Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation

Author:

Gale Daniel J.1,Areshenkoff Corson N.12,Standage Dominic I.1,Nashed Joseph Y.1,Markello Ross D.3,Flanagan J. Randall12ORCID,Smallwood Jonathan12,Gallivan Jason P.124ORCID

Affiliation:

1. Centre for Neuroscience, Queen’s University, Kingston, ON K7L 3N6, Canada

2. Department of Psychology, Queen’s University, Kingston, ON K7L 3N6, Canada

3. Montréal Neurological Institute, McGill University, Montréal, QC H3A 0G4, Canada

4. Department of Biomedical and Molecular Sciences, Queen’s University, Kingston, ON K7L 3N6, Canada

Abstract

Sensorimotor learning is a dynamic, systems-level process that involves the combined action of multiple neural systems distributed across the brain. Although much is known about the specialized cortical systems that support specific components of action (such as reaching), we know less about how cortical systems function in a coordinated manner to facilitate adaptive behavior. To address this gap, our study measured human brain activity using functional MRI (fMRI) while participants performed a classic sensorimotor adaptation task and used a manifold learning approach to describe how behavioral changes during adaptation relate to changes in the landscape of cortical activity. During early adaptation, areas in the parietal and premotor cortices exhibited significant contraction along the cortical manifold, which was associated with their increased covariance with regions in the higher-order association cortex, including both the default mode and fronto-parietal networks. By contrast, during Late adaptation, when visuomotor errors had been largely reduced, a significant expansion of the visual cortex along the cortical manifold was associated with its reduced covariance with the association cortex and its increased intraconnectivity. Lastly, individuals who learned more rapidly exhibited greater covariance between regions in the sensorimotor and association cortices during early adaptation. These findings are consistent with a view that sensorimotor adaptation depends on changes in the integration and segregation of neural activity across more specialized regions of the unimodal cortex with regions in the association cortex implicated in higher-order processes. More generally, they lend support to an emerging line of evidence implicating regions of the default mode network (DMN) in task-based performance.

Funder

Canadian Institutes of Health Research

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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