Increasing human motor skill acquisition by driving theta-gamma coupling

Haya Akkad, Joshua Dupont-Hadwen, Edward Kane, Carys Evans, Liam Barrett, Amba Frese, Irena Tetkovic, Sven Bestmann, Charlotte J Stagg, Haya Akkad, Joshua Dupont-Hadwen, Edward Kane, Carys Evans, Liam Barrett, Amba Frese, Irena Tetkovic, Sven Bestmann, Charlotte J Stagg

Abstract

Skill learning is a fundamental adaptive process, but the mechanisms remain poorly understood. Some learning paradigms, particularly in the memory domain, are closely associated with gamma activity that is amplitude modulated by the phase of underlying theta activity, but whether such nested activity patterns also underpin skill learning is unknown. Here, we addressed this question by using transcranial alternating current stimulation (tACS) over sensorimotor cortex to modulate theta-gamma activity during motor skill acquisition, as an exemplar of a non-hippocampal-dependent task. We demonstrated, and then replicated, a significant improvement in skill acquisition with theta-gamma tACS, which outlasted the stimulation by an hour. Our results suggest that theta-gamma activity may be a common mechanism for learning across the brain and provides a putative novel intervention for optimizing functional improvements in response to training or therapy.

Keywords: human; motor learning; neuroscience; non-invasive brain stimulation; theta-gamma coupling; transcranial alternating current stimulation.

Conflict of interest statement

HA, JD, EK, CE, LB, AF, IT, SB, CS No competing interests declared

© 2021, Akkad et al.

Figures

Figure 1.. Theta–gamma transcranial alternating current stimulation…
Figure 1.. Theta–gamma transcranial alternating current stimulation (tACS) protocol and task.
(A) Electrode montage: the theta–gamma tACS montage was delivered with one electrode centred over right M1 (red, C4) and the other over the parietal vertex (blue, Pz). Insert: electrical field distribution projected on a rendered reconstruction of the cortical surface in a single individual, demonstrating significant current within M1. (B) tACS waveform: a 75 Hz gamma rhythm was amplitude modulated by the peak (theta–gamma peak [TGP]; upper panel) or trough (theta–gamma trough [TGT]; lower panel) envelope of a 2 mA peak-to-peak 6 Hz theta rhythm. (C) Experimental design: all subjects performed a baseline block, followed by five task blocks. In experiment 2, to assess the duration of behavioural effects, subjects performed an additional two task blocks 75 min after the initial task was complete. Each block consisted of 70 trials with an inter-block interval of 2 min, apart from a 10 min and 1 hr break after blocks 4 and 5, respectively. Stimulation was delivered for 20 min during the first three blocks. (D) Trial design: all trials began with three auditory warning tones acting as a ready-steady-go cue. At the third tone, participants abducted their thumb along the x-axis as quickly as possible and were given online visual feedback of their performance via a screen positioned in front of them. Feedback was presented as a scrolling bar chart with the magnitude of acceleration displayed on a trial-by-trial basis; a green bar indicated acceleration was higher than the previous trial and a red bar indicated the opposite.
Figure 2.. Theta–gamma peak (TGP)-transcranial alternating current…
Figure 2.. Theta–gamma peak (TGP)-transcranial alternating current stimulation (tACS) enhances motor skill acquisition.
Mean ballistic thumb abduction acceleration for each stimulation condition. Each point represents the mean of 10 trials across participants and the error bars depict the standard error between participants. (A) Experiment 1: during stimulation, TGP significantly increased skill acquisition over the course of the experiment (i.e. acceleration gain), compared to sham and theta–gamma trough (TGT). (B) Experiment 2: when replicated in an independent sample, skill acquisition was again significantly greater in the TGP stimulation group compared with sham. This effect was maintained for at least 75 min after stimulation.
Figure 2—figure supplement 1.. Transcranial alternating current…
Figure 2—figure supplement 1.. Transcranial alternating current stimulation (tACS) does not modulate behavioural variability.
There was no effect of tACS on variability in terms of acceleration within blocks in either (A) experiment 1 or (B) experiment 2.

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