Testosterone and its metabolites - modulators of brain functions

• Autorzy: Durdiakova J. , Ostatnikova D. , Celec P.
• Języki publikacji: EN

Abstrakty

EN

Testosterone is a steroid sex hormone with an important role in the physiology in both sexes. It is involved in the development of morphological and functional parameters of the body via multiple molecular mechanisms. Intensive research focused on testosterone reveals associations with cognitive abilities and behavior and its causative role in sex differences in cognition. Testosterone modulates brain structure and the differentiation of neurons during intrauterine development with profound effects on brain functions during postnatal life. In this review we summarize the effects of testosterone on brain physiology and cognition with respect to the underlying molecular mechanisms.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2011
• Tom: 71
• Numer: 4
• Opis fizyczny: p.434-454,fig.,ref.

Twórcy

autor

Durdiakova J.

• Institute of Molecular Biomedicine, Comenius University, Blatislava, Slovakia
• Institute of Physiology, Comenius University, Bratislava, Slovakia

autor

Ostatnikova D.

• Institute of Physiology, Comenius University, Bratislava, Slovakia

autor

Celec P.

• Institute of Molecular Biomedicine, Comenius University, Blatislava, Slovakia
• Institute of Pathophysiology, Comenius University, Bratislava, Slovakia
• Department of Molecular Biology, Comenius University, Bratislava, Slovakia

Bibliografia

• Ahmed EI, Zehr JL, Schulz KM, Lorenz BH, DonCarlos LL, Sisk CL (2008) Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions. Nat Neurosci 11: 995-997.
• Alekseyenko OV, Baum MJ, Cherry JA (2006) Sex and gonadal steroid modulation of pheromone receptor gene expression in the mouse vomeronasal organ. Neuroscience 140: 1349-1357.
• Anderson B, Harvey T (1996) Alterations in cortical thick­ness and neuronal density in the frontal cortex of Albert Einstein. Neurosci Lett 210: 161-164.
• Anderson US, Perea EF, Becker DV, Ackerman JM, Shapiro JR, Neuberg SL, Kenrick DT (2010) I have only eyes for you: Ovulation redirects attention (but not memory) to attractive men. J Exp Soc Psychol 46: 804-808.
• Askew EB, Gampe RTJ, Stanley TB, Faggart JL, Wilson EM (2007) Modulation of androgen receptor activation function 2 by testosterone and dihydrotestosterone. J Biol Chem 282: 25801-25816.
• 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: 144-8.
• 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: 11-19.
• Baron S, Manin M, Beaudoin C, Leotoing L, Communal Y, Veyssiere G, Morel L (2004) Androgen receptor mediates non-genomic activation of phosphatidylinositol 3-OH kinase in androgen-sensitive epithelial cells. J Biol Chem 279: 14579-14586.
• Belcher A, Martin J, Bowman N, Davis V, Agarwal V (2009) 2d:4d ratios in relation to breast cancer susceptibility among different ethnic groups. J Invest Med 57: 209­210.
• Ben-Hur H, Thole HH, Mashiah A, Insler V, Berman V, Shezen E, Elias D, Zuckerman A, Ornoy A (1997) Estrogen, progesterone and testosterone receptors in human fetal cartilaginous tissue: immunohistochemical studies. Calcif Tissue Int 60: 420-526.
• Bennet NC, Gardiner, R. A., Hooper, J. D., Johnson, D. W., Gobe, G. C (2010) Molecular cell biology of androgen receptor signaling. Int J Biochem Cell Biol biochemistry 42: 813-827.
• Benten WP, Lieberherr M, Stamm O, Wrehlke C, Guo Z, Wunderlich F (1999) Testosterone signaling through internalizable surface receptors in androgen receptor-free macrophages. Mol Biol Cell 10: 3113-3123.
• Bhasin S (2000) The dose-dependent effects of testosterone on sexual function and on muscle mass and function. Mayo Clin Proc 75 (Suppl): S70-75; discussion S75- 76.
• Bimonte-Nelson HA, Singleton RS, Nelson ME, Eckman CB, Barber J, Scott TY, Granholm AC (2003) Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Exp Neurol 181: 301-312.
• Bimonte HA, Nelson ME, Granholm AC (2003) Age-related deficits as working memory load increases: relationships with growth factors. Neurobiol Aging 24: 37-48.
• Blakemore SJ (2008) The social brain in adolescence. Nat Rev Neurosci 9: 267-277.
• Bloom MS, Houston AS, Mills JL, Molloy CA, Hediger ML (2010) Finger bone immaturity and 2D:4D ratio measure­ment error in the assessment of the hyperandrogenic hypothesis for the etiology of autism spectrum disorders. Physiol Behav 100: 221-224.
• Bramen JE, Hranilovich JA, Dahl RE, Forbes EE, Chen J, Toga AW, Dinov ID, Worthman CM, Sowell ER (2011. Puberty influences medial temporal lobe and cortical gray matter maturation differently in boys than girls matched for sexual maturity. Cereb Cortex 21: 636-646.
• Brosnan MJ (2006) Digit ratio and faculty membership: implications for the relationship between prenatal testos­terone and academia. Br J Psychol 97: 455-466.
• Brosnan MJ (2008) Digit ratio as an indicator of numeracy relative to literacy in 7-year-old British schoolchildren. Br J Psychol 99: 75-85.
• Brown-Sequard CE (1889) The effects produced on man by subcutaneous injections of liquid obtained from the tes­ticles of animals. Lancet 2: 105-107.
• Brown WM, Hines M, Fane BA, Breedlove SM (2002) Masculinized finger length patterns in human males and females with congenital adrenal hyperplasia. Horm Behav 42: 380-386.
• Bull R, Davidson WA, Nordman E (2010) Prenatal testoster­one, visual-spatial memory, and numerical skills in young children. Learn Individ Differ 20: 246-250.
• Carre JM (2009) No place like home: testosterone responses to victory depend on game location. Am J Hum Biol 21: 392-394.
• Carre JM, Putnam SK (2010) Watching a previous victory produces an increase in testosterone among elite hockey players. Psychoneuroendocrinology 35: 475-479.
• Carreau S, Lambard S, Delalande C, Denis-Galeraud I, Bilinska B, Bourguiba S (2003) Aromatase expression and role of estrogens in male gonad: a review. Reprod Biol Endocrinol 1: 35-41.
• Celec P, Ostatnikova D, Putz Z, Kudela M (2002) The cir- calunar cycle of salivary testosterone and the visual-spa­tial performance. Bratisl Lek Listy 103: 49-69.
• Chamberlain NL, Driver ED, Miesfeld RL (1994) The length and location of CAG trinucleotide repeats in androgen receptor N-terminal domain affect transactiva- tion function. Nucleic Acids Res 22: 3181-3186.
• Chmelar R, Buchanan G, Need EF, Tilley W, Greenberg NM (2007) Androgen receptor coregulators and their involve­ment in the development and progression of prostate cancer. Int J Cancer 120: 719-733.
• Choong CS, Kemppainen JA, Wilson EM (1998) Evolution of the primate androgen receptor: a structural basis for disease. J Mol Evol 47: 334-342.
• Choong CS, Wilson EM (1998) Trinucleotide repeats in the human androgen receptor: a molecular basis for disease. J Mol Endocrinol 21: 235-257.
• 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: 122­132.
• 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 Rev 29: 353-384.
• Collaer ML, Hines M (1995) Human behavioral sex differ­ences: a role for gonadal hormones during early develop­ment? Psychol Bull 118: 45-107.
• Cook IA, Morgan ML, Dunkin JJ, David S, Witte E, Lufkin R, Abrams M, Rosenberg S, Leuchter AF (2002) Estrogen replacement therapy is associated with less progression of subclinical structural brain disease in normal elderly women: a pilot study. Int J Geriatr Psychiatry 17: 610-618.
• Cooke BM, Tabibnia G, Breedlove SM (1999) A brain sex­ual dimorphism controlled by adult circulating andro­gens. Proc Natl Acad Sci U S A 96: 7538-7540.
• Cooke BM, Breedlove SM, Jordan CL (2003) Both estrogen receptors and androgen receptors contribute to testoster­one-induced changes in the morphology of the medial amygdala and sexual arousal in male rats. Horm Behav 43: 336-346.
• Cooke BM, Jordan CL, Breedlove SM (2007) Pubertal growth of the medial amygdala delayed by short photope­riods in the Siberian hamster, Phodopus sungorus. Horm Behav 52: 283-288.
• Cornil CA, Ball GF, Balthazart J, Charlier TD (2011. Organizing effects of sex steroids on brain aromatase activity in quail. PloS One 6: e19196.
• Cui Y, Shu XO, Cai Q, Jin F, Cheng JR, Cai H, Gao YT, Zheng W (2005) Association of breast cancer risk with a common functional polymorphism (Asp327Asn) in the sex hormone-binding globulin gene. Cancer Epidemiol Biomarkers Prev 14: 1096-1101.
• d'Anglemont de Tassigny X, Colledge WH (2010) The role of kisspeptin signaling in reproduction. Physiology 25: 207-217.
• Daniel JM, Winsauer PJ, Moerschbaecher JM (2003) Castration in rats impairs performance during acquisition of a working memory task and exacerbates deficits in working memory produced by scopolamine and mecam- ylamine. Psychopharmacology 170: 294-300.
• Daniel JM, Lee CD (2004) Estrogen replacement in ovariec- tomized rats affects strategy selection in the Morris water maze. Neurobiol Learn Mem 82: 142-149.
• Davidson JM, Chen JJ, Crapo L, Gray GD, Greenleaf WJ, Catania JA (1983) Hormonal changes and sexual function in aging men. J Clin Endocrinol Metab 57: 71-77.
• Davis EC, Popper P, Gorski RA (1996) The role of apoptosis in sexual differentiation of the rat sexually dimorphic nucleus of the preoptic area. Brain Res 734: 10-18.
• Devine A, Kelly J, Heneghan H, Dwyer R, Kerin M (2010) Digit ratio (2d:4d) as a predictor of breast cancer predis­position. Ir J Med Sci 179: 42-43.
• Ding D, Xu L, Menon M, Reddy GP, Barrack ER (2004) Effect of a short CAG (glutamine) repeat on human androgen receptor function. Prostate 58: 23-32.
• Driscoll I, Resnick SM (2007) Testosterone and cognition in normal aging and Alzheimer's disease: An update. Curr Alzheimer Res 4: 33-45.
• 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: 356-359.
• Escasa MJ, Casey JF, Gray PB (2010) Salivary testosterone levels in men at a U.S. sex club. Arch Sex Behav 40: 921-926.
• Estebanez-Perpina E, Moore JMR, Mar E, Delgado- Rodrigues E, Nguyen P, Baxter JD, Buehrer BM, Webb P (2005) The molecular mechanism of coactivator utiliza­tion in ligand-dependent transactivation by the androgen receptor. J Biol Chem 280: 8060-8068.
• Finegan JA, Bartleman B, Wong PY (1989) A window for the study of prenatal sex hormone influences on postnatal development. J Genet Psychol 150: 101-112.
• Fink G, Sumner BEH, McQueen JK, Wilson H, Rosie R (1988) Sex steroid control of mood, mental state and memory. Clin Exp Pharmacol Physiol 25: 764-775.
• Fitch RH, Denenberg VH (1998) A role for ovarian hor­mones in sexual differentiation of the brain. Behav Brain Sci 21: 311-352.
• Foradori CD, Weiser MJ, Handa RJ (2008) Non-genomic actions of androgens. Front Neuroendocrinol 29: 169-181.
• Forstmeier W, Mueller JC, Kempenaers B (2010) A poly­morphism in the oestrogen receptor gene explains covari- ance between digit ratio and mating behaviour. Proc Biol Sci 277: 3353-3361.
• Garcia-Falgueras A, Swaab DF (2008) A sex difference in the hypothalamic uncinate nucleus: relationship to gender identity. Brain 131: 3132-3146.
• Geschwind N, Galaburda AM (1985) Cerebral lateralization. Biological mechanisms, associations, and pathology: III. A hypothesis and a program for research. Arch Neurol 42: 634-654.
• Goel N, Bale TL (2008) Organizational and activational effects of testosterone on masculinization of female physiological and behavioral stress responses. Endocrinology 149: 6399-6405.
• Gogtay N, Thompson PM (2010) Mapping gray matter development: implications for typical development and vulnerability to psychopathology. Brain Cogn 72: 6-15.
• Goldey KL, van Anders SM (2010) Sexy thoughts: effects of sexual cognitions on testosterone, cortisol, and arousal in women. Horm Behav 59: 754-764.
• Goldstein JM, Jerram M, Abbs B, Whitfield-Gabrieli S, Makris N (2010) Sex differences in stress response cir­cuitry activation dependent on female hormonal cycle. J Neurosci 30: 431-438.
• Gomez-Gil E, Canizares S, Torres A, de la Torre F, Halperin I, Salamero M (2009) Androgen treatment effects on memory in female-to-male transsexuals. Psychoneuroendocrinology 34: 110-117.
• Gomez DM, Newman SW (1992) Differential projections of the anterior and posterior regions of the medial amygdaloid nucleus in the Syrian hamster. J Comp Neurol 317: 195­218.
• Gorski RA, Gordon JH, Shryne JE, Southam AM (1978) Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res 148: 333-346.
• Gouchie C, Kimura D (1991) The relationship between tes­tosterone levels and cognitive-ability patterns. Psychoneuroendocrinology 16: 323-334.
• Greenland KJ, Zajac JD (2004) Kennedy's disease: patho­genesis and clinical approaches. Intern Med J 34: 279­286.
• Greenland KJ, Beilin J, Castro J, Varghese PN, Zajac JD (2004) Polymorphic CAG repeat length in the androgen receptor gene and association with neurodegeneration in a heterozygous female carrier of Kennedy's disease. J Neurol 251: 35-41.
• Griksiene R, Ruksenas O (2011) Effects of hormonal contra­ceptives on mental rotation and verbal fluency. Psychoneuroendocrinology 36: 1239-1248.
• Haggarty P, Hoad G, Harris SE, Starr JM, Fox HC, Deary IJ, Whalley LJ (2010) Human intelligence and polymor­phisms in the DNA methyltransferase genes involved in epigenetic marking. PloS One 5: e11329.
• Hau M, Wikelski M, Soma KK, Wingfield JC (2000) Testosterone and year-round territorial aggression in a tropical bird. Gen Comp Endocrinol 117: 20-33.
• Hausmann M, Slabbekoorn D, Van Goozen SH, Cohen- Kettenis PT, Gunturkun O (2000) Sex hormones affect spatial abilities during the menstrual cycle. Behav Neurosci 114: 1245-1250.
• Heil M, Kavsek M, Rolke B, Beste C, Jansen P (2011) Mental rotation in female fraternal twins: Evidence for intra-uterine hormone transfer? Biol Psychol 86: 90-93.
• Hines M, Golombok S, Rust J, Johnston KJ, Golding J (2002) Testosterone during pregnancy and gender role behavior of preschool children: a longitudinal, population study. Child Dev 73: 1678-1687.
• Hines M (2010) Sex-related variation in human behavior and the brain. Trends Cogn Sci 14: 448-456.
• Hiort O (2002) Androgens and puberty. Best Pract Res Clin Endocrinol Metab 16: 31-41.
• Hodosy J, Pales J, Ostatnikova D, Celec P (2010) The effects of exogenous testosterone on spatial memory in rats. Cent Eur J Biol 5: 466-471.
• Hogervorst E, Combrinck M, Smith AD (2003) Testosterone and gonadotropin levels in men with dementia. Neuro Endocrinol Lett 24: 203-208.
• Holesova Z, Ostatnikova D, Minarik G, Ficek A, Putz Z, Celec P (2006) Has the bain a gender? Homeostasis 44: 1-2.
• Huang X, Harlan RE (1993) Absence of androgen receptors in LHRH immunoreactive neurons. Brain Res 624: 309­311.
• Hugdahl K, Thomsen T, Ersland L (2006) Sex differences in visuo-spatial processing: An fMRI study of mental rota­tion. Neuropsychologia 44: 1575-1583.
• Hurd PL, Vaillancourt KL, Dinsdale NL (2010) Aggression, digit ratio and variation in androgen receptor and monoam- ine oxidase A genes in men. Behav Genet 41: 443-456.
• Ibanez MA, Gu G, Simerly RB (2001) Target-dependent sexual differentiation of a limbic-hypothalamic neural pathway. J Neurosci 21: 4652-5659.
• Janowsky JS, Oviatt SK, Orwoll ES (1994) Testosterone influences spatial cognition in older men. Behav Neurosci 108: 325-332.
• Kasperk CH, Wergedal JE, Farley JR, Linkhart TA, Turner RT, Baylink DJ (1989) Androgens directly stimulate pro­liferation of bone-cells in vitro. Endocrinology 124: 1576-1578.
• Kempel P, Gohlke B, Klempau J, Zinsberger P, Reuter M, Hennig J (2005) Second-to-fourth digit length, testoster­one and spatial ability. Intelligence 33: 215-230.
• Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE (2005) Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62: 493-602.
• Khosla S, Riggs BL, Atkinson EJ, Oberg AL, Mavilia C, Del Monte F, Melton LJ, 3rd, Brandi ML (2004) Relationship of estrogen receptor genotypes to bone mineral density and to rates of bone loss in men. J Clin Endocrinol Metab 89: 1808-1816.
• Kittles RA, Young D, Weinrich S, Hudson J, Argyropoulos G, Ukoli F, Adams-Campbell L, Dunston GM (2001) Extent of linkage disequilibrium between the androgen receptor gene CAG and GGC repeats in human popula­tions: implications for prostate cancer risk. Hum Genet 109: 253-261.
• Konkle AT, McCarthy MM (2011) Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain. Endocrinology 152: 223-235.
• Kooy RF, Reyniers E, Storm K, Vits L, van Velzen D, de Ruiter PE, Brinkmann AO, de Paepe A, Willems PJ (1999) CAG repeat contraction in the androgen receptor gene in three brothers with mental retardation. Am J Med Genet 85: 209-213.
• Korenbrot CC, Paup DC, Gorski RA (1975) Effects of tes­tosterone propionate or dihydrotestosterone propionate on plasma FSH and LH levels in neonatal rats and on sexual differentiation of the brain. Endocrinology 97: 709-717.
• Krajmer P, Spajdel M, Kubranska A, Ostatnikova D (2011) 2D:4D finger ratio in Slovak Autism Spectrum Disorder population. Bratisl Lek Listy 112: 377-379.
• Kristensen VN, Harada N, Yoshimura N, Haraldsen E, Lonning PE, Erikstein B, Karesen R, Kristensen T, B0rresen-Dale AL (2000) Genetic variants of CYP19 (aromatase) and breast cancer risk. Oncogene 19: 1329­1333.
• Lawson JS, Inglis J (1983) A laterality index of cognitive impairment after hemispheric damage: a measure derived from a principal-components analysis of the Wechsler Adult Intelligence Scale. J Consult Clin Psychol 51: 832-840.
• Li J, Al-Azzawi F (2009) Mechanism of androgen receptor action. Maturitas 63: 142-148.
• Lippa RA (2006) Finger lengths, 2D:4D ratios, and their relation to gender-related personality traits and the big five. Biol Psychol 71: 116-121.
• Lobotsky J, Wyss HI, Segre EJ, Lloyd CW (1964) Plasma testosterone in the normal woman. J Clin Endocrinol Metab 24: 1261-1265.
• Lustig RH (1996) In vitro models for the effects of sex hor­mones on neurons. Ann N Y Acad Sci 784: 370-380.
• Maccoby EE, Doering CH, Jacklin CN, Kraemer H (1979) Concentrations of sex hormones in umbilical-cord blood: their relation to sex and birth order of infants. Child Dev 50: 632-642.
• MacLusky NJ, Hajszan T, Prange-Kiel J, Leranth C (2006) Androgen modulation of hippocampal synaptic plasticity. Neuroscience 138: 957-965.
• Maheu FS, Merke DP, Schroth EA, Keil MF, Hardin J, Poeth K, Pine DS, Ernst M (2008) Steroid abnormalities and the developing brain: Declarative memory for emotionally arousing and neutral material in children with congenital adrenal hyperplasia. Psychoneuroendocrinology 33: 238­245.
• Makridakis NM, Ross RK, Pike MC, Crocitto LE, Kolonel LN, Pearce CL, Henderson BE, Reichardt JK (1999) Association of mis-sense substitution in SRD5A2 gene with prostate cancer in African- American and Hispanic men in Los Angeles, USA. Lancet 354: 975-978.
• Malas MA, Dogan S, Evcil EH, Desdicioglu K (2006) Fetal development of the hand, digits and digit ratio (2D:4D). Early Hum Dev 82: 469-475.
• Manning JT, Scutt D, Wilson J, Lewis-Jones DI (1998) The ratio of 2nd to 4th digit length: a predictor of sperm num­bers and concentrations of testosterone, luteinizing hor­mone and oestrogen. Hum Reprod 13: 3000-3004.
• Manning JT, Barley L, Walton J, Lewis-Jones DI, Trivers RL, Singh D, Thornhill R, Rohde P, Bereczkei T, Henzi P et al (2000) The 2nd:4th digit ratio, sexual dimorphism, popula­tion differences, and reproductive success. evidence for sexually antagonistic genes? Evol Hum Behav 21: 163— 183.
• Manning JT, Taylor RP (2001) Second to fourth digit ratio and male ability in sport: implications for sexual selection in humans. Evol Hum Behav 22: 61-69.
• Manning JT (2007) The androgen receptor gene: a major modifier of speed of neuronal transmission and intelli­gence? Med Hypotheses 68: 802-804.
• Manning JT, Fink B (2008) Digit ratio (2D:4D), dominance, reproductive success, asymmetry, and sociosexuality in the BBC Internet Study. Am J Hum Biol 20: 451-461.
• Manson JE (2008) Prenatal exposure to sex steroid hor­mones and behavioral/cognitive outcomes. Metabolism 57 (Suppl 2) S16-21.
• Marazziti D, Canale D (2004) Hormonal changes when fall­ing in love. Psychoneuroendocrinology 29: 931-936.
• Martin DM, Burns NR, Wittert G (2009) Free testosterone levels, attentional control, and processing speed perfor­mance in aging men. Neuropsychology 23: 158-167.
• Maruyama Y, Aoki N, Suzuki Y, Ohno Y, Imamura M, Saika T, Sinohara H, Yamamoto T (1987) Sex-steroid-binding plasma protein (SBP), testosterone, oestradiol and dehy- droepiandrosterone (DHEA) in prepuberty and puberty. Acta Endocrinol 114: 60-67.
• Matsumoto A (2001) Androgen stimulates neuronal plastic­ity in the perineal motoneurons of aged male rats. J Comp Neurol 430: 389-395.
• Matsumoto A (2005) Testosterone prevents synaptic loss in the perineal motoneuron pool in the spinal cord in male rats exposed to chronic stress. STRESS 8: 133-140.
• Matsunaga M, Ukena K, Tsutsui K (2002) Androgen biosyn­thesis in the quail brain. Brain Res 948: 180-185.
• McEwen BS, Alves SE, Bulloch K, Weiland NG (1997) Ovarian steroids and the brain: implications for cognition and aging. Neurology 48: S8-S15.
• McKeever WF (1995) Hormone and hemisphericity hypoth­eses regarding cognitive sex differences: possible future explanatory power, but current empirical chaos. Learn Individ Differ 7: 323-340.
• Medland SE, Zayats T, Glaser B, Nyholt DR, Gordon SD, Wright MJ, Montgomery GW, Campbell MJ, Henders AK, Timpson NJ et al (2010) A variant in LIN28B is associated with 2D:4D finger-length ratio, a putative ret­rospective biomarker of prenatal testosterone exposure. Am J Hum Genet 86: 419-525.
• Mensah-Nyagan AG, Do-Rego JL, Feuilloley M, Marcual A, Lange C, Pelletier G, Vaudry H (1996) In vivo and in vitro evidence for the biosynthesis of testosterone in the telencephalon of the female frog. J Neurochem 67: 413— 422.
• Morris JA, Jordan CL, Breedlove SM (2004) Sexual differ­entiation of the vertebrate nervous system. Nat Neurosci 7: 1034-1039.
• Mrazik M, Dombrowski SC (2010) The neurobiological foundations of giftednes. Roeper Review 32: 224-234.
• Mueller SC, Temple V, Oh E, VanRyzin C, Williams A, Cornwell B, Grillon C, Pine DS, Ernst M, Merke DP (2008) Early androgen exposure modulates spatial cogni­tion in congenital adrenal hyperplasia (CAH). Psychoneuroendocrinology 33: 973-980.
• Nelson PS, Clegg N, Arnold H, Ferguson C, Bonham M, White J, Hood L, Lin B (2002) The program of androgen- responsive genes in neoplastic prostate epithelium. Proc Natl Acad Sci U S A 99: 11890-11895.
• Ngun TC, Ghahramani N, Sanchez FJ, Bocklandt S, Vilain E (2010) The genetics of sex differences in brain and behavior. Front Neuroendocrinol 32: 227-246.
• Nordeen EJ, Nordeen KW, Sengelaub DR, Arnold AP (1985) Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science 229: 671­673.
• O'Connor DB, Archer J, Hair WM, Wu FC (2001) Activational effects of testosterone on cognitive function in men. Neuropsychologia 39: 1385-1394.
• Olson EA, Collins PF, Hooper CJ, Muetzel R, Lim KO, Luciana M (2009) White matter integrity predicts delay discounting behavior in 9- to 23-year-olds: a diffusion tensor imaging study. J Cogn Neurosci 21: 1406-1421.
• Ostatnikova D, Putz Z, Celec P, Hodosy J (2002) May tes­tosterone levels and their fluctuations influence cognitive performance in humans? Scr Med 75: 245-254.
• Ostatnikova D, Celec P, Putz Z, Hodosy J, Schmidt F, Laznibatova J, Kudela M (2007) Intelligence and salivary testosterone levels in prepubertal children. Neuropsychologia 45: 1378-1385.
• Ostatnikova D, Hodosy J, Skoknova M, Putz Z, Kudela M, Celec P (2010) Spatial abilities during the circalunar cycle in both sexes. Learn Individ Differ 20: 484-487.
• Paul SN, Kato BS, Hunkin JL, Vivekanandan S, Spector TD (2006) The big finger: the second to fourth digit ratio is a predictor of sporting ability in women. Br J Sports Med 40: 981-983.
• Poletti A, Melcangi RC, Negri-Cesi P, Maggi R, Martini L (1994) Steroid binding and metabolism in the luteinizing hormone-releasing hormone-producing neuronal cell line GT1-1. Endocrinology 135: 2623-2628.
• Powers ML, Florini JR (1975) Direct effect of testosterone on muscle-cells in tissue-culture. Endocrinology 97: 1043-1047.
• Quigley CA (2002) Editorial: The postnatal gonadotropin and sex steroid surge-insights from the androgen insensitivity syndrome. J Clin Endocrinol Metab 87: 24-28.
• Rahman Q, Wilson GD (2003) Sexual orientation and the 2nd to 4th finger length ratio: evidence for organising effects of sex hormones or developmental instability? Psychoneuroendocrinology 28: 288-303.
• Ramirez VD, Zheng J (1996) Membrane sex-steroid recep­tors in the brain. Front Neuroendocrinol 17: 402-439.
• Romano M, Rubolini D, Martinelli R, Bonisoli Alquati A, Saino N (2005) Experimental manipulation of yolk testosterone affects digit length ratios in the ring- necked pheasant (Phasianus colchicus). Horm Behav 48: 342-346.
• Romeo RD, Diedrich SL, Sisk CL (2000) Effects of gonadal steroids during pubertal development on androgen and estrogen receptor-alpha immunoreactivity in the hypo­thalamus and amygdala. J Neurobiol 44: 361-368.
• Romeo RD, Waters EM, McEwen BS (2004) Steroid- induced hippocampal synaptic plasticity: sex differences and similarities. Neuron Glia Biol 1: 219-229.
• Rose KA, Stapleton G, Dott K, Kieny MP, Best R, Schwarz M, Russell DW, Bjorkhem I, Seckl J, Lathe R (1997) Cyp7b, a novel brain cytochrome P450, catalyzes the synthesis of neurosteroids 7alpha-hydroxy dehydroepi- androsterone and 7alpha-hydroxy pregnenolone. Proc Natl Acad Sci U S A 94: 4925-4930.
• Roy AK, Chatterjee B (1995) Androgen action. Crit Rev Eukaryot Gene Expr 5: 157-176.
• Sanders G, Sjodin M, de Chastelaine M (2002) On the elu­sive nature of sex differences in cognition: hormonal influences contributing to within-sex variation. Arch Sex Behav 31: 145-152.
• Sandstrom NJ, Kim JH, Wasserman MA (2006) Testosterone modulates performance on a spatial working memory task in male rats. Horm Behav 50: 18-26.
• Shakil T, Hoque AN, Husain M, Belsham DD (2002) Differential regulation of gonadotropin-releasing hor­mone secretion and gene expression by androgen: mem­brane versus nuclear receptor activation. Mol Endocrinol 16: 2592-2602.
• Sharma D, Chaturvedi CM (2011) Testosterone modulates pituitary vasotocin receptor expression and adrenal activ­ity in osmotically stressed chicken. Comp Biochem Physiol A Mol Integr Physiol 158: 87-93.
• Shen HC, Buchanan G, Butler LM, Prescott J, Henderson M, Tilley WD, Coetzee GA (2005) GRIP1 mediates the interaction between the amino- and carboxyl-termini of the androgen receptor. Biol Chem 386: 69-74.
• Shepard RN, Metzler J (1971) Mental rotation of three-di­mensional objects. Science 171: 701-703.
• Shidaifat F (2009) Age-dependent expression of 5alpha-re- ductase and androgen receptors mRNA by the canine prostate. Physiol Res 58: 155-158.
• Simerly RB (2002) Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25: 407­536.
• Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA (2005a) Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 146: 3686­3692.
• Smith JT, Dungan HM, Stoll EA, Gottsch ML, Braun RE, Eacker SM, Clifton DK, Steiner RA (2005b) Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 146: 2976­2984.
• Spritzer MD, Daviau ED, Coneeny MK, Engelman SM, Prince WT, Rodriguez-Wisdom KN (2011) Effects of testosterone on spatial learning and memory in adult male rats. Horm Behav 59: 484-496.
• Stanton SJ, Liening SH, Schultheiss OC (2011) Testosterone is positively associated with risk taking in the Iowa Gambling Task. Horm Behav 59: 252-256.
• Swaab DF, Hofman MA (1990) An enlarged suprachias- matic nucleus in homosexual men. Brain Res 537: 141­148.
• Swaab DF (2007) Sexual differentiation of the brain and behavior. Best Pract Res Clin Endocrinol Metab 21: 431-444.
• Toppari J, Skakkebaek NE (1998) Sexual differentiation and environmental endocrine disrupters. Baillieres Best Pract Res Clin Endocrinol Metab 12: 143-156.
• Trueb RM (2002) Molecular mechanisms of androgenetic alopecia. Exp Gerontol 37: 981-990.
• Tut TG, Ghadessy FJ, Trifiro MA, Pinsky L, Yong EL (1997) Long polyglutamine tracts in the androgen recep­tor are associated with reduced trans-activation, impaired sperm production, and male infertility. J Clin Endocrinol Metab 82: 3777-3782.
• Valla JM, Ganzel BL, Yoder KJ, Chen GM, Lyman LT, Sidari AP, Keller AE, Maendel JW, Perlman JE, Wong
• SK, Belmonte MK (2010) More than maths and mind- reading: sex differences in empathizing/systemizing covariance. Autism Res 3: 174-184.
• Valla JM, Ceci SJ (2011) Can sex differences in science be tied to the long reach of prenatal hormones?: Brain orga­nization theory, digit ratio (2D/4D), and sex differences in preferences and cognition. Perspect Psychol Sci 6: 147­149.
• van Goozen SH, Slabbekoorn D, Gooren LJ, Sanders G, Cohen-Kettenis PT (2002) Organizing and activating effects of sex hormones in homosexual transsexuals. Behav Neurosci 116: 982-988.
• 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: 3448-3452.
• van Wingen G, Mattern C, Verkes RJ, Buitelaar J, Fernandez G (2010) Testosterone reduces amygdala-orbitofrontal cortex coupling. Psychoneuroendocrinology 35: 105­113.
• Von Horn A, Backman L, Davidsson T, Hansen S (2010) Empathizing, systemizing and finger length ratio in a Swedish sample. Scand J Psychol 51: 31-37.
• Weise M, De-Levi S, Barnes KM, Gafni RI, Abad V, Baron J (2001) Effects of estrogen on growth plate senescence and epiphyseal fusion. Proc Natl Acad Sci U S A 98: 6871-6876.
• Welling LL, Jones BC, DeBruine LM, Smith FG, Feinberg DR, Little AC, Al-Dujaili EA (2008) Men report stron­ger attraction to femininity in women's faces when their testosterone levels are high. Horm Behav 54: 703-708.
• Westberg L, Henningsson S, Landen M., Annerbrink K, Melke J, Nilsson S, Rosmond R, Holm G, Anckarsater H, Eriksson E (2009) Influence of androgen receptor repeat polymorphisms on personality traits in men. J Psychiatry Neurosci 34: 205-213.
• Williams CL, Meck WH (1991) The organizational effects of gonadal-steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 16: 155-176.
• Witelson SF, Nowakowski RS (1991) Left out axons make men right: a hypothesis for the origin of handed­ness and functional asymmetry. Neuropsychologia 29: 327-333.
• Wolf OT, Kirschbaum C (2002) Endogenous estradiol and testosterone levels are associated with cognitive perfor­mance in older women and men. Horm Behav 41: 259­266.
• Wood RI, Newman SW (1995) Integration of chemosensory and hormonal cues is essential for mating in the male Syrian hamster. J Neurosci 15: 7261-7269.
• Wood RI, Coolen LM (1997) Integration of chemosensory and hormonal cues is essential for sexual behaviour in the male Syrian hamster: role of the medial amygdaloid nucleus. Neuroscience 78: 1027-1035.
• Wu XY, Li ZL, Wu CY, Liu YM, Lin H, Wang SH, Xiao WF (2010) Endocrine traits of polycystic ovary syndrome in prenatally androgenized female Sprague-Dawley rats. Endocr J 57: 201-209.
• Yamazaki H, Shimada T (1997) Progesterone and testoster­one hydroxylation by cytochromes P450 2C19, 2C9, and 3A4 in human liver microsomes. Arch Biochem Biophys 346: 161-169.
• Zehr JL, Todd BJ, Schulz KM, McCarthy MM, Sisk CL (2006) Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster. J Neurobiol 66: 478-590.
• Zhou JN, Hofman MA, Gooren LJ, Swaab DF (1995) A sex difference in the human brain and its relation to trans- sexuality. Nature 378: 68-70.

Uwagi

Rekord w opracowaniu