Transcranial direct current stimulation facilitates response inhibition through dynamic modulation of the fronto-basal ganglia network

Marco Sandrini; Benjamin Xu; Rita Volochayev; Oluwole Awosika; Wen-Tung Wang; John A Butman; Leonardo G Cohen

doi:10.1016/j.brs.2019.08.004

Transcranial direct current stimulation facilitates response inhibition through dynamic modulation of the fronto-basal ganglia network

Brain Stimul. 2020 Jan-Feb;13(1):96-104. doi: 10.1016/j.brs.2019.08.004. Epub 2019 Aug 7.

Authors

Marco Sandrini¹, Benjamin Xu², Rita Volochayev³, Oluwole Awosika³, Wen-Tung Wang⁴, John A Butman⁵, Leonardo G Cohen³

Affiliations

¹ Human Cortical Physiology and Neurorehabilitation Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, 20892, USA; Center for Neuroscience and Regenerative Medicine, Uniformed Services University of Health Sciences, Bethesda, MD, 20814, USA; Department of Psychology, University of Roehampton, London, SW15 4JD, UK.
² Human Cortical Physiology and Neurorehabilitation Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, 20892, USA; Center for Neuroscience and Regenerative Medicine, Uniformed Services University of Health Sciences, Bethesda, MD, 20814, USA. Electronic address: benxu1@mail.nih.gov.
³ Human Cortical Physiology and Neurorehabilitation Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, 20892, USA.
⁴ Center for Neuroscience and Regenerative Medicine, Uniformed Services University of Health Sciences, Bethesda, MD, 20814, USA.
⁵ Center for Neuroscience and Regenerative Medicine, Uniformed Services University of Health Sciences, Bethesda, MD, 20814, USA; Radiology and Imaging Sciences, National Institutes of Health, Clinical Center, Bethesda, MD, 20892, USA.

Abstract

Background: Response inhibition refers to the ability to stop an on-going action quickly when it is no longer appropriate. Previous studies showed that transcranial direct current stimulation (tDCS) applied with the anode over the right inferior frontal cortex (rIFC), a critical node of the fronto-basal ganglia inhibitory network, improved response inhibition. However, the tDCS effects on brain activity and network connectivity underlying this behavioral improvement are not known.

Objective: This study aimed to address the effects of tDCS applied with the anode over the rIFC on brain activity and network functional connectivity underlying the behavioral change in response inhibition.

Methods: Thirty participants performed a stop-signal task in a typical laboratory setting as a baseline during the first study visit (i.e., Session 1). In the second visit (at least 24 h after Session 1), all participants underwent resting-state functional magnetic resonance imaging (rsfMRI) scans before and after 1.5 mA tDCS (Anodal or Sham). Immediately following the post-tDCS rsfMRI, participants performed the same stop-signal task as in Session 1 during an event-related fMRI (efMRI) scan in a 3T scanner. Changes in task performance, i.e., the stop-signal response time (SSRT), a measure of response inhibition efficiency, was determined relative to the participants' own baseline performance in Session 1.

Results: Consistent with previous findings, Anodal tDCS facilitated the SSRT. efMRI results showed that Anodal tDCS strengthened the functional connectivity between right pre-supplementary motor area (rPreSMA) and subthalamic nuclei during Stop responses. rsfMRI revealed changes in intrinsic connectivity between rIFC and caudate, and between rIFC, rPreSMA, right inferior parietal cortex (rIPC), and right dorsolateral prefrontal cortex (rDLPFC) after Anodal tDCS. In addition, corresponding to the regions of rsfMRI connectivity change, the efMRI BOLD signal in the rDLPFC and rIPC during Go responses accounted for 74% of the variance in SSRT after anodal tDCS, indicating an effect of tDCS on the Go-Stop process.

Conclusion: These results indicate that tDCS with the anode over the rIFC facilitates response inhibition by modulating neural activity and functional connectivity in the fronto-basal ganglia as well as rDLPFC and rIPC as an integral part of the response inhibition network.

Keywords: Brain stimulation; Inhibitory control; Prefrontal cortex; Response inhibition; fMRI; tDCS.

Publication types

Research Support, N.I.H., Intramural
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Adult
Basal Ganglia / physiology*
Connectome
Female
Humans
Magnetic Resonance Imaging
Male
Motor Cortex / physiology
Prefrontal Cortex / physiology*
Reaction Time
Transcranial Direct Current Stimulation / methods*

Grants and funding

Z01 NS002978-10/ImNIH/Intramural NIH HHS/United States