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Sensory-motor cortices shape functional connectivity dynamics in the human brain

Author

Listed:
  • Xiaolu Kong

    (National University of Singapore
    Yong Loo Lin School of Medicine
    National University of Singapore)

  • Ru Kong

    (National University of Singapore
    Yong Loo Lin School of Medicine
    National University of Singapore)

  • Csaba Orban

    (National University of Singapore
    Yong Loo Lin School of Medicine
    National University of Singapore)

  • Peng Wang

    (Max Planck Institute for Human Cognitive and Brain Sciences)

  • Shaoshi Zhang

    (National University of Singapore
    Yong Loo Lin School of Medicine
    National University of Singapore
    Integrative Sciences and Engineering Programme (ISEP), National University of Singapore)

  • Kevin Anderson

    (Harvard University)

  • Avram Holmes

    (Yale University
    Yale University)

  • John D. Murray

    (Yale University)

  • Gustavo Deco

    (Universitat Pompeu Fabra
    Universitat Barcelona)

  • Martijn Heuvel

    (Amsterdam University Medical Center)

  • B. T. Thomas Yeo

    (National University of Singapore
    Yong Loo Lin School of Medicine
    National University of Singapore
    Integrative Sciences and Engineering Programme (ISEP), National University of Singapore)

Abstract

Large-scale biophysical circuit models provide mechanistic insights into the micro-scale and macro-scale properties of brain organization that shape complex patterns of spontaneous brain activity. We developed a spatially heterogeneous large-scale dynamical circuit model that allowed for variation in local synaptic properties across the human cortex. Here we show that parameterizing local circuit properties with both anatomical and functional gradients generates more realistic static and dynamic resting-state functional connectivity (FC). Furthermore, empirical and simulated FC dynamics demonstrates remarkably similar sharp transitions in FC patterns, suggesting the existence of multiple attractors. Time-varying regional fMRI amplitude may track multi-stability in FC dynamics. Causal manipulation of the large-scale circuit model suggests that sensory-motor regions are a driver of FC dynamics. Finally, the spatial distribution of sensory-motor drivers matches the principal gradient of gene expression that encompasses certain interneuron classes, suggesting that heterogeneity in excitation-inhibition balance might shape multi-stability in FC dynamics.

Suggested Citation

  • Xiaolu Kong & Ru Kong & Csaba Orban & Peng Wang & Shaoshi Zhang & Kevin Anderson & Avram Holmes & John D. Murray & Gustavo Deco & Martijn Heuvel & B. T. Thomas Yeo, 2021. "Sensory-motor cortices shape functional connectivity dynamics in the human brain," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26704-y
    DOI: 10.1038/s41467-021-26704-y
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    References listed on IDEAS

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    1. Kevin M. Anderson & Meghan A. Collins & Rowena Chin & Tian Ge & Monica D. Rosenberg & Avram J. Holmes, 2020. "Transcriptional and imaging-genetic association of cortical interneurons, brain function, and schizophrenia risk," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    2. Michael J. Hawrylycz & Ed S. Lein & Angela L. Guillozet-Bongaarts & Elaine H. Shen & Lydia Ng & Jeremy A. Miller & Louie N. van de Lagemaat & Kimberly A. Smith & Amanda Ebbert & Zackery L. Riley & Chr, 2012. "An anatomically comprehensive atlas of the adult human brain transcriptome," Nature, Nature, vol. 489(7416), pages 391-399, September.
    3. Casey Paquola & Reinder Vos De Wael & Konrad Wagstyl & Richard A I Bethlehem & Seok-Jun Hong & Jakob Seidlitz & Edward T Bullmore & Alan C Evans & Bratislav Misic & Daniel S Margulies & Jonathan Small, 2019. "Microstructural and functional gradients are increasingly dissociated in transmodal cortices," PLOS Biology, Public Library of Science, vol. 17(5), pages 1-28, May.
    4. Cedric Huchuan Xia & Zongming Ma & Rastko Ciric & Shi Gu & Richard F. Betzel & Antonia N. Kaczkurkin & Monica E. Calkins & Philip A. Cook & Angel García de la Garza & Simon N. Vandekar & Zaixu Cui & T, 2018. "Linked dimensions of psychopathology and connectivity in functional brain networks," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    5. Raphaël Liégeois & Jingwei Li & Ru Kong & Csaba Orban & Dimitri Van De Ville & Tian Ge & Mert R. Sabuncu & B. T. Thomas Yeo, 2019. "Resting brain dynamics at different timescales capture distinct aspects of human behavior," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
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