Development of structure–function coupling in human brain networks during youth

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Significance

The human brain is organized into a hierarchy of functional systems that evolve in childhood and adolescence to support the dynamic control of attention and behavior. However, it remains unknown how developing white-matter architecture supports coordinated fluctuations in neural activity underlying cognition. We document marked remodeling of structure–function coupling in youth, which aligns with cortical hierarchies of functional specialization and evolutionary expansion. Further, we demonstrate that structure–function coupling in rostrolateral prefrontal cortex supports age-related improvements in executive ability. These findings have broad relevance for accounts of experience-dependent plasticity in healthy development and abnormal development associated with neuropsychiatric illness.

Abstract

The protracted development of structural and functional brain connectivity within distributed association networks coincides with improvements in higher-order cognitive processes such as executive function. However, it remains unclear how white-matter architecture develops during youth to directly support coordinated neural activity. Here, we characterize the development of structure–function coupling using diffusion-weighted imaging and n-back functional MRI data in a sample of 727 individuals (ages 8 to 23 y). We found that spatial variability in structure–function coupling aligned with cortical hierarchies of functional specialization and evolutionary expansion. Furthermore, hierarchy-dependent age effects on structure–function coupling localized to transmodal cortex in both cross-sectional data and a subset of participants with longitudinal data ( n = 294). Moreover, structure–function coupling in rostrolateral prefrontal cortex was associated with executive performance and partially mediated age-related improvements in executive function. Together, these findings delineate a critical dimension of adolescent brain development, whereby the coupling between structural and functional connectivity remodels to support functional specialization and cognition.

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Author and article information

Journal

Journal ID (nlm-ta): Proc Natl Acad Sci U S A

Journal ID (iso-abbrev): Proc. Natl. Acad. Sci. U.S.A

Journal ID (hwp): pnas

Journal ID (pmc): pnas

Journal ID (publisher-id): PNAS

Title: Proceedings of the National Academy of Sciences of the United States of America

Publisher: National Academy of Sciences

ISSN (Print): 0027-8424

ISSN (Electronic): 1091-6490

Publication date (Print): 7 January 2020

Publication date (Electronic): 24 December 2019

Publication date PMC-release: 24 December 2019

Volume: 117

Issue: 1

Pages: 771-778

Affiliations

[1] ^aDepartment of Psychiatry, University of Pennsylvania , Philadelphia, PA 19104;

[2] ^bLifespan Brain Institute, Children’s Hospital of Philadelphia , Philadelphia, PA 19104;

[3] ^cDepartment of Bioengineering, Stanford University , Stanford, CA 94305;

[4] ^dDepartment of Psychological and Brain Sciences, Indiana University Bloomington , Bloomington, IN 47405;

[5] ^eDepartment of Radiology, University of Pennsylvania , Philadelphia, PA 19104;

[6] ^fDepartment of Psychiatry, Yale University School of Medicine , New Haven, CT 06510;

[7] ^gPenn Statistics in Imaging and Visualization Center, Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania , Philadelphia, PA 19104;

[8] ^hCenter for Biomedical Image Computing and Analytics, University of Pennsylvania , Philadelphia, PA 19104;

[9] ⁱDevelopmental Neurogenomics Unit, National Institute of Mental Health , Bethesda, MD 20814;

[10] ^jDepartment of Neurology, University of Pennsylvania , Philadelphia, PA 19104;

[11] ^kDepartment of Bioengineering, University of Pennsylvania , Philadelphia, PA 19104;

[12] ^lDepartment of Electrical and Systems Engineering, University of Pennsylvania , Philadelphia, PA 19104;

[13] ^mDepartment of Physics and Astronomy, University of Pennsylvania , Philadelphia, PA 19104;

[14] ⁿSanta Fe Institute , Santa Fe, NM 87501

Author notes

¹To whom correspondence may be addressed. Email: sattertt@ 123456pennmedicine.upenn.edu .

Edited by Marcus E. Raichle, Washington University in St. Louis, St. Louis, MO, and approved November 27, 2019 (received for review July 12, 2019)

Author contributions: G.L.B., R.E.G., R.C.G., D.S.B., and T.D.S. designed research; G.L.B. performed research; Z.C., D.R.R., R.C., R.F.B., B.L., M.C., P.A.C., C.H.X., T.M.M., K.R., D.J.O., A.F.A.-B., R.T.S., A.R., D.S.B., and T.D.S. contributed new reagents/analytic tools; G.L.B., Z.C., R.C., and T.M.M. analyzed data; and G.L.B. and T.D.S. wrote the paper.