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A mind-body interface alternates with effector-specific regions in motor cortex

Authors
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,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,Nico U.F. Dosenbach,Evan Gordon,Roselyne Chauvin,Andrew Van,Michael Myers,Timothy Laumann,Dillan Newbold,Charles Lynch,Nicole Seider,Samuel Krimmel,Kristen Scheidter,Ruth Miller,David Montez,Carolina D’Andrea,Damion Demeter,Deanna Barch,Christopher Smyser,Cynthia Rogers,Kelly Botteron,John Pruett,Jon Willie,Joshua Shimony,Benjamin Kay,Scott Norris,Chad Sylvester,Jonathan Power,Deanna Greene,Jarod Roland,Steven Petersen,Marcus Raichle,Damien Fair
+74 authors
,Nico Dosenbach
Published
Oct 28, 2022
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Abstract

SUMMARY Primary motor cortex (M1) has been thought to form a continuous somatotopic homunculus extending down precentral gyrus from foot to face representations 1,2 . The motor homunculus has remained a textbook pillar of functional neuroanatomy, despite evidence for concentric functional zones 3 and maps of complex actions 4 . Using our highest precision functional magnetic resonance imaging (fMRI) data and methods, we discovered that the classic homunculus is interrupted by regions with sharpy distinct connectivity, structure, and function, alternating with effector-specific (foot, hand, mouth) areas. These inter-effector regions exhibit decreased cortical thickness and strong functional connectivity to each other, and to prefrontal, insular, and subcortical regions of the Cingulo-opercular network (CON), critical for executive action 5 and physiological control 6 , arousal 7 , and processing of errors 8 and pain 9 . This interdigitation of action control-linked and motor effector regions was independently verified in the three largest fMRI datasets. Macaque and pediatric (newborn, infant, child) precision fMRI revealed potential cross-species analogues and developmental precursors of the inter-effector system. An extensive battery of motor and action fMRI tasks documented concentric somatotopies for each effector, separated by the CON-linked inter-effector regions. The inter-effector regions lacked movement specificity and co-activated during action planning (coordination of hands and feet), and axial body movement (e.g., abdomen, eyebrows). These results, together with prior work demonstrating stimulation-evoked complex actions 4 and connectivity to internal organs (e.g., adrenal medulla) 10 , suggest that M1 is punctuated by an integrative system for implementing whole-body action plans. Thus, two parallel systems intertwine in motor cortex to form an integrate-isolate pattern: effector-specific regions (foot, hand, mouth) for isolating fine motor control, and a mind-body interface (MBI) for the integrative whole-organism coordination of goals, physiology, and body movement.

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