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Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence
Open accessAbstract
Humans have systematic sex differences in brain-related behavior, cognition, and pattern of mental illness risk. Many of these differences emerge during adolescence, a developmental period of intense neurostructural and endocrine change. Here, by creating "movies" of sexually dimorphic brain development using longitudinal in vivo structural neuroimaging, we show regionally specific sex differences in development of the cerebral cortex during adolescence. Within cortical subsystems known to underpin domains of cognitive behavioral sex difference, structural change is faster in the sex that tends to perform less well within the domain in question. By stratifying participants through molecular analysis of the androgen receptor gene, we show that possession of an allele conferring more efficient functioning of this sex steroid receptor is associated with "masculinization" of adolescent cortical maturation. Our findings extend models first established in rodents, and suggest that in humans too, sex and sex steroids shape brain development in a spatiotemporally specific manner, within neural systems known to underpin sexually dimorphic behaviors.
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Items 101–200 of 276
The Sexual Differentiation of the Human Brain: Role of Sex Hormones Versus Sex Chromosomes
Bakker, J. (2018) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_70 · Cited by 49
“2010), cortical thickness development (Raznahan et al. 2010), and WM growth (Perrin et al.”
BackgroundMapping cortical anatomy in preschool aged children with autism using surface-based morphometry
Raznahan, A., Lenroot, R., Thurm, A. E., Gozzi, M., Hanley, A., Spence, S. J., Swedo, S. E., & Giedd, J. N. (2012) · NeuroImage Clinical · doi:10.1016/j.nicl.2012.10.005 · Cited by 50
“…et al., 2008) SBM method to fi ne-map CT and SA across the cortical sheet, we tested the hypothesis that regions of the cortex previously reported as structurally abnormal in older groups with ASD (Chung et al., 2005; Ecker et al., 2010; Hadjikhani et al., 2006; Raznahan et al., 2010b) (see Fig.”
BackgroundMethodInfluentialPrenatal and pubertal testosterone affect brain lateralization
Beking, T., Geuze, R. H., van Faassen, M. H. J. R., Kema, I. P., Kreukels, B. P. C., & Groothuis, T. G. G. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.10.027 · Cited by 48
“Raznahan et al. (2010) investigated the relation between the efficiency of the androgen receptor and grey matter thickness in the brain.”
InfluentialGettler, L. T., Ryan, C. P., Eisenberg, D. T. A., Rzhetskaya, M., Hayes, M. G., Feranil, A. B., Bechayda, S. A., & Kuzawa, C. W. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.10.012 · Cited by 45
Bao, J., Mahaman, Y. A. R., Liu, R., Wang, J., Zhang, Z., Zhang, B., & Wang, X. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00347 · Cited by 47
“…evidence indicates that there are some differences in structure, development, enzyme activity, and chemistry of the central nervous system (CNS) between female and male mammals (Becker et al., 2005; Cahill, 2006; McCarthy, 2009; Raznahan et al., 2010; Ruigrok et al., 2014; Forger et al., 2016).”
BackgroundLongitudinal Development of Hormone Levels and Grey Matter Density in 9 and 12-Year-Old Twins
Brouwer, R. M., Koenis, M. M. G., Schnack, H. G., van Baal, G. C. M., van Soelen, I. L. C., Boomsma, D. I., & Pol, H. E. H. (2015) · Behavior Genetics · doi:10.1007/s10519-015-9708-8 · Cited by 44
“2013b), and testosterone receptors (Raznahan et al. 2010).”
InfluentialHepatic Cannabinoid Signaling in the Regulation of Alcohol-Associated Liver Disease
Yang, K. (2021) · Alcohol research · doi:10.35946/arcr.v41.1.11 · Cited by 52
Lepage, J., Mazaika, P. K., Hong, D. S., Raman, M. M., & Reiss, A. L. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs195 · Cited by 44
Sex-related differences in intrinsic brain dynamism and their neurocognitive correlates
de Lacy, N., McCauley, E., Kutz, J. N., & Calhoun, V. D. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116116 · Cited by 42
Testosterone, Cortisol and Financial Risk-Taking
Herbert, J. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00101 · Cited by 47
“Furthermore, the frontal lobes mature later in boys than girls (Lenroot and Giedd, 2010; Raznahan et al., 2010; Mills et al., 2014).”
BackgroundRovio, S., Pahkala, K., Nevalainen, J., Juonala, M., Salo, P., Kähönen, M. A. P., Hutri‐Kähönen, N., Lehtimäki, T. J., Jokinen, E. V., Laitinen, T. P., et al. (2015) · Neuropsychology · doi:10.1037/neu0000239 · Cited by 39
Sex differences in the developmental neuroscience of adolescent substance use risk
Heitzeg, M. M., Hardee, J. E., & Beltz, A. M. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.01.020 · Cited by 41
Green, T., Naylor, P. E., & Davies, W. (2017) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-017-9205-x · Cited by 38
“The structure of the parietal lobe [16-18], 147”
BackgroundIncome inequality, gene expression, and brain maturation during adolescence
Parker, N., Wong, A. P., Leonard, G. T., Perron, M., Pike, G. B., Richer, L., Veillette, S., Pausová, Z., & Paus, T. (2017) · Scientific Reports · doi:10.1038/s41598-017-07735-2 · Cited by 39
du Plessis, M. R., Smeekens, S., Cillessen, A. H. N., Whittle, S., & Güroğlu, B. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.02706 · Cited by 45
“Finally, we took sex into account, given (a) sex differences in peer victimization, (b) sex differences in neural development (Raznahan et al., 2010) and in function of the vlPFC (Vijayakumar et al.”
BackgroundMethodThe MRi-Share database: brain imaging in a cross-sectional cohort of 1870 university students
Tsuchida, A., Laurent, A., Crivello, F., Petit, L., Joliot, M., Pepe, A., Beguedou, N., Gueye, M.-F., Verrecchia, V., Nozais, V., et al. (2021) · Brain Structure and Function · doi:10.1007/s00429-021-02334-4 · Cited by 40
Kilpatrick, L. A., Holmberg, M., Manzouri, A., & Savic, I. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14420 · Cited by 35
“Additionally, we did not carry out correlational analyses between sex hormone levels and the degree of change in Cth, as the effects of sex hormones on the brain are complex and plasma levels do not linearly reflect the specific effects on the brain receptors (e.g., the effect of same amount of testosterone on the and…”
BackgroundShahab, S., Stefanik, L., Foussias, G., Lai, M., Anderson, K. K., & Voineskos, A. N. (2017) · Schizophrenia Bulletin · doi:10.1093/schbul/sbx049 · Cited by 34
“Studies fulfilling the following criteria were included: (1) included individuals with a diagnosis of schizophrenia, (2) included a control group of healthy individuals, (3) included both sexes in the patient and the control groups, (4) used diffusion tensor imaging, and (5) involved analyzing metrics of white matter…”
MethodHummer, T. A., Wang, Y., Kronenberger, W. G., Dunn, D. W., & Mathews, V. P. (2014) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2014.11.009 · Cited by 36
“Furthermore, although sex differences in brain development have been examined previously (Silveri et al., 2006; Asato et al., 2010; Raznahan et al., 2010), their relationship to cognitive and emotional development has yet to be fully integrated into this research.”
BackgroundAlarcón, G., Cservenka, A., Fair, D. A., & Nagel, B. J. (2014) · Brain Research · doi:10.1016/j.brainres.2014.09.057 · Cited by 34
“…and gray and white matter volumes in adolescent boys (Peper et al., 2009; Perrin et al., 2008), and regional effects of androgen receptor function have been related to cortical thinning of frontal brain areas (Raznahan et al., 2010), highlighting the relevance of testosterone on brain maturation.”
Considering the role of adolescent sex steroids in schizophrenia
Owens, S. J., Murphy, C. E., Purves-Tyson, T. D., Weickert, T. W., & Weickert, C. S. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12538 · Cited by 33
“Further, a longitudinal study examining cortical maturation found that a specific AR genotype is associated with a greater rate of region-specific cortical grey matter thinning during adolescence in both males and females (22).”
Fetal and Postnatal Development of the Cortex: MRI and Genetics
Dubois, J., & Dehaene‐Lambertz, G. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-397025-1.00194-9 · Cited by 33
“During adolescence, the pattern of differences in cortical thickness between genders accelerates, notably a wave of maturation sweeps frontal subregions with a delay in males compared with females (Raznahan et al., 2010) probably related to the earlier female puberty.”
BackgroundInfluentialCerebral sex dimorphism and sexual orientation
Manzouri, A., & Savić, I. (2017) · Human Brain Mapping · doi:10.1002/hbm.23908 · Cited by 34
“…in life (Bramen et al., 2012; Nguyen, 2017; Nguyen et al., 2013; Nopoulos, Flaum, O’leary, & Andreasen, 2000; Savic & Arver, 2014), or changes in androgen receptor binding properties, which may occur, for example, as an effect of different CAG repeats (Paus et al., 2010; Raznahan et al., 2010).”
BackgroundContributions of neuroimaging to understanding sex differences in cocaine abuse.
Andersen, M. L., Sawyer, E. K., & Howell, L. L. (2011) · Experimental and Clinical Psychopharmacology · doi:10.1037/a0025219 · Cited by 34
“Raznahan et al. (2010) recently created “movies” of brain development in adolescents using longitudinal in vivo structural neuroimaging, demonstrating that regionally-specific sex-differences occur during development of the cerebral cortex in adolescence.”
BackgroundThe emergence of long-range language network structural covariance and language abilities
Qi, T., Schaadt, G., Cafiero, R., Bräuer, J., Skeide, M. A., & Friederici, A. D. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.02.014 · Cited by 31
“Therefore, longitudinal studies are required to sufficiently examine the dynamic trajectory of the brain's structural covariance during development (Raznahan et al., 2010).”
BackgroundCirculating androgens correlate with resting-state MRI in transgender men
Mueller, S. C., Wierckx, K., Jackson, K., & T'Sjoen, G. G. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.07.212 · Cited by 31
“For example, inferior frontal gyrus volume (IFG, BA44/45) is modulated by the androgen receptor (AR) gene in women (Raznahan et al., 2010), IFG is larger in women than in men (Ruigrok et al., 2014), and is an area that displays sex differences in activation patterns in prefrontally-mediated tasks…”
BackgroundInfluentialPubertal testosterone correlates with adolescent impatience and dorsal striatal activity
Laube, C., Lorenz, R. C., & van den Bos, W. (2019) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2019.100749 · Cited by 33
“In addition, gonadal hormones have been associated with variation in the speed of brain maturation during adolescence (Raznahan et al., 2010).”
BackgroundBrumback, T., Arbel, Y., Donchin, E., & Goldman, M. S. (2012) · Psychophysiology · doi:10.1111/j.1469-8986.2012.01444.x · Cited by 29
“It is more likely, therefore, that the gender differences were a result of differences in the underlying biology resulting in greater efficiency of processing in girls in our sample (e.g., Peper et al., 2011; Raznahan et al., 2010, 2011).”
ResultClarkson, T., Kang, E., Capriola-Hall, N. N., Lerner, M. D., Jarcho, J. M., & Prinstein, M. J. (2019) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374416.2019.1678167 · Cited by 29
“This is consistent with literature suggesting the continued development of brain regions is positively associated with social processing into early adulthood (Anderson, Bechara, Damasio, Tranel, & Damasio, 1999; Boehme et al., 2017; Cicchetti, et al., 2016; Raznahan et al., 2010).”
ResultEvolutionary perspective on sex differences in the expression of neurological diseases
Geary, D. C. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.06.001 · Cited by 27
Ravindranath, O., Calabro, F. J., Foran, W., & Luna, B. (2022) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2022.101162 · Cited by 27
“However, some human studies have shown that sex differences in the structure of the lateral PFC, such as cortical thickness, emerge at the onset of puberty (Nelson and Guyer, 2011; Raznahan et al., 2010), suggesting that puberty may have a unique influence in this area of the brain.”
Sex differences in resting-state cerebral activity alterations in internet gaming disorder
Sun, Y., Wang, Y., Han, X., Jiang, W., Ding, W., Cao, M., Du, Y., Lin, F., Xu, J., & Zhou, Y. (2018) · Brain Imaging and Behavior · doi:10.1007/s11682-018-9955-4 · Cited by 27
The sleep EEG topography in children and adolescents shows sex differences in language areas
Ringli, M., Kurth, S., Huber, R., & Jenni, O. G. (2013) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2013.04.008 · Cited by 25
Sex Differences in the Stability of Self-Regulation Across Childhood
Coyne, M. A., Vaske, J. C., Boisvert, D. L., & WRIGHT, J. P. (2015) · Journal of Developmental and Life-Course Criminology · doi:10.1007/s40865-015-0001-6 · Cited by 25
“’s [50] analysis of 284 healthy individuals from ages 9 to 22 showed that regions of the frontal lobes were slower to mature (as measured by loss of cortical thickness) for males than for females.”
BackgroundSex differences in brain structure among adolescents with bipolar disorder
Mitchell, R. H. B., Metcalfe, A. W. S., Islam, A. H., Toma, S., Patel, R. R., Fıksenbaum, L., Korczak, D. J., MacIntosh, B. J., & Goldstein, B. I. (2018) · Bipolar Disorders · doi:10.1111/bdi.12663 · Cited by 26
Measures of Brain Connectivity and Cognition by Sex in US Children
Tomasi, D. G., & Volkow, N. D. (2023) · JAMA Network Open · doi:10.1001/jamanetworkopen.2023.0157 · Cited by 27
Editorial: Developmental neuroscience comes of age
Leckman, J. F., & March, J. S. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2011.02378.x · Cited by 28
Socio-cultural effects on children's initiation of joint attention
Gavrilov, Y., Rotem, S., Ofek, R., & Geva, R. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00286 · Cited by 26
“Girls seem to be more attuned to socio-cultural contexts and to social expectations than boys, as also enabled and manifested by the earlier maturation of the VFPC among girls (Raznahan et al., 2010).”
BackgroundKelly, K. R., DeSimone, K., Gallie, B. L., & Steeves, J. K. E. (2014) · NeuroImage Clinical · doi:10.1016/j.nicl.2014.11.020 · Cited by 26
“, 2010) and peaks between 8 and 9 years of age (Raznahan et al., 2010).”
BackgroundSullivan, E. V., Lane, B., Kwon, D., Meloy, M. J., Tapert, S. F., Brown, S. A., Colrain, I. M., Baker, F. C., Bellis, M. D. D., Clark, D. B., et al. (2016) · Brain Imaging and Behavior · doi:10.1007/s11682-016-9634-2 · Cited by 24
“Despite the growing number of prospective studies of brain development and themultifactorial data collected in large samples (Raznahan et al. 2011; Sowell et al. 2004; Sullivan et al. 2011; Storsve et al. 2014; Shaw et al. 2008; Wierenga et al. 2014; Raznahan et al. 2010; Bava et al. 2010) (for review, Stiles and Jern…”
Bart, C. P., Titone, M. K., Ng, T. H., Nusslock, R., & Alloy, L. B. (2021) · Clinical Psychology Review · doi:10.1016/j.cpr.2021.102035 · Cited by 31
“In adolescence, females reach peak structural development in both the striatum and PFC quicker than boys (Raznahan et al., 2010, 2014), and these changes may be why we see sex differences in different risk pathways to SUDs (for review see Heitzeg, Hardee, & Beltz, 2018).”
Long-Term Impacts of Post-weaning Social Isolation on Nucleus Accumbens Function
Bendersky, C. J., Milian, A. A., Andrus, M. D., Torre, U. D. L., & Walker, D. M. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.745406 · Cited by 24
Adolescence, créativité et transformation de Soi
Barbot, B., & Lubart, T. (2012) · Enfance · doi:10.4074/s0013754512003059 · Cited by 33
Ho, A., Villacis, A. J., Svirsky, S. E., Foilb, A. R., & Romeo, R. D. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20987 · Cited by 22
“Although it is still unclear what factor(s) mediate these morphological changes during puberty, a few studies have provided evidence that gonadal hormones may be involved (Nunez et al., 2002; Cooke et al., 2007; Perrin et al., 2008; Raznahan et al., 2010).”
BackgroundWhat can allostasis tell us about anabolic–androgenic steroid addiction?
Hildebrandt, T., Yehuda, R., & Alfano, L. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000393 · Cited by 23
“The most relevant of these adolescent changes to our proposed model involves the remodeling of the stress system neurons that are activated by androgens and their metabolites (Raznahan et al., 2010).”
BackgroundDalmida, S. G., Aduloju-Ajijola, N., Clayton-Jones, D. L., Thomas, T. L., Erazo-Toscano, R., Lewis, R., Fleming, T., Taylor, S., & Lunyong, M. (2016) · Journal of Transcultural Nursing · doi:10.1177/1043659616678660 · Cited by 23
Schneider, M. R., Adler, C. M., Whitsel, R. M., Weber, W., Mills, N. P., Bitter, S. M., Eliassen, J. C., Strakowski, S. M., & DelBello, M. P. (2012) · PubMed · Cited by 21
Lian, J., Pan, B., & Deng, C. (2016) · Pharmacological Reports · doi:10.1016/j.pharep.2016.06.003 · Cited by 20
“In view of the fact that there are gender differences in both brain development and antipsychotic effects in adults [6], it is very important to investigate whether there is gender difference in the effects of APDs on dopamine and 5-HT neurotransmission; to date, no study has been published in female juvenile animals.”
Huang, R., Geng, Z., & Siraj, I. (2022) · Early Education and Development · doi:10.1080/10409289.2022.2056695 · Cited by 27
“Neuroimaging studies have suggested that there are significant gender differences in the development of brain regions that are implicated in self-regulation, such as the frontal and temporal lobes (Cowell et al., 1994; Raznahan et al., 2010).”
BackgroundKaller, C. P., Heinze, K., Mader, I., Unterrainer, J. M., Rahm, B., Weiller, C., & Schumacher, L. V. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.08.032 · Cited by 20
“Gonadal hormones are generally known to affect brain organization (e.g., Raznahan et al., 2010; Witte et al., 2010; for a review, see Peper et al., 2011 ) and the middle frontal gyrus is a region with high density of sex hormone receptors during developmentally critical stages (Goldstein et al.,…”
Maturational Changes in Human Dorsal and Ventral Visual Networks
Ciesielski, K. T. R., Stern, M. E., Diamond, A. D., Khan, S., Busa, E., Goldsmith, T. E., van der Kouwe, A. J. W., Fischl, B. R., & Rosen, B. R. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz053 · Cited by 19
Sex Differences in Brain and Behavioral Development
Beltz, A. M., Blakemore, J. E., & Berenbaum, S. A. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397267-5.00064-9 · Cited by 21
Cortical thickness and prosocial behavior in school-age children: A population-based MRI study
Thijssen, S., Wildeboer, A., Muetzel, R. L., Bakermans‐Kranenburg, M. J., Marroun, H. E., Albert Hofman, D., Jaddoe, V. W. V., van der Lugt, A., Verhulst, F. C., Tiemeier, H. W., et al. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1014063 · Cited by 18
“As gender differences in prosocial behavior and cortical development have been well characterized in the literature (Baillargeon et al., 2011; Eisenberg et al., 2007; Mutlu et al., 2013; Raznahan et al., 2010), we expect that the association between cortical thickness and prosocial behavior may be moderated by gender.”
BackgroundSex differences in brain and behavioral development
Beltz, A. M., Kelly, D. P., & Berenbaum, S. A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814411-4.00027-5 · Cited by 21
Sarma, M. S., Kuo, P. X., Bechayda, S. A., Kuzawa, C. W., & Gettler, L. T. (2017) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.11.029 · Cited by 18
Black, S. R., Lerner, M. D., Shirtcliff, E. A., & Klein, D. N. (2017) · Biological Psychology · doi:10.1016/j.biopsycho.2017.11.004 · Cited by 18
“There is also evidence for sex differences in androgen receptors in the brain (Raznahan et al., 2010; Tsai, Taniguchi, Samoza, & Ridder, 2015), which could lead to dissimilar endocrine reactions to stress exposure in males versus females.”
BackgroundMorphologic alterations of the fear circuitry: the role of sex hormones and oral contraceptives
Brouillard, A., Davignon, L., Turcotte, A.-M., & Marin, M. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1228504 · Cited by 21
Weisinger, B., GREENSTEIN, D. K., Mattai, A. A., CLASEN, L. S., Lalonde, F. M., Feldman, S. J., Miller, R., Tossell, J. W., Vyas, N. S., Stidd, R., et al. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr049 · Cited by 17
Wiglesworth, A., Fiecas, M. J. A., Xu, M., Neher, A., Padilla, L. E., Carosella, K. A., Roediger, D. J., Mueller, B. A., Luciana, M. M., Klimes‐Dougan, B., et al. (2023) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2022.101195 · Cited by 19
“There is evidence of spatial heterogeneity of CT change between sexes; although males demonstrate increased cortex thickness in a number of frontal regions by age 9, by age 22 they demonstrate accelerated cortical thinning compared to females (Raznahan et al., 2010).”
Nuruddin, S., Wojniusz, S., Ropstad, E., Krogenæs, A., Evans, N. P., Robinson, J. E., Solbakk, A., Amiry-Moghaddam, M. R., & Haraldsen, I. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.12.027 · Cited by 17
Determinant factors of gender identity: a commentary
Liao, L.-M., Audi, L., Magritte, E., Meyer-Bahlburg, H. F. L., & Quigley, C. A. (2012) · Journal of Pediatric Urology · doi:10.1016/j.jpurol.2012.09.009 · Cited by 23
Wang, Y., Zhu, D., Zhao, L., Wang, X., Zhang, Z., Hu, B., Wu, D., & Zheng, W. (2024) · NeuroImage · doi:10.1016/j.neuroimage.2024.120660 · Cited by 17
“Accumulating evidence has documented sex differences in brain anatomy from early childhood to late adulthood (Efstathios et al., 2017; Raznahan et al., 2010).”
BackgroundTransient sex differences during adolescence on auditory perceptual tasks
Huyck, J. J., & Wright, B. A. (2017) · Developmental Science · doi:10.1111/desc.12574 · Cited by 16
Tan, G. C.-Y., Chu, C., Lee, Y. T., Tan, C. C. K., Ashburner, J., Wood, N. W., & Frackowiak, R. S. J. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117087 · Cited by 17
Mueller, S. C. (2013) · Journal of Neuroendocrinology · doi:10.1111/jne.12048 · Cited by 15
Abé, C., Rahman, Q., Långström, N., Rydén, E., Ingvar, M., & Landén, M. (2018) · Brain and Behavior · doi:10.1002/brb3.998 · Cited by 17
Gautam, P., Cherbuin, N., Sachdev, P. S., Wen, W. X., & Anstey, K. J. (2013) · Neuroradiology · doi:10.1007/s00234-013-1144-y · Cited by 15
“Longitudinal studies of children show that cortical thickness changes are dynamic with reports of both regional increases as well as decreases in cortical thickness over time until puberty and young adulthood [17–20].”
BackgroundThe influence of pubertal maturation on antisaccade performance
Ordaz, S. J., Fritz, B. L., Forbes, E. E., & Luna, B. (2017) · Developmental Science · doi:10.1111/desc.12568 · Cited by 14
“Further, developmental neuroimaging studies have shown that genotypic variability in androgen receptor, which relates to capacity for testosterone to exert effects on the brain, alters the rate of thinning in inhibitory control- relevant areas of cortex (Raznahan et al., 2010).”
BackgroundInfluentialCampbell, C. E., Mezher, A. F., Tyszka, J. M., Nagel, B. J., Eckel, S. P., & Herting, M. M. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2021.105604 · Cited by 14
Grey matter volume correlates with virtual water maze task performance in boys with androgen excess
Mueller, S. C., Merke, D. P., Leschek, E., Fromm, S. J., Grillon, C., Cornwell, B. R., VanRyzin, C., & Ernst, M. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.09.022 · Cited by 14
“Grey matter volume (GMV) of the brain has been shown to be influenced by sex and age (Neufang et al., 2009; Peper et al., 2009; Raznahan et al., 2010).”
Effects of Adult Female Rat Androgenization on Brain Morphology and Metabolomic Profile
Pérez-Laso, C., Cerdán, S., Junqué, C., Gómez, Á., Ortega, E., Mora, M., Avendaño, C., Gómez‐Gil, E., del Cerro, M. C. R., & Guillamón, A. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx163 · Cited by 14
“Under physiological and pathological conditions, testosterone is known to decrease cortical volume and thickness and the volume of subcortical structures in humans (Merke et al. 2003; Raznahan et al. 2010; Bramen et al. 2011; Peper et al. 2011).”
BackgroundMultimodal MRI suggests that male homosexuality may be linked to cerebral midline structures
Manzouri, A., & Savic, I. (2018) · PLoS ONE · doi:10.1371/journal.pone.0203189 · Cited by 14
“Given the normal testosterone levels in our HoM (S1 Supplemental Information, S1 Table), such a tentative hypoandrogenization might mirror a weaker androgen receptor expression or function [62].”
BackgroundRoeske, J., Long, X., Perdue, M. V., Long, M., Geeraert, B., Ghasoub, M., Yeates, K. O., & Lebel, C. A. (2025) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2025.101568 · Cited by 18
“Our observation of earlier PFC maturation in females aligns with work that examined females and males separately (Brain Development Cooperative Group, 2012; Frere et al., 2020; Len-root et al., 2007; Raznahan et al., 2010; Remer et al., 2017).”
Sex Differences in Adolescent Neurobiological Risk for Substance Use and Substance Use Disorders
Dir, A. L., & Hulvershorn, L. A. (2019) · Current Addiction Reports · doi:10.1007/s40429-019-00276-w · Cited by 14
Parker, N., Dídac Vidal-piñeiro, A., French, L., Shin, J., Adams, H. H. H., Brodaty, H., Cox, S. R., Deary, I. J., Fjell, A. M., Frenzel, S., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz108 · Cited by 14
“From childhood through to early adulthood, there is a combination of a rapid decline in cortical thickness (Gogtay et al. 2004; Raznahan et al. 2010; Tamnes et al. 2010) concurrent with a unique blend of novel stress exposures and increases in stress- and sex-hormone production (Lupien et al.”
BackgroundCreativity Development of High-Achieving Students
Hemdan, A. H., & Kazem, A. M. (2019) · Creativity Research Journal · doi:10.1080/10400419.2019.1641684 · Cited by 13
“MOHAMED AND KAZEM of the decrease of the grey matter (Raznahan et al., 2010).”
Sex, gender diversity, and brain structure in early adolescence
Torgerson, C. M., Ahmadi, H., Choupan, J., Fan, C. C., Blosnich, J. R., & Herting, M. M. (2024) · Human Brain Mapping · doi:10.1002/hbm.26671 · Cited by 12
“However, cortical thickness has been linked to the length of CAG repeats in the androgen receptor gene — a measure which influences androgen receptor sensitivity (Raznahan et al., 2010; Zitzmann, 2009).”
BackgroundLongitudinal Sex-at-Birth and Age Analyses of Cortical Structure in the ABCD Study
Marshall, A. T., Adise, S., Kan, E., & Sowell, E. R. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1091-24.2025 · Cited by 13
Parenting Styles Predict Future-Oriented Cognition in Children: A Cross-Sectional Study
Sadeghi, S., Ayoubi, S., & Brand, S. (2022) · Children · doi:10.3390/children9101589 · Cited by 11
“There is evidence that the development of the prefrontal cortex occurs later in males than in females, although those of males are consistently greater in volume and thickness [80,81], particularly through adolescence.”
BackgroundThe role of puberty on physical and brain development: A longitudinal study in male Rhesus Macaques
Kovacs-Balint, Z. A., Raper, J., Richardson, R., Gopakumar, A., Kettimuthu, K., Higgins, M. K., Feczko, E., Earl, E., Ethun, K. F., Li, L., et al. (2023) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2023.101237 · Cited by 11
“Altogether, these studies suggest a peak in brain volume growth followed by reduction during puberty (via several cellular processes including grey matter -GM- pruning (Paus et al. 2010; Raznahan et al. 2010; Peper et al. 2011).”
Foland‐Ross, L. C., Ghasemi, E., Wun, V. L., Aye, T., Kowal, K., ROSS, J. L., & Reiss, A. L. (2023) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgad487 · Cited by 11
Neurogenesis in the neonatal rat hippocampus is regulated by sexually dimorphic epigenetic modifiers
Stockman, S. L., Kight, K. E., Bowers, J. M., & McCarthy, M. M. (2022) · Biology of Sex Differences · doi:10.1186/s13293-022-00418-2 · Cited by 13
“Data confirmed the previously reported sex difference in that vehicle-treated males administered BrdU on PN0 and PN1 had more BrdU + cells in the DG granule cell layer than vehicle treated female littermates on PN2 (t[10] = 5.”
BackgroundResultInfluentialCognitive Development and Aging
Rapp, P. R., & Bachevalier, J. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-385870-2.00043-3 · Cited by 12
From mice to men: Biological factors in the development of sexuality
LeVay, S. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.02.002 · Cited by 10
Feraco, T., & Cona, G. (2022) · Intelligence · doi:10.1016/j.intell.2022.101669 · Cited by 11
Westwater, M. L., Mallard, T. T., Warrier, V., Bethlehem, R. A. I., Scheinost, D., Grillon, C., Fletcher, P. C., Seidlitz, J., & Ernst, M. (2023) · Nature Mental Health · doi:10.1038/s44220-023-00101-4 · Cited by 11
“developmental characteristics that have been previously associated with brain morphometry: age, sex [54,55], intelligence [56], years of parental education, pubertal development [57] and Euler number (see Supplementary Material).”
BackgroundClemens, B., Votinov, M., Puiu, A. A., Schüppen, A., Hüpen, P., Neulen, J., Derntl, B., & Habel, U. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10071454 · Cited by 9
“When it comes to genetic or hormonal mechanisms causing such neurodevelopmental differences in the first place, several studies [21,49] suggested that specific α and β gene polymorphisms of sex hormone receptors are linked to GI.”
BackgroundBagheri‐Nesami, M., & Kamali, M. (2022) · Journal of Nursing and Midwifery Sciences · doi:10.4103/jnms.jnms_97_22 · Cited by 9
Niu, Y., Wang, T., Shan, L., Li, W., Hu, X., Wu, X., & Jin, F. (2020) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10034 · Cited by 9
Owens, S. J., Purves-Tyson, T. D., Webster, M. J., & Weickert, C. S. (2019) · Psychiatry Research · doi:10.1016/j.psychres.2019.112503 · Cited by 9
Can age at sexual maturity act as a predictive biomarker for prodromal negative symptoms?
Ramanathan, S., Miewald, J. M., Montrose, D. M., & Keshavan, M. S. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2015.02.019 · Cited by 9
“In humans, puberty has been associated with changes in gray matter volume (Neufang et al., 2009), density (J. S. Peper et al., 2009), thickness (Raznahan et al., 2010) and white matter development (Ladouceur, 2012; J. Peper, Hulshoff Pol, Crone, & Van Honk, 2011).”
BackgroundInfluentialChen, Y., & Li, C. R. (2022) · Journal of Experimental Psychopathology · doi:10.1177/20438087221080057 · Cited by 8
“Boys and girls showed different patterns in VS volumetric development (Dennison et al., 2013; Raznahan et al., 2010), which may account for higher vulnerability of males to externalizing pathology (Dir & Hulvershorn, 2019).”
BackgroundLiu, D., Shen, L., Tao, Y., Kuang, Y., Cai, L., Wang, D., He, M., Tong, X., Zhou, S., Sun, J., et al. (2019) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2019.4274 · Cited by 8
Description of Neuropsychological Profile in Patients with 22q11 Syndrome
Joga‐Elvira, L., & Sandra, P.-R. (2023) · Genes · doi:10.3390/genes14071347 · Cited by 7
“The first cause is the distribution of the sample; being a sample composed of 70% male subjects, it is known from the literature and functional magnetic resonance imaging (fMRI) studies that males may perform slightly better in certain tasks related to spatial or visuospatial memory due to a higher activation in certa…”
BackgroundAssociations between brain network, puberty, and behaviors in boys with Klinefelter syndrome
Li, R., Foland‐Ross, L. C., Jordan, T. L., Marzelli, M., ROSS, J. L., & Reiss, A. L. (2024) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-024-02501-y · Cited by 7
“Several areas of the brain are densely populated with andro - gen receptors and undergo dynamic changes during puberty in typically developing populations when testosterone sharply increases [25–27].”
Kim, G.-W., Kim, Y., Park, K., & Jeong, G. (2019) · International Journal of Impotence Research · doi:10.1038/s41443-019-0111-5 · Cited by 7
Kollndorfer, K., Novak, A., Nenning, K., Fischmeister, F. P. S., Seidl, R., Langs, G., Kasprian, G. J., Prayer, D., & Bartha, L. (2023) · Frontiers in Psychology · doi:10.3389/fpsyg.2023.1196707 · Cited by 7
“Previous studies have shown that CTh linearly decreases with age in healthy development (Sowell et al., 2004; Raznahan et al., 2010).”
BackgroundLiu, D., Shen, L., Tao, Y., KUANG, Y., CAI, L., Wang, D., He, M., Tong, X., Zhou, S., Sun, J., et al. (2014) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2014.2015 · Cited by 7
“Previous studies have demonstrated that AR is involved in a series of developmental and physiological functions, particularly in male sexual differentiation (7), the maintenance of adolescent sexual maturation (8), sperm production (9) and male sex hormone regulation (10).”
Monahan, K. C., Guyer, A. E., Silk, J. S., Doremus‐Fitzwater, T. L., & Steinberg, L. D. (2016) · Wiley eBooks · doi:10.1002/9781119125556.devpsy219 · Cited by 7
Pharmachosexology: Use of Sex Hormones in Psychiatric Conditions
Fisher, A. D., Ristori, J., & Maggi, M. (2018) · Trends in andrology and sexual medicine · doi:10.1007/978-3-319-68306-5_19 · Cited by 6
Metadata
- Authors
- Raznahan, A., Lee, Y., Stidd, R., Long, R., Greenstein, D., Clasen, L., Addington, A., Gogtay, N., Rapoport, J. L., & Giedd, J. N.
- Affiliations
- King's College London (GB)
- National Institute of Mental Health (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-09-14
- Volume
- 107
- Issue
- 39
- Pages
- 16988-16993
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2947865
- OpenAlex
- W2097394514
- Cited by
- 278
- References
- 55
- Citations by year
- 2026: 7 · 2025: 10 · 2024: 9 · 2023: 17 · 2022: 14 · 2021: 14 · 2020: 22 · 2019: 16 · 2018: 16 · 2017: 26 · 2016: 23 · 2015: 20 · 2014: 20 · 2013: 21 · 2012: 23
- FWCI
- 8.33
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research Portal (King's College London) (submittedVersion)
- Funders
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Sexual Differentiation and Disorders
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Sex and Gender in Healthcare
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- sex differences, androgen signaling, androgen receptor gene, cortical maturation, adolescence, cortical development, sex steroids, masculinization, sex differences in cognition, neuroendocrine development
- MeSH terms
- Adolescent, Adolescent Behavior, Androgens, Animals, Brain Mapping, Cerebral Cortex, Female, Humans, Male, Receptors, Androgen, Sex Characteristics, Sex Factors, Genetic Variation, Signal Transduction, Adolescent Development
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