Theta but not beta power is positively associated with better explicit motor task learning

Joris Van Der Cruijsen,Mana Manoochehri,Zeb D Jonker,Eleni-Rosalina Andrinopoulou,Maarten A Frens,Gerard M Ribbers,Alfred C Schouten,Ruud W Selles

doi:10.1016/j.neuroimage.2021.118373

Joris Van Der Cruijsen, Mana Manoochehri + Show 6 more

Open Access

https://doi.org/10.1016/j.neuroimage.2021.118373

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Abstract

Neurophysiologic correlates of motor learning that can be monitored during neurorehabilitation interventions can facilitate the development of more effective learning methods. Previous studies have focused on the role of the beta band (14–30 Hz) because of its clear response during motor activity. However, it is difficult to discriminate between beta activity related to learning a movement and performing the movement. In this study, we analysed differences in the electroencephalography (EEG) power spectra of complex and simple explicit sequential motor tasks in healthy young subjects. The complex motor task (CMT) allowed EEG measurement related to motor learning. In contrast, the simple motor task (SMT) made it possible to control for EEG activity associated with performing the movement without significant motor learning. Source reconstruction of the EEG revealed task-related activity from 5 clusters covering both primary motor cortices (M1) and 3 clusters localised to different parts of the cingulate cortex (CC). We found no association between M1 beta power and learning, but the CMT produced stronger bilateral beta suppression compared to the SMT. However, there was a positive association between contralateral M1 theta (5–8 Hz) and alpha (8–12 Hz) power and motor learning, and theta and alpha power in the posterior mid-CC and posterior CC were positively associated with greater motor learning. These findings suggest that the theta and alpha bands are more related to motor learning than the beta band, which might merely relate to the level of perceived difficulty during learning.

Highlights

Motor learning—defined as acquiring new skills, improving existing skills, or regaining/reinforcing skills through practice—is critical for developing motor function at all stages of life Magill and Anderson (2017)
The cluster centres were approximated to the contralateral (c)M1 and ipsilateral (i)M1 and cingulate cortex (CC) (anterior mid-CC [anterior mid-cingulate cortex (aMCC)], posterior [p]MCC (Vogt, 2016), and posterior CC [posterior cingulate cortex (PCC)])
The PCC cluster exhibited an alpha eventrelated desynchronization (ERD) and theta event-related synchronization (ERS) burst-like pattern time-locked to the metronome, and trial execution was accompanied by beta ERD in both motor learning tasks

Summary

Introduction

Motor learning—defined as acquiring new skills, improving existing skills, or regaining/reinforcing skills through practice—is critical for developing motor function at all stages of life Magill and Anderson (2017). Differences in brain structure and function (Tomassini et al, 2011) and genetic factors (McHughen et al, 2010) contribute to the variability in motor learning capacity amongst healthy individuals To better understand this variability, investigators have analysed neurophysiologic correlates of motor learning by electroencephalography (EEG)/magnetoencephalography (MEG). In addition to the beta band, motor learning has been suggested to be related to theta (5–8 Hz), alpha (8–12 Hz), and gamma (60–90 Hz) frequency band modulation (Boonstra et al, 2007; Meissner et al, 2018; Sugata et al, 2018; Zhuang et al, 1997) None of these studies controlled for brain activity associated with performing the movement; it is unclear whether the activity is associated with motor learning

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