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

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 Monk, Ryland L. Miller, Athanasia Metoki, David F. Montez, Annie Zheng, Immanuel Elbau, Thomas Madison, Tomoyuki Nishino, Michael J. Myers, Sydney Kaplan, Carolina Badke D’Andrea, Damion V. Demeter, Matthew Feigelis, Julian S. B. Ramirez, Ting Xu, Deanna M. Barch, Christopher D. Smyser, Cynthia E. Rogers, Jan Zimmermann, Kelly N. Botteron, John R. Pruett, Jon T. Willie, Peter Brunner, Joshua S. Shimony, Benjamin P. Kay, Scott Marek, Scott A. Norris, Caterina Gratton, Chad M. Sylvester, Jonathan D. Power, Conor Liston, Deanna J. Greene, Jarod L. Roland, Steven E. Petersen, Marcus E. Raichle, Timothy O. Laumann, Damien A. Fair and Nico U. F. Dosenbach ()
Additional contact information
Evan M. Gordon: Washington University School of Medicine
Roselyne J. Chauvin: Washington University School of Medicine
Andrew N. Van: Washington University School of Medicine
Aishwarya Rajesh: Washington University School of Medicine
Ashley Nielsen: Washington University School of Medicine
Dillan J. Newbold: Washington University School of Medicine
Charles J. Lynch: Weill Cornell Medicine
Nicole A. Seider: 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
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
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
Christopher D. Smyser: Washington University School of Medicine
Cynthia E. Rogers: Weill Cornell 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
Peter Brunner: Washington University in St. Louis
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
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
Marcus E. Raichle: Washington University School of Medicine
Timothy O. Laumann: Washington University School of Medicine
Damien A. Fair: University of Minnesota
Nico U. F. Dosenbach: Washington University School of Medicine

Nature, 2023, vol. 617, issue 7960, 351-359

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41586-023-05964-2

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