Testosterone and the brain: from cognition to autism
Jazyk angličtina Země Česko Médium print
Typ dokumentu časopisecké články, přehledy
PubMed
33464922
PubMed Central
PMC8603719
DOI
10.33549/physiolres.934592
PII: 934592
Knihovny.cz E-zdroje
- MeSH
- autistická porucha metabolismus patologie MeSH
- kognice fyziologie MeSH
- lidé MeSH
- mozek účinky léků patologie MeSH
- pohlavní dimorfismus MeSH
- sexuální faktory MeSH
- testosteron metabolismus MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- testosteron MeSH
Sex and gender matter in all aspects of life. Humans exhibit sexual dimorphism in anatomy, physiology, but also pathology. Many of the differences are due to sex chromosomes and, thus, genetics, other due to endocrine factors such as sex hormones, some are of social origin. Over the past decades, huge number of scientific studies have revealed striking sex differences of the human brain with remarkable behavioral and cognitive consequences. Prenatal and postnatal testosterone influence brain structures and functions, respectively. Cognitive sex differences include especially certain spatial and language tasks, but they also affect many other aspects of the neurotypical brain. Sex differences of the brain are also relevant for the pathogenesis of neuropsychiatric disorders such as autism spectrum disorders, which are much more prevalent in the male population. Structural dimorphism in the human brain was well-described, but recent controversies now question its importance. On the other hand, solid evidence exists regarding gender differences in several brain functions. This review tries to summarize the current understanding of the complexity of the effects of testosterone on brain with special focus on their role in the known sex differences in healthy individuals and people in the autism spectrum.
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ALBERTSSON-WIKLAND K, ROSBERG S, LANNERING B, DUNKEL L, SELSTAM G, NORJAVAARA E. Twenty-four-hour profiles of luteinizing hormone, follicle-stimulating hormone, testosterone, and estradiol levels: a semilongitudinal study throughout puberty in healthy boys. J Clin Endocrinol Metab. 1997;82:541–549. doi: 10.1210/jcem.82.2.3778. PubMed DOI
ALEXANDER GM, SON T. Androgens and eye movements in women and men during a test of mental rotation ability. Horm Behav. 2007;52:197–204. doi: 10.1016/j.yhbeh.2007.01.011. PubMed DOI PMC
ARDALAN M, CHUMAK T, VEXLER Z, MALLARD C. Sex-dependent effects of perinatal inflammation on the brain: Implication for neuro-psychiatric disorders. Int J Mol Sci. 2019;20:2270. doi: 10.3390/ijms20092270. PubMed DOI PMC
ARNOLD AP. The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Horm Behav. 2009;55:570–578. doi: 10.1016/j.yhbeh.2009.03.011. PubMed DOI PMC
ARNOLD AP, BREEDLOVE SM. Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav. 1985;19:469–498. doi: 10.1016/0018-506X(85)90042-X. PubMed DOI
AUYEUNG B, BARON-COHEN S, ASHWIN E, KNICKMEYER R, TAYLOR K, HACKETT G. Fetal testosterone and autistic traits. Br J Psychol. 2009a;100:1–22. doi: 10.1348/000712608X311731. PubMed DOI
AUYEUNG B, BARON-COHEN S, ASHWIN E, KNICKMEYER R, TAYLOR K, HACKETT G, HINES M. Fetal testosterone predicts sexually differentiated childhood behavior in girls and in boys. Psychol Sci. 2009b;20:144–148. doi: 10.1111/j.1467-9280.2009.02279.x. PubMed DOI PMC
AUYEUNG B, BARON-COHEN S, ASHWIN E, KNICKMEYER R, TAYLOR K, HACKETT G, HINES M. Fetal testosterone predicts sexually differentiated childhood behavior in girls and in boys. Psychol Sci. 2009c;20:144–148. doi: 10.1111/j.1467-9280.2009.02279.x. PubMed DOI PMC
BARBIERI RL. The endocrinology of the menstrual cycle. Methods Mol Biol. 2014;1154:145–169. doi: 10.1007/978-1-4939-0659-8_7. PubMed DOI
BARON-COHEN S. The extreme male brain theory of autism. Trends Cogn Sci. 2002;6:248–254. doi: 10.1016/S1364-6613(02)01904-6. PubMed DOI
BARON-COHEN S. Testing the extreme male brain (EMB) theory of autism: let the data speak for themselves. Cogn Neuropsychiatry. 2005;10:77–81. doi: 10.1080/13546800344000336. PubMed DOI
BARON-COHEN S, AUYEUNG B, NORGAARD-PEDERSEN B, HOUGAARD DM, ABDALLAH MW, MELGAARD L, COHEN AS, CHAKRABARTI B, RUTA L, LOMBARDO MV. Elevated fetal steroidogenic activity in autism. Mol Psychiatry. 2015;20:369–376. doi: 10.1038/mp.2014.48. PubMed DOI PMC
BARON-COHEN S, LOMBARDO MV, AUYEUNG B, ASHWIN E, CHAKRABARTI B, KNICKMEYER R. Why are autism spectrum conditions more prevalent in males? PLoS Biol. 2011;9:e1001081. doi: 10.1371/journal.pbio.1001081. PubMed DOI PMC
BEATON AA, RUDLING N, KISSLING C, TAURINES R, THOME J. Digit ratio (2D:4D), salivary testosterone, and handedness. Laterality. 2011;16:136–155. doi: 10.1080/13576500903410369. PubMed DOI
BEAVEN CM, INGRAM JR, GILL ND, HOPKINS WG. Ultradian rhythmicity and induced changes in salivary testosterone. Eur J Appl Physiol. 2010;110:405–413. doi: 10.1007/s00421-010-1518-3. PubMed DOI
BEKING T, GEUZE RH, Van FAASSEN M, KEMA IP, KREUKELS BPC, GROOTHUIS TGG. Prenatal and pubertal testosterone affect brain lateralization. Psychoneuroendocrinology. 2018;88:78–91. doi: 10.1016/j.psyneuen.2017.10.027. PubMed DOI
BENBOW CP. Sex differences in mathematical reasoning ability in intellectually talented preadolescents: Their nature, effects, and possible causes. Behavioral and Brain Sciences. 1988;11:169–232. doi: 10.1017/S0140525X00049244. DOI
BHATTA S, BLAIR JA, CASADESUS G. Luteinizing hormone involvement in aging female cognition: Not all is estrogen loss. Front Endocrinol (Lausanne) 2018;9:544. doi: 10.3389/fendo.2018.00544. PubMed DOI PMC
BLAIR JA, BHATTA S, McGEE H, CASADESUS G. Luteinizing hormone: Evidence for direct action in the CNS. Horm Behav. 2015;76:57–62. doi: 10.1016/j.yhbeh.2015.06.020. PubMed DOI PMC
BRAMEN JE, HRANILOVICH JA, DAHL RE, CHEN J, ROSSO C, FORBES EE, DINOV ID, WORTHMAN CM, SOWELL ER. Sex matters during adolescence: testosterone-related cortical thickness maturation differs between boys and girls. PLoS One. 2012;7:e33850. doi: 10.1371/journal.pone.0033850. PubMed DOI PMC
BURKITT J, WIDMAN D, SAUCIER DM. Evidence for the influence of testosterone in the performance of spatial navigation in a virtual water maze in women but not in men. Horm Behav. 2007;51:649–654. doi: 10.1016/j.yhbeh.2007.03.007. PubMed DOI
CALLARD GV, TARRANT AM, NOVILLO A, YACCI P, CIACCIA L, VAJDA S, CHUANG GY, KOZAKOV D, GREYTAK SR, SAWYER S, HOOVER C, COTTER KA. Evolutionary origins of the estrogen signaling system: insights from amphioxus. J Steroid Biochem Mol Biol. 2011;127:176–188. doi: 10.1016/j.jsbmb.2011.03.022. PubMed DOI PMC
CARLEZON WA, KIM W, MISSIG G, FINGER BC, LANDINO SM, ALEXANDER AJ, MOKLER EL, ROBBINS JO, LI Y, BOLSHAKOV VY, McDOUGLE CJ, KIM K-S. Maternal and early postnatal immune activation produce sex-specific effects on autism-like behaviors and neuroimmune function in mice. Sci Rep. 2019;9:16928. doi: 10.1038/s41598-019-53294-z. PubMed DOI PMC
CELEC P, MESEZNIKOV G, OSTATNIKOVA D, HODOSY J. Changes in well-being but not in spatial ability across the menstrual cycle. Biol Rhythm Res. 2011;42:255–259. doi: 10.1080/09291016.2010.513524. DOI
CELEC P, OSTANIKOVA D, SKOKNOVA M, HODOSY J, PUTZ Z, KUDELA M. Salivary sex hormones during the menstrual cycle. Endocr J. 2009a;56:521–523. doi: 10.1507/endocrj.K09E-020. PubMed DOI
CELEC P, OSTATNIKOVA D, HODOSY J. On the effects of testosterone on brain behavioral functions. Front Neurosci. 2015;9:12. doi: 10.3389/fnins.2015.00012. PubMed DOI PMC
CELEC P, OSTATNIKOVA D, HODOSY J, PUTZ Z, KUDELA M. Increased one week soybean consumption affects spatial abilities but not sex hormone status in men. Int J Food Sci Nutr. 2007a;58:424–428. doi: 10.1080/09637480701253490. PubMed DOI
CELEC P, OSTATNIKOVA D, HODOSY J, SKOKNOVA M, PUTZ Z, KUDELA M. Infradian dynamics and variability of salivary testosterone in men and women. Biol Rhythm Res. 2007b;38:367–372. doi: 10.1080/09291010600981797. DOI
CELEC P, OSTATNIKOVA D, HOLESOVA Z, MINARIK G, FICEK A, KELEMENOVA S, PUTZ Z, KUDELA M. Spatial abilities in prepubertal intellectually gifted boys and genetic polymorphisms related to testosterone metabolism. J Psychophysiology. 2009b;23:1–6. doi: 10.1027/0269-8803.23.1.1. DOI
CELEC P, OSTATNIKOVA D, PUTZ Z, HODOSY J, BURSKY P, STARKA L, HAMPL R, KUDELA M. Circatrigintan cycle of salivary testosterone in human male. Biol Rhythm Res. 2003;34:305–315. doi: 10.1076/brhm.34.3.305.18807. DOI
CELEC P, OSTATNIKOVA D, PUTZ Z, KUDELA M. The circalunar cycle of salivary testosterone and the visual-spatial performance. Bratisl Lek Listy. 2002;103:59–69. PubMed
CELEC P, TRETINAROVA D, MINARIK G, FICEK A, SZEMES T, LAKATOSOVA S, SCHMIDTOVA E, TURNA J, KADASI L, OSTATNIKOVA D. Genetic polymorphisms related to testosterone metabolism in intellectually gifted boys. PLoS One. 2013;8:e54751. doi: 10.1371/journal.pone.0054751. PubMed DOI PMC
CHERRIER MM, ASTHANA S, PLYMATE S, BAKER L, MATSUMOTO AM, PESKIND E, RASKIND MA, BRODKIN K, BREMNER W, PETROVA A, LATENDRESSE S, CRAFT S. Testosterone supplementation improves spatial and verbal memory in healthy older men. Neurology. 2001;57:80–88. doi: 10.1212/WNL.57.1.80. PubMed DOI
CHERRIER MM, MATSUMOTO AM, AMORY JK, ASTHANA S, BREMNER W, PESKIND ER, RASKIND MA, CRAFT S. Testosterone improves spatial memory in men with Alzheimer disease and mild cognitive impairment. Neurology. 2005;64:2063–2068. doi: 10.1212/01.WNL.0000165995.98986.F1. PubMed DOI
CHOE MS, ORTIZ-MANTILLA S, MAKRIS N, GREGAS M, BACIC J, HAEHN D, KENNEDY D, PIENAAR R, CAVINESS VS, JR, BENASICH AA, GRANT PE. Regional infant brain development: an MRI-based morphometric analysis in 3 to 13 month olds. Cereb Cortex. 2013;23:2100–2117. doi: 10.1093/cercor/bhs197. PubMed DOI PMC
CHURA LR, LOMBARDO MV, ASHWIN E, AUYEUNG B, CHAKRABARTI B, BULLMORE ET, BARON-COHEN S. Organizational effects of fetal testosterone on human corpus callosum size and asymmetry. Psychoneuroendocrinology. 2010;35:122–132. doi: 10.1016/j.psyneuen.2009.09.009. PubMed DOI
COHEN-BENDAHAN CC, BUITELAAR JK, Van GOOZEN SH, ORLEBEKE JF, COHEN-KETTENIS PT. 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. 2005;47:230–237. doi: 10.1016/j.yhbeh.2004.10.006. PubMed DOI
COLLAER ML, HINES M. Human behavioral sex differences: a role for gonadal hormones during early development? Psychol Bull. 1995;118:55–107. doi: 10.1037/0033-2909.118.1.55. PubMed DOI
COLVERT E, TICK B, McEWEN F, STEWART C, CURRAN SR, WOODHOUSE E, GILLAN N, HALLETT V, LIETZ S, GARNETT T, RONALD A, PLOMIN R, RIJSDIJK F, HAPPE F, BOLTON P. Heritability of autism spectrum disorder in a UK population-based twin sample. JAMA Psychiatry. 2015;72:415–423. doi: 10.1001/jamapsychiatry.2014.3028. PubMed DOI PMC
CONNOLLY PB, RESKO JA. Prenatal testosterone differentiates brain regions controlling gonadotropin release in guinea pigs. Biol Reprod. 1994;51:125–130. doi: 10.1095/biolreprod51.1.125. PubMed DOI
CONSTANTINO JN, GROSZ D, SAENGER P, CHANDLER DW, NANDI R, EARLS FJ. Testosterone and aggression in children. J Am Acad Child Adolesc Psychiatry. 1993;32:1217–1222. doi: 10.1097/00004583-199311000-00015. PubMed DOI
COURVOISIER DS, RENAUD O, GEISER C, PASCHKE K, GAUDY K, JORDAN K. Sex hormones and mental rotation: an intensive longitudinal investigation. Horm Behav. 2013;63:345–351. doi: 10.1016/j.yhbeh.2012.12.007. PubMed DOI
De LACOSTE MC, HORVATH DS, WOODWARD DJ. Possible sex differences in the developing human fetal brain. J Clin Exp Neuropsychol. 1991;13:831–846. doi: 10.1080/01688639108405101. PubMed DOI
DEARY IJ, STRAND S, SMITH P, FERNANDEZ C. Intelligence and educational achievement. Intelligence. 2007;35:13–21. doi: 10.1016/j.intell.2006.02.001. DOI
DEARY IJ. Intelligence. Curr Biol. 2013;23:R673–R676. doi: 10.1016/j.cub.2013.07.021. PubMed DOI
DEONI SCL, DEAN DC, 3RD, REMER J, DIRKS H, O’MUIRCHEARTAIGH J. Cortical maturation and myelination in healthy toddlers and young children. NeuroImage. 2015;115:147–161. doi: 10.1016/j.neuroimage.2015.04.058. PubMed DOI PMC
DIPIETRO JA, VOEGTLINE KM. The gestational foundation of sex differences in development and vulnerability. Neuroscience. 2017;342:4–20. doi: 10.1016/j.neuroscience.2015.07.068. PubMed DOI PMC
DOMONKOS E, BORBELYOVA V, CSONGOVA M, BOSY M, KACMAROVA M, OSTATNIKOVA D, HODOSY J, CELEC P. Sex differences and sex hormones in anxiety-like behavior of aging rats. Horm Behav. 2017a;93:159–165. doi: 10.1016/j.yhbeh.2017.05.019. PubMed DOI
DOMONKOS E, BORBELYOVA V, KOLATOROVA L, CHLUPACOVA T, OSTATNIKOVA D, HODOSY J, STARKA L, CELEC P. Sex differences in the effect of prenatal testosterone exposure on steroid hormone production in adult rats. Physiol Res. 2017b;66(Suppl 3):S367–S374. doi: 10.33549/physiolres.933722. PubMed DOI
DOMONKOS E, HODOSY J, OSTATNIKOVA D, CELEC P. On the role of testosterone in anxiety-like behavior across life in experimental rodents. Front Endocrinol (Lausanne) 2018;9:441. doi: 10.3389/fendo.2018.00441. PubMed DOI PMC
DUNCAN J. Frontal lobe function and general intelligence: why it matters. Cortex. 2005;41:215–217. doi: 10.1016/S0010-9452(08)70896-7. PubMed DOI
DUNCAN J, SEITZ RJ, KOLODNY J, BOR D, HERZOG H, AHMED A, NEWELL FN, EMSLIE H. A neural basis for general intelligence. Science. 2000;289:457–460. doi: 10.1126/science.289.5478.457. PubMed DOI
DURDIAKOVA J, CELEC P, LAZNIBATOVA J, MINARIK G, LAKATOSOVA S, KUBRANSKA A, OSTATNIKOVA D. Differences in salivary testosterone, digit ratio and empathy between intellectually gifted and control boys. Intelligence. 2015;48:76–84. doi: 10.1016/j.intell.2014.11.002. DOI
DURDIAKOVA J, LAKATOSOVA S, KUBRANSKA A, LAZNIBATOVA J, FICEK A, OSTATNIKOVA D, CELEC P. Mental rotation in intellectually gifted boys is affected by the androgen receptor CAG repeat polymorphism. Neuropsychologia. 2013;51:1693–1698. doi: 10.1016/j.neuropsychologia.2013.05.016. PubMed DOI
DURDIAKOVA J, OSTATNIKOVA D, CELEC P. Testosterone and its metabolites - modulators of brain functions. Acta Neurobiol Exp (Wars) 2011;71:434–454. PubMed
FILOVA B, DOMONKOS E, BORBELYOVA V, BABICKOVA J, TOTHOVA L, OSTATNIKOVA D, CELEC P, HODOSY J. Does the non-genomic effect of testosterone on social anxiety require the presence of a classical steroid receptor? Acta Neurobiol Exp (Wars) 2015a;75:457–461. PubMed
FILOVA B, MALINOVA M, BABICKOVA J, TOTHOVA L, OSTATNIKOVA D, CELEC P, HODOSY J. Effects of testosterone and estradiol on anxiety and depressive-like behavior via a non-genomic pathway. Neuroscience Bulletin. 2015b;31:288–296. doi: 10.1007/s12264-014-1510-8. PubMed DOI PMC
FILOVA B, OSTATNIKOVA D, CELEC P, HODOSY J. The effect of testosterone on the formation of brain structures. Cells Tissues Organs. 2013;197:169–177. doi: 10.1159/000345567. PubMed DOI
FLANNERY KA, LIEDERMAN J, DALY L, SCHULTZ J. Male prevalence for reading disability is found in a large sample of black and white children free from ascertainment bias. J Int Neuropsychol Soc. 2000;6:433–442. doi: 10.1017/S1355617700644016. PubMed DOI
GAUGLER T, KLEI L, SANDERS SJ, BODEA CA, GOLDBERG AP, LEE AB, MAHAJAN M, MANAA D, PAWITAN Y, REICHERT J, RIPKE S, SANDIN S. Most genetic risk for autism resides with common variation. Nat Genet. 2014;46:881–885. doi: 10.1038/ng.3039. PubMed DOI PMC
GESCHWIND N, GALABURDA AM. Cerebral lateralization. Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Arch Neurol. 1985;42:428–459. doi: 10.1001/archneur.1985.04060050026008. PubMed DOI
GHOSH D, EGBUTA C, LO J. Testosterone complex and non-steroidal ligands of human aromatase. J Steroid Biochem Mol Biol. 2018;181:11–19. doi: 10.1016/j.jsbmb.2018.02.009. PubMed DOI PMC
GILMORE JH, LIN W, PRASTAWA MW, LOONEY CB, VETSA YS, KNICKMEYER RC, EVANS DD, SMITH JK, HAMER RM, LIEBERMAN JA, GERIG G. Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. J Neurosci. 2007;27:1255–1260. doi: 10.1523/JNEUROSCI.3339-06.2007. PubMed DOI PMC
GOEL N, BALE TL. Organizational and activational effects of testosterone on masculinization of female physiological and behavioral stress responses. Endocrinology. 2008;149:6399–6405. doi: 10.1210/en.2008-0433. PubMed DOI PMC
GORE AC, MARTIEN KM, GAGNIDZE K, PFAFF D. Implications of prenatal steroid perturbations for neurodevelopment, behavior, and autism. Endocr Rev. 2014;35:961–991. doi: 10.1210/er.2013-1122. PubMed DOI PMC
GOUCHIE C, KIMURA D. The relationship between testosterone levels and cognitive ability patterns. Psychoneuroendocrinology. 1991;16:323–334. doi: 10.1016/0306-4530(91)90018-O. PubMed DOI
GREENLAND KJ, BEILIN J, CASTRO J, VARGHESE PN, ZAJAC JD. Polymorphic CAG repeat length in the androgen receptor gene and association with neurodegeneration in a heterozygous female carrier of Kennedy’s disease. J Neurol. 2004;251:35–41. doi: 10.1007/s00415-004-0266-x. PubMed DOI
GRIMSHAW GM, SITARENIOS G, FINEGAN JA. Mental rotation at 7 years: relations with prenatal testosterone levels and spatial play experiences. Brain Cogn. 1995;29:85–100. doi: 10.1006/brcg.1995.1269. PubMed DOI
GUIGNARD MM, PESQUIES PC, SERRURIER BD, MERINO DB, REINBERG AE. Circadian rhythms in plasma levels of cortisol, dehydroepiandrosterone, delta 4-androstenedione, testosterone and dihydrotestosterone of healthy young men. Acta Endocrinol (Copenh) 1980;94:536–545. doi: 10.1530/acta.0.0940536. PubMed DOI
GUR RC, TURETSKY BI, MATSUI M, YAN M, BILKER W, HUGHETT P, GUR RE. Sex differences in brain gray and white matter in healthy young adults: Correlations with cognitive performance. J Neurosci. 1999;19:4065–4072. doi: 10.1523/JNEUROSCI.19-10-04065.1999. PubMed DOI PMC
HARDEN KP, KRETSCH N, TACKETT JL, TUCKER-DROB EM. Genetic and environmental influences on testosterone in adolescents: evidence for sex differences. Dev Psychobiol. 2014;56:1278–1289. doi: 10.1002/dev.21207. PubMed DOI PMC
HAUSMANN M, SCHOOFS D, ROSENTHAL HE, JORDAN K. Interactive effects of sex hormones and gender stereotypes on cognitive sex differences--a psychobiosocial approach. Psychoneuroendocrinology. 2009;34:389–401. doi: 10.1016/j.psyneuen.2008.09.019. PubMed DOI
HEDGES LV, NOWELL A. Sex differences in mental test scores, variability, and numbers of high-scoring individuals. Science. 1995;269:41–45. doi: 10.1126/science.7604277. PubMed DOI
HENNINGSSON S, JONSSON L, LJUNGGREN E, WESTBERG L, GILLBERG C, RASTAM M, ANCKARSATER H, NYGREN G, LANDEN M, THURESSON K, BETANCUR C, LEBOYER M, GILLBERG C, ERIKSSON E, MELKE J. Possible association between the androgen receptor gene and autism spectrum disorder. Psychoneuroendocrinology. 2009;34:752–761. doi: 10.1016/j.psyneuen.2008.12.007. PubMed DOI
HILLEKE EHP, PEGGY TC-K, NEELTJE EMVH, JISKA SP, RACHEL GHB, WIEPKE C, HUGO GS, LOUIS JGG, RENÉ SK. Changing your sex changes your brain: influences of testosterone and estrogen on adult human brain structure. Eur J Endocrinol. 2006;155(Suppl 1):S107–S114. doi: 10.1530/eje.1.02248. DOI
HILLMER AM, HANNEKEN S, RITZMANN S, BECKER T, FREUDENBERG J, BROCKSCHMIDT FF, FLAQUER A, FREUDENBERG-HUA Y, JAMRA RA, METZEN C, HEYN U, SCHWEIGER N, BETZ RC, BLAUMEISER B, HAMPE J, SCHREIBER S, SCHULZE TG, HENNIES HC, SCHUMACHER J, PROPPING P, RUZICKA T, CICHON S, WIENKER TF, KRUSE R, NOTHEN MM. Genetic variation in the human androgen receptor gene is the major determinant of common early-onset androgenetic alopecia. Am J Hum Genet. 2005;77:140–148. doi: 10.1086/431425. PubMed DOI PMC
HINES M. Prenatal testosterone and gender-related behaviour. Eur J Endocrinol. 2006;155(Suppl 1):S115–S121. doi: 10.1530/eje.1.02236. PubMed DOI
HIORT O. The differential role of androgens in early human sex development. BMC Medicine. 2013;11:152. doi: 10.1186/1741-7015-11-152. PubMed DOI PMC
HODOSY J, OSTATNIKOVA D, KUDELA M, CELEC P. Behavioral effects of physical exercise and exogenous testosterone in male rats. Neurophysiology. 2012a;44:409–413. doi: 10.1007/s11062-012-9312-y. DOI
HODOSY J, OSTATNIKOVA D, RILJAK V, MYSLIVECEK J, CELEC P. The effect of rapid and depot testosterone and estradiol on spatial performance in water maze. Cent Eur J Biol. 2012b;7:596–602. doi: 10.2478/s11535-012-0046-z. DOI
HODOSY J, ZELMANOVA D, MAJZUNOVA M, FILOVA B, MALINOVA M, OSTATNIKOVA D, CELEC P. The anxiolytic effect of testosterone in the rat is mediated via the androgen receptor. Pharmacol Biochem Behav. 2012c;102:191–195. doi: 10.1016/j.pbb.2012.04.005. PubMed DOI
HOFFMAN JF, WRIGHT CL, McCARTHY MM. A critical period in Purkinje cell development is mediated by local estradiol synthesis, disrupted by inflammation, and has enduring consequences only for males. J Neurosci. 2016;36:10039–10049. doi: 10.1523/JNEUROSCI.1262-16.2016. PubMed DOI PMC
HYDE JS, FENNEMA E, LAMON SJ. Gender differences in mathematics performance: a meta-analysis. Psychol Bull. 1990;107:139–155. doi: 10.1037/0033-2909.107.2.139. PubMed DOI
INGALHALIKAR M, SMITH A, PARKER D, SATTERTHWAITE TD, ELLIOTT MA, RUPAREL K, HAKONARSON H, GUR RE, GUR RC, VERMA R. Sex differences in the structural connectome of the human brain. Proc Natl Acad Sci U S A. 2014;111:823–828. doi: 10.1073/pnas.1316909110. PubMed DOI PMC
IRVINE RA, MA H, YU MC, ROSS RK, STALLCUP MR, COETZEE GA. Inhibition of p160-mediated coactivation with increasing androgen receptor polyglutamine length. Hum Mol Genet. 2000;9:267–274. doi: 10.1093/hmg/9.2.267. PubMed DOI
IVELL R, ANAND-IVELL R, MORLEY SD. Endocrinology of the Fetal Testis. In: Simoni M, Huhtaniemi IT, editors. Endocrinology of the Testis and Male Reproduction. Cham: Springer International Publishing; 2017. pp. 245–272. DOI
JOHNSON W, CAROTHERS A, DEARY IJ. Sex differences in variability in general intelligence: a new look at the old question. Perspect Psychol Sci. 2008;3:518–531. doi: 10.1111/j.1745-6924.2008.00096.x. PubMed DOI
KNICKMEYER R, BARON-COHEN S, FANE BA, WHEELWRIGHT S, MATHEWS GA, CONWAY GS, BROOK CG, HINES M. Androgens and autistic traits: A study of individuals with congenital adrenal hyperplasia. Horm Behav. 2006;50:148–153. doi: 10.1016/j.yhbeh.2006.02.006. PubMed DOI
KNICKMEYER R, BARON-COHEN S, RAGGATT P, TAYLOR K. Foetal testosterone, social relationships, and restricted interests in children. J Child Psychol Psychiatry. 2005;46:198–210. doi: 10.1111/j.1469-7610.2004.00349.x. PubMed DOI
KNICKMEYER RC, BARON-COHEN S. Fetal testosterone and sex differences in typical social development and in autism. J Child Neurol. 2006;21:825–845. doi: 10.1177/08830738060210101601. PubMed DOI
KOOLSCHIJN PC, CRONE EA. Sex differences and structural brain maturation from childhood to early adulthood. Dev Cogn Neurosci. 2013;5:106–118. doi: 10.1016/j.dcn.2013.02.003. PubMed DOI PMC
KRAJMER P, SPAJDEL M, KUBRANSKA A, OSTATNIKOVA D. 2D:4D finger ratio in Slovak autism spectrum disorder population. Bratisl Lek Listy. 2011;112:377–379. PubMed
LAI M-C, LOMBARDO MV, BARON-COHEN S. Autism. Lancet. 2014;383:896–910. doi: 10.1016/S0140-6736(13)61539-1. PubMed DOI
LEE DM, ULUBAEV A, TAJAR A, PYE SR, PENDLETON N, PURANDARE N, O’NEILL TW, O’CONNOR DB, LABRIE F, PLATT H, PAYNE D, BARTFAI G, BOONEN S, CASANUEVA FF, FINN JD, FORTI G, GIWERCMAN A, HAN TS, HUHTANIEMI IT, KULA K, LEAN ME, PUNAB M, SILMAN AJ, VANDERSCHUEREN D, WU FC. Endogenous hormones, androgen receptor CAG repeat length and fluid cognition in middle-aged and older men: results from the European Male Ageing Study. Eur J Endocrinol. 2010;162:1155–1164. doi: 10.1530/EJE-09-0970. PubMed DOI
LIEDERMAN J, KANTROWITZ L, FLANNERY K. Male vulnerability to reading disability is not likely to be a myth: a call for new data. J Learn Disabil. 2005;38:109–129. doi: 10.1177/00222194050380020201. PubMed DOI
LINN MC, PETERSEN AC. Emergence and characterization of sex differences in spatial ability: a meta-analysis. Child Dev. 1985;56:1479–1498. doi: 10.2307/1130467. PubMed DOI
LOMBARDO MV, ASHWIN E, AUYEUNG B, CHAKRABARTI B, TAYLOR K, HACKETT G, BULLMORE ET, BARON-COHEN S. Fetal testosterone influences sexually dimorphic gray matter in the human brain. J Neurosci. 2012;32:674–680. doi: 10.1523/JNEUROSCI.4389-11.2012. PubMed DOI PMC
LOSECAAT VERMEER AB, RIECANSKY I, EISENEGGER C. Competition, testosterone, and adult neurobehavioral plasticity. Prog Brain Res. 2016;229:213–238. doi: 10.1016/bs.pbr.2016.05.004. PubMed DOI
LUDERS E, TOGA AW. Sex differences in brain anatomy. Prog Brain Res. 2010;186:3–12. doi: 10.1016/B978-0-444-53630-3.00001-4. PubMed DOI
MacLUSKY NJ, BOWLBY DA, BROWN TJ, PETERSON RE, HOCHBERG RB. Sex and the developing brain: suppression of neuronal estrogen sensitivity by developmental androgen exposure. Neurochem Res. 1997;22:1395–1414. doi: 10.1023/A:1022027408234. PubMed DOI
MacLUSKY NJ, HAJSZAN T, PRANGE-KIEL J, LERANTH C. Androgen modulation of hippocampal synaptic plasticity. Neuroscience. 2006;138:957–965. doi: 10.1016/j.neuroscience.2005.12.054. PubMed DOI
MANNING JT, BARLEY L, WALTON J, LEWIS-JONES DI, TRIVERS RL, SINGH D, THORNHILL R, ROHDE P, BERECZKEI T, HENZI P, SOLER M, SZWED A. The 2nd:4th digit ratio, sexual dimorphism, population differences, and reproductive success. evidence for sexually antagonistic genes? Evol Hum Behav. 2000;21:163–183. doi: 10.1016/S1090-5138(00)00029-5. PubMed DOI
MANNING JT, FINK B. Digit ratio (2D:4D), dominance, reproductive success, asymmetry, and sociosexuality in the BBC Internet Study. Am J Hum Biol. 2008;20:451–461. doi: 10.1002/ajhb.20767. PubMed DOI
MANNING JT, ROBINSON SJ. 2nd to 4th digit ratio and a universal mean for prenatal testosterone in homosexual men. Med Hypotheses. 2003;61:303–306. doi: 10.1016/S0306-9877(03)00184-1. PubMed DOI
MANNING JT, SCUTT D, WILSON J, LEWIS-JONES DI. The ratio of 2nd to 4th digit length: a predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Hum Reprod. 1998;13:3000–3004. doi: 10.1093/humrep/13.11.3000. PubMed DOI
McCARTHY MM, WRIGHT CL, SCHWARZ JM. New tricks by an old dogma: mechanisms of the Organizational/Activational Hypothesis of steroid-mediated sexual differentiation of brain and behavior. Horm Behav. 2009;55:655–665. doi: 10.1016/j.yhbeh.2009.02.012. PubMed DOI PMC
MOFFAT SD, HAMPSON E. A curvilinear relationship between testosterone and spatial cognition in humans: possible influence of hand preference. Psychoneuroendocrinology. 1996;21:323–337. doi: 10.1016/0306-4530(95)00051-8. PubMed DOI
MOROTE J, TABERNERO AJ, ALVAREZ OSSORIO JL, CIRIA JP, DOMINGUEZ-ESCRIG JL, VAZQUEZ F, ANGULO J, LOPEZ FJ, De la IGLESIA R, ROMERO J. Cognitive function in patients with prostate cancer receiving luteinizing hormone-releasing hormone analogues: a prospective, observational, multicenter study. Int J Radiat Oncol Biol Phys. 2017;98:590–594. doi: 10.1016/j.ijrobp.2017.02.219. PubMed DOI
MRAZIK M, DOMBROWSKI SC. The neurobiological foundations of giftedness. Roeper Rev. 2010;32:224–234. doi: 10.1080/02783193.2010.508154. DOI
NATHAN L, SHI W, DINH H, MUKHERJEE TK, WANG X, LUSIS AJ, CHAUDHURI G. Testosterone inhibits early atherogenesis by conversion to estradiol: critical role of aromatase. Proc Natl Acad Sci U S A. 2001;98:3589–3593. doi: 10.1073/pnas.051003698. PubMed DOI PMC
O’BOYLE MW, ALEXANDER JE, BENBOW CP. Enhanced right hemisphere activation in the mathematically precocious: a preliminary EEG investigation. Brain Cogn. 1991;17:138–153. doi: 10.1016/0278-2626(91)90073-H. PubMed DOI
O’CONNOR DB, ARCHER J, HAIR WM, WU FC. Activational effects of testosterone on cognitive function in men. Neuropsychologia. 2001;39:1385–1394. doi: 10.1016/S0028-3932(01)00067-7. PubMed DOI
OERTER KE, URIARTE MM, ROSE SR, BARNES KM, CUTLER GB., JR Gonadotropin secretory dynamics during puberty in normal girls and boys. J Clin Endocrinol Metab. 1990;71:1251–1258. doi: 10.1210/jcem-71-5-1251. PubMed DOI
OSTATNIKOVA D, CELEC P, PUTZ Z, HODOSY J, SCHMIDT F, LAZNIBATOVA J, KUDELA M. Intelligence and salivary testosterone levels in prepubertal children. Neuropsychologia. 2007;45:1378–1385. doi: 10.1016/j.neuropsychologia.2006.10.018. PubMed DOI
OSTATNIKOVA D, HODOSY J, SKOKNOVA M, PUTZ Z, KUDELA M, CELEC P. Spatial abilities during the circalunar cycle in both sexes. Learn Indiv Differ. 2010;20:484–487. doi: 10.1016/j.lindif.2010.05.004. DOI
OSTATNIKOVA D, KUBRANSKA A, MARCINCAKOVA V, PIVOVARCIOVA A, BABKOVA-DURDIAKOVA J. Neuroendocrine contribution to autism etiology. Act Nerv Super Rediviva. 2016;58:65–68.
OSTATNIKOVA D, LAZNIBATOVA J, PUTZ Z, MATASEJE A, DOHNANYIOVA M, PASTOR K. Salivary testosterone levels in intellectually gifted and non-intellectually gifted preadolescents: an exploratory study. High Abil Stud. 2000;11:41–54. doi: 10.1080/713669174. DOI
OSTATNIKOVA D, LAZNIBATOVA J, PUTZ Z, MATASEJE A, DOHNANYIOVA M, PASTOR K. Biological aspects of intellectual giftedness. Studia Psychol. 2002;44:3–13.
PETERING RC, BROOKS NA. Testosterone therapy: Review of clinical applications. Am Fam Physician. 2017;96:441–449. PubMed
PHOENIX CH, GOY RW, GERALL AA, YOUNG WC. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology. 1959;65:369–382. doi: 10.1210/endo-65-3-369. PubMed DOI
PINTZKA CW, EVENSMOEN HR, LEHN H, HABERG AK. Changes in spatial cognition and brain activity after a single dose of testosterone in healthy women. Behav Brain Res. 2016;298:78–90. doi: 10.1016/j.bbr.2015.10.056. PubMed DOI
PIVOVARCIOVA A, HNILICOVA S, OSTATNIKOVA D, MACE FC. Testosterone and explosive aggression in autism spectrum disorders. Neuro Endocrinol Lett. 2014;35:553–559. PubMed
PIVOVARCIOVA A, HNILICOVA S, OSTATNIKOVA D, MACE FC. Bio-behavioral model of aggression in autism spectrum disorders-pilot study. Bratisl Lek Listy. 2015;116:702–706. doi: 10.4149/BLL_2015_137. PubMed DOI
PUTS DA, CARDENAS RA, BAILEY DH, BURRISS RP, JORDAN CL, BREEDLOVE SM. Salivary testosterone does not predict mental rotation performance in men or women. Horm Behav. 2010;58:282–289. doi: 10.1016/j.yhbeh.2010.03.005. PubMed DOI
RAY WJ, NEWCOMBE N, SEMON J, COLE PM. Spatial abilities, sex differences and EEG functioning. Neuropsychologia. 1981;19:719–722. doi: 10.1016/0028-3932(81)90010-5. PubMed DOI
REINBERG A, LAGOGUEY M, CHAUFFOURNIER JM, CESSELIN F. Circannual and circadian rhythms in plasma testosterone in five healthy young Parisian males. Acta Endocrinol (Copenh) 1975;80:732–734. doi: 10.1530/acta.0.0800732. PubMed DOI
RITCHIE SJ, COX SR, SHEN X, LOMBARDO MV, REUS LM, ALLOZA C, HARRIS MA, ALDERSON HL, HUNTER S, NEILSON E, LIEWALD DCM, AUYEUNG B, WHALLEY HC, LAWRIE SM, GALE CR, BASTIN ME, McINTOSH AM, DEARY IJ. Sex differences in the adult human brain: evidence from 5216 UK biobank participants. Cereb Cortex. 2018;28:2959–2975. doi: 10.1093/cercor/bhy109. PubMed DOI PMC
ROMEO RD, RICHARDSON HN, SISK CL. Puberty and the maturation of the male brain and sexual behavior: recasting a behavioral potential. Neurosci Biobehav Rev. 2002;26:381–391. doi: 10.1016/S0149-7634(02)00009-X. PubMed DOI
RUIGROK AN, SALIMI-KHORSHIDI G, LAI MC, BARON-COHEN S, LOMBARDO MV, TAIT RJ, SUCKLING J. A meta-analysis of sex differences in human brain structure. Neurosci Biobehav Rev. 2014;39:34–50. doi: 10.1016/j.neubiorev.2013.12.004. PubMed DOI PMC
RYLAARSDAM L, GUEMEZ-GAMBOA A. Genetic causes and modifiers of autism spectrum disorder. Front Cell Neurosci. 2019;13 doi: 10.3389/fncel.2019.00385. PubMed DOI PMC
SANDERS B, SOARES MP. Sexual maturation and spatial ability in college students. Dev Psychol. 1986;22:199–203. doi: 10.1037/0012-1649.22.2.199. DOI
SANDIN S, LICHTENSTEIN P, KUJA-HALKOLA R, HULTMAN C, LARSSON H, REICHENBERG A. The heritability of autism spectrum disorder. JAMA. 2017;318:1182–1184. doi: 10.1001/jama.2017.12141. PubMed DOI PMC
SHUTE VJ, PELLEGRINO JW, HUBERT L, REYNOLDS RW. The relationship between androgen levels and human spatial abilities. Bull Psychon Soc. 1983;21:465–468. doi: 10.3758/BF03330010. DOI
SCHMIDTOVA E, KELEMENOVA S, CELEC P, FICEK A, OSTATNIKOVA D. Polymorphisms in genes involved in testosterone metabolism in Slovak autistic boys. Endocrinologist. 2010;20:245–249. doi: 10.1097/TEN.0b013e3181f661d2. DOI
SCHULZ KM, ZEHR JL, SALAS-RAMIREZ KY, SISK CL. Testosterone programs adult social behavior before and during, but not after, adolescence. Endocrinology. 2009;150:3690–3698. doi: 10.1210/en.2008-1708. PubMed DOI PMC
SKLAR P, SVANTESSON O, REICHENBERG A, HULTMAN CM, DEVLIN B, ROEDER K, BUXBAUM JD, JIANG YH, YUEN RK, JIN X, WANG M, CHEN N, WU X, JU J, MEI J, SHI Y, HE M, WANG G, LIANG J, WANG Z, ET AL. Detection of clinically relevant genetic variants in autism spectrum disorder by whole-genome sequencing. Nat Genet. 2013;93:249–263. doi: 10.1016/j.ajhg.2013.06.012. PubMed DOI PMC
SMITH RP, COWARD RM, KOVAC JR, LIPSHULTZ LI. The evidence for seasonal variations of testosterone in men. Maturitas. 2013;74:208–212. doi: 10.1016/j.maturitas.2012.12.003. PubMed DOI
SUCHONOVA M, BORBELYOVA V, RENCZES E, KONECNA B, VLKOVA B, HODOSY J, OSTATNIKOVA D, CELEC P. Does the 2nd and 4th digit ratio reflect prenatal androgen exposure? Bratisl Lek Listy. 2019;120:703–710. doi: 10.4149/BLL_2019_119. PubMed DOI
TAN U, TAN M. Curvelinear correlations between total testosterone levels and fluid intelligence in men and women. Int J Neurosci. 1998;95:77–83. doi: 10.3109/00207459809000651. PubMed DOI
TAO M, YANG D, LIU W. Learning effect and its prediction for cognitive tests used in studies on indoor environmental quality. Energy Buildings. 2019;197:87–98. doi: 10.1016/j.enbuild.2019.05.044. DOI
TORDJMAN S, FERRARI P, SULMONT V, DUYME M, ROUBERTOUX P. Androgenic activity in autism. Am J Psychiatry. 1997;154:1626–1627. doi: 10.1176/ajp.154.11.1626-a. PubMed DOI
VUOKSIMAA E, KAPRIO J, ERIKSSON CJ, ROSE RJ. Pubertal testosterone predicts mental rotation performance of young adult males. Psychoneuroendocrinology. 2012;37:1791–1800. doi: 10.1016/j.psyneuen.2012.03.013. PubMed DOI PMC
WABER DP. Sex differences in cognition: a function of maturation rate? Science. 1976;192:572–574. doi: 10.1126/science.1257795. PubMed DOI
WILSON CA, DAVIES DC. The control of sexual differentiation of the reproductive system and brain. Reproduction. 2007;133:331–359. doi: 10.1530/REP-06-0078. PubMed DOI
WITELSON SF, NOWAKOWSKI RS. Left out axons make men right: a hypothesis for the origin of handedness and functional asymmetry. Neuropsychologia. 1991;29:327–333. doi: 10.1016/0028-3932(91)90046-B. PubMed DOI
WRIGHT CL, HOFFMAN JH, McCARTHY MM. Evidence that inflammation promotes estradiol synthesis in human cerebellum during early childhood. Transl Psychiatry. 2019;9:58. doi: 10.1038/s41398-018-0363-8. PubMed DOI PMC
XU XJ, ZHANG HF, SHOU XJ, LI J, JING WL, ZHOU Y, QIAN Y, HAN SP, ZHANG R, HAN JS. Prenatal hyperandrogenic environment induced autistic-like behavior in rat offspring. Physiol Behav. 2015;138:13–20. doi: 10.1016/j.physbeh.2014.09.014. PubMed DOI
YAFFE K, EDWARDS ER, LUI LY, ZMUDA JM, FERRELL RE, CAULEY JA. Androgen receptor CAG repeat polymorphism is associated with cognitive function in older men. Biol Psychiatry. 2003;54:943–946. doi: 10.1016/S0006-3223(03)00115-X. PubMed DOI
YPSILANTI A, GANOU M, KOIDOU I, GROUIOS G. Digit ratio (2D:4D) in individuals with intellectual disability: investigating the role of testosterone in the establishment of cerebral lateralisation. Laterality. 2008;13:527–544. doi: 10.1080/13576500802117164. PubMed DOI
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