IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-26704-y.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-26704-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-26704-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Golia Shafiei & Ben D. Fulcher & Bradley Voytek & Theodore D. Satterthwaite & Sylvain Baillet & Bratislav Misic, 2023. "Neurophysiological signatures of cortical micro-architecture," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Sofie L. Valk & Ting Xu & Casey Paquola & Bo-yong Park & Richard A. I. Bethlehem & Reinder Vos de Wael & Jessica Royer & Shahrzad Kharabian Masouleh & Şeyma Bayrak & Peter Kochunov & B. T. Thomas Yeo , 2022. "Genetic and phylogenetic uncoupling of structure and function in human transmodal cortex," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Vincent Bazinet & Justine Y. Hansen & Reinder Vos de Wael & Boris C. Bernhardt & Martijn P. Heuvel & Bratislav Misic, 2023. "Assortative mixing in micro-architecturally annotated brain connectomes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Svenja Küchenhoff & Şeyma Bayrak & Rachel G. Zsido & Amin Saberi & Boris C. Bernhardt & Susanne Weis & H. Lina Schaare & Julia Sacher & Simon Eickhoff & Sofie L. Valk, 2024. "Relating sex-bias in human cortical and hippocampal microstructure to sex hormones," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    5. Aleksandr Talishinsky & Jonathan Downar & Petra E. Vértes & Jakob Seidlitz & Katharine Dunlop & Charles J. Lynch & Heather Whalley & Andrew McIntosh & Fidel Vila-Rodriguez & Zafiris J. Daskalakis & Da, 2022. "Regional gene expression signatures are associated with sex-specific functional connectivity changes in depression," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    6. Stefano Berto & Alex H. Treacher & Emre Caglayan & Danni Luo & Jillian R. Haney & Michael J. Gandal & Daniel H. Geschwind & Albert A. Montillo & Genevieve Konopka, 2022. "Association between resting-state functional brain connectivity and gene expression is altered in autism spectrum disorder," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    7. 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.
    8. Justine Y. Hansen & Golia Shafiei & Jacob W. Vogel & Kelly Smart & Carrie E. Bearden & Martine Hoogman & Barbara Franke & Daan Rooij & Jan Buitelaar & Carrie R. McDonald & Sanjay M. Sisodiya & Lianne , 2022. "Local molecular and global connectomic contributions to cross-disorder cortical abnormalities," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    9. Stuart Oldham & Gareth Ball, 2023. "A phylogenetically-conserved axis of thalamocortical connectivity in the human brain," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    10. Ang Li & Haiyang Liu & Xu Lei & Yini He & Qian Wu & Yan Yan & Xin Zhou & Xiaohan Tian & Yingjie Peng & Shangzheng Huang & Kaixin Li & Meng Wang & Yuqing Sun & Hao Yan & Cheng Zhang & Sheng He & Ruquan, 2023. "Hierarchical fluctuation shapes a dynamic flow linked to states of consciousness," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    11. Junjiao Feng & Liang Zhang & Chunhui Chen & Jintao Sheng & Zhifang Ye & Kanyin Feng & Jing Liu & Ying Cai & Bi Zhu & Zhaoxia Yu & Chuansheng Chen & Qi Dong & Gui Xue, 2022. "A cognitive neurogenetic approach to uncovering the structure of executive functions," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    12. Sungyong Um & Bin Zhang & Sunil Wattal & Youngjin Yoo, 2023. "Software Components and Product Variety in a Platform Ecosystem: A Dynamic Network Analysis of WordPress," Information Systems Research, INFORMS, vol. 34(4), pages 1339-1374, December.
    13. Adam R. Pines & Bart Larsen & Zaixu Cui & Valerie J. Sydnor & Maxwell A. Bertolero & Azeez Adebimpe & Aaron F. Alexander-Bloch & Christos Davatzikos & Damien A. Fair & Ruben C. Gur & Raquel E. Gur & H, 2022. "Dissociable multi-scale patterns of development in personalized brain networks," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Alessandra Griffa & Mathieu Mach & Julien Dedelley & Daniel Gutierrez-Barragan & Alessandro Gozzi & Gilles Allali & Joanes Grandjean & Dimitri Ville & Enrico Amico, 2023. "Evidence for increased parallel information transmission in human brain networks compared to macaques and male mice," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    15. Meeli Mullari & Nicolas Fossat & Niels H. Skotte & Andrea Asenjo-Martinez & David T. Humphreys & Jens Bukh & Agnete Kirkeby & Troels K. H. Scheel & Michael L. Nielsen, 2023. "Characterising the RNA-binding protein atlas of the mammalian brain uncovers RBM5 misregulation in mouse models of Huntington’s disease," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    16. Manish Saggar & James M. Shine & Raphaël Liégeois & Nico U. F. Dosenbach & Damien Fair, 2022. "Precision dynamical mapping using topological data analysis reveals a hub-like transition state at rest," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    17. Tharick A. Pascoal & Mira Chamoun & Elad Lax & Hsiao-Ying Wey & Monica Shin & Kok Pin Ng & Min Su Kang & Sulantha Mathotaarachchi & Andrea L. Benedet & Joseph Therriault & Firoza Z. Lussier & Frederic, 2022. "[11C]Martinostat PET analysis reveals reduced HDAC I availability in Alzheimer’s disease," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    18. Tingting Bo & Jie Li & Ganlu Hu & Ge Zhang & Wei Wang & Qian Lv & Shaoling Zhao & Junjie Ma & Meng Qin & Xiaohui Yao & Meiyun Wang & Guang-Zhong Wang & Zheng Wang, 2023. "Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    19. Maria Osetrova & Anna Tkachev & Waltraud Mair & Patricia Guijarro Larraz & Olga Efimova & Ilia Kurochkin & Elena Stekolshchikova & Nickolay Anikanov & Juat Chin Foo & Amaury Cazenave-Gassiot & Aleksan, 2024. "Lipidome atlas of the adult human brain," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    20. Lynne Krohn & Karl Heilbron & Cornelis Blauwendraat & Regina H. Reynolds & Eric Yu & Konstantin Senkevich & Uladzislau Rudakou & Mehrdad A. Estiar & Emil K. Gustavsson & Kajsa Brolin & Jennifer A. Rus, 2022. "Genome-wide association study of REM sleep behavior disorder identifies polygenic risk and brain expression effects," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26704-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.