Increasing human motor skill acquisition by driving theta-gamma coupling.

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

doi:10.7554/elife.67355

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.

Highlights

The acquisition of motor skills is a central part of our everyday lives, from learning new behaviours such as riding a bike to the recovery of function after brain injury such as a stroke [1,2,3,4]
To a previous study in the spatial working memory domain [39], in the active transcranial alternating current stimulation (tACS) condition, participants received (1) theta-gamma peak stimulation (TGP; Figure 1A), whereby gamma frequency (75 Hz) stimulation was delivered during the peak of a 6 Hz theta envelope as is found naturally in the human motor cortex [29], or (2) an active control, theta-gamma trough (TGT) stimulation, whereby the gamma stimulation was delivered in the negative half of the theta envelope
Our results suggest that driving γ activity during the peak, but not the trough, of θ oscillations improves motor skill acquisition. θ-γ PAC has consistently been demonstrated to relate to learning in the rodent CA1 [13,14,15,16], where oscillations in the θ (5-12 Hz) band become dominant during active exploration [42], and have been widely hypothesised to allow information coming into CA1 from distant regions to be divided into discrete units for processing [43,44]

Summary

Introduction

The acquisition of motor skills is a central part of our everyday lives, from learning new behaviours such as riding a bike to the recovery of function after brain injury such as a stroke [1,2,3,4]. Acquisition of motor skills is linked to a number of cortical and subcortical brain regions, but among these, primary motor cortex (M1) is thought to play a central role [1,2,4,5], making this a key target for neurorehabilitative interventions [6,7,8]. The mechanisms underpinning learning have been extensively studied in the hippocampus, where theta-amplitude-coupled mid-gamma frequency activity (θ-γ phaseamplitude coupling; PAC) has been hypothesised as a key learning-related mechanism. Gamma coherence in the hippocampus alters during learning [9] and memory retrieval [10], and its relative synchrony during task predicts subsequent recall [11,12]

Methods

Results

Discussion

Conclusion