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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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A meta-analysis of sex differences in human brain structure
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“In recent years, a number of MRI studies have investigated the relationships between structural brain development, gender and puberty (e.g. Raznahan et al., 2010).”
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“Using a longitudinal sample of participants ages 9–22 years, Raznahan et al. (2010) observed differences in cortical maturation, with males demonstrating a thicker cortex in frontopolar regions at younger ages and subsequent greater cortical thinning than females during adolescence.”
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“Second, differing trajectories of structural brain development between males and females during adolescence (Giedd et al., 1999; Raznahan et al., 2010) suggests that averaging results across both sexes might result in noisy data that are not representative of either sex.”
Eliot, L., Ahmed, A., Khan, H., & Patel, J. Y. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.02.026 · Cited by 379
Sexual differentiation of human behavior: Effects of prenatal and pubertal organizational hormones
Berenbaum, S. A., & Beltz, A. M. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.03.001 · Cited by 360
“In cortical areas important for cognition, brain development was found to be faster in the sex that usually performs worse in that domain, and androgen responsivity was linked to ‘‘masculinization’’ of adolescent cortical maturation [132].”
A critical review of sex differences in decision-making tasks: Focus on the Iowa Gambling Task
van den Bos, R., Homberg, J. R., & de Visser, L. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.10.002 · Cited by 348
Review: magnetic resonance imaging of male/female differences in human adolescent brain anatomy
Giedd, J. N., Raznahan, A., Mills, K. L., & Lenroot, R. (2012) · Biology of Sex Differences · doi:10.1186/2042-6410-3-19 · Cited by 339
“In a recently published study [87], we sought to directly assess the spatial convergence between the regions where sex, and sex steroid signaling modulated cortical maturation across human adolescents.”
BackgroundFetal Testosterone Influences Sexually Dimorphic Gray Matter in the Human Brain
Lombardo, M. V., Ashwin, E., Auyeung, B., Chakrabarti, B., Taylor, K., Hackett, G., Bullmore, E. T., & Baron-Cohen, S. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4389-11.2012 · Cited by 302
“, 2002), though the two likely interact (McCarthy et al., 2009; Paus et al., 2010; Raznahan et al., 2010; McCarthy and Arnold, 2011).”
BackgroundLongitudinal four-dimensional mapping of subcortical anatomy in human development
Raznahan, A., Shaw, P. W., Lerch, J. P., Clasen, L. S., Greenstein, D., Berman, R., Pipitone, J., Chakravarty, M. M., & Giedd, J. N. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1316911111 · Cited by 312
“These hotspots of sexually dimorphic striatal, pallidal, and thalamic maturation represent candidate substrates for adolescent-emergent sex differences in liability to disorders of mood and behavioral control—especially when considered alongside recent longitudinal structural neuroimaging evidence for co-occurring sex…”
BackgroundRaznahan, A., Lerch, J. P., Lee, N., Greenstein, D. K., Wallace, G. L., Stockman, M., CLASEN, L. S., Shaw, P. W., & Giedd, J. N. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.028 · Cited by 304
“First, by replicating our earlier report of sexually dimorphic CT change within the left FPC (Raznahan et al., 2010)—despite using a different methodology within a largely independent sample of scans—our data firmly establishes the FPC as key a region of interest for researchers seeking to delineate human brain system…”
InfluentialDumontheil, I. (2014) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2014.07.009 · Cited by 293
Puberty and structural brain development in humans
Herting, M. M., & Sowell, E. R. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.12.003 · Cited by 328
Vijayakumar, N., Allen, N. B., Youssef, G. J., Dennison, M., Yücel, M., Simmons, J. G., & Whittle, S. (2016) · Human Brain Mapping · doi:10.1002/hbm.23154 · Cited by 287
“The most common explanation for potential sex differences in cortical development is the sexually dimorphic effects of puberty, with support coming from experimental studies on animal and more recently observational studies in humans [Bramen et al., 2011; Peper et al., 2009; Raznahan et al., 2010; Sisk and Foster, 200…”
ResultSex differences and the neurobiology of affective disorders
Rubinow, D. R., & Schmidt, P. J. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0148-z · Cited by 286
Pfefferbaum, A., Rohlfing, T., Rosenbloom, M. J., Chu, W., Colrain, I. M., & Sullivan, E. V. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2012.10.008 · Cited by 256
“Developmental trajectories for regional cortical volumes and surface area analysis revealed curvilinear growth and sexual dimorphism varying by cortical, allocortical, and subcortical tissue structures and developmental stage (also see Raznahan et al., 2010, 2011a).”
BackgroundPubertal onset as a critical transition for neural development and cognition
Juraska, J. M., & Willing, J. (2016) · Brain Research · doi:10.1016/j.brainres.2016.04.012 · Cited by 249
“Taking a different approach, Raznahan et al. (2010) found that a more efficient androgen receptor allele was associated with more cortical thinning during adolescence in both sexes, even while sex differences persisted in the rate of frontal maturation.”
Herting, M. M., Gautam, P., Spielberg, J. M., Kan, E., Dahl, R. E., & Sowell, E. R. (2014) · Human Brain Mapping · doi:10.1002/hbm.22575 · Cited by 224
Sex steroids and brain structure in pubertal boys and girls: a mini-review of neuroimaging studies
Peper, J. S., Pol, H. E. H., Crone, E. A., & van Honk, J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.02.014 · Cited by 211
“Finally, data described in this mini-review have made use of different ways for quantifying gray matter estimates, that is, gray matter volume (Neufang et al., 2009; Bramen et al., 2011), gray matter density (Peper et al., 2009a) or cortical thickness (Raznahan et al., 2010).”
BackgroundMethodResultInfluentialThe development of the ventral prefrontal cortex and social flexibility
Nelson, E. E., & Guyer, A. E. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.01.002 · Cited by 201
Gur, R. E., & Gur, R. C. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.035 · Cited by 211
“Similar effects are reported for several parameters of brain structure and function (Raznahan et al., 2010).”
Puberty and adolescent sexuality
Fortenberry, J. D. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.03.007 · Cited by 200
“Imaging studies show that differences in cortical sub-systems associated with visio-spatial perception (typically more advanced in male adolescents) are associated with functional polymorphisms in the androgen-receptor gene (Raznahan et al., 2010).”
BackgroundSex differences in thickness, and folding developments throughout the cortex
Mutlu, A. K., Schneider, M., Debbané, M., Badoud, D., Eliez, S., & Schaer, M. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.05.076 · Cited by 206
“Indeed, when measuring the development at the local level, the same authors (Raznahan et al., 2010) observed faster cortical thinning in males than females in almost the entire frontal lobe, but reaching statistical significance only in the left frontopolar region.”
Amlien, I. K., Fjell, A. M., Tamnes, C. K., Grydeland, H., Krogsrud, S. K., Chaplin, T. A., Rosa, M. G. P., & Walhovd, K. B. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu214 · Cited by 195
Testosterone-Related Cortical Maturation Across Childhood and Adolescence
Nguyen, T., McCracken, J. T., Ducharme, S., Botteron, K. N., Mahabir, M., Johnson, W., Israël, M., Evans, A. C., Karama, S., & for the Brain Development Cooperative Group (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs125 · Cited by 200
Dumontheil, I. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.04.012 · Cited by 186
Adolescence and Reward: Making Sense of Neural and Behavioral Changes Amid the Chaos
Walker, D. M., Bell, M. R., Flores, C., Gulley, J. M., Willing, J., & Paul, M. J. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1834-17.2017 · Cited by 193
Sex/gender differences in cognition, neurophysiology, and neuroanatomy
Jäncke, L. (2018) · F1000Research · doi:10.12688/f1000research.13917.1 · Cited by 196
Emergence of sex differences in the development of substance use and abuse during adolescence
Kuhn, C. M. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.06.003 · Cited by 192
“Finally, while thinning of the cortex occurs in both boys and girls, the sex difference (thickness greater in boys than girls) diminishes in critical prefrontal areas during adolescence, and girls attain adult thickness in these areas related to executive function and behavioral inhibition before boys (Raznahan et al.…”
BackgroundDoes puberty mark a transition in sensitive periods for plasticity in the associative neocortex?
Piekarski, D. J., Johnson, C. M., Boivin, J. R., Thomas, A. W., Lin, W. C., Delevich, K., M. Galarce, E., & Wilbrecht, L. (2017) · Brain Research · doi:10.1016/j.brainres.2016.08.042 · Cited by 175
“, 2001), including in the frontal cortex (Bramen et al., 2011; Gogtay et al., 2004; Herting et al., 2014; Herting et al., 2015; Koolschijn et al., 2014; Neufang et al., 2009; Peper et al., 2009a; Raznahan et al., 2010).”
BackgroundSex differences in brain‐derived neurotrophic factor signaling and functions
Chan, C. B., & Ye, K. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23863 · Cited by 193
“The central nervous system (CNS) is different in structure, activity, development, and chemistry in female compared with male mammals (Raznahan et al., 2010; Ruigrok et al., 2014; Forger et al., 2016).”
BackgroundMultifaceted origins of sex differences in the brain
McCarthy, M. M. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0106 · Cited by 176
Bramen, J. E., Hranilovich, J. A., Dahl, R. E., Chen, J. Z.-J., Rosso, C., Forbes, E. E., Dinov, I. D., Worthman, C. M., & Sowell, E. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033850 · Cited by 170
“Further, longitudinal studies have shown that during puberty, the temporal lobes mature/thicken more rapidly in boys than girls [35].”
BackgroundResultInfluentialCortical Thickness in Untreated Transsexuals
Zubiaurre‐Elorza, L., Junqué, C., Gómez‐Gil, E., Segovia, S., Carrillo, B., Rametti, G., & Guillamón, A. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs267 · Cited by 165
“Brain development from childhood to adulthood is characterized by decreases in gray matter (Giedd et al. 1996; Reiss et al. 1996; Shaw et al. 2008; Raznahan et al. 2010) that follows a heterogeneous dynamic (Shaw et al.”
BackgroundInfluentialAdolf Pfefferbaum, A., Torsten Rohlfing, B., Pohl, K. M., Lane, B., Chu, W., Kwon, D., Nichols, B. N., Brown, S. A., Tapert, S. F., Cummins, K. M., et al. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv205 · Cited by 172
“Underlying this complementary pattern of gray matter and white matter volume dynamics are regional differences in the timing of these changes (Bava et al. 2010; Raznahan et al. 2010) (for review, Toga et al. 2006; Stiles and Jernigan 2010; Giedd et al. 2014).”
BackgroundDeCasien, A. R., Guma, E., Liu, S., & Raznahan, A. (2022) · Biology of Sex Differences · doi:10.1186/s13293-022-00448-w · Cited by 149
“, [105, 106]), or readers to mistakenly conclude that reported sex differences are being taken by their authors to imply evidence for a sexual dimorphism [1].”
BackgroundSotiras, A., Toledo, J. B., Gur, R. E., Gur, R. C., Satterthwaite, T. D., & Davatzikos, C. A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1620928114 · Cited by 148
“As in prior reports, we found that mean cortical thickness in males was initially greater than that in females throughout most of the association cortex [an effect that was inverted at 20 y (35)] and that primary motor and somatosensory networks mature before higher-order association cortices (4, 5).”
ResultA longitudinal study: changes in cortical thickness and surface area during pubertal maturation
Herting, M. M., Gautam, P., Spielberg, J. M., Dahl, R. E., & Sowell, E. R. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119774 · Cited by 142
“To our knowledge, only three studies have examined longitudinally how puberty or hormones impact cortical thickness [18,19,20], and no study in this area has examined surface area.”
BackgroundResultInfluentialSex steroids and schizophrenia
Markham, J. A. (2011) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-011-9184-2 · Cited by 154
ALL OUR SONS: THE DEVELOPMENTAL NEUROBIOLOGY AND NEUROENDOCRINOLOGY OF BOYS AT RISK
Schore, A. N. (2017) · Infant Mental Health Journal · doi:10.1002/imhj.21616 · Cited by 153
“I also cited the study of Raznahan et al. (2010) on androgen signaling and cortical maturation in adolescence showing a focally accentuated “protracted cortical maturation” in males, as compared to females, in the orbitofrontal and ventromedial cortices.”
BackgroundLadouceur, C. D., Peper, J. S., Crone, E. A., & Dahl, R. E. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.06.002 · Cited by 154
“Such hypotheses would need to be tested using longitudinal studies with larger samples of at-risk youth combined with genetic information (Raznahan et al., 2010) and accurate measurement of pubertal maturation to determine whether puberty-related changes in these white matter tracts indeed represent neurodevelopmental…”
A Review of the Status of Brain Structure Research in Transsexualism
Guillamón, A., Junqué, C., & Gómez‐Gil, E. (2016) · Archives of Sexual Behavior · doi:10.1007/s10508-016-0768-5 · Cited by 144
“ThethicknessofthehumancortexpresentsanF[Mpatternof sexdifferences (Imet al., 2006;Luders,Narr,Zaidel,Thompson, & Toga, 2006; Raznahan et al., 2010; Shaw et al., 2008; Sowell et al., 2007;Zubiaurre-Elorza et al., 2013) and it becomes thinner over the first three decades of life (Shaw et al., 2008).”
BackgroundInfluentialMakris, N., Swaab, D. F., van der Kouwe, A. J. W., Abbs, B., Boriel, D., Handa, R. J., Tobet, S. A., & Goldstein, J. M. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.12.008 · Cited by 133
“This role has been demonstrated for many years in model animals and more recently in humans (Bao and Swaab, 2011; Goldstein et al., 2001; Raznahan et al., 2010).”
The Influence of Sex Steroids on Structural Brain Maturation in Adolescence
Koolschijn, P. C. M. P., Peper, J. S., & Crone, E. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0083929 · Cited by 128
“[21] stepwise effects of androgen receptor transcriptional activity across adolescence were associated with cortical thinning in the inferior frontal gyrus (IFG), a region critically involved in executive functions such as inhibition.”
Jernigan, T. L., Baaré, W. F. C., Stiles, J., & Madsen, K. S. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53884-0.00019-1 · Cited by 126
Impact of Sex and Gonadal Steroids on Neonatal Brain Structure
Knickmeyer, R. C., Wang, J., Zhu, H., Geng, X., Woolson, S., Hamer, R. M., Konneker, T., Styner, M., & Gilmore, J. H. (2014) · Cerebral Cortex · doi:10.1093/cercor/bht125 · Cited by 109
“increase of loss) in the left inferior frontal gyrus (Raznahan et al. 2010).”
BackgroundHandedness and the X chromosome: The role of androgen receptor CAG-repeat length
Arning, L., Ocklenburg, S., Schulz, S., Vanessa Ness, A., Gerding, W. M., Hengstler, J. G., Falkenstein, M., Epplen, J. T., Güntürkün, O., & Beste, C. (2015) · Scientific Reports · doi:10.1038/srep08325 · Cited by 112
Effects of Cross-Sex Hormone Treatment on Cortical Thickness in Transsexual Individuals
Zubiaurre‐Elorza, L., Junqué, C., Gómez‐Gil, E., & Guillamón, A. (2014) · The Journal of Sexual Medicine · doi:10.1111/jsm.12491 · Cited by 114
Adolescent brain development: Implications for the juvenile criminal justice system.
Luna, B., & Wright, C. M. (2015) · American Psychological Association eBooks · doi:10.1037/14643-005 · Cited by 115
Hammerslag, L. R., & Gulley, J. M. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.04.008 · Cited by 120
“In eneral, males start with thicker frontal cortical tissue at age 9, ut undergo more rapid thinning compared to females [72].”
BackgroundAccelerated longitudinal cortical thinning in adolescence
Zhou, D., Lebel, C. A., Treit, S., Evans, A. C., & Beaulieu, C. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.10.005 · Cited by 118
“Longitudinal studies in children and/or adolescents report widespread areas of cortical thinning encompassing all the lobes (Sowell et al., 2004; Raznahan et al., 2010; van Soelen et al., 2012; Alemán-Gómez et al., 2013; Shaw et al., 2013; Burgaleta et al., 2014).”
InfluentialLadouceur, C. D. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00065 · Cited by 112
Adolescent sleep patterns in humans and laboratory animals
Hagenauer, M. H., & Lee, T. M. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.01.013 · Cited by 101
“…development driven by androgens (Campbell et al., 2012), and recent studies link androgen receptor polymorphisms and adolescent cortical pruning (Raznahan et al., 2010), further suggesting a connection between the two phenomena, although it remains unclear whether the relevant androgens are of…”
Brain Sex Differences Related to Gender Identity Development: Genes or Hormones?
Ristori, J., Cocchetti, C., Romani, A., Mazzoli, F., Vignozzi, L., Maggi, M., & Fisher, A. D. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21062123 · Cited by 98
“[55] speculated that gonadal hormones may maintain or increase basic neuroanatomical differences between sexes in puberty and maybe later on.”
BackgroundSex Differences in the Effect of Puberty on Hippocampal Morphology
Satterthwaite, T. D., Vandekar, S., Wolf, D. H., Ruparel, K., Roalf, D. R., Jackson, C. T., Elliott, M. A., Bilker, W. B., Calkins, M. E., Prabhakaran, K., et al. (2013) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2013.12.002 · Cited by 102
“It should be noted that several other studies have examined the effect of puberty, sex hormones, or polymorphisms of the androgen receptor and either did not find significant effects in the medial temporal lobe(51) or did not evaluate it because of a focus on cortical thickness.(9,52) Taken together, although 1 study…”
BackgroundLarge-Scale Transcriptomics Studies Provide Insight Into Sex Differences in Depression
Seney, M. L., Glausier, J. R., & Sibille, E. L. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.12.025 · Cited by 100
Sun, Y., Lee, R., Yu, C., Collinson, S. L., Thakor, N. V., Bezerianos, A., & Sim, K. (2015) · PLoS ONE · doi:10.1371/journal.pone.0118857 · Cited by 96
“Nonetheless, previous longitudinal studies mainly examined brain development during childhood or adolescence [8–10] or focused on GM changes over time [11,12].”
BackgroundMolecular basis of Gender Dysphoria: androgen and estrogen receptor interaction
Fernández, R., Guillamón, A., Cortés-Cortés, J., Gómez‐Gil, E., Jácome, M. A., Esteva, I., Almaraz, M., Mora, M., Aranda, G. B., & Pásaro, E. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.07.032 · Cited by 95
Sex differences in brain plasticity: a new hypothesis for sex ratio bias in autism
Mottron, L., Duret, P., Mueller, S., Moore, R. D., d’Arc, B. F., Jacquemont, S., & Xiong, L. (2015) · Molecular Autism · doi:10.1186/s13229-015-0024-1 · Cited by 104
“Other studies have shown that cortical modifications occurring from childhood to adulthood differ according to sex [105,106].”
BackgroundIntrinsic connectivity networks from childhood to late adolescence: Effects of age and sex
Solé‐Padullés, C., Castro‐Fornieles, J., de la Serna, E., Calvo, R. M., Baeza, I., Moyá, J., Lázaro, L., Rosa, M., Bargalló, N., & Sugranyes, G. (2015) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.11.004 · Cited by 94
Pohl, K. M., Sullivan, E. V., Rohlfing, T., Chu, W., Kwon, D., Nichols, B. N., Zhang, Y., Brown, S. A., Tapert, S. F., Cummins, K., et al. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.01.061 · Cited by 85
“…to the complexity of neurodevelopment is heterochronicity in regional timing of maturation that characterizes gray matter volume decline andwhitematter volume increase (Bava et al., 2010b; Raznahan et al., 2010, 2012) (for review, Giedd et al., 2014; Stiles and Jernigan, 2010; Toga et al., 2006).”
Positive effects of early androgen therapy on the behavioral phenotype of boys with 47,XXY
Samango‐Sprouse, C. A., Stapleton, E. J., Lawson, P. A., Mitchell, F. L., Sadeghin, T., Powell, S., & Gropman, A. L. (2015) · American Journal of Medical Genetics Part C Seminars in Medical Genetics · doi:10.1002/ajmg.c.31437 · Cited by 92
“…have been shown to have an organizational effect on social behaviors, cognitive abilities, language function, anxiety and fear reactivity during childhood and adolescence [Knickmeyer and Baron-Cohen, 2006; Bergman et al., 2010; Raznahan et al., 2010; Lombardo et al., 2012; Nguyen et al., 2013].”
BackgroundInfluentialSamango‐Sprouse, C. A., Sadeghin, T., Mitchell, F. L., Dixon, T., Stapleton, E. J., Kingery, M., & Gropman, A. L. (2013) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.35769 · Cited by 91
“Brain morphology as well as linear growth varies between males and females and hormones exert a fundamental and significant influence on these differences [Neufang et al., 2009; Peper et al., 2009; Raznahan et al., 2010; Mueller et al., 2011].”
BackgroundSchneider, S., Peters, J., Bromberg, U., Brassen, S., Menz, M. M., Miedl, S. F., Loth, E., Banaschewski, T., Barbot, A., Barker, G., et al. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.02.019 · Cited by 84
“…as females perform better in language-related tasks and males seem to have a visuo-spatial processing advantage, but also in cortical maturation as well as in regional gray and white matter trajectories (De Bellis et al., 2001; Raznahan et al., 2010; Stokes and Klee, 2009; Voyer et al., 1995).”
An Allometric Analysis of Sex and Sex Chromosome Dosage Effects on Subcortical Anatomy in Humans
Reardon, P. K., CLASEN, L. S., Giedd, J. N., Blumenthal, J. D., Lerch, J. P., Chakravarty, M. M., & Raznahan, A. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3195-15.2016 · Cited by 89
“Although advances in structural neuroimaging have been leveraged to map sex-differences in human cortical anatomy at high spatiotemporal resolution (Raznahan et al., 2010; Escorial et al., 2015; Giedd et al., 2015), most studies of sexdifferences in subcortical anatomy have examined bulk volumes rather than fine-mappi…”
BackgroundVisceral fat is associated with lower executive functioning in adolescents
Schwartz, D. H., Leonard, G. T., Perron, M., Richer, L., Syme, C. A., Veillette, S., Pausová, Z., & Paus, T. (2013) · International Journal of Obesity · doi:10.1038/ijo.2013.104 · Cited by 92
Markham, J. A., Mullins, S. E., & Koenig, J. I. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23262 · Cited by 89
“…TERMS: adolescence; schizophrenia; sex differences; puberty; cognition; estrogen Longitudinal neuroimaging studies have revealed that the prefrontal cortex (PFC) undergoes significant sex-specific changes in volume during adolescence (Lenroot et al., 2007; Raznahan et al., 2010, 2011).”
BackgroundROSS, J. L., Kushner, H., Kowal, K., Bardsley, M. Z., Davis, S., Reiss, A. L., Tartaglia, N. R., & Roeltgen, D. P. (2017) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2017.02.036 · Cited by 86
Androgens During Infancy, Childhood, and Adolescence: Physiology and Use in Clinical Practice
Mason, K. A., Schoelwer, M. J., & Rogol, A. D. (2020) · Endocrine Reviews · doi:10.1210/endrev/bnaa003 · Cited by 87
Adolescent sleep and the foundations of prefrontal cortical development and dysfunction
Anastasiades, P. G., de Vivo, L., Bellesi, M., & Jones, M. W. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102338 · Cited by 89
Sexual differentiation of brain and other tissues: Five questions for the next 50 years
Arnold, A. P. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104691 · Cited by 75
Vijayakumar, N., Whittle, S., Dennison, M., Yücel, M., Simmons, J., & Allen, N. B. (2014) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2013.12.002 · Cited by 71
“…evidence of females maturing earlier than males (Lenroot et al., 2007; Mutlu et al., 2013), one study has found greater cortical thinning in males (Raznahan et al., 2010), and others have failed to identify any sex differences (Koolschijn and Crone, 2013; Sowell et al., 2007; van Soelen et al.,…”
InfluentialWhere is the “g” in creativity? A specialization–differentiation hypothesis
Barbot, B., & Tinio, P. P. L. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.01041 · Cited by 73
“This is evidenced by imaging studies showing a decrease of gray matter during adolescence (Raznahan et al., 2010), which in turn, might account for the creative cognition “slumps” that are often observed during adolescence (e.”
BackgroundKoenis, M. M. G., Brouwer, R. M., Swagerman, S. C., van Soelen, I. L. C., Boomsma, D. I., & Pol, H. E. H. (2017) · Human Brain Mapping · doi:10.1002/hbm.23885 · Cited by 72
“, 2001), and their brains also develop at a different pace during adolescence (Gogtay et al., 2004; Gur and Gur, 2016; Raznahan et al., 2010).”
BackgroundMankiw, C., Park, M. T. M., Reardon, P. K., Fish, A. M., CLASEN, L. S., GREENSTEIN, D. K., Giedd, J. N., Blumenthal, J. D., Lerch, J. P., Chakravarty, M. M., et al. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2158-16.2017 · Cited by 76
“…there is convergent evidence of regionally specific neuroanatomical sex differences in the human cerebrum from multiple in vivo structural neuroimaging studies (Gur et al., 2002; Sowell et al., 2003; Raznahan et al., 2010; Rear- Received June 29, 2016; revised Jan. 30, 2017; accepted Feb. 1, 2017.”
BackgroundX-chromosome regulation and sex differences in brain anatomy
Raznahan, A., & Distèche, C. M. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.024 · Cited by 69
“fine-grained and developmentally-sensitive sMRI studies of other anatomical properties of the brain - such as cortical thickness(Raznahan et al., 2010) and subcortical shape(Raznahan et al.”
Hales, P. W., Kawadler, J. M., Aylett, S., Kirkham, F. J., & Clark, C. A. (2014) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2014.17 · Cited by 70
Multi-scale radiomic analysis of sub-cortical regions in MRI related to autism, gender and age
Chaddad, A., Desrosiers, C., & Toews, M. (2017) · Scientific Reports · doi:10.1038/srep45639 · Cited by 70
Shared effects of DISC1 disruption and elevated WNT signaling in human cerebral organoids
Srikanth, P., Lagomarsino, V. N., Muratore, C., Ryu, S. C., He, A., Taylor, W. M., Zhou, C. Q., Arellano, M., & Young‐Pearse, T. L. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0122-x · Cited by 69
Where Sex Meets Gender: How Sex and Gender Come Together to Cause Sex Differences in Mental Illness
Christiansen, D. M., McCarthy, M. M., & Seeman, M. V. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.856436 · Cited by 65
“The developmental trajectory of the brain differs by region and by sex such that the pace of maturation of large areas of the brain, such as the prefrontal cortex and the hippocampus, differs in boys and girls (60, 61).”
BackgroundDouet, V., Chang, L., Cloak, C. C., & Ernst, T. M. (2013) · Brain Imaging and Behavior · doi:10.1007/s11682-013-9260-1 · Cited by 68
“However, girls with the more " efficient " short AR gene had more rapid thinning of the left inferior frontal gyrus (Raznahan et al. 2010).”
The effects of puberty on white matter development in boys
Menzies, L. A., Goddings, A., Whitaker, K. J., Blakemore, S., & Viner, R. (2014) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2014.10.002 · Cited by 74
Goldstein, J. M., Holsen, L. M., Handa, R. J., & Tobet, S. A. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00247 · Cited by 64
“Recently, a number of new studies have emerged further characterizing sex-dependent circuitry (Ruigrok et al., 2013), connectivity (Ingalhalikar et al., 2014), and potential mechanisms (Raznahan et al., 2010; Kang et al., 2011; Goldstein et al., 2013; Lenz et al., 2013; Nguyen et al., 2013).”
BackgroundThe (CA)n Polymorphism of ERβ Gene is Associated with FtM Transsexualism
Fernández, R., Esteva, I., Gómez‐Gil, E., Rumbo, T., Almaraz, M. C., Roda, E., Haro‐Mora, J. J., Guillamón, A., & Pásaro, E. (2013) · The Journal of Sexual Medicine · doi:10.1111/jsm.12398 · Cited by 62
Possible Neurobiological Underpinnings of Homosexuality and Gender Dysphoria
Manzouri, A., & Savic, I. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy090 · Cited by 69
“In addition, it has been shown that the possession of an allele conferring more efficient function of the androgen receptor (AR) is associated with a relatively thinner Cth specifically in the inferior parietal cortex in males and the inferior frontal cortex in females (Raznahan et al. 2010).”
BackgroundBrain network interactions in transgender individuals with gender incongruence
Uribe, C., Junqué, C., Gómez‐Gil, E., Abós, A., Mueller, S. C., & Guillamón, A. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116613 · Cited by 60
“Each variant of gender has a brain phenotype that might be due to differences in cortical development probably due to differences in the efficiency of sex hormone receptors (Guillamon et al., 2016; Raznahan et al., 2010).”
Geniole, S. N., MacDonell, E. T., & McCormick, C. M. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.04.006 · Cited by 62
“…in specific neural regions is not possible in human studies, another approachwould be to consider variation in efficiency of androgen receptor signaling based on genotype (e.g., Raznahan et al., 2010; Manuck et al., 2010) as a factor in the relationship between testosterone and aggression.”
Nguyen, T., Lew, J., Albaugh, M. D., Botteron, K. N., Hudziak, J. J., Fonov, V., Collins, D. L., Ducharme, S., & McCracken, J. T. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.12.005 · Cited by 66
“…thickness across puberty in several regions involved in cognitive control and emotional regulation, from our group and others (Bramen et al., 2011; Koolschijn et al., 2014; Neufang et al., 2009; Nguyen et al., 2013a; Paus et al., 2010; Peper et al., 2011; Raznahan et al., 2010; Witte et al., 2010).”
BackgroundThe impact of adolescent stress experiences on neurobiological development
Iacono, L. L., & Carola, V. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.09.040 · Cited by 64
Brain morphology of childhood aggressive behavior: A multi-informant study in school-age children
Thijssen, S., Ringoot, A. P., Wildeboer, A., Bakermans‐Kranenburg, M. J., Marroun, H. E., Albert Hofman, D., Jaddoe, V. W. V., Verhulst, F. C., Tiemeier, H. W., van IJzendoorn, M. H., et al. (2015) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-015-0344-9 · Cited by 53
Association Study of ERβ, AR, and CYP19A 1 Genes and MtF Transsexualism
Fernández, R., Esteva, I., Gómez‐Gil, E., Rumbo, T., Almaraz, M. C., Roda, E., Haro‐Mora, J. J., Guillamón, A., & Pásaro, E. (2014) · The Journal of Sexual Medicine · doi:10.1111/jsm.12673 · Cited by 51
Raznahan, A., GREENSTEIN, D. K., Lee, Y., Long, R., CLASEN, L. S., Gochman, P., Addington, A. M., Giedd, J. N., Rapoport, J. L., & Gogtay, N. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.05.032 · Cited by 50
“Cortical thickness (CT) was studied as a developmentally sensitive (Raznahan et al., 2010) sMRI index of cortical structure that can be mapped at high-spatial resolution and is well established to vary in a regionally specific manner according to genetic (Lenroot et al.”
BackgroundHerlitz, A., Reuterskiöld, L., Lovén, J., Thilers, P. P., & Rehnman, J. (2013) · Developmental Neuropsychology · doi:10.1080/87565641.2012.759580 · Cited by 63
“Findings of sex differences in the development of gray and white matter volumes during adolescence (Lenroot et al., 2007; Raznahan et al., 2010), as well as increased sex differences in gray matter volumes of the medial temporal lobe in later as compared to earlier stages of pubertal maturation…”
BackgroundAromatase inhibition rapidly affects in a reversible manner distinct features of birdsong
Alward, B. A., de Bournonville, C., Chan, T. T., Balthazart, J., Cornil, C. A., & Ball, G. F. (2016) · Scientific Reports · doi:10.1038/srep32344 · Cited by 49
Slumps and Jumps: Another Look at Developmental Changes in Creative Abilities
Gralewski, J., Lebuda, I., Gajda, A., Jankowska, D. M., & Wiśniewska, E. (2016) · Creativity Theories – Research – Applications · doi:10.1515/ctra-2016-0011 · Cited by 49
“Another reason behind the crisis in creative abilities may be the previously men- tioned rapid developmental changes in the brain which occur throughout maturation (Blakemore & Choudhury, 2006), especially the decrease of grey matter (Raznahan et al., 2010).”
BackgroundThe molecular mechanisms of sexual orientation and gender identity
Fisher, A. D., Ristori, J., Morelli, G., & Maggi, M. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.08.008 · Cited by 49
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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