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Dissociable Multi-scale Patterns of Development in Personalized Brain Networks

Adam R. Pines, Bart Larsen, Zaixu Cui, Valerie J. Sydnor, Maxwell A. Bertolero, Azeez Adebimpe, Aaron F. Alexander-Bloch, Christos Davatzikos, Damien A. Fair, Ruben C. Gur, Raquel E. Gur, Hongming Li, Michael P. Milham, Tyler M. Moore, Kristin Murtha, View ORCID ProfileLinden Parkes, Sharon L. Thompson-Schill, Sheila Shanmugan, Russell T. Shinohara, Sarah M. Weinstein, View ORCID ProfileDanielle S. Bassett, Yong Fan, Theodore D. Satterthwaite
doi: https://doi.org/10.1101/2021.07.07.451458
Adam R. Pines
aThe Penn Lifespan Informatics and Neuroimaging Center
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Bart Larsen
aThe Penn Lifespan Informatics and Neuroimaging Center
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Zaixu Cui
aThe Penn Lifespan Informatics and Neuroimaging Center
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Valerie J. Sydnor
aThe Penn Lifespan Informatics and Neuroimaging Center
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Maxwell A. Bertolero
aThe Penn Lifespan Informatics and Neuroimaging Center
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Azeez Adebimpe
aThe Penn Lifespan Informatics and Neuroimaging Center
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Aaron F. Alexander-Bloch
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Christos Davatzikos
cDepartments of Radiology of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Damien A. Fair
jDepartment of Pediatrics, College of Education and Human Development, University of Minnesota, Minneapolis, MN 55455, USA
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Ruben C. Gur
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
cDepartments of Radiology of the University of Pennsylvania, Philadelphia, PA 19104, USA
hDepartments of Neurology of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Raquel E. Gur
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Hongming Li
cDepartments of Radiology of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Michael P. Milham
kCenter for Biomedical Imaging and Neuromodulation, Santa Fe, NM 87051, USA
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Tyler M. Moore
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Kristin Murtha
aThe Penn Lifespan Informatics and Neuroimaging Center
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Linden Parkes
aThe Penn Lifespan Informatics and Neuroimaging Center
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
dDepartments of Bioengineering of the University of Pennsylvania, Philadelphia, PA 19104, USA
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  • ORCID record for Linden Parkes
Sharon L. Thompson-Schill
gDepartments of Psychology of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Sheila Shanmugan
aThe Penn Lifespan Informatics and Neuroimaging Center
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Russell T. Shinohara
iDepartments of Biostatistics, Epidemiology, and Informatics of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Sarah M. Weinstein
iDepartments of Biostatistics, Epidemiology, and Informatics of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Danielle S. Bassett
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
dDepartments of Bioengineering of the University of Pennsylvania, Philadelphia, PA 19104, USA
eDepartments of Electrical & Systems Engineering of the University of Pennsylvania, Philadelphia, PA 19104, USA
fDepartments of Physics & Astronomy of the University of Pennsylvania, Philadelphia, PA 19104, USA
hDepartments of Neurology of the University of Pennsylvania, Philadelphia, PA 19104, USA
lNathan Kline Institute, NY 10962, USA Santa Fe Institute, Santa Fe, NM 87051, USA
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Yong Fan
cDepartments of Radiology of the University of Pennsylvania, Philadelphia, PA 19104, USA
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Theodore D. Satterthwaite
aThe Penn Lifespan Informatics and Neuroimaging Center
bDepartments of Psychiatry, Neurodevelopment & Psychosis Section of the University of Pennsylvania, Philadelphia, PA 19104, USA
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  • For correspondence: sattert@pennmedicine.upenn.edu
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SUMMARY

The brain is organized into networks at multiple resolutions, or scales, yet studies of functional network development typically focus on a single scale. Here, we derived personalized functional networks across 29 scales in a large sample of youths (n=693, ages 8-23 years) to identify multi-scale patterns of network re-organization related to neurocognitive development. We found that developmental shifts in inter-network coupling systematically adhered to and strengthened a functional hierarchy of cortical organization. Furthermore, we observed that scale-dependent effects were present in lower-order, unimodal networks, but not higher-order, transmodal networks. Finally, we found that network maturation had clear behavioral relevance: the development of coupling in unimodal and transmodal networks dissociably mediated the emergence of executive function. These results delineate maturation of multi-scale brain networks, which varies according to a functional hierarchy and impacts cognitive development.

Competing Interest Statement

Dr. Shinohara has consulting income from Genentech/Roche and Octave Bioscience. All other authors report no competing interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 09, 2021.
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Dissociable Multi-scale Patterns of Development in Personalized Brain Networks
Adam R. Pines, Bart Larsen, Zaixu Cui, Valerie J. Sydnor, Maxwell A. Bertolero, Azeez Adebimpe, Aaron F. Alexander-Bloch, Christos Davatzikos, Damien A. Fair, Ruben C. Gur, Raquel E. Gur, Hongming Li, Michael P. Milham, Tyler M. Moore, Kristin Murtha, Linden Parkes, Sharon L. Thompson-Schill, Sheila Shanmugan, Russell T. Shinohara, Sarah M. Weinstein, Danielle S. Bassett, Yong Fan, Theodore D. Satterthwaite
bioRxiv 2021.07.07.451458; doi: https://doi.org/10.1101/2021.07.07.451458
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Dissociable Multi-scale Patterns of Development in Personalized Brain Networks
Adam R. Pines, Bart Larsen, Zaixu Cui, Valerie J. Sydnor, Maxwell A. Bertolero, Azeez Adebimpe, Aaron F. Alexander-Bloch, Christos Davatzikos, Damien A. Fair, Ruben C. Gur, Raquel E. Gur, Hongming Li, Michael P. Milham, Tyler M. Moore, Kristin Murtha, Linden Parkes, Sharon L. Thompson-Schill, Sheila Shanmugan, Russell T. Shinohara, Sarah M. Weinstein, Danielle S. Bassett, Yong Fan, Theodore D. Satterthwaite
bioRxiv 2021.07.07.451458; doi: https://doi.org/10.1101/2021.07.07.451458

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