2001, 74:213-226.
39. Ellis L., Hellberg J. Fetal exposure to prescription drugs and adult sexual orientation. Pers. Indiv. Differ. 2005, 38:225-236.
40. Farrag A.K., Khedr E.M., Abdel-Aleem H., Rageh T.A. Effect of surgical menopause on cognitive functions. Dement. Geriatr. Cogn. Disord. 2002, 13:193-198.
41. Finegan J.A., Bartleman B., Wong P.Y. A window for the study of prenatal sex hormone influences on postnatal development. J. Genet. Psychol. 1989, 150:101-112.
42. Flisher A.J., Ziervogel C.F., Chalton D.O., Leger P.H., Robertson B.A. Risk-taking behaviour of Cape Peninsula high-school students. Part VI. Road-related behaviour. S. Afr. Med. J. 1993, 83:486-490.
43. Garcia-Falgueras A., Swaab D.F. A sex difference in the hypothalamic uncinate nucleus: relationship to gender identity. Brain 2008, 131:3132-3146.
44. Geerlings M.I., Strozyk D., Masaki K., Remaley A.T., Petrovitch H., Ross G.W., White L.R., Launer L.J. Endogenous sex hormones, cognitive decline, and future dementia in old men. Ann. Neurol. 2006, 60:346-355.
45. Gillies G.E., Linton E.A., Lowry P.J. Corticotropin releasing activity of the new CRF is potentiated several times by vasopressin. Nature 1982, 299:355-357.
46. Giordano R., Bo M., Pellegrino M., Vezzari M., Baldi M., Picu A., Balbo M., Bonelli L., Migliaretti G., Ghigo E., Arvat E. Hypothalamus-pituitary-adrenal hyperactivity in human aging is partially refractory to stimulation by mineralocorticoid receptor blockade. J. Clin. Endocrinol. Metab. 2005, 90:5656-5662.
47. Gispen-de Wied C.C., Westenberg H.G., Koppeschaar H.P., Thijssen J.H., van Ree J.M. Stimulation of the pituitary-adrenal axis with a low dose [Arg8]-vasopressin in depressed patients and healthy subjects. Eur. Neuropsychopharmacol. 1992, 2:411-419.
48. Goldstein J.M., Seidman L.J., Horton N.J., Makris N., Kennedy D.N., Caviness V.S., Faraone S.V., Tsuang M.T. Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cereb. Cortex 2001, 11:490-497.
49. Goldstein J.M., Seidman L.J., O'Brien L.M., Horton N.J., Kennedy D.N., Makris N., Caviness V.S., Faraone S.V., Tsuang M.T. Impact of normal sexual dimorphisms on sex differences in structural brain abnormalities in schizophrenia assessed by magnetic resonance imaging. Arch. Gen. Psychiatry 2002, 59:154-164.
50. Goldstein J.M., Jerram M., Abbs B., Whitfield-Gabrieli S., Makris N. Sex differences in stress response circuitry activation dependent on female hormonal cycle. J. Neurosci. 2010, 30:431-438.
51. Gomez-Gil E., Esteva I., Carrasco R., Almaraz M.C., Pasaro E., Salamero M., Guillamon A. Birth order and ratio of brothers to sisters in Spanish transsexuals. Arch. Sex Behav. 2010.
52. Goncharova N.D., Lapin B.A. Effects of aging on hypothalamic-pituitary-adrenal system function in non-human primates. Mech. Ageing Dev. 2002, 123:1191-1201.
53. Good C.D., Johnsrude I., Ashburner J., Henson R.N., Friston K.J., Frackowiak R.S. Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains. Neuroimage 2001, 14:685-700.
54. Goodwin R.D., Gotlib I.H. Gender differences in depression: the role of personality factors. Psychiatry Res. 2004, 126:135-142.
55. Gore A.C. Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Front Neuroendocrinol. 2008, 29:358-374.
56. Green R. Sexual identity of 37 children raised by homosexual or transsexual parents. Am. J. Psychiatry 1978, 135:692-697.
57. Hamer D.H., Hu S., Magnuson V.L., Hu N., Pattatucci A.M. A linkage between DNA markers on the X chromosome and male sexual orientation. Science 1993, 261:321-327.
58. Hassett J.M., Siebert E.R., Wallen K. Sex differences in rhesus monkey toy preferences parallel those of children. Horm. Behav. 2008, 54:359-364.
59. Hebert L.E., Scherr P.A., McCann J.J., Beckett L.A., Evans D.A. Is the risk of developing Alzheimer's disease greater for women than for men?. Am. J. Epidemiol. 2001, 153:132-136.
60. Heuser I. Depression, endocrinologically a syndrome of premature aging?. Maturitas 2002, 41(Suppl. 1):S19-S23.
61. M. Hines, G.M. Alexander, Monkeys, girls, boys and toys: a confirmation Letter regarding " Sex differences in toy preferences: striking parallels between monkeys and humans" , Horm. Behav. 54 (2008) 478-479; author reply 480-481.
62. Hines M., Golombok S., Rust J., Johnston K.J., Golding J. Testosterone during pregnancy and gender role behavior of preschool children: a longitudinal, population study. Child Dev. 2002, 73:1678-1687.
63. Hofman M.A., Swaab D.F. The sexually dimorphic nucleus of the preoptic area in the human brain: a comparative morphometric study. J. Anat. 1989, 164:55-72.
64. Howland J., Hingson R., Mangione T.W., Bell N., Bak S. Why are most drowning victims men? Sex differences in aquatic skills and behaviors. Am. J. Public Health 1996, 86:93-96.
65. Iijima M., Arisaka O., Minamoto F., Arai Y. Sex differences in children's free drawings: a study on girls with congenital adrenal hyperplasia. Horm. Behav. 2001, 40:99-104.
66. Inestrosa N.C., Marzolo M.P., Bonnefont A.B. Cellular and molecular basis of estrogen's neuroprotection. Potential relevance for Alzheimer's disease. Mol. Neurobiol. 1998, 17:73-86.
67. Ishunina T.A., Swaab D.F. Vasopressin and oxytocin neurons of the human supraoptic and paraventricular nucleus: size changes in relation to age and sex. J. Clin. Endocrinol. Metab. 1999, 84:4637-4644.
68. Kajantie E., Phillips D.I. The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 2006, 31:151-178.
69. Kinnunen L.H., Moltz H., Metz J., Cooper M. Differential brain activation in exclusively homosexual and heterosexual men produced by the selective serotonin reuptake inhibitor, fluoxetine. Brain Res. 2004, 1024:251-254.
70. Koutcherov Y., Paxinos G., Mai J.K. Organization of the human medial preoptic nucleus. J. Comp. Neurol. 2007, 503:392-406.
71. Kovacs K.J., Miklos I.H., Bali B. GABAergic mechanisms constraining the activity of the hypothalamo-pituitary-adrenocortical axis. Ann. NY Acad. Sci. 2004, 1018:466-476.
72. 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. 2000, 85:2034-2041.
73. Kudielka B.M., Hellhammer J., Hellhammer D.H., Wolf O.T., Pirke K.M., Varadi E., Pilz J., Kirschbaum C. Sex differences in endocrine and psychological responses to psychosocial stress in healthy elderly subjects and the impact of a 2-week dehydroepiandrosterone treatment. J. Clin. Endocrinol. Metab. 1998, 83:1756-1761.
74. Letenneur L., Launer L.J., Andersen K., Dewey M.E., Ott A., Copeland J.R., Dartigues J.F., Kragh-Sorensen P., Baldereschi M., Brayne C., Lobo A., Martinez-Lage J.M., Stijnen T., Hofman A. Education and the risk for Alzheimer's disease: sex makes a difference. EURODEM pooled analyses. EURODEM Incidence Research Group. Am. J. Epidemiol. 2000, 151:1064-1071.
75. LeVay S. A difference in hypothalamic structure between heterosexual and homosexual men. Science 1991, 253:1034-1070.
76. LeVay S., Hamer D.H. Evidence for a biological influence in male homosexuality. Sci. Am. 1994, 270:44-49.
77. Lubin F.D., Roth T.L., Sweatt J.D. Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J. Neurosci. 2008, 28:10576-10586.
78. Lund T.D., Munson D.J., Haldy M.E., Handa R.J. Androgen inhibits, while oestrogen enhances, restraint-induced activation of neuropeptide neurones in the paraventricular nucleus of the hypothalamus. J. Neuroendocrinol. 2004, 16:272-278.
79. Manly J.J., Merchant C.A., Jacobs D.M., Small S.A., Bell K., Ferin M., Mayeux R. Endogenous estrogen levels and Alzheimer's disease among postmenopausal women. Neurology 2000, 54:833-837.
80. Mathews G.A., Fane B.A., Conway G.S., Brook C.G., Hines M. Personality and congenital adrenal hyperplasia: possible effects of prenatal androgen exposure. Horm. Behav. 2009, 55:285-291.
81. Mayer A., Lahr G., Swaab D.F., Pilgrim C., Reisert I. The Y-chromosomal genes SRY and ZFY are transcribed in adult human brain. Neurogenetics 1998, 1:281-288.
82. Mazur A., Booth A. Testosterone and dominance in men. Behav. Brain Sci. 1998, 21:353-363. (discussion 363-397).
83. McCarthy M.M., Auger A.P., Bale T.L., De Vries G.J., Dunn G.A., Forger N.G., Murray E.K., Nugent B.M., Schwarz J.M., Wilson M.E. The epigenetics of sex differences in the brain. J. Neurosci. 2009, 29:12815-12823.
84. McGowan P.O., Sasaki A., D'Alessio A.C., Dymov S., Labonte B., Szyf M., Turecki G., Meaney M.J. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 2009, 12:342-348.
85. Meyer-Bahlburg H.F. Gender identity outcome in female-raised 46, XY persons with penile agenesis, cloacal exstrophy of the bladder, or penile ablation. Arch. Sex Behav. 2005, 34:423-438.
86. Meyer-Bahlburg H.F.L., Ehrhardt A.A., Rosen L.R., Gruen R.S., Veridiano N.P., Vann F.H., Neuwalder H.F. Prenatal estrogens and the development of homosexual orientation. Dev. Psychol. 1995, 31:12-21.
87. Meyer-Bahlburg H.F., Gruen R.S., New M.I., Bell J.J., Morishima A., Shimshi M., Bueno Y., Vargas I., Baker S.W. Gender change from female to male in classical congenital adrenal hyperplasia. Horm. Behav. 1996, 30:319-332.
88. Miller D.B., O'Callaghan J.P. Aging, stress and the hippocampus. Ageing Res. Rev. 2005, 4:123-140.
89. Moffat S.D., Zonderman A.B., Metter E.J., Blackman M.R., Harman S.M., Resnick S.M. Longitudinal assessment of serum free testosterone concentration predicts memory performance and cognitive status in elderly men. J. Clin. Endocrinol. Metab. 2002, 87:5001-5007.
90. Money J. Ablatio penis: normal male infant sex-reassigned as a girl. Arch. Sex Behav. 1975, 4:65-71.
91. Money J., Erhardt A.A. Man and Woman. Boy and Girl: The Differentiation and Dimorphism of Gender Identity from Conception to Maturity 1972, Johns Hopkins University Press, Baltimore.
92. Mustanski B.S., Dupree M.G., Nievergelt C.M., Bocklandt S., Schork N.J., Hamer D.H. A genomewide scan of male sexual orientation. Hum. Genet. 2005, 116:272-278.
93. T.C. Ngun, N. Ghahramani, F.J. Sanchez, S. Bocklandt, E. Vilain, The genetics of sex differences in brain and behavior, Front Neuroendocrinol. (2010), in press, doi:10.1016/j.yfrne.2010.10.001.
94. Nordenstrom A., Servin A., Bohlin G., Larsson A., Wedell A. 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. 2002, 87:5119-5124.
95. Paus T., Otaky N., Caramanos Z., MacDonald D., Zijdenbos A., D'Avirro D., Gutmans D., Holmes C., Tomaiuolo F., Evans A.C. In vivo morphometry of the intrasulcal gray matter in the human cingulate, paracingulate, and superior-rostral sulci: hemispheric asymmetries, gender differences and probability maps. J. Comp. Neurol. 1996, 376:664-673.
96. Piccinelli M., Wilkinson G. Gender differences in depression: the role of personality factors. Br. J. Psychiatry 2000, 177:486-492.
97. Pope H.G., Kouri E.M., Hudson J.I. Effects of supraphysiologic doses of testosterone on mood and aggression in normal men: a randomized controlled trial. Arch. Gen. Psychiatry 2000, 57:133-140. (discussion 155-156).
98. Pruessner J.C., Collins D.L., Pruessner M., Evans A.C. Age and gender predict volume decline in the anterior and posterior hippocampus in early adulthood. J. Neurosci. 2001, 21:194-200.
99. Pujol J., Lopez A., Deus J., Cardoner N., Vallejo J., Capdevila A., Paus T. Anatomical variability of the anterior cingulate gyrus and basic dimensions of human personality. Neuroimage 2002, 15:847-855.
100. Reiner W.G., Gearhart J.P. Discordant sexual identity in some genetic males with cloacal exstrophy assigned to female sex at birth. N. Engl. J. Med. 2004, 350:333-341.
101. Reul J.M., de Kloet E.R. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 1985, 117:2505-2511.
102. Rivier C., Vale W. Interaction of corticotropin-releasing factor and arginine vasopressin on adrenocorticotropin secretion in vivo. Endocrinology 1983, 113:939-942.
103. Roca C.A., Schmidt P.J., Deuster P.A., Danaceau M.A., Altemus M., Putnam K., Chrousos G.P., Nieman L.K., Rubinow D.R. Sex-related differences in stimulated hypothalamic-pituitary-adrenal axis during induced gonadal suppression. J. Clin. Endocrinol. Metab. 2005, 90:4224-4231.
104. Rubin R.T., Rhodes M.E., O'Toole S., Czambel R.K. Sexual diergism of hypothalamo-pituitary-adrenal cortical responses to low-dose physostigmine in elderly vs. young women and men. Neuropsychopharmacology 2002, 26:672-681.
105. Salehi A., Ocampo M., Verhaagen J., Swaab D.F. P75 neurotrophin receptor in the nucleus basalis of meynert in relation to age, sex, and Alzheimer's disease. Exp. Neurol. 2000, 161:245-258.
106. Savic I., Lindstrom P. PET and MRI show differences in cerebral asymmetry and functional connectivity between homo- and heterosexual subjects. Proc. Natl. Acad. Sci. USA 2008, 105:9403-9408.
107. Schonknecht P., Pantel J., Klinga K., Jensen M., Hartmann T., Salbach B., Schroder J. Reduced cerebrospinal fluid estradiol levels are associated with increased beta-amyloid levels in female patients with Alzheimer's disease. Neurosci. Lett. 2001, 307:122-124.
108. Seeman M.V. Psychopathology in women and men: focus on female hormones. Am. J. Psychiatry 1997, 154:1641-1647.
109. Seidman S.N. Testosterone deficiency and depression in aging men: pathogenic and therapeutic implications. J. Gend. Specif. Med. 2001, 4:44-48.
110. Seidman S.N., Araujo A.B., Roose S.P., Devanand D.P., Xie S., Cooper T.B., McKinlay J.B. Low testosterone levels in elderly men with dysthymic disorder. Am. J. Psychiatry 2002, 159:456-459.
111. Selye H. The Stress of Life 1956, McGraw-Hill, New York.
112. Senanarong V., Vannasaeng S., Poungvarin N., Ploybutr S., Udompunthurak S., Jamjumras P., Fairbanks L., Cummings J.L. Endogenous estradiol in elderly individuals: cognitive and noncognitive associations. Arch. Neurol. 2002, 59:385-389.
113. Shamim W., Yousufuddin M., Bakhai A., Coats A.J., Honour J.W. Gender differences in the urinary excretion rates of cortisol and androgen metabolites. Ann. Clin. Biochem. 2000, 37(Pt 6):770-774.
114. Spratt D. Sex differences in the brain. J. Neuroendocrinol. 2000, 12:597-598.
115. Strube M.J., Turner C.W., Cerro D., Stevens J., Hinchey F. Interpersonal aggression and the type A coronary-prone behavior pattern: a theoretical distinction and practical implications. J. Pers. Soc. Psychol. 1984, 47:839-847.
116. Swaab D.F. The human hypothalamus. Basic and clinical aspects. Part I: nuclei of the hypothalamus. Handbook of Clinical Neurology 2003, Elsevier, Amsterdam. M.J. Aminoff, F. Boller, D.F. Swaab (Eds.).
117. Swaab D.F. The human hypothalamus. Basic and clinical aspects. Part II: neuropathology of the hypothalamus and adjacent brain structures. Handbook of Clinical Neurology 2004, Elsevier, Amsterdam. M.J. Aminoff, F. Boller, D.F. Swaab (Eds.).
118. Swaab D.F. Sexual orientation and its basis in brain structure and function. Proc. Natl. Acad. Sci. USA 2008, 105:10273-10274.
119. Swaab D.F., Fliers E. A sexually dimorphic nucleus in the human brain. Science 1985, 228:1112-1115.
120. Swaab D.F., Garcia-Falgueras A. Sexual differentiation of the human brain in relation to gender identity and sexual orientation. Funct. Neurol. 2009, 24:17-28.
121. Swaab D.F., Hofman M.A. Sexual differentiation of the human brain. A historical perspective. Prog. Brain. Res. 1984, 61:361-374.
122. Swaab D.F., Hofman M.A. Sexual differentiation of the human hypothalamus: ontogeny of the sexually dimorphic nucleus of the preoptic area. Brain Res. Dev. Brain Res. 1988, 44:314-318.
123. Swaab D.F., Hofman M.A. An enlarged suprachiasmatic nucleus in homosexual men. Brain. Res. 1990, 537:141-148.
124. Swaab D.F., Fliers E., Partiman T.S. The suprachiasmatic nucleus of the human brain in relation to sex, age and senile dementia. Brain Res 1985, 342:37-44.
125. Swaab D.F., Gooren L.J., Hofman M.A. The human hypothalamus in relation to gender and sexual orientation. Prog. Brain Res. 1992, 93:205-217. (discussion 217-219).
126. Takano K., Utsunomiya H., Ono H., Ohfu M., Okazaki M. Normal development of the pituitary gland: assessment with three-dimensional MR volumetry. AJNR Am. J. Neuroradiol. 1999, 20:312-315.
127. Taylor S.E., Klein L.C., Lewis B.P., Gruenewald T.L., Gurung R.A., Updegraff J.A. Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol. Rev. 2000, 107:411-429.
128. Ter Horst G.J., Wichmann R., Gerrits M., Westenbroek C., Lin Y. Sex differences in stress responses: focus on ovarian hormones. Physiol. Behav. 2009, 97:239-249.
129. Titus-Ernstoff L., Perez K., Hatch E.E., Troisi R., Palmer J.R., Hartge P., Hyer M., Kaufman R., Adam E., Strohsnitter W., Noller K., Pickett K.E., Hoover R. Psychosexual characteristics of men and women exposed prenatally to diethylstilbestrol. Epidemiology 2003, 14:155-160.
130. Traustadottir T., Bosch P.R., Matt K.S. Gender differences in cardiovascular and hypothalamic-pituitary-adrenal axis responses to psychological stress in healthy older adult men and women. Stress 2003, 6:133-140.
131. Tsai H.W., Grant P.A., Rissman E.F. Sex differences in histone modifications in the neonatal mouse brain. Epigenetics 2009, 4:47-53.
132. Uhart M., Chong R.Y., Oswald L., Lin P.I., Wand G.S. Gender differences in hypothalamic-pituitary-adrenal (HPA) axis reactivity. Psychoneuroendocrinology 2006, 31:642-652.
133. Vamvakopoulos N.C., Chrousos G.P. Evidence of direct estrogenic regulation of human corticotropin-releasing hormone gene expression. Potential implications for the sexual dimophism of the stress response and immune/inflammatory reaction. J. Clin. Invest. 1993, 92:1896-1902.
134. van de Beek C., van Goozen S.H., Buitelaar J.K., Cohen-Kettenis P.T. Prenatal sex hormones (maternal and amniotic fluid) and gender-related play behavior in 13-month-old Infants. Arch. Sex Behav. 2009, 38:6-15.
135. van Londen L., Goekoop J.G., van Kempen G.M., Frankhuijzen-Sierevogel A.C., Wiegant V.M., van der Velde E.A., De Wied D. Plasma levels of arginine vasopressin elevated in patients with major depression. Neuropsychopharmacology 1997, 17:284-292.
136. Vierhapper H., Nowotny P., Waldhausl W. Sex-specific differences in cortisol production rates in humans. Metabolism 1998, 47:974-976.
137. Wallen K., Hassett J.M. Sexual differentiation of behaviour in monkeys: role of prenatal hormones. J. Neuroendocrinol. 2009, 21:421-426.
138. Wallien M.S., Cohen-Kettenis P.T. Psychosexual outcome of gender-dysphoric children. J. Am. Acad. Child Adolesc. Psychiatry 2008, 47:1413-1423.
139. Wang S.S., Kamphuis W., Huitinga I., Zhou J.N., Swaab D.F. Gene expression analysis in the human hypothalamus in depression by laser microdissection and real-time PCR: the presence of multiple receptor imbalances. Mol. Psychiatry 2008, 13:786-799. 741.
140. Wilhelm K., Parker G., Hadzi-Pavlovic D. Fifteen years on: evolving ideas in researching sex differences in depression. Psychol. Med. 1997, 27:875-883.
141. Williams C.L., Pleil K.E. Toy story: why do monkey and human males prefer trucks? Comment on " Sex differences in rhesus monkey toy preferences parallel those of children" by Hassett, Siebert and Wallen. Horm. Behav. 2008, 54:355-358.
142. 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. 2000, 85:2664-2669.
143. Wolf O.T., Kirschbaum C. Endogenous estradiol and testosterone levels are associated with cognitive performance in older women and men. Horm. Behav. 2002, 41:259-266.
144. Wu M.V., Manoli D.S., Fraser E.J., Coats J.K., Tollkuhn J., Honda S., Harada N., Shah N.M. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 2009, 139:61-72.
145. Yaffe K., Lui L.Y., Grady D., Cauley J., Kramer J., Cummings S.R. Cognitive decline in women in relation to non-protein-bound oestradiol concentrations. Lancet 2000, 356:708-712.
146. 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 1995, 378:68-70.
147. Zubenko G.S., Stiffler J.S., Hughes H.B., Hurtt M.R., Kaplan B.B. Initial results of a genome survey for novel Alzheimer's disease risk genes: association with a locus on the X chromosome. Am. J. Med. Genet. 1998, 81:196-205.
148. Zucker K.J., Bradley S.J., Oliver G., Blake J., Fleming S., Hood J. Psychosexual development of women with congenital adrenal hyperplasia. Horm. Behav. 1996, 30:300-318.