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

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.

Effects of transcranial direct current stimulation of left and right inferior frontal gyrus on creative divergent thinking are moderated by changes in inhibition control

“…However, a later study by Friehs and Frings (2019) did not find a modulation of error rates in any form but only a significant increase in SSRT after cathodal tDCS (c-tDCS). Sandrini et al (2020) further verified that both the rDLPFC and right inferior parietal cortex (rIPC) represent an essential part of the fronto-basal-ganglia network, which is critical for rapid response inhibition. Accordingly, Aron et al (2014) proposed that DLPFC implements task rules rather than inhibition.…”

“…Besides IFG, the right dorsolateral prefrontal cortex (rDLPFC) may be engaged in active inhibitory processing of both motor and higher level memory representations (Penolazzi et al 2014;Frings 2018, 2019;Sandrini et al 2020). Using tDCS, Penolazzi et al (2014) reported that cathodal stimulation over rDLPFC leads to decreased inhibition during the standard retrieval-practice paradigm (RPP).…”

tDCS over the inferior frontal gyri and visual cortices did not improve response inhibition

“…However, these types of distant bipolar montages can result in widespread and diffuse neuromodulation 33,45,46 . In fact, a recent study showed that anodal IFG stimulation not only altered the functional connectivity and neural activity in the fronto-basal-ganglia network presumed to implement response inhibition, but that it also induced activity changes in both the dorsolateral prefrontal and the inferior parietal cortices 47 . Such widespread modulations raise the possibility that other regions might drive the previously reported effects.…”

Transcranial Direct Current Stimulation Combined With Cognitive Training Induces Response Inhibition Facilitation Through Distinct Neural Responses According to the Stimulation Site: A Follow-up Event-Related Potentials Study

“…6 While CRPs may promote the development of an automatic association between a specific cue and a No-go response 7 by enhancing frontal top-down inhibitory control, 8 active tDCS over the right inferior frontal cortex (rIFC) or the right dorsolateral prefrontal cortex (rDLPFC) is thought to induce specific neural modifications including the fronto-basal-ganglia network. 9,10 In a recent meta-analysis, Khaleghi et al 11 highlight that unilateral tDCS over DLPFC leads to less risk-taking behaviors in healthy individuals through the neuromodulation of the meso-cortico-limbic dopamine system. Combining training with tDCS is nowadays thought to improve training outcomes through synergistic effects, as tDCS may enhance the training effect by facilitating learning through specific neuroplastic changes, while training could magnify the acute effect of the neuroplasticity intervention.…”