Driving human motor cortical oscillations leads to behaviorally relevant changes in local GABAA inhibition: A tACS-TMS study

Magdalena Nowak*, Emily Hinson, Freek Van Ede, Alek Pogosyan, Andrea Guerra, Andrew Quinn, Peter Brown, Charlotte J. Stagg

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Beta and gamma oscillations are the dominant oscillatory activity in the human motor cortex (M1). However, their physiological basis and precise functional significance remain poorly understood. Here, we used transcranial magnetic stimulation (TMS) to examine the physiological basis and behavioral relevance of driving beta and gamma oscillatory activity in the human M1 using transcranial alternating current stimulation (tACS). tACS was applied using a sham-controlled crossover design at individualized intensity for 20 min and TMSwas performed at rest (before, during, and after tACS) and during movement preparation (before and after tACS).Wedemonstrated that driving gamma frequency oscillations using tACS led to a significant, duration-dependent decrease in local resting-state GABAA inhibition, as quantified by short interval intracortical inhibition. The magnitude of this effect was positively correlated with the magnitude of GABAA decrease duringmovementpreparation,whengammaactivity in motor circuitry isknownto increase. In addition,gamma tACS-induced change in GABAA inhibition was closely related to performance in a motor learning task such that subjects who demonstrated a greater increase in GABAA inhibition also showed faster short-term learning. The findings presented here contribute to our understanding of the neurophysiological basis of motor rhythms and suggest that tACS may have similar physiological effects to endogenously driven local oscillatory activity. Moreover, the ability to modulate local interneuronal circuits by tACS in a behaviorally relevant manner provides a basis for tACS as a putative therapeutic intervention.

Original languageEnglish
Pages (from-to)4481-4492
Number of pages12
JournalThe Journal of Neuroscience
Volume37
Issue number17
DOIs
Publication statusPublished - 26 Apr 2017
Externally publishedYes

Funding

This work was carried out in the National Institute for Health Research Oxford Biomedical Research Centre based at Oxford University Hospitals, National Health Service Foundation Trust, Oxford University. M.N. is funded by the Wellcome Trust. C.J.S. holds a Sir Henry Dale Fellowship funded by the Wellcome Trust and the Royal Society (Grant 102584/Z/13/Z). P.B. is funded by the Medical Research Council (Grant MC_UU_12024/1) and the National Institute of Health Research Oxford Biomedical Research Centre. F.v.E. is funded by a Newton International Fellowship from the Royal Society and the British Academy (Grant NF140330) and a Marie Sklodowska-Curie Fellowship from the European Commission (ACCESS2WM).

FundersFunder number
National Health Service Foundation Trust
Sir Henry Dale Fellowship
National Institute of Health Research Oxford Biomedical Research Centre
University of Oxford
National Institute for Health Research Oxford Biomedical Research Centre
UK Research and Innovation
European CommissionACCESS2WM
Wellcome Trust102584
Royal Society102584/Z/13/Z
Medical Research CouncilMC_UU_12024/1
British AcademyNF140330

    Keywords

    • Concurrent tACS and TMS
    • GABA inhibition
    • Gamma oscillations
    • Motor excitability
    • Motor learning
    • tACS

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