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Mapping Continued Brain Growth and Gray Matter Density Reduction in Dorsal Frontal Cortex: Inverse Relationships during Postadolescent Brain Maturation
Open accessAbstract
Recent in vivo structural imaging studies have shown spatial and temporal patterns of brain maturation between childhood, adolescence, and young adulthood that are generally consistent with postmortem studies of cellular maturational events such as increased myelination and synaptic pruning. In this study, we conducted detailed spatial and temporal analyses of growth and gray matter density at the cortical surface of the brain in a group of 35 normally developing children, adolescents, and young adults. To accomplish this, we used high-resolution magnetic resonance imaging and novel computational image analysis techniques. For the first time, in this report we have mapped the continued postadolescent brain growth that occurs primarily in the dorsal aspects of the frontal lobe bilaterally and in the posterior temporo-occipital junction bilaterally. Notably, maps of the spatial distribution of postadolescent cortical gray matter density reduction are highly consistent with maps of the spatial distribution of postadolescent brain growth, showing an inverse relationship between cortical gray matter density reduction and brain growth primarily in the superior frontal regions that control executive cognitive functioning. Inverse relationships are not as robust in the posterior temporo-occipital junction where gray matter density reduction is much less prominent despite late brain growth in these regions between adolescence and adulthood. Overall brain growth is not significant between childhood and adolescence, but close spatial relationships between gray matter density reduction and brain growth are observed in the dorsal parietal and frontal cortex. These results suggest that progressive cellular maturational events, such as increased myelination, may play as prominent a role during the postadolescent years as regressive events, such as synaptic pruning, in determining the ultimate density of mature frontal lobe cortical gray matter.
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“Prior imaging studies show regional nonlinear changes in gray matter (GM) density during childhood and adolescence with prepubertal increase followed by postpubertal loss (11–14).”
From Dynamic mapping of human cortical development during childhood through early adulthood (2004) · cites this paper as [12]
In the citing paper
“A further MRI study of 35 normally developing children (7-11 years), adolescents (12-16 years) and young adults (23-30 years) demonstrated a sharp acceleration in the loss of grey matter between childhood and adolescence in the dorsal prefrontal cortex and the parietal cortex (Sowell et al., 2001).”
From Development of the adolescent brain: implications for executive function and social cognition (2006) · cites this paper as Sowell et al., 2001
In the citing paper
“The gradual decrease in grey matter density that occurs after puberty in certain brain regions has been attributed to post-pubescent synaptic pruning (Giedd et al., 1999a;Sowell et al., 2001;Gogtay et al., 2004).”
From Development of the adolescent brain: implications for executive function and social cognition (2006) · cites this paper as Sowell et al., 2001
In the citing paper
“One such study of participants aged between 7 and 30 revealed that the loss of grey matter in the frontal cortex accelerated during adulthood between the early 20s and up to the age of 30 (Sowell et al., 2001).”
From Development of the adolescent brain: implications for executive function and social cognition (2006) · cites this paper as Sowell et al., 2001
In the citing paper
“protracted maturation of the prefrontal cortex (PFC) and parietal regions”
From Adolescent risk taking, impulsivity, and brain development: Implications for prevention (2010) · cites this paper as Sowell, Thompson, Tessner, & Toga, 2001
In the citing paper
“Previous studies have shown that right frontal cortical thinning occurs prior to left frontal cortical thinning in children 5--11 years of age (Sowell et al. 2001).”
From Puberty influences medial temporal lobe and cortical gray matter maturation differently in boys than girls matched for sexual maturity (2011) · cites this paper as Sowell et al. 2001
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The Cambridge Handbook of Applied School Psychology
Worrell, T. L. H. F. C. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108235532 · Cited by 15
Mergler, A., Spencer, F. H., & Patton, W. (2007) · The Australian Educational and Developmental Psychologist · doi:10.1017/s0816512200029060 · Cited by 15
Cognitive Screening for Children and Adolescents: General Limits or Ceiling Effects?
Bornholt, L. J., Ajersch, S., Fisher, I. H., Markham, R. H., & Ouvrier, R. (2010) · Journal of Child Neurology · doi:10.1177/0883073809352686 · Cited by 15
“Therefore, it would seem that the transition to mature cognitive processing levels associated with the prefrontal cortex would occur during late childhood and adolescence.(16,17) Certain specific cognitive functions appear to continue to develop as adolescents mature (eg, see functional neuroimaging of response inhibi…”
BackgroundGomes, H., Duff, M., Barnhardt, J., Barrett, S., & Ritter, W. (2007) · Psychophysiology · doi:10.1111/j.1469-8986.2007.00555.x · Cited by 15
Sharp, A., Young, M. S., & Moore, K. A. (2019) · The Journal of Behavioral Health Services & Research · doi:10.1007/s11414-019-09649-5 · Cited by 15
Nicotine Effects on White Matter Microstructure in Young Adults
Kangiser, M. M., Thomas, A. M., Kaiver, C. M., & Lisdahl, K. M. (2018) · Archives of Clinical Neuropsychology · doi:10.1093/arclin/acy101 · Cited by 17
Towards a neurodevelopmental cognitive perspective of temporal processing
Buzi, G., Eustache, F., Droit‐Volet, S., Desaunay, P., & Hinault, T. (2024) · Communications Biology · doi:10.1038/s42003-024-06641-4 · Cited by 21
Impact of human immunodeficiency virus on neurocognition and risky behaviors in young adults
Baker, L. M., Paul, R. H., Heaps, J. M., Westerhaus, E. T., Chang, J. Y., Williams, S. C., Brier, M. R., Plax, K. L., & Ances, B. M. (2014) · Journal of NeuroVirology · doi:10.1007/s13365-014-0264-4 · Cited by 15
“Although the brain has reached its full adult size by about 5 to 10 years of age (Giedd et al. 1996; Reiss et al. 1996), more subtle developments occur over a longer period of time (Jernigan et al. 1991; Reiss et al. 1996; Giedd et al. 1999; Sowell et al. 2001).”
BackgroundPerformance on an episodic encoding task yields further insight into functional brain development
McAuley, T., Brahmbhatt, S. B., & Barch, D. M. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.08.042 · Cited by 13
Prefrontal and Occipital Asymmetry and Volume in Boys with Autism Spectrum Disorder
Knaus, T. A., Tager-Flusberg, H. B., Mock, J. R., Dauterive, R., & Foundas, A. L. (2012) · Cognitive and Behavioral Neurology · doi:10.1097/wnn.0b013e318280e154 · Cited by 14
“As typically developing children and adolescents grow up, their white matter volume expands and their gray matter volume shrinks.(32,33) Studies of children with ASD have shown different developmental patterns, with brain overgrowth before age 2, and then a plateau (for reviews, see Redcay and Courchesne34 and Schuman…”
BackgroundPaediatric major depressive disorder: neurobiology and implications for early intervention
Cullen, K. R., Klimes‐Dougan, B., Kumra, S., & Schulz, S. C. (2009) · Early Intervention in Psychiatry · doi:10.1111/j.1751-7893.2009.00131.x · Cited by 15
Correlation between baseline regional gray matter volume and global gray matter volume decline rate
Taki, Y., Kinomura, S., Sato, K., Goto, R., Wu, K., Kawashima, R., & Fukuda, H. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.09.071 · Cited by 14
“…pruning and progressive cellular events such as myelination occur simultaneously in the brain during childhood, adolescence, and young adulthood, and both types of event could result in the appearance of regional gray matter volume decline or cortical thinning on MR images (Sowell et al., 2001).”
Resting gamma power is linked to reading ability in adolescents
Tierney, A. T., Strait, D. L., & Kraus, N. (2013) · Developmental Science · doi:10.1111/desc.12094 · Cited by 14
Smith, C. T., Steel, E. A., Parrish, M. H., Kelm, M. K., & Boettiger, C. A. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00627 · Cited by 13
“…and Bickel, 2014; Behan et al., 2015; Cho et al., 2015; Massar et al., 2015), and the development of frontal structures remains incomplete until the early-to-mid twenties (Sowell et al., 1999; Casey et al., 2000; Sowell et al., 2001; Giedd, 2004; Gogtay et al., 2004; Lenroot and Giedd, 2006).”
BackgroundPrenatal Development of the Human Fetal Telencephalon
Judáš, M. (2010) · Medical radiology · doi:10.1007/174_2010_119 · Cited by 14
Kennedy, J. T., Astafiev, S. V., Golosheykin, S., Korucuoglu, O., & Anokhin, A. P. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.05.053 · Cited by 14
“…adolescence is a significant period in the development of the frontostriatal reward and inhibition regions (DePasque and Galvan, 2017; Galvan 2005; Sowell 2001) which are related to the overeating behaviors associated with obesity (Maayan et al., 2011; Su et al., 2017; van der Laan et al., 2016).”
BackgroundMagnusson, K. R., & Brim, B. C. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.00158-6 · Cited by 14
Ren, S., Chang, M., Yin, Z., Feng, R., Wei, Y., Duan, J., Jiang, X., Wei, S., Tang, Y., Wang, F., et al. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.01010 · Cited by 14
“Interestingly a similar directionality of the normal development of the brain has been reported in the previous findings (14, 17, 26).”
ResultJuvenile Transfer in the United States
Bishop, D. M. (2009) · Springer eBooks · doi:10.1007/978-0-387-89295-5_6 · Cited by 13
New insights into the neurobiology of sexual maturation
Sisk, C. L. (2006) · Sexual & Relationship Therapy · doi:10.1080/14681990500470009 · Cited by 14
“Human adolescent development also involves widespread changes in the gross morphology of the brain (Gogtay et al., 2004; Sowell et al., 1999, 2001, 2002).”
Brain Atlases of Normal and Diseased Populations
Toga, A. W., & Thompson, P. M. (2005) · International review of neurobiology · doi:10.1016/s0074-7742(05)66001-1 · Cited by 14
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Ahrens, E. T., Blumenthal, J. D., Jacobs, R. E., & Giedd, J. N. (2000) · Elsevier eBooks · doi:10.1016/b978-012692545-6/50021-0 · Cited by 13
Maturational trajectories of pericortical contrast in typical brain development
Drakulich, S., Thiffault, A.-C., Olafson, E. R., Parent, O., Labbe, A., Albaugh, M. D., Khundrakpam, B. S., Ducharme, S., Evans, A. C., Chakravarty, M. M., et al. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.117974 · Cited by 12
Winstone, J., Shafique, H. S., Clemmer, M. E., Mackie, K., & Wager‐Miller, J. (2022) · Cannabis and Cannabinoid Research · doi:10.1089/can.2021.0025 · Cited by 13
Neural Mechanisms and Children’s Intellectual Development
Takeuchi, H., & Kawashima, R. (2015) · The Neuroscientist · doi:10.1177/1073858415610294 · Cited by 13
de Almeida, J., Jourdan, I., Murer, M. G., & Belforte, J. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062978 · Cited by 12
“Adolescence has been associated with changes in circuit wiring, as seen at the level of synaptic spines [61] and brain imaging [62], which could have a parallel in neural synchrony.”
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00004-3 · Cited by 14
Stoica, T., Knight, L. K., Naaz, F., Ramic, M., & Depue, B. E. (2019) · Brain and Behavior · doi:10.1002/brb3.1413 · Cited by 14
Zhou, L., Zhen, Z., Liu, J., & Zhou, K. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa180 · Cited by 13
Lifespan trait development: Toward an adequate theory of personality
McCrae, R. R., Bolle, M. D., Löckenhoff, C. E., & Terracciano, A. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-813995-0.00023-6 · Cited by 16
Growth Patterns of Neuropsychological Functions in Indian Children
Kar, B. R., Rao, S. L., Chandramouli, B. A., & Thennarasu, K. (2011) · Frontiers in Psychology · doi:10.3389/fpsyg.2011.00240 · Cited by 13
“Neurodevelopmental events follow non-linear trends (Giedd et al., 1996; Sowell et al., 2001).”
WORKING MEMORY: DEVELOPMENT, DISORDERS AND TRAINING
Westerberg, H. (2004) · Figshare · Cited by 13
Metadata
- Authors
- Sowell, E. R., Thompson, P. M., Tessner, K. D., & Toga, A. W.
- Affiliations
- University of California, Los Angeles (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2001-11-15
- Volume
- 21
- Issue
- 22
- Pages
- 8819-8829
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6762261
- OpenAlex
- W2095621691
- Cited by
- 983
- References
- 34
- Citations by year
- 2026: 12 · 2025: 19 · 2024: 24 · 2023: 24 · 2022: 27 · 2021: 34 · 2020: 78 · 2019: 52 · 2018: 35 · 2017: 28 · 2016: 37 · 2015: 51 · 2014: 45 · 2013: 67 · 2012: 50
- FWCI
- 10.83
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (9601356)
- National Institutes of Health (5t32mh016381-20)
- National Institute of Mental Health (K01 MH 01733, 5-T32-MH16381, K01MH001733, P20 MH/DA52176)
- National Institute of Neurological Disorders and Stroke (NS38753, R01NS038753)
- National Center for Research Resources (P41RR013642, RR 13642, P41 RR13642)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Keywords
- brain maturation, myelination, synaptic pruning, parietal cortex, executive function, developmental neuroimaging, children, adolescents and young adults
- MeSH terms
- Adolescent, Adult, Aging, Brain, Brain Mapping, Cell Count, Child, Female, Frontal Lobe, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Occipital Lobe, Temporal Lobe
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