Individual differences in frontal midline theta activity during visuomotor adaptation are related to execution noise

Jonker, Zeb D.; van der Vliet, Rick; Maquelin, Guido; van der Cruijsen, Joris; Ribbers, Gerard M.; Selles, Ruud W.; Donchin, Opher; Frens, Maarten A. · 2020 · Crossref

DOI: 10.1101/2020.07.12.188581

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Summary

This study investigates the neurophysiological correlates of implicit motor adaptation, specifically focusing on frontal midline theta activity (FMΘ) during visuomotor tasks with small, gradual perturbations. Previous research established that FMΘ correlates with error magnitude in motor adaptation, but it remained unclear whether this activity persists during implicit learning (unconscious adaptation driven by small errors), drives between-trial error correction, or relates to individual differences in motor learning parameters such as execution and planning noise. The authors aimed to replicate a prior visuomotor adaptation experiment with a larger cohort to address these gaps. The researchers recruited 60 participants who performed 900 trials of ballistic reaching movements using a robotic handle, with visual feedback provided via a cursor on a screen. The experiment included baseline trials and perturbation trials where the cursor position was gradually shifted by up to 9 degrees. Electroencephalography (EEG) was recorded simultaneously. Movement data were analyzed using a Bayesian state-space model to estimate individual parameters for adaptation rate, planning noise, and execution noise. EEG data were processed to analyze time-domain amplitudes and frequency-domain power, particularly focusing on theta band activity (4–8 Hz) at frontal midline channels. The results demonstrated that FMΘ is present even during small perturbations that likely invoke implicit adaptation. However, FMΘ did not predict between-trial error correction, indicating it does not directly drive the adaptive motor updates. Instead, the sensitivity of FMΘ to error magnitude varied significantly across individuals. Specifically, participants with higher execution noise exhibited lower FMΘ sensitivity to error magnitude. The authors found that this relationship was fully explained by error probability rather than error magnitude alone. When FMΘ was modeled against the probability of an error occurring (based on individual error distributions), the correlation with execution noise disappeared. This suggests that FMΘ reflects a surprise-like saliency signal, responding to the unexpectedness of an error relative to an individual’s internal noise model, rather than the absolute size of the error. These findings imply that frontal midline theta activity serves as a neural marker for surprise or saliency during motor performance, potentially signaling when an error is unexpected given the individual’s motor noise characteristics. This challenges the view that FMΘ directly encodes error magnitude for corrective learning and instead positions it as a signal that may drive awareness or cognitive control in response to salient, unexpected errors. The study provides a refined understanding of the role of FMΘ in implicit motor learning, linking neural activity to individual differences in motor execution noise.

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