Comparison of online and offline applications of dual-site transcranial alternating current stimulation (tACS) over the pre-supplementary motor area (preSMA) and right inferior frontal gyrus (rIFG) for improving response inhibition

Hakuei Fujiyama; AlexandraG Williams; Jane Tan; Oron Levin; Mark R Hinder

doi:10.1016/j.neuropsychologia.2023.108737

Comparison of online and offline applications of dual-site transcranial alternating current stimulation (tACS) over the pre-supplementary motor area (preSMA) and right inferior frontal gyrus (rIFG) for improving response inhibition

Neuropsychologia. 2023 Dec 15:191:108737. doi: 10.1016/j.neuropsychologia.2023.108737. Epub 2023 Nov 22.

Authors

Hakuei Fujiyama¹, AlexandraG Williams², Jane Tan³, Oron Levin⁴, Mark R Hinder⁵

Affiliations

¹ School of Psychology, Murdoch University, Western Australia, Australia; Centre for Healthy Ageing, Health Futures Institute, Murdoch University, Western Australia, Australia; Centre for Molecular Medicine and Innovative Therapeutics, Murdoch University, Western Australia, Australia. Electronic address: H.Fujiyama@murdoch.edu.au.
² School of Psychology, Murdoch University, Western Australia, Australia.
³ School of Psychology, Murdoch University, Western Australia, Australia; Centre for Healthy Ageing, Health Futures Institute, Murdoch University, Western Australia, Australia.
⁴ Department of Health Promotion and Rehabilitation, Lithuanian Sports University, Kaunas, Lithuania; Movement Control & Neuroplasticity Research Group, Group Biomedical Sciences, Catholic University Leuven, Leuven, Belgium.
⁵ Sensorimotor Neuroscience and Ageing Research Group, School of Psychological Sciences, College of Health and Medicine, University of Tasmania, Tasmania, Australia.

PMID: 37995902
DOI: 10.1016/j.neuropsychologia.2023.108737

Abstract

The efficacy of transcranial alternating current stimulation (tACS) is thought to be brain state-dependent, such that tACS during task performance would be hypothesised to offer greater potential for improving performance compared to tACS at rest. However, to date, no empirical study has tested this postulation. The current study compared the effects of dual-site beta tACS applied during a stop signal task (online) to the effects of the same tACS protocol applied prior to the task (offline) and a sham control stimulation in 53 young, healthy adults (32 female; 18-35 yrs). The right inferior frontal gyrus (rIFG) and centre (midline) of the pre-supplementary motor area (preSMA), which are thought to play critical roles in action cancellation, were simultaneously stimulated, sending phase-synchronised stimulation for 15 min with the aim of increasing functional connectivity. The offline group showed significant within-group improvement in response inhibition without showing overt task-related changes in functional connectivity measured with EEG connectivity analysis, suggesting offline tACS is efficacious in inducing behavioural changes potentially via a post-stimulation early plasticity mechanism. In contrast, neither the online nor sham group showed significant improvements in response inhibition. However, EEG connectivity analysis revealed significantly increased task-related functional connectivity following online stimulation and a medium effect size observed in correlation analyses suggested that an increase in functional connectivity in the beta band at rest was potentially associated with an improvement in response inhibition. Overall, the results indicate that both online and offline dual-site beta tACS can be beneficial in improving inhibitory control via distinct underlying mechanisms.

Keywords: Functional connectivity; Inferior frontal gyrus; Inhibitory control; Pre-supplementary motor area; Timing; Transcranial alternating current stimulation; stop signal task.

MeSH terms

Adult
Brain
Female
Humans
Motor Cortex* / physiology
Prefrontal Cortex
Task Performance and Analysis
Transcranial Direct Current Stimulation* / methods