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Functional Brain Networks Develop from a “Local to Distributed” Organization

Author

Listed:
  • Damien A Fair
  • Alexander L Cohen
  • Jonathan D Power
  • Nico U F Dosenbach
  • Jessica A Church
  • Francis M Miezin
  • Bradley L Schlaggar
  • Steven E Petersen

Abstract

The mature human brain is organized into a collection of specialized functional networks that flexibly interact to support various cognitive functions. Studies of development often attempt to identify the organizing principles that guide the maturation of these functional networks. In this report, we combine resting state functional connectivity MRI (rs-fcMRI), graph analysis, community detection, and spring-embedding visualization techniques to analyze four separate networks defined in earlier studies. As we have previously reported, we find, across development, a trend toward ‘segregation’ (a general decrease in correlation strength) between regions close in anatomical space and ‘integration’ (an increased correlation strength) between selected regions distant in space. The generalization of these earlier trends across multiple networks suggests that this is a general developmental principle for changes in functional connectivity that would extend to large-scale graph theoretic analyses of large-scale brain networks. Communities in children are predominantly arranged by anatomical proximity, while communities in adults predominantly reflect functional relationships, as defined from adult fMRI studies. In sum, over development, the organization of multiple functional networks shifts from a local anatomical emphasis in children to a more “distributed” architecture in young adults. We argue that this “local to distributed” developmental characterization has important implications for understanding the development of neural systems underlying cognition. Further, graph metrics (e.g., clustering coefficients and average path lengths) are similar in child and adult graphs, with both showing “small-world”-like properties, while community detection by modularity optimization reveals stable communities within the graphs that are clearly different between young children and young adults. These observations suggest that early school age children and adults both have relatively efficient systems that may solve similar information processing problems in divergent ways.Author Summary: The first two decades of life represent a period of extraordinary developmental change in sensory, motor, and cognitive abilities. One of the ultimate goals of developmental cognitive neuroscience is to link the complex behavioral milestones that occur throughout this time period with the equally intricate functional and structural changes of the underlying neural substrate. Achieving this goal would not only give us a deeper understanding of normal development but also a richer insight into the nature of developmental disorders. In this report, we use computational analyses, in combination with a recently developed MRI technique that measures spontaneous brain activity, to help us to understand the principles that guide the maturation of the human brain. We find that brain regions in children communicate with other regions more locally but that over age communication becomes more distributed. Interestingly, the efficiency of communication in children (measured as a ‘small world’ network) is comparable to that of the adult. We argue that these findings have important implications for understanding both the maturation and the function of neural systems in typical and atypical development.

Suggested Citation

  • Damien A Fair & Alexander L Cohen & Jonathan D Power & Nico U F Dosenbach & Jessica A Church & Francis M Miezin & Bradley L Schlaggar & Steven E Petersen, 2009. "Functional Brain Networks Develop from a “Local to Distributed” Organization," PLOS Computational Biology, Public Library of Science, vol. 5(5), pages 1-14, May.
  • Handle: RePEc:plo:pcbi00:1000381
    DOI: 10.1371/journal.pcbi.1000381
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    References listed on IDEAS

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    Cited by:

    1. Hui Wang & Chen Chen & Hsieh Fushing, 2012. "Extracting Multiscale Pattern Information of fMRI Based Functional Brain Connectivity with Application on Classification of Autism Spectrum Disorders," PLOS ONE, Public Library of Science, vol. 7(10), pages 1-14, October.
    2. Margaret A Sheridan & Khaled Sarsour & Douglas Jutte & Mark D'Esposito & W Thomas Boyce, 2012. "The Impact of Social Disparity on Prefrontal Function in Childhood," PLOS ONE, Public Library of Science, vol. 7(4), pages 1-13, April.
    3. Peter K Boulos & Manish S Dalwani & Jody Tanabe & Susan K Mikulich-Gilbertson & Marie T Banich & Thomas J Crowley & Joseph T Sakai, 2016. "Brain Cortical Thickness Differences in Adolescent Females with Substance Use Disorders," PLOS ONE, Public Library of Science, vol. 11(4), pages 1-20, April.
    4. Jianzhong Chen & Angela Tam & Valeria Kebets & Csaba Orban & Leon Qi Rong Ooi & Christopher L. Asplund & Scott Marek & Nico U. F. Dosenbach & Simon B. Eickhoff & Danilo Bzdok & Avram J. Holmes & B. T., 2022. "Shared and unique brain network features predict cognitive, personality, and mental health scores in the ABCD study," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Audrey C. Luo & Valerie J. Sydnor & Adam Pines & Bart Larsen & Aaron F. Alexander-Bloch & Matthew Cieslak & Sydney Covitz & Andrew A. Chen & Nathalia Bianchini Esper & Eric Feczko & Alexandre R. Franc, 2024. "Functional connectivity development along the sensorimotor-association axis enhances the cortical hierarchy," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Anna Peng & Natasha Z Kirkham & Denis Mareschal, 2018. "Information processes of task-switching and modality-shifting across development," PLOS ONE, Public Library of Science, vol. 13(6), pages 1-18, June.

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