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PMID: 28242797 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Intramural Research Support, N.I.H., Extramural

Development of the Cerebral Cortex across Adolescence: A Multisample Study of Inter-Related Longitudinal Changes in Cortical Volume, Surface Area, and Thickness.

Tamnes CK, Herting MM, Goddings AL, Meuwese R, Blakemore SJ, Dahl RE, Güroğlu B, Raznahan A, Sowell ER, Crone EA, Mills KL

Abstract

Before we can assess and interpret how developmental changes in human brain structure relate to cognition, affect, and motivation, and how these processes are perturbed in clinical or at-risk populations, we must first precisely understand typical brain development and how changes in different structural components relate to each other. We conducted a multisample magnetic resonance imaging study to investigate the development of cortical volume, surface area, and thickness, as well as their inter-relationships, from late childhood to early adulthood (7-29 years) using four separate longitudinal samples including 388 participants and 854 total scans. These independent datasets were processed and quality-controlled using the same methods, but analyzed separately to study the replicability of the results across sample and image-acquisition characteristics. The results consistently showed widespread and regionally variable nonlinear decreases in cortical volume and thickness and comparably smaller steady decreases in surface area. Further, the dominant contributor to cortical volume reductions during adolescence was thinning. Finally, complex regional and topological patterns of associations between changes in surface area and thickness were observed. Positive relationships were seen in sulcal regions in prefrontal and temporal cortices, while negative relationships were seen mainly in gyral regions in more posterior cortices. Collectively, these results help resolve previous inconsistencies regarding the structural development of the cerebral cortex from childhood to adulthood, and provide novel insight into how changes in the different dimensions of the cortex in this period of life are inter-related.SIGNIFICANCE STATEMENT Different measures of brain anatomy develop differently across adolescence. Their precise trajectories and how they relate to each other throughout development are important to know if we are to fully understand both typical development and disorders involving aberrant brain development. However, our understanding of such trajectories and relationships is still incomplete. To provide accurate characterizations of how different measures of cortical structure develop, we performed an MRI investigation across four independent datasets. The most profound anatomical change in the cortex during adolescence was thinning, with the largest decreases observed in the parietal lobe. There were complex regional patterns of associations between changes in surface area and thickness, with positive relationships seen in sulcal regions in prefrontal and temporal cortices, and negative relationships seen mainly in gyral regions in more posterior cortices.

Keywords
MRI brain development gray matter morphometry replication
MeSH Terms
Adolescent Adult Aging/pathology,physiology Cerebral Cortex/anatomy & histology,growth & development Child Female Humans Imaging, Three-Dimensional/methods Longitudinal Studies Magnetic Resonance Imaging/methods Male Organ Size/physiology Reproducibility of Results Sensitivity and Specificity Young Adult
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Tamnes Christian K
Department of Psychology, University of Oslo, 0317 Oslo, Norway, [email protected].
Herting Megan M
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California 90032.
Goddings Anne-Lise
Institute of Child Health and.
Meuwese Rosa
Brain and Development Research Center, Institute of Psychology, and. | Leiden Institute for Brain and Cognition, Leiden University, 2300 RA Leiden, The Netherlands.
Blakemore Sarah-Jayne
Institute of Cognitive Neuroscience, University College London, London WC1N 1EH United Kingdom.
Dahl Ronald E ORCID
Institute of Human Development, University of California Berkeley, Berkeley, California 94720.
Güroğlu Berna
Brain and Development Research Center, Institute of Psychology, and. | Leiden Institute for Brain and Cognition, Leiden University, 2300 RA Leiden, The Netherlands.
Raznahan Armin
Child Psychiatry Branch, National Institute of Mental Health, Bethesda, Maryland 20814.
Sowell Elizabeth R
Children's Hospital of Los Angeles, Los Angeles, California 90027, and.
Crone Eveline A
Brain and Development Research Center, Institute of Psychology, and. | Leiden Institute for Brain and Cognition, Leiden University, 2300 RA Leiden, The Netherlands.
Mills Kathryn L ORCID
Department of Psychology, University of Oregon, Eugene, Oregon 97403.
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Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2017-00-22
Epub
2017-00-27
Pages
3402-3412
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC5373125
Subset
IM
Grants
NICHD NIH HHS · R01 HD053893 · United States
NIMH NIH HHS · R01 MH087563 · United States
NIMH NIH HHS · K01 MH108761 · United States
NIMH NIH HHS · R01 MH107418 · United States
NIDA NIH HHS · R01 DA018910 · United States
Medical Research Council · G1100402 · United Kingdom
Wellcome Trust · United Kingdom
NICHD NIH HHS · F32 HD078084 · United States
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