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Sex Differences in Brain Maturation during Childhood and Adolescence
Abstract
Brain development during childhood and adolescence is characterized by both progressive myelination and regressive pruning processes. However, sex differences in brain maturation remain poorly understood. Magnetic resonance imaging was used to examine the relationships between age and sex with cerebral gray and white matter volumes and corpus callosal areas in 118 healthy children and adolescents (61 males and 57 females), aged 6-17 years. Gender groups were similar on measures of age, handedness, socioeconomic status and Full Scale IQ. Significant age-related reductions in cerebral gray and increases in white matter volumes and corpus callosal areas were evident, while intracranial and cerebral volumes did not change significantly. Significant sex by age interactions were seen for cerebral gray and white matter volumes and corpus callosal areas. Specifically, males had more prominent age-related gray matter decreases and white matter volume and corpus callosal area increases compared with females. While these data are from a cross-sectional sample and need to be replicated in a longitudinal study, the findings suggest that there are age-related sex differences in brain maturational processes. The study of age-related sex differences in cerebral pruning and myelination may aid in understanding the mechanism of several developmental neuropsychiatric disorders.
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“To limit treatment‐related variability and inherent sex differences in brain development (De Bellis et al., 2001; Gur et al., 1999; Lange, Giedd, Castellanos, Vaituzis, & Rapoport, 1997; Kang, Herron, & Woods, 2011), while maximizing eligible participants, we restricted this study to males only.”
From Brain structure, working memory and response inhibition in childhood leukemia survivors (2017) · cites this paper as De Bellis et al., 2001
In the citing paper
“Firstly, sex is known to modulate brain development (De Bellis et al., 2001; Gur et al., 1999; Lange et al., 1997; Kang et al., 2011) so that manifestation of late effects at any given age may depend on sex (Anderson & Kunin‐Batson, 2009; Buizer, de Sonneville, van den Heuvel‐Eibrink, & Veerman, 2005).”
From Brain structure, working memory and response inhibition in childhood leukemia survivors (2017) · cites this paper as De Bellis et al., 2001
In the citing paper
“Sex differences in applying the model learned from one sex on another support multiple studies suggesting earlier maturation in females (De Bellis et al. 2001;Lenroot et al. 2007).”
From Imaging Patterns of Brain Development and their Relationship to Cognition (2015) · cites this paper as De Bellis et al. 2001
In the citing paper
“We validated the sensitivity of this index to the well-established sex difference in maturation, which is earlier in females (De Bellis et al. 2001;Lenroot et al. 2007), by applying the male predictors to the female sample and vice versa.”
From Imaging Patterns of Brain Development and their Relationship to Cognition (2015) · cites this paper as De Bellis et al. 2001
In the citing paper
“In addition to age, pubertal status and hormone titers significantly interact with sex to affect white matter volume in multiple tracts in the human brain, including those connecting higher association cortices (Asato et al., 2010; Chavarria et al., 2014; De Bellis et al., 2001; Herting et al., 2012; Peper et al., 2008; Perrin et al., 2008; Perrin et al., 2009).”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as De Bellis et al., 2001
In the citing paper
“When controlling for age, both pubertal hormones and stage of puberty correlate with changes in gray matter across adolescent development in disparate regions of cortex (De Bellis et al., 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., 2”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as De Bellis et al., 2001
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“It is possible that our findings may reflect sex differences in brain maturation due to variations in neuronal myelination and synaptic pruning; this may be exacerbated by RT due to variations in neurobiological changes between the sexes during brain development (De Bellis et al., 2001).”
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“…and relative white matter volumes compared with girls and considerably steeper white matter increases during adolescence (Giedd et al., 1999; De Bellis et al., 2001; Lenroot et al., 2007; Perrin et al., 2009), perhaps due to the presence of testosterone (Herting et al., 2012, but see Peper et…”
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“The maturational processes occurring in adolescence involve a refinement of neuronal circuitry, with both progressive and regressive changes, such as myelination and synaptic pruning (De Bellis et al., 2001).”
BackgroundPost‐pubertal emergence of alterations in locomotor activity in stop null mice
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“It is also the case that the human brain exhibits significant changes in structure and function during adolescence (Huttenlocher, 1979; Huttenlocher et al., 1982; De Bellis et al., 2000; De Bellis et al., 2001; De Bellis et al., 2005).”
BackgroundGender-Specific Differences in the Central Nervous System’s Response to Anesthesia
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“However, subtle age-related gender differences in cognitive and brain maturational processes have been reported (e.g., De Bellis et al., 2001).”
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Klotho gene polymorphism, brain structure and cognition in early-life development
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“Boys and girls also follow different trajectories of white matter growth during development (De Bellis et al. 2001; Giedd et al. 1999).”
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BackgroundPain mechanisms in the transgender individual: a review
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“Regarding gender differences in brain maturation, the volumes of the frontal and parietal gray matter peak earlier in females (Giedd et al., 1999), and the slope of the reduction in gray matter volume in adolescence is steeper in males than in females (De Bellis et al., 2001).”
Prenatal Development of the Human Fetal Telencephalon
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“Age-related differences in cerebral WM volumes during adolescence have previously been shown to differ between gender (De Bellis et al., 2001).”
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“Although the exact mechanism remains unknown, it is possible that the sex-related differences in brain maturation (De Bellis et al. 2001; Koolschijn and Crone 2013) and connectivity (Sun et al. 2015) as well as the differential activation of cortical areas during motor tasks (Lissek et al. 2007)…”
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“The finding that girls were less likely to develop normal gross motor skills than boys is in line with studies that have indicated that boys were better off than girls in terms of development of specific aspects of the brain(64,65).”
ResultLongitudinal Sex-at-Birth and Age Analyses of Cortical Structure in the ABCD Study
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What is special about the adolescent (JME) brain?
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“filaments [122,123] or glial proliferation [124].”
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“…striatal, caudal and other regions (Neufang et al., 2009), as well as on the developmental slopes of gray matter volume reduction and white matter volume increase showing earlier maturation in females than males (De Bellis et al., 2001; Giedd et al., 1997, 2006; Sowell et al., 2003, 2007).”
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“A significant number of women experience heightened stress, anxiety, and depression during pregnancy (Casey et al., 2008; De Bellis et al., 2001; Dunkel, 2011; Gerardin et al., 2011).”
Eyolfson, E., Yamakawa, G. R., Griep, Y., Collins, R., Carr, T. H., Wang, M., Lohman, A. W., & Mychasiuk, R. (2020) · Cerebral Cortex Communications · doi:10.1093/texcom/tgaa002 · Cited by 12
Steinmann, S., Lyall, A. E., Langhein, M., Nägele, F. L., Rauh, J., Karayumak, S. C., Zhang, F., Mußmann, M., Billah, T., Makris, N., et al. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.686967 · Cited by 11
“Indeed, it has been consistently reported that white matter growth during puberty and adolescence follows a striking sexual dimorphism: age-related increases in white matter occur much more steeply in boys when compared to girls (76, 77).”
BackgroundVerona, J. A. G., Macías, J. A., Pastor, J. F., de Paz, F., Barbosa, M., Maniega, M. A., Román, J. M. S. S., López, A., Alvarez-Alfageme, I., González, L. R., et al. (2003) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 11
McMurray, M. S., Oğuz, İ., Rumple, A., Paniagua, B., Styner, M. A., & Johns, J. M. (2014) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2014.11.007 · Cited by 11
“This is in contrast with a number of studies completed in humans at similar developmental ages, which showed larger callosum volumes in males (De Bellis et al., 2001; Sowell et al., 2002).”
ResultKraus, E. (2006) · Elsevier eBooks · doi:10.1016/b978-032303186-8.50012-5 · Cited by 11
Quantifying cerebral changes in adolescence with MRI and deformation based morphometry
Riddle, W. R., DonLevy, S. C., Wushensky, C. A., Dawant, B. M., Fitzpatrick, J. M., & Price, R. R. (2008) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.21450 · Cited by 11
“Decreases in gray matter may reflect the dendrite pruning process and increases in white matter volumes could be due to myelination, increases in axonal size, and/or glial cell proliferation (5).”
BackgroundThe Neurodevelopmental Model of Schizophrenia: Updated
Bearden, C. E., MEYER, S. E., Loewy, R. L., Niendam, T. A., & Cannon, T. D. (2015) · Wiley eBooks · doi:10.1002/9780470939406.ch14 · Cited by 11
Towbin, K. E., Solages, M. M., & Stubbe, D. E. (2015) · Wiley eBooks · doi:10.1002/9781118753378.ch12 · Cited by 12
Comparative analysis of brain age prediction using structural and diffusion MRIs in neonates
Fang, Z., Pan, N., Liu, S., Li, H., Pan, M., Zhang, J., Li, Z., Liu, M., & Ge, X. (2024) · NeuroImage · doi:10.1016/j.neuroimage.2024.120815 · Cited by 10
“The gender differences observed in FA-based predictions suggest that the integrity of white matter is influenced by gender-specific factors, aligning with studies showing different patterns of white matter development in males and females(De Bellis et al., 2001).”
BackgroundGyral window mapping of typical cortical folding using MRI
Dombroski, B. A., Switala, A. E., El-Baz, A. S., & Casanova, M. F. (2011) · Translational Neuroscience · doi:10.2478/s13380-011-0018-1 · Cited by 10
The Impact of Stress Within and Across Generations: Neuroscientific and Epigenetic Considerations
Miller, C. W. T. (2021) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000300 · Cited by 13
Richards, G., & Smith, A. P. (2016) · Frontiers in Nutrition · doi:10.3389/fnut.2016.00052 · Cited by 10
“Children and adolescents are known to commonly consume caffeine (16), and may also be particularly sensitive to its effects due to continued brain development, myelination, and synaptic pruning (17, 18).”
BackgroundA Biocultural Life History Approach to the Developmental Psychobiology of Male Aggression
Worthman, C. M., & Brown, R. A. (2005) · Cambridge University Press eBooks · doi:10.1017/cbo9780511499883.010 · Cited by 10
Age-related brain activation during forward and backward verbal memory tasks
Manan, H. A., Franz, E. A., Yusoff, A. N., & Mukari, S. Z. S. (2014) · Neurology Psychiatry and Brain Research · doi:10.1016/j.npbr.2014.08.001 · Cited by 10
Recognizing and Managing Long-Term Sequelae of Childhood Maltreatment
Scheid, J. M. (2003) · Pediatric Annals · doi:10.3928/0090-4481-20030601-07 · Cited by 10
Gender-related hearing, balance and speech disorders
Zanon, A., Sorrentino, F., Franz, L., & Brotto, D. (2019) · Hearing Balance and Communication · doi:10.1080/21695717.2019.1615812 · Cited by 10
Brain Development During Adolescence
Ashtari, M., & Cyckowski, L. L. (2011) · Springer eBooks · doi:10.1007/978-1-4419-1795-9_72 · Cited by 10
Juvenile competency to stand trial in criminal court and brain function
Mayzer, R., Bradley, A. R., Rusinko, H. M., & Ertelt, T. W. (2009) · Journal of Forensic Psychiatry and Psychology · doi:10.1080/14789940903174089 · Cited by 12
Malik, M. A., Weber, A., Lang, D. J., Vanderwal, T., & Zwicker, J. G. (2024) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2024.1276057 · Cited by 12
Absence of P 300 Reduction in S outh A frican Treatment‐Naïve Adolescents with Alcohol Dependence
Cuzen, N. L., Andrew, C. M., Thomas, K. G. F., Stein, D. J., & Fein, G. (2012) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2012.01837.x · Cited by 9
Gray matter asymmetry in the orbitofrontal cortex in relation to psychopathic traits in adolescents
Lam, B. Y., Huang, Y., & Gao, Y. (2020) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2020.10.003 · Cited by 11
Sex differences in cognitive-motor components of braking in older adults
Casamento‐Moran, A., Patel, P. J., Zablocki, V., Christou, E. A., & Lodha, N. (2022) · Experimental Brain Research · doi:10.1007/s00221-022-06330-w · Cited by 10
Prevalence, severity and risk factors for speech disorders in US children
Choo, A. L., Smith, S. A., & Li, H. (2022) · Journal of Monolingual and Bilingual Speech · doi:10.1558/jmbs.20879 · Cited by 10
The Role of Puberty and Sex on Brain Structure in Adolescents With Anxiety Following Concussion
Santos, J. P. L., Kontos, A. P., Holland, C. L., Suss, S. J., Stiffler, R. S., Bitzer, H. B., Colorito, A. T., Shaffer, M. A., Skeba, A. S., Iyengar, S., et al. (2022) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2022.09.013 · Cited by 9
Khazen, T., Shrivastava, K., Jada, R., Hatoum, O. A., & Maroun, M. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.02.011 · Cited by 9
Taman, F. D., Kervancıoğlu, P., Kervancioglu, A. S., & Turhan, B. (2019) · Child s Nervous System · doi:10.1007/s00381-019-04369-9 · Cited by 9
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Kerasidis, H., & Simmons, J. (2021) · Clinical EEG and Neuroscience · doi:10.1177/1550059421989112 · Cited by 9
Hay, R. E., Reynolds, J. E., Grohs, M., Paniukov, D., Giesbrecht, G. F., Letourneau, N., Dewey, D., & Lebel, C. (2019) · doi:10.1101/692335 · Cited by 7
Lane, J. M., Curtin, P. C. P., Chelonis, J. J., Pantic, I., Martínez-Medina, S., Téllez‐Rojo, M. M., & Wright, R. O. (2023) · Environmental Research · doi:10.1016/j.envres.2023.116880 · Cited by 8
Ban, M., He, J., Wang, D., Cao, Y., Kong, L., Yuan, F., Qian, Z., & Zhu, X. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.05.001 · Cited by 9
The effect of perspective and content on brain activation during mentalizing in young females
Veroude, K., Keulers, E. H. H., Evers, E. A. T., Stiers, P. L. J., Krabbendam, L., & Jolles, J. (2011) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803395.2011.630650 · Cited by 8
Metadata
- Authors
- De Bellis, M. D.
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2001-06-01
- Volume
- 11
- Issue
- 6
- Pages
- 552-557
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2119268056
- Cited by
- 728
- References
- 49
- Citations by year
- 2026: 10 · 2025: 26 · 2024: 28 · 2023: 20 · 2022: 28 · 2021: 31 · 2020: 27 · 2019: 42 · 2018: 36 · 2017: 29 · 2016: 34 · 2015: 31 · 2014: 36 · 2013: 39 · 2012: 32
- FWCI
- 14.78
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (1r03mh043687-01)
- National Institute on Alcohol Abuse and Alcoholism (AA08746-08, P50AA008746)
- National Institute of Mental Health (P01MH041712, MH-41712, K08MH001324, MH 01180, 5 K08 MHO1324-02, MH-43687, K02MH001180)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- sex differences, brain maturation, brain development, childhood, adolescence, gray matter volume, white matter volume, corpus callosum, myelination, synaptic pruning, intracranial volume
- MeSH terms
- Adolescent, Age Factors, Brain, Child, Female, Humans, Magnetic Resonance Imaging, Male, Myelin Sheath, Puberty, Sex Characteristics, Linear Models
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