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

doi:10.1038/s41467-022-30244-4

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

Institute of Child Development

Research output: Contribution to journal › Article › peer-review

59 Scopus citations

Abstract

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 derive 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 reflect and strengthen 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 are dissociably related to the emergence of executive function. These results suggest that the development of functional brain networks align with and refine a hierarchy linked to cognition.

Original language	English (US)
Article number	2647
Journal	Nature communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-30244-4
State	Published - Dec 2022

Bibliographical note

Funding Information:
This study was supported by grants from the National Institute of Health: F31 MH123063-01A1 (A.P.), R01MH113550 (T.D.S. and D.S.B.), R01EB022573 (C.D., Y.F., and T.D.S.), R01MH120482 (T.D.S. and M.M.), RF1MH116920 (T.D.S. and D.S.B.), R37MH125829 (D.F. and T.D.S.), R01MH112847 (R.T.S. and T.D.S.), K99MH127293 and T32MH014654 (B.L.). V.J.S. was supported by a National Science Foundation Graduate Research Fellowship (DGE-1845298). L.P. was supported by the National Institute Of Mental Health of the National Institutes of Health under Award Number K99MH127296 and a 2020 NARSAD Young Investigator Grant from the Brain & Behavior Research Foundation. The PNC was supported by MH089983 and MH089924. Additional support was provided by the Lifespan Brain Institute at Penn and the Children’s Hospital of Philadelphia and the Dowshen Program for Neuroscience. The content is solely the responsibility of the authors and does not represent the official views of any of the funding agencies.

Publisher Copyright:
© 2022, The Author(s).

Publisher link

10.1038/s41467-022-30244-4

Find It

Find It at U of M Libraries

Cite this

Pines, A. R., Larsen, B., Cui, Z., Sydnor, V. J., Bertolero, M. A., Adebimpe, A., Alexander-Bloch, A. F., Davatzikos, C., Fair, D. A., Gur, R. C., Gur, R. E., Li, H., Milham, M. P., Moore, T. M., Murtha, K., Parkes, L., Thompson-Schill, S. L., Shanmugan, S., Shinohara, R. T., ... Satterthwaite, T. D. (2022). Dissociable multi-scale patterns of development in personalized brain networks. Nature communications, 13(1), Article 2647. https://doi.org/10.1038/s41467-022-30244-4

Pines, AR, Larsen, B, Cui, Z, Sydnor, VJ, Bertolero, MA, Adebimpe, A, Alexander-Bloch, AF, Davatzikos, C, Fair, DA, Gur, RC, Gur, RE, Li, H, Milham, MP, Moore, TM, Murtha, K, Parkes, L, Thompson-Schill, SL, Shanmugan, S, Shinohara, RT, Weinstein, SM, Bassett, DS, Fan, Y & Satterthwaite, TD 2022, 'Dissociable multi-scale patterns of development in personalized brain networks', Nature communications, vol. 13, no. 1, 2647. https://doi.org/10.1038/s41467-022-30244-4

@article{64f53dd1dd0849d8af3f0847684e0b3c,

title = "Dissociable multi-scale patterns of development in personalized brain networks",

abstract = "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 derive personalized functional networks across 29 scales in a large sample of youths (n = 693, ages 8{\textendash}23 years) to identify multi-scale patterns of network re-organization related to neurocognitive development. We found that developmental shifts in inter-network coupling reflect and strengthen 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 are dissociably related to the emergence of executive function. These results suggest that the development of functional brain networks align with and refine a hierarchy linked to cognition.",

author = "Pines, \{Adam R.\} and Bart Larsen and Zaixu Cui and Sydnor, \{Valerie J.\} and Bertolero, \{Maxwell A.\} and Azeez Adebimpe and Alexander-Bloch, \{Aaron F.\} and Christos Davatzikos and Fair, \{Damien A.\} and Gur, \{Ruben C.\} and Gur, \{Raquel E.\} and Hongming Li and Milham, \{Michael P.\} and Moore, \{Tyler M.\} and Kristin Murtha and Linden Parkes and Thompson-Schill, \{Sharon L.\} and Sheila Shanmugan and Shinohara, \{Russell T.\} and Weinstein, \{Sarah M.\} and Bassett, \{Danielle S.\} and Yong Fan and Satterthwaite, \{Theodore D.\}",

note = "Funding Information: This study was supported by grants from the National Institute of Health: F31 MH123063-01A1 (A.P.), R01MH113550 (T.D.S. and D.S.B.), R01EB022573 (C.D., Y.F., and T.D.S.), R01MH120482 (T.D.S. and M.M.), RF1MH116920 (T.D.S. and D.S.B.), R37MH125829 (D.F. and T.D.S.), R01MH112847 (R.T.S. and T.D.S.), K99MH127293 and T32MH014654 (B.L.). V.J.S. was supported by a National Science Foundation Graduate Research Fellowship (DGE-1845298). L.P. was supported by the National Institute Of Mental Health of the National Institutes of Health under Award Number K99MH127296 and a 2020 NARSAD Young Investigator Grant from the Brain \& Behavior Research Foundation. The PNC was supported by MH089983 and MH089924. Additional support was provided by the Lifespan Brain Institute at Penn and the Children{\textquoteright}s Hospital of Philadelphia and the Dowshen Program for Neuroscience. The content is solely the responsibility of the authors and does not represent the official views of any of the funding agencies. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = dec,

doi = "10.1038/s41467-022-30244-4",

language = "English (US)",

volume = "13",

journal = "Nature communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "1",

}

TY - JOUR

T1 - Dissociable multi-scale patterns of development in personalized brain networks

AU - Pines, Adam R.

AU - Larsen, Bart

AU - Cui, Zaixu

AU - Sydnor, Valerie J.

AU - Bertolero, Maxwell A.

AU - Adebimpe, Azeez

AU - Alexander-Bloch, Aaron F.

AU - Davatzikos, Christos

AU - Fair, Damien A.

AU - Gur, Ruben C.

AU - Gur, Raquel E.

AU - Li, Hongming

AU - Milham, Michael P.

AU - Moore, Tyler M.

AU - Murtha, Kristin

AU - Parkes, Linden

AU - Thompson-Schill, Sharon L.

AU - Shanmugan, Sheila

AU - Shinohara, Russell T.

AU - Weinstein, Sarah M.

AU - Bassett, Danielle S.

AU - Fan, Yong

AU - Satterthwaite, Theodore D.

N1 - Funding Information: This study was supported by grants from the National Institute of Health: F31 MH123063-01A1 (A.P.), R01MH113550 (T.D.S. and D.S.B.), R01EB022573 (C.D., Y.F., and T.D.S.), R01MH120482 (T.D.S. and M.M.), RF1MH116920 (T.D.S. and D.S.B.), R37MH125829 (D.F. and T.D.S.), R01MH112847 (R.T.S. and T.D.S.), K99MH127293 and T32MH014654 (B.L.). V.J.S. was supported by a National Science Foundation Graduate Research Fellowship (DGE-1845298). L.P. was supported by the National Institute Of Mental Health of the National Institutes of Health under Award Number K99MH127296 and a 2020 NARSAD Young Investigator Grant from the Brain & Behavior Research Foundation. The PNC was supported by MH089983 and MH089924. Additional support was provided by the Lifespan Brain Institute at Penn and the Children’s Hospital of Philadelphia and the Dowshen Program for Neuroscience. The content is solely the responsibility of the authors and does not represent the official views of any of the funding agencies. Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - 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 derive 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 reflect and strengthen 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 are dissociably related to the emergence of executive function. These results suggest that the development of functional brain networks align with and refine a hierarchy linked to cognition.

AB - 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 derive 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 reflect and strengthen 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 are dissociably related to the emergence of executive function. These results suggest that the development of functional brain networks align with and refine a hierarchy linked to cognition.

UR - https://www.scopus.com/pages/publications/85130634583

UR - https://www.scopus.com/pages/publications/85130634583#tab=citedBy

U2 - 10.1038/s41467-022-30244-4

DO - 10.1038/s41467-022-30244-4

M3 - Article

C2 - 35551181

AN - SCOPUS:85130634583

SN - 2041-1723

VL - 13

JO - Nature communications

JF - Nature communications

IS - 1

M1 - 2647

ER -

Dissociable multi-scale patterns of development in personalized brain networks

Abstract

Bibliographical note

Publisher link

Find It

Other files and links

Fingerprint

Cite this