Transcutaneous auricular vagus nerve stimulation enhanced emotional inhibitory control via increasing intrinsic prefrontal couplings

Siyu Zhu; Qi Liu; Xiaolu Zhang; Menghan Zhou; Xinqi Zhou; Fangyuan Ding; Rong Zhang; Benjamin Becker; Keith M Kendrick; Weihua Zhao

doi:10.1016/j.ijchp.2024.100462

Transcutaneous auricular vagus nerve stimulation enhanced emotional inhibitory control via increasing intrinsic prefrontal couplings

Int J Clin Health Psychol. 2024 Apr-Jun;24(2):100462. doi: 10.1016/j.ijchp.2024.100462. Epub 2024 Apr 17.

Authors

Siyu Zhu^{1

2

3}, Qi Liu¹, Xiaolu Zhang⁴, Menghan Zhou¹, Xinqi Zhou⁵, Fangyuan Ding⁶, Rong Zhang⁷, Benjamin Becker^{1

8}, Keith M Kendrick¹, Weihua Zhao¹

Affiliations

¹ The Center of Psychosomatic Medicine, Sichuan Provincial Center for Mental Health, Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China, Chengdu, 611731, PR China.
² The Laboratory of Sport Psychology, School of Sport Training, Chengdu Sport University, Chengdu, 610041, PR China.
³ Sichuan Key Laboratory of Psychology and Behavior of Discipline Inspection and Supervision, Sichuan Normal University, Chengdu 610066, PR China.
⁴ Anhui Children's Hospital, Pediatric Hospital Affiliated to Fudan University, Hefei 230051, PR China.
⁵ Institute of Brain and Psychological Science, Sichuan Normal University, Chengdu, 610066, PR China.
⁶ College of National Culture and Cognitive Science, Guizhou Minzu University, Guiyang, 550025, PR China.
⁷ Neuroscience Research Institute, Key Laboratory for Neuroscience, Ministry of Education of China, National Committee of Health and Family Planning of China and Department of Neurobiology, School of Basic Medical Sciences, Peking University, Beijing, 100191, PR China.
⁸ The State Key Laboratory of Brain and Cognitive Sciences, The University of Hong Kong, Department of Psychology, Hong Kong, 999077, PR China.

Abstract

Background: Inhibitory control represents a core executive function that critically facilitates adaptive behavior and survival in an ever-changing environment. Non-invasive transcutaneous auricular vagus nerve stimulation (taVNS) has been hypothesized to improve behavioral inhibition performance, however the neurocomputational mechanism of taVNS-induced neuroenhancement remains elusive.

Method: In the current study, we investigated the efficacy of taVNS in a sham-controlled between-subject functional near infrared spectroscopy (fNIRS) experiment with an emotional face Go/No-Go paradigm in ninety healthy young adults.

Results: After a data quality check, eighty-two subjects were included in the final data analysis. Behaviorally, the taVNS improved No-Go response accuracy, together with computational modeling using Hierarchical Bayesian estimation of the Drift Diffusion Model (HDDM) indicating that it specifically reduced the information accumulation rate for Go responses, and this was negatively associated with increased accuracy of No-Go responses. On the neural level, taVNS enhanced engagement of the bilateral inferior frontal gyrus (IFG) during inhibition of angry expression faces and modulated functional couplings (FCs) within the prefrontal inhibitory control network. Mediation models revealed that taVNS-induced facilitation of inhibitory control was critically mediated by a decreased information accumulation for Go responses and concomitantly enhanced neurofunctional coupling between the inferior and orbital frontal cortex.

Discussion: Our findings demonstrate a potential for taVNS to improve emotional inhibitory control via reducing pre-potent responses and enhancing FCs within prefrontal inhibitory control networks, suggesting a promising therapeutic role in treating specific disorders characterized by inhibitory control deficits.

Keywords: Computational modeling; Dynamic functional connectivity; Inhibitory control; Mediation model; Transcutaneous auricular vagus nerve stimulation.