Progressive Stabilization of Brain Network Dynamics during Childhood and Adolescence

Tianyuan Lei; Xuhong Liao; Xiaodan Chen; Tengda Zhao; Yuehua Xu; Mingrui Xia; Jiaying Zhang; Yunman Xia; Xiaochen Sun; Yongbin Wei; Weiwei Men; Yanpei Wang; Mingming Hu; Gai Zhao; Bin Du; Siya Peng; Menglu Chen; Qian Wu; Shuping Tan; Jia Hong Gao; Shaozheng Qin; Sha Tao; Qi Dong; Yong He

doi:10.1093/cercor/bhab263

Progressive Stabilization of Brain Network Dynamics during Childhood and Adolescence

Tianyuan Lei, Xuhong Liao^*, Xiaodan Chen, Tengda Zhao, Yuehua Xu, Mingrui Xia, Jiaying Zhang, Yunman Xia, Xiaochen Sun, Yongbin Wei, Weiwei Men, Yanpei Wang, Mingming Hu, Gai Zhao, Bin Du, Siya Peng, Menglu Chen, Qian Wu, Shuping Tan, Jia Hong GaoShaozheng Qin, Sha Tao, Qi Dong, Yong He

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Functional brain networks require dynamic reconfiguration to support flexible cognitive function. However, the developmental principles shaping brain network dynamics remain poorly understood. Here, we report the longitudinal development of large-scale brain network dynamics during childhood and adolescence, and its connection with gene expression profiles. Using a multilayer network model, we show the temporally varying modular architecture of child brain networks, with higher network switching primarily in the association cortex and lower switching in the primary regions. This topographical profile exhibits progressive maturation, which manifests as reduced modular dynamics, particularly in the transmodal (e.g., default-mode and frontoparietal) and sensorimotor regions. These developmental refinements mediate age-related enhancements of global network segregation and are linked with the expression profiles of genes associated with the enrichment of ion transport and nucleobase-containing compound transport. These results highlight a progressive stabilization of brain dynamics, which expand our understanding of the neural mechanisms that underlie cognitive development.

Original language	English
Pages (from-to)	1024-1039
Number of pages	16
Journal	Cerebral Cortex
Volume	32
Issue number	5
Early online date	10 Aug 2021
DOIs	https://doi.org/10.1093/cercor/bhab263
Publication status	Published - 1 Mar 2022

Bibliographical note

Funding Information:
T.L., X.L., S.T., Q.D., and Y.H. designed the research; W.M., Y.W., M.H.,G.Z., B.D., S.P., M.C., S.T., J.G., S.Q., S.T., and Q.D. collected the data; T.L. and X.L. performed the research; X.C., T.Z., Y.X., M.X., Y.X., X.S., Y.W., and Q.W. provided technical assistance; and T.L., X.L., T.Z., J.Z., and Y.H. wrote the paper.

Publisher Copyright:
© 2021 The Author(s) 2021. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: [email protected].

Funding

T.L., X.L., S.T., Q.D., and Y.H. designed the research; W.M., Y.W., M.H.,G.Z., B.D., S.P., M.C., S.T., J.G., S.Q., S.T., and Q.D. collected the data; T.L. and X.L. performed the research; X.C., T.Z., Y.X., M.X., Y.X., X.S., Y.W., and Q.W. provided technical assistance; and T.L., X.L., T.Z., J.Z., and Y.H. wrote the paper.

Keywords

brain development
connectomics
gene expression
resting-state fMRI

Access to Document

10.1093/cercor/bhab263

Persistent URL (handle)

Persistent link

Cite this

@article{f8748a9b7c1446edb7c419a110b26bfd,

title = "Progressive Stabilization of Brain Network Dynamics during Childhood and Adolescence",

abstract = "Functional brain networks require dynamic reconfiguration to support flexible cognitive function. However, the developmental principles shaping brain network dynamics remain poorly understood. Here, we report the longitudinal development of large-scale brain network dynamics during childhood and adolescence, and its connection with gene expression profiles. Using a multilayer network model, we show the temporally varying modular architecture of child brain networks, with higher network switching primarily in the association cortex and lower switching in the primary regions. This topographical profile exhibits progressive maturation, which manifests as reduced modular dynamics, particularly in the transmodal (e.g., default-mode and frontoparietal) and sensorimotor regions. These developmental refinements mediate age-related enhancements of global network segregation and are linked with the expression profiles of genes associated with the enrichment of ion transport and nucleobase-containing compound transport. These results highlight a progressive stabilization of brain dynamics, which expand our understanding of the neural mechanisms that underlie cognitive development. ",

keywords = "brain development, connectomics, gene expression, resting-state fMRI",

author = "Tianyuan Lei and Xuhong Liao and Xiaodan Chen and Tengda Zhao and Yuehua Xu and Mingrui Xia and Jiaying Zhang and Yunman Xia and Xiaochen Sun and Yongbin Wei and Weiwei Men and Yanpei Wang and Mingming Hu and Gai Zhao and Bin Du and Siya Peng and Menglu Chen and Qian Wu and Shuping Tan and Gao, {Jia Hong} and Shaozheng Qin and Sha Tao and Qi Dong and Yong He",

note = "Funding Information: T.L., X.L., S.T., Q.D., and Y.H. designed the research; W.M., Y.W., M.H.,G.Z., B.D., S.P., M.C., S.T., J.G., S.Q., S.T., and Q.D. collected the data; T.L. and X.L. performed the research; X.C., T.Z., Y.X., M.X., Y.X., X.S., Y.W., and Q.W. provided technical assistance; and T.L., X.L., T.Z., J.Z., and Y.H. wrote the paper. Publisher Copyright: {\textcopyright} 2021 The Author(s) 2021. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: [email protected].",

year = "2022",

month = mar,

day = "1",

doi = "10.1093/cercor/bhab263",

language = "English",

volume = "32",

pages = "1024--1039",

journal = "Cerebral Cortex",

issn = "1047-3211",

publisher = "Oxford University Press",

number = "5",

}

Lei, T, Liao, X, Chen, X, Zhao, T, Xu, Y, Xia, M, Zhang, J, Xia, Y, Sun, X, Wei, Y, Men, W, Wang, Y, Hu, M, Zhao, G, Du, B, Peng, S, Chen, M, Wu, Q, Tan, S, Gao, JH, Qin, S, Tao, S, Dong, Q & He, Y 2022, 'Progressive Stabilization of Brain Network Dynamics during Childhood and Adolescence', Cerebral Cortex, vol. 32, no. 5, pp. 1024-1039. https://doi.org/10.1093/cercor/bhab263

TY - JOUR

T1 - Progressive Stabilization of Brain Network Dynamics during Childhood and Adolescence

AU - Lei, Tianyuan

AU - Liao, Xuhong

AU - Chen, Xiaodan

AU - Zhao, Tengda

AU - Xu, Yuehua

AU - Xia, Mingrui

AU - Zhang, Jiaying

AU - Xia, Yunman

AU - Sun, Xiaochen

AU - Wei, Yongbin

AU - Men, Weiwei

AU - Wang, Yanpei

AU - Hu, Mingming

AU - Zhao, Gai

AU - Du, Bin

AU - Peng, Siya

AU - Chen, Menglu

AU - Wu, Qian

AU - Tan, Shuping

AU - Gao, Jia Hong

AU - Qin, Shaozheng

AU - Tao, Sha

AU - Dong, Qi

AU - He, Yong

N1 - Funding Information: T.L., X.L., S.T., Q.D., and Y.H. designed the research; W.M., Y.W., M.H.,G.Z., B.D., S.P., M.C., S.T., J.G., S.Q., S.T., and Q.D. collected the data; T.L. and X.L. performed the research; X.C., T.Z., Y.X., M.X., Y.X., X.S., Y.W., and Q.W. provided technical assistance; and T.L., X.L., T.Z., J.Z., and Y.H. wrote the paper. Publisher Copyright: © 2021 The Author(s) 2021. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: [email protected].

PY - 2022/3/1

Y1 - 2022/3/1

N2 - Functional brain networks require dynamic reconfiguration to support flexible cognitive function. However, the developmental principles shaping brain network dynamics remain poorly understood. Here, we report the longitudinal development of large-scale brain network dynamics during childhood and adolescence, and its connection with gene expression profiles. Using a multilayer network model, we show the temporally varying modular architecture of child brain networks, with higher network switching primarily in the association cortex and lower switching in the primary regions. This topographical profile exhibits progressive maturation, which manifests as reduced modular dynamics, particularly in the transmodal (e.g., default-mode and frontoparietal) and sensorimotor regions. These developmental refinements mediate age-related enhancements of global network segregation and are linked with the expression profiles of genes associated with the enrichment of ion transport and nucleobase-containing compound transport. These results highlight a progressive stabilization of brain dynamics, which expand our understanding of the neural mechanisms that underlie cognitive development.

AB - Functional brain networks require dynamic reconfiguration to support flexible cognitive function. However, the developmental principles shaping brain network dynamics remain poorly understood. Here, we report the longitudinal development of large-scale brain network dynamics during childhood and adolescence, and its connection with gene expression profiles. Using a multilayer network model, we show the temporally varying modular architecture of child brain networks, with higher network switching primarily in the association cortex and lower switching in the primary regions. This topographical profile exhibits progressive maturation, which manifests as reduced modular dynamics, particularly in the transmodal (e.g., default-mode and frontoparietal) and sensorimotor regions. These developmental refinements mediate age-related enhancements of global network segregation and are linked with the expression profiles of genes associated with the enrichment of ion transport and nucleobase-containing compound transport. These results highlight a progressive stabilization of brain dynamics, which expand our understanding of the neural mechanisms that underlie cognitive development.

KW - brain development

KW - connectomics

KW - gene expression

KW - resting-state fMRI

UR - http://www.scopus.com/inward/record.url?scp=85125681297&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85125681297&partnerID=8YFLogxK

U2 - 10.1093/cercor/bhab263

DO - 10.1093/cercor/bhab263

M3 - Article

C2 - 34378030

AN - SCOPUS:85125681297

SN - 1047-3211

VL - 32

SP - 1024

EP - 1039

JO - Cerebral Cortex

JF - Cerebral Cortex

IS - 5

ER -

Progressive Stabilization of Brain Network Dynamics during Childhood and Adolescence

Abstract

Bibliographical note

Funding

Keywords

Access to Document

Persistent URL (handle)

Other files and links

Fingerprint

Cite this