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Developmental increases in white matter network controllability support a growing diversity of brain dynamics

Author

Listed:
  • Evelyn Tang

    (University of Pennsylvania)

  • Chad Giusti

    (University of Pennsylvania)

  • Graham L. Baum

    (University of Pennsylvania)

  • Shi Gu

    (University of Pennsylvania)

  • Eli Pollock

    (University of Pennsylvania)

  • Ari E. Kahn

    (University of Pennsylvania)

  • David R. Roalf

    (University of Pennsylvania)

  • Tyler M. Moore

    (University of Pennsylvania)

  • Kosha Ruparel

    (University of Pennsylvania)

  • Ruben C. Gur

    (University of Pennsylvania)

  • Raquel E. Gur

    (University of Pennsylvania)

  • Theodore D. Satterthwaite

    (University of Pennsylvania)

  • Danielle S. Bassett

    (University of Pennsylvania
    University of Pennsylvania)

Abstract

As the human brain develops, it increasingly supports coordinated control of neural activity. The mechanism by which white matter evolves to support this coordination is not well understood. Here we use a network representation of diffusion imaging data from 882 youth ages 8–22 to show that white matter connectivity becomes increasingly optimized for a diverse range of predicted dynamics in development. Notably, stable controllers in subcortical areas are negatively related to cognitive performance. Investigating structural mechanisms supporting these changes, we simulate network evolution with a set of growth rules. We find that all brain networks are structured in a manner highly optimized for network control, with distinct control mechanisms predicted in child vs. older youth. We demonstrate that our results cannot be explained by changes in network modularity. This work reveals a possible mechanism of human brain development that preferentially optimizes dynamic network control over static network architecture.

Suggested Citation

  • Evelyn Tang & Chad Giusti & Graham L. Baum & Shi Gu & Eli Pollock & Ari E. Kahn & David R. Roalf & Tyler M. Moore & Kosha Ruparel & Ruben C. Gur & Raquel E. Gur & Theodore D. Satterthwaite & Danielle , 2017. "Developmental increases in white matter network controllability support a growing diversity of brain dynamics," Nature Communications, Nature, vol. 8(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_s41467-017-01254-4
    DOI: 10.1038/s41467-017-01254-4
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    Cited by:

    1. Huili Sun & Rongtao Jiang & Wei Dai & Alexander J. Dufford & Stephanie Noble & Marisa N. Spann & Shi Gu & Dustin Scheinost, 2023. "Network controllability of structural connectomes in the neonatal brain," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    2. Disheng Tang & Joel Zylberberg & Xiaoxuan Jia & Hannah Choi, 2024. "Stimulus type shapes the topology of cellular functional networks in mouse visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. S. Parker Singleton & Andrea I. Luppi & Robin L. Carhart-Harris & Josephine Cruzat & Leor Roseman & David J. Nutt & Gustavo Deco & Morten L. Kringelbach & Emmanuel A. Stamatakis & Amy Kuceyeski, 2022. "Receptor-informed network control theory links LSD and psilocybin to a flattening of the brain’s control energy landscape," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

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