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      Early Development of Functional Network Segregation Revealed by Connectomic Analysis of the Preterm Human Brain

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          Abstract

          Human brain functional networks are topologically organized with nontrivial connectivity characteristics such as small-worldness and densely linked hubs to support highly segregated and integrated information processing. However, how they emerge and change at very early developmental phases remains poorly understood. Here, we used resting-state functional MRI and voxel-based graph theory analysis to systematically investigate the topological organization of whole-brain networks in 40 infants aged around 31 to 42 postmenstrual weeks. The functional connectivity strength and heterogeneity increased significantly in primary motor, somatosensory, visual, and auditory regions, but much less in high-order default-mode and executive-control regions. The hub and rich-club structures in primary regions were already present at around 31 postmenstrual weeks and exhibited remarkable expansions with age, accompanied by increased local clustering and shortest path length, indicating a transition from a relatively random to a more organized configuration. Moreover, multivariate pattern analysis using support vector regression revealed that individual brain maturity of preterm babies could be predicted by the network connectivity patterns. Collectively, we highlighted a gradually enhanced functional network segregation manner in the third trimester, which is primarily driven by the rapid increases of functional connectivity of the primary regions, providing crucial insights into the topological development patterns prior to birth.

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          Author and article information

          Journal
          Cereb Cortex
          Cereb. Cortex
          cercor
          Cerebral Cortex (New York, NY)
          Oxford University Press
          1047-3211
          1460-2199
          March 2017
          03 March 2016
          01 March 2018
          : 27
          : 3
          : 1949-1963
          Affiliations
          [1 ] State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University , Beijing 100875, China
          [2 ] Department of Radiology, Children's Hospital of Philadelphia , Philadelphia, PA 19104, USA
          [3 ] Department of Pediatrics and
          [4 ] Department of Radiology, University of Texas Southwestern Medical Center , Dallas, TX 75390, USA
          [5 ] Department of Radiology, University of Pennsylvania , Philadelphia, PA 19104, USA
          Author notes
          [* ]Address correspondence to Yong He, State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China. Email: yong.he@ 123456bnu.edu.cn ; Hao Huang, Department of Radiology, University of Pennsylvania, Philadelphia, PA 19104, USA. Email: huangh6@ 123456email.chop.edu
          Article
          PMC6059235 PMC6059235 6059235 bhw038
          10.1093/cercor/bhw038
          6059235
          26941380
          © The Author 2016. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com
          Page count
          Pages: 15
          Funding
          Funded by: National Institutes of Health 10.13039/100000002
          Funded by: Natural Science Foundation of China 10.13039/501100001809
          Award ID: 91432115
          Award ID: 31221003
          Funded by: National Science Fund for Distinguished Young Scholars
          Award ID: 81225012
          Funded by: 111 Project
          Award ID: B07008
          Funded by: Open Research Fund of the State Key Laboratory of Cognitive Neuroscience and Learning
          Award ID: CNLYB1407
          Categories
          Original Articles

          connectome, preterm, hub, functional connectivity, rich club

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