The maturation and cognitive relevance of structural brain network organization from early infancy to childhood
•Cortical thickness networks were mapped longitudinally from infancy to six years.•Brain network segregation increased between early infancy and six years.•Brain networks became less integrated across the first six years of life.•Brain maturation across the first year related to motor learning at 8–...
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Published in | NeuroImage (Orlando, Fla.) Vol. 238; p. 118232 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Amsterdam
Elsevier Inc
01.09.2021
Elsevier Limited Elsevier |
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Online Access | Get full text |
ISSN | 1053-8119 1095-9572 1095-9572 |
DOI | 10.1016/j.neuroimage.2021.118232 |
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Abstract | •Cortical thickness networks were mapped longitudinally from infancy to six years.•Brain network segregation increased between early infancy and six years.•Brain networks became less integrated across the first six years of life.•Brain maturation across the first year related to motor learning at 8–10 years.
The interactions of brain regions with other regions at the network level likely provide the infrastructure necessary for cognitive processes to develop. Specifically, it has been theorized that in infancy brain networks become more modular, or segregated, to support early cognitive specialization, before integration across networks increases to support the emergence of higher-order cognition. The present study examined the maturation of structural covariance networks (SCNs) derived from longitudinal cortical thickness data collected between infancy and childhood (0–6 years). We assessed modularity as a measure of network segregation and global efficiency as a measure of network integration. At the group level, we observed trajectories of increasing modularity and decreasing global efficiency between early infancy and six years. We further examined subject-based maturational coupling networks (sbMCNs) in a subset of this cohort with cognitive outcome data at 8–10 years, which allowed us to relate the network organization of longitudinal cortical thickness maturation to cognitive outcomes in middle childhood. We found that lower global efficiency of sbMCNs throughout early development (across the first year) related to greater motor learning at 8–10 years. Together, these results provide novel evidence characterizing the maturation of brain network segregation and integration across the first six years of life, and suggest that specific trajectories of brain network maturation contribute to later cognitive outcomes. |
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AbstractList | The interactions of brain regions with other regions at the network level likely provide the infrastructure necessary for cognitive processes to develop. Specifically, it has been theorized that in infancy brain networks become more modular, or segregated, to support early cognitive specialization, before integration across networks increases to support the emergence of higher-order cognition. The present study examined the maturation of structural covariance networks (SCNs) derived from longitudinal cortical thickness data collected between infancy and childhood (0–6 years). We assessed modularity as a measure of network segregation and global efficiency as a measure of network integration. At the group level, we observed trajectories of increasing modularity and decreasing global efficiency between early infancy and six years. We further examined subject-based maturational coupling networks (sbMCNs) in a subset of this cohort with cognitive outcome data at 8–10 years, which allowed us to relate the network organization of longitudinal cortical thickness maturation to cognitive outcomes in middle childhood. We found that lower global efficiency of sbMCNs throughout early development (across the first year) related to greater motor learning at 8–10 years. Together, these results provide novel evidence characterizing the maturation of brain network segregation and integration across the first six years of life, and suggest that specific trajectories of brain network maturation contribute to later cognitive outcomes. The interactions of brain regions with other regions at the network level likely provide the infrastructure necessary for cognitive processes to develop. Specifically, it has been theorized that in infancy brain networks become more modular, or segregated, to support early cognitive specialization, before integration across networks increases to support the emergence of higher-order cognition. The present study examined the maturation of structural covariance networks (SCNs) derived from longitudinal cortical thickness data collected between infancy and childhood (0-6 years). We assessed modularity as a measure of network segregation and global efficiency as a measure of network integration. At the group level, we observed trajectories of increasing modularity and decreasing global efficiency between early infancy and six years. We further examined subject-based maturational coupling networks (sbMCNs) in a subset of this cohort with cognitive outcome data at 8-10 years, which allowed us to relate the network organization of longitudinal cortical thickness maturation to cognitive outcomes in middle childhood. We found that lower global efficiency of sbMCNs throughout early development (across the first year) related to greater motor learning at 8-10 years. Together, these results provide novel evidence characterizing the maturation of brain network segregation and integration across the first six years of life, and suggest that specific trajectories of brain network maturation contribute to later cognitive outcomes.The interactions of brain regions with other regions at the network level likely provide the infrastructure necessary for cognitive processes to develop. Specifically, it has been theorized that in infancy brain networks become more modular, or segregated, to support early cognitive specialization, before integration across networks increases to support the emergence of higher-order cognition. The present study examined the maturation of structural covariance networks (SCNs) derived from longitudinal cortical thickness data collected between infancy and childhood (0-6 years). We assessed modularity as a measure of network segregation and global efficiency as a measure of network integration. At the group level, we observed trajectories of increasing modularity and decreasing global efficiency between early infancy and six years. We further examined subject-based maturational coupling networks (sbMCNs) in a subset of this cohort with cognitive outcome data at 8-10 years, which allowed us to relate the network organization of longitudinal cortical thickness maturation to cognitive outcomes in middle childhood. We found that lower global efficiency of sbMCNs throughout early development (across the first year) related to greater motor learning at 8-10 years. Together, these results provide novel evidence characterizing the maturation of brain network segregation and integration across the first six years of life, and suggest that specific trajectories of brain network maturation contribute to later cognitive outcomes. •Cortical thickness networks were mapped longitudinally from infancy to six years.•Brain network segregation increased between early infancy and six years.•Brain networks became less integrated across the first six years of life.•Brain maturation across the first year related to motor learning at 8–10 years. The interactions of brain regions with other regions at the network level likely provide the infrastructure necessary for cognitive processes to develop. Specifically, it has been theorized that in infancy brain networks become more modular, or segregated, to support early cognitive specialization, before integration across networks increases to support the emergence of higher-order cognition. The present study examined the maturation of structural covariance networks (SCNs) derived from longitudinal cortical thickness data collected between infancy and childhood (0–6 years). We assessed modularity as a measure of network segregation and global efficiency as a measure of network integration. At the group level, we observed trajectories of increasing modularity and decreasing global efficiency between early infancy and six years. We further examined subject-based maturational coupling networks (sbMCNs) in a subset of this cohort with cognitive outcome data at 8–10 years, which allowed us to relate the network organization of longitudinal cortical thickness maturation to cognitive outcomes in middle childhood. We found that lower global efficiency of sbMCNs throughout early development (across the first year) related to greater motor learning at 8–10 years. Together, these results provide novel evidence characterizing the maturation of brain network segregation and integration across the first six years of life, and suggest that specific trajectories of brain network maturation contribute to later cognitive outcomes. |
ArticleNumber | 118232 |
Author | Wang, Li Lin, Weili Li, Gang Cohen, Jessica R. Sheridan, Margaret A. Wu, Zhengwang Woodburn, Mackenzie Bricken, Cheyenne L. |
AuthorAffiliation | c Department of Radiology, University of North Carolina, Chapel Hill, United States b Biomedical Research Imaging Center, University of North Carolina, Chapel Hill, United States a Department of Psychology & Neuroscience, University of North Carolina, Chapel Hill, United States d Carolina Institute of Developmental Disabilities, University of North Carolina, Chapel Hill, United States |
AuthorAffiliation_xml | – name: c Department of Radiology, University of North Carolina, Chapel Hill, United States – name: b Biomedical Research Imaging Center, University of North Carolina, Chapel Hill, United States – name: a Department of Psychology & Neuroscience, University of North Carolina, Chapel Hill, United States – name: d Carolina Institute of Developmental Disabilities, University of North Carolina, Chapel Hill, United States |
Author_xml | – sequence: 1 givenname: Mackenzie surname: Woodburn fullname: Woodburn, Mackenzie email: mawoodbu@live.unc.edu organization: Department of Psychology & Neuroscience, University of North Carolina, Chapel Hill, United States – sequence: 2 givenname: Cheyenne L. surname: Bricken fullname: Bricken, Cheyenne L. organization: Department of Psychology & Neuroscience, University of North Carolina, Chapel Hill, United States – sequence: 3 givenname: Zhengwang surname: Wu fullname: Wu, Zhengwang organization: Biomedical Research Imaging Center, University of North Carolina, Chapel Hill, United States – sequence: 4 givenname: Gang surname: Li fullname: Li, Gang organization: Biomedical Research Imaging Center, University of North Carolina, Chapel Hill, United States – sequence: 5 givenname: Li surname: Wang fullname: Wang, Li organization: Biomedical Research Imaging Center, University of North Carolina, Chapel Hill, United States – sequence: 6 givenname: Weili surname: Lin fullname: Lin, Weili organization: Biomedical Research Imaging Center, University of North Carolina, Chapel Hill, United States – sequence: 7 givenname: Margaret A. surname: Sheridan fullname: Sheridan, Margaret A. organization: Department of Psychology & Neuroscience, University of North Carolina, Chapel Hill, United States – sequence: 8 givenname: Jessica R. surname: Cohen fullname: Cohen, Jessica R. organization: Department of Psychology & Neuroscience, University of North Carolina, Chapel Hill, United States |
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Keywords | Early brain development Cognition Longitudinal MRI Maturational coupling Structural covariance networks |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceptualization: M.A.W., W.L., M.A.S., and J.R.C.; Methodology: M.A.W., Z.W., G.L., L.W., W.L., M.A.S., and J.R.C.; Formal analysis: M.A.W.; Investigation: M.A.W., C.L.B., W.L., M.A.S., and J.R.C.; Writing – Original Draft: M.A.W., M.A.S., and J.R.C.; Writing – Review & Editing: M.A.W., Z.W., G.L., L.W., W.L., M.A.S., and J.R.C; Visualization: M.A.W.; Supervision: W.L., M.A.S., and J.R.C.; Project Administration: W.L., M.A.S., and J.R.C.; Funding Acquisition: G.L., L.W., W.L., M.A.S., and J.R.C. Author contributions |
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Snippet | •Cortical thickness networks were mapped longitudinally from infancy to six years.•Brain network segregation increased between early infancy and six... The interactions of brain regions with other regions at the network level likely provide the infrastructure necessary for cognitive processes to develop.... |
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StartPage | 118232 |
SubjectTerms | Brain Brain architecture Childhood Children Cognition Cognition & reasoning Cognitive ability Cognitive development Early brain development Executive function Integration Longitudinal MRI Maturation Maturational coupling Motor skill learning Specialization Structural covariance networks |
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Title | The maturation and cognitive relevance of structural brain network organization from early infancy to childhood |
URI | https://www.clinicalkey.com/#!/content/1-s2.0-S1053811921005097 https://dx.doi.org/10.1016/j.neuroimage.2021.118232 https://www.proquest.com/docview/2554331029 https://www.proquest.com/docview/2538050296 https://pubmed.ncbi.nlm.nih.gov/PMC8372198 https://doaj.org/article/56dfda2dc6f54cb58942347c509bffee |
Volume | 238 |
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