Reconfigurations of cortical manifold structure during reward-based motor learning.

Publisher: eLife Sciences Publications, Ltd Country of Publication: England NLM ID: 101579614 Publication Model: Electronic Cited Medium: Internet ISSN: 2050-084X (Electronic) Linking ISSN: 2050084X NLM ISO Abbreviation: Elife Subsets: MEDLINE

Original Publication: Cambridge, UK : eLife Sciences Publications, Ltd., 2012-

Magnetic Resonance Imaging* ; Reward* ; Learning*/physiology; Humans ; Male ; Female ; Adult ; Young Adult ; Sensorimotor Cortex/physiology ; Sensorimotor Cortex/diagnostic imaging ; Brain Mapping ; Motor Activity/physiology ; Cerebral Cortex/physiology ; Cerebral Cortex/diagnostic imaging

Adaptive motor behavior depends on the coordinated activity of multiple neural systems distributed across the brain. While the role of sensorimotor cortex in motor learning has been well established, how higher-order brain systems interact with sensorimotor cortex to guide learning is less well understood. Using functional MRI, we examined human brain activity during a reward-based motor task where subjects learned to shape their hand trajectories through reinforcement feedback. We projected patterns of cortical and striatal functional connectivity onto a low-dimensional manifold space and examined how regions expanded and contracted along the manifold during learning. During early learning, we found that several sensorimotor areas in the dorsal attention network exhibited increased covariance with areas of the salience/ventral attention network and reduced covariance with areas of the default mode network (DMN). During late learning, these effects reversed, with sensorimotor areas now exhibiting increased covariance with DMN areas. However, areas in posteromedial cortex showed the opposite pattern across learning phases, with its connectivity suggesting a role in coordinating activity across different networks over time. Our results establish the neural changes that support reward-based motor learning and identify distinct transitions in the functional coupling of sensorimotor to transmodal cortex when adapting behavior.
Competing Interests: QN, CA, AD, JN, JW, TZ, RF, JS No competing interests declared, DG, JG is an employee of Voxel AI Inc. This funding source had no role in the design, management, data analysis, presentation, or interpretation and write-up of the data
(© 2023, Nick et al.)

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PJT175012 Canada CAPMC CIHR; RGPIN-2017-04684 Natural Sciences and Engineering Research Council of Canada

Keywords: brain connectivity; human; mainfold; motor learning; neuroscience; reaching; reinforcement learning

Dryad 10.5061/dryad.7sqv9s512

Date Created: 20240625 Date Completed: 20240625 Latest Revision: 20240627

20240627

PMC11198988

10.7554/eLife.91928

38916598