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Atypical functional connectome hierarchy in autism

Author

Listed:
  • Seok-Jun Hong

    (McGill University
    Center for the Developing Brain, Child Mind Institute)

  • Reinder Vos de Wael

    (McGill University)

  • Richard A. I. Bethlehem

    (University of Cambridge)

  • Sara Lariviere

    (McGill University)

  • Casey Paquola

    (McGill University)

  • Sofie L. Valk

    (Medical Faculty, Heinrich Heine University
    Research Centre Jülich)

  • Michael P. Milham

    (Center for the Developing Brain, Child Mind Institute
    Nathan Kline Institute)

  • Adriana Di Martino

    (Autism Center, Child Mind Institute)

  • Daniel S. Margulies

    (Frontlab, Institut du Cerveau et de la Moelle épinière, UPMC UMRS 1127, Inserm U 1127)

  • Jonathan Smallwood

    (University of York)

  • Boris C. Bernhardt

    (McGill University)

Abstract

One paradox of autism is the co-occurrence of deficits in sensory and higher-order socio-cognitive processing. Here, we examined whether these phenotypical patterns may relate to an overarching system-level imbalance—specifically a disruption in macroscale hierarchy affecting integration and segregation of unimodal and transmodal networks. Combining connectome gradient and stepwise connectivity analysis based on task-free functional magnetic resonance imaging (fMRI), we demonstrated atypical connectivity transitions between sensory and higher-order default mode regions in a large cohort of individuals with autism relative to typically-developing controls. Further analyses indicated that reduced differentiation related to perturbed stepwise connectivity from sensory towards transmodal areas, as well as atypical long-range rich-club connectivity. Supervised pattern learning revealed that hierarchical features predicted deficits in social cognition and low-level behavioral symptoms, but not communication-related symptoms. Our findings provide new evidence for imbalances in network hierarchy in autism, which offers a parsimonious reference frame to consolidate its diverse features.

Suggested Citation

  • Seok-Jun Hong & Reinder Vos de Wael & Richard A. I. Bethlehem & Sara Lariviere & Casey Paquola & Sofie L. Valk & Michael P. Milham & Adriana Di Martino & Daniel S. Margulies & Jonathan Smallwood & Bor, 2019. "Atypical functional connectome hierarchy in autism," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-08944-1
    DOI: 10.1038/s41467-019-08944-1
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    Cited by:

    1. Tatsuya Osaki & Tomoya Duenki & Siu Yu A. Chow & Yasuhiro Ikegami & Romain Beaubois & Timothée Levi & Nao Nakagawa-Tamagawa & Yoji Hirano & Yoshiho Ikeuchi, 2024. "Complex activity and short-term plasticity of human cerebral organoids reciprocally connected with axons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. 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.
    3. Zirui Huang & George A. Mashour & Anthony G. Hudetz, 2023. "Functional geometry of the cortex encodes dimensions of consciousness," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Mühlberger, Wolfgang, 2022. "Iraks Suche nach dem Gesellschaftsvertrag: Ein Ansatz zur Förderung gesellschaftlichen Zusammenhalts und staatlicher Resilienz," IDOS Discussion Papers 13/2022, German Institute of Development and Sustainability (IDOS).
    5. Julie Ottoy & Min Su Kang & Jazlynn Xiu Min Tan & Lyndon Boone & Reinder Vos de Wael & Bo-yong Park & Gleb Bezgin & Firoza Z. Lussier & Tharick A. Pascoal & Nesrine Rahmouni & Jenna Stevenson & Jaime , 2024. "Tau follows principal axes of functional and structural brain organization in Alzheimer’s disease," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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