Pre-movement changes in sensorimotor beta oscillations predict motor adaptation drive

Henry T. Darch,Iain D. Gilchrist,Richard Apps,Nadia L. Cerminara

doi:10.1038/s41598-020-74833-z

Henry T. Darch, Iain D. Gilchrist + Show 2 more

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https://doi.org/10.1038/s41598-020-74833-z

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Abstract

Beta frequency oscillations in scalp electroencephalography (EEG) recordings over the primary motor cortex have been associated with the preparation and execution of voluntary movements. Here, we test whether changes in beta frequency are related to the preparation of adapted movements in human, and whether such effects generalise to other species (cat). Eleven healthy adult humans performed a joystick visuomotor adaptation task. Beta (15–25 Hz) scalp EEG signals recorded over the motor cortex during a pre-movement preparatory phase were, on average, significantly reduced in amplitude during early adaptation trials compared to baseline, late adaptation, or aftereffect trials. The changes in beta were not related to measurements of reaction time or reach duration. We also recorded local field potential (LFP) activity within the primary motor cortex of three cats during a prism visuomotor adaptation task. Analysis of these signals revealed similar reductions in motor cortical LFP beta frequencies during early adaptation. This effect was present when controlling for any influence of the reaction time and reach duration. Overall, the results are consistent with a reduction in pre-movement beta oscillations predicting an increase in adaptive drive in upcoming task performance when motor errors are largest in magnitude and the rate of adaptation is greatest.

Highlights

Beta frequency oscillations in scalp electroencephalography (EEG) recordings over the primary motor cortex have been associated with the preparation and execution of voluntary movements
These findings suggest that motor cortical areas support a long-term memory trace of established motor programs, into which newly learned dynamics are integrated
We found that beta frequency power recorded over the motor cortex as scalp EEG in humans, or directly from the primary motor cortex as local field potential (LFP) activity in cats, was reduced prior to movement in trials in the early adaptation phase of a joystick visuomotor adaptation task or when target mis-reaches occurred in a prism visuomotor adaptation task

Summary

Introduction

Beta frequency oscillations in scalp electroencephalography (EEG) recordings over the primary motor cortex have been associated with the preparation and execution of voluntary movements. The beta rebound has been observed to be attenuated during trials in which large errors are m ade[21], and this has been attributed to a reduction in the subject’s confidence in the motor program, prompting subsequent adjustment or exploratory m ovements[22] This is considered to reflect a role in feedback error processing to modify subsequent motor actions, possibly indicating an adaptive drive—defined here as neuronal signals generated in response to an increase in behavioural error computed to support modification of subsequent motor actions. The present study sought to clarify whether changes in pre-movement beta oscillations are consistent with an increase in adaptive drive

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