Journal Article

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

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

2023

Overview

Motor cortex (M1) has been thought to form a continuous somatotopic homunculus extending down the precentral gyrus from foot to face representations 1 , 2 , despite evidence for concentric functional zones 3 and maps of complex actions 4 . 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 action 5 and physiological control 6 , arousal 7 , errors 8 and pain 9 . 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 actions 4 and connectivity to internal organs 10 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. Functional MRI studies across ages show that the classic homunculus of the motor cortex in humans is in fact discontinuous, alternating with action control-linked regions termed the somato-cognitive action network.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 59/36 / 59/57 / 631/378/2632/1323 / 631/378/2632/1368 / 631/378/2632/1663 / 631/378/2649/2150 / Adrenal medulla / Animals / Brain Mapping - methods / Child / Cognition / Cognitive ability / Cortex (motor) / Datasets as Topic / Feet / Foot - physiology / Functional magnetic resonance imaging / Hand - physiology / Homunculus / Humanities and Social Sciences / Humans / Infant / Infant, Newborn / Macaca - anatomy & histology / Macaca - physiology / Magnetic resonance / Magnetic Resonance Imaging / Motor Cortex - anatomy & histology / Motor Cortex - physiology / Motor task performance / Mouth / Mouth - physiology / multidisciplinary / Neuroimaging / Pediatrics / Physiology / Precentral gyrus / Science / Science (multidisciplinary) / Structure-function relationships