Changes in resting state functional connectivity associated with dynamic adaptation of wrist movements

Abstract

Dynamic adaptation is an error-driven process of adjusting planned motor actions to changes in task dynamics (1). Adapted motor plans are consolidated into motor memories that contribute to better performance on re-exposure to the same dynamic condition. In parallel, dynamic perturbations can be compensated for by alternate motor control processes, such as co-contraction, that contribute to error reduction (2). Whether these control strategies share the same neural resources for memory formation is unclear. To address this gap in knowledge, we used a novel fMRI-compatible wrist robot, the MR-SoftWrist (3), to identify neural processes specific to dynamic adaptation and subsequent memory formation. Using the MR-SoftWrist, we acquired fMRI during a motor performance and a dynamic perturbation task to localize brain networks of interest. Resting state fMRI scans were acquired immediately before and after task performance to quantify changes in resting state functional connectivity (rsFC) within these networks. Twenty-four hours later, we assessed behavioral retention of training. A variance decomposition analysis was used to isolate behavior associated with adaptation versus alternate error reduction strategies. Immediately after the dynamic perturbation task, rsFC significantly increased within the corticothalamic-cerebellar network of the trained wrist and decreased interhemispherically within the cortical sensorimotor network. These changes were associated to behavioral measures of initial acquisition and retention, indicative of memory formation. Variance decomposition analysis revealed that increases within the cortico-thalamic-cerebellar network were associated with adaptation, while interhemispheric decreases in rsFC within the sensorimotor network were associated with alternate error reduction processes. Significance Statement Motor memory formation processes have been studied using resting state functional connectivity (rsFC) before and after exposure to adaptation tasks. However, due to technical limitations, previous studies have not investigated rsFC within brain regions localized during task execution, nor quantified rsFC within minutes after task performance. The present study used an fMRI-compatible wrist robot to localize relevant brain regions during dynamic adaptation within the cortico-thalamic-cerebellar network and bilateral sensorimotor network. Immediately following dynamic adaptation, we measured significant changes in rsFC within these networks, that were associated with adaptation behavior and with gains in behavior assessed 24 hours later, indicative of memory formation. Variance decomposition analysis identified distinct rsFC networks associated with adaptation specific processes, and with alternate motor control strategies.