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A somato-cognitive action network alternates with effector regions in motor cortex

Author

Listed:
  • Evan M. Gordon

    (Washington University School of Medicine)

  • Roselyne J. Chauvin

    (Washington University School of Medicine)

  • Andrew N. Van

    (Washington University School of Medicine
    Washington University in St. Louis)

  • Aishwarya Rajesh

    (Washington University School of Medicine)

  • Ashley Nielsen

    (Washington University School of Medicine)

  • Dillan J. Newbold

    (Washington University School of Medicine
    New York University Langone Medical Center)

  • Charles J. Lynch

    (Weill Cornell Medicine)

  • Nicole A. Seider

    (Washington University School of Medicine
    Washington University School of Medicine)

  • Samuel R. Krimmel

    (Washington University School of Medicine)

  • Kristen M. Scheidter

    (Washington University School of Medicine)

  • Julia Monk

    (Washington University School of Medicine)

  • Ryland L. Miller

    (Washington University School of Medicine
    Washington University School of Medicine)

  • Athanasia Metoki

    (Washington University School of Medicine)

  • David F. Montez

    (Washington University School of Medicine)

  • Annie Zheng

    (Washington University School of Medicine)

  • Immanuel Elbau

    (Weill Cornell Medicine)

  • Thomas Madison

    (University of Minnesota)

  • Tomoyuki Nishino

    (Washington University School of Medicine)

  • Michael J. Myers

    (Washington University School of Medicine)

  • Sydney Kaplan

    (Washington University School of Medicine)

  • Carolina Badke D’Andrea

    (Washington University School of Medicine
    Washington University School of Medicine
    University of California San Diego)

  • Damion V. Demeter

    (University of California San Diego)

  • Matthew Feigelis

    (University of California San Diego)

  • Julian S. B. Ramirez

    (Child Mind Institute)

  • Ting Xu

    (Child Mind Institute)

  • Deanna M. Barch

    (Washington University School of Medicine
    Washington University School of Medicine
    Washington University in St. Louis)

  • Christopher D. Smyser

    (Washington University School of Medicine
    Washington University School of Medicine
    Washington University School of Medicine)

  • Cynthia E. Rogers

    (Weill Cornell Medicine
    Washington University School of Medicine)

  • Jan Zimmermann

    (University of Minnesota)

  • Kelly N. Botteron

    (Washington University School of Medicine)

  • John R. Pruett

    (Washington University School of Medicine)

  • Jon T. Willie

    (Washington University School of Medicine
    Weill Cornell Medicine
    Washington University School of Medicine)

  • Peter Brunner

    (Washington University in St. Louis
    Washington University School of Medicine)

  • Joshua S. Shimony

    (Washington University School of Medicine)

  • Benjamin P. Kay

    (Washington University School of Medicine)

  • Scott Marek

    (Washington University School of Medicine)

  • Scott A. Norris

    (Washington University School of Medicine
    Washington University School of Medicine)

  • Caterina Gratton

    (Florida State University)

  • Chad M. Sylvester

    (Washington University School of Medicine)

  • Jonathan D. Power

    (Weill Cornell Medicine)

  • Conor Liston

    (Weill Cornell Medicine)

  • Deanna J. Greene

    (University of California San Diego)

  • Jarod L. Roland

    (Washington University School of Medicine)

  • Steven E. Petersen

    (Washington University School of Medicine
    Washington University School of Medicine
    Washington University in St. Louis
    Washington University in St. Louis)

  • Marcus E. Raichle

    (Washington University School of Medicine
    Washington University School of Medicine
    Washington University in St. Louis
    Washington University in St. Louis)

  • Timothy O. Laumann

    (Washington University School of Medicine)

  • Damien A. Fair

    (University of Minnesota
    University of Minnesota
    University of Minnesota)

  • Nico U. F. Dosenbach

    (Washington University School of Medicine
    Washington University School of Medicine
    Washington University in St. Louis
    Washington University in St. Louis)

Abstract

Motor cortex (M1) has been thought to form a continuous somatotopic homunculus extending down the precentral gyrus from foot to face representations1,2, despite evidence for concentric functional zones3 and maps of complex actions4. Here, using precision functional magnetic resonance imaging (fMRI) methods, we find that the classic homunculus is interrupted by regions with distinct connectivity, structure and function, alternating with effector-specific (foot, hand and mouth) areas. These inter-effector regions exhibit decreased cortical thickness and strong functional connectivity to each other, as well as to the cingulo-opercular network (CON), critical for action5 and physiological control6, arousal7, errors8 and pain9. This interdigitation of action control-linked and motor effector regions was verified in the three largest fMRI datasets. Macaque and pediatric (newborn, infant and child) precision fMRI suggested cross-species homologues and developmental precursors of the inter-effector system. A battery of motor and action fMRI tasks documented concentric effector somatotopies, separated by the CON-linked inter-effector regions. The inter-effectors lacked movement specificity and co-activated during action planning (coordination of hands and feet) and axial body movement (such as of the abdomen or eyebrows). These results, together with previous studies demonstrating stimulation-evoked complex actions4 and connectivity to internal organs10 such as the adrenal medulla, suggest that M1 is punctuated by a system for whole-body action planning, the somato-cognitive action network (SCAN). In M1, two parallel systems intertwine, forming an integrate–isolate pattern: effector-specific regions (foot, hand and mouth) for isolating fine motor control and the SCAN for integrating goals, physiology and body movement.

Suggested Citation

  • Evan M. Gordon & Roselyne J. Chauvin & Andrew N. Van & Aishwarya Rajesh & Ashley Nielsen & Dillan J. Newbold & Charles J. Lynch & Nicole A. Seider & Samuel R. Krimmel & Kristen M. Scheidter & Julia Mo, 2023. "A somato-cognitive action network alternates with effector regions in motor cortex," Nature, Nature, vol. 617(7960), pages 351-359, May.
  • Handle: RePEc:nat:nature:v:617:y:2023:i:7960:d:10.1038_s41586-023-05964-2
    DOI: 10.1038/s41586-023-05964-2
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    Cited by:

    1. Youzhi Qu & Kai Fu & Linjing Wang & Yu Zhang & Haiyan Wu & Quanying Liu, 2024. "Hypergraph-Based Multitask Feature Selection with Temporally Constrained Group Sparsity Learning on fMRI," Mathematics, MDPI, vol. 12(11), pages 1-16, June.

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