The right inferior frontal gyrus as pivotal node and effective regulator of the basal ganglia-thalamocortical response inhibition circuit

Qian Zhuang; Lei Qiao; Lei Xu; Shuxia Yao; Shuaiyu Chen; Xiaoxiao Zheng; Jialin Li; Meina Fu; Keshuang Li; Deniz Vatansever; Stefania Ferraro; Keith M Kendrick; Benjamin Becker

doi:10.1093/psyrad/kkad016

The right inferior frontal gyrus as pivotal node and effective regulator of the basal ganglia-thalamocortical response inhibition circuit

Psychoradiology. 2023 Oct 13:3:kkad016. doi: 10.1093/psyrad/kkad016. eCollection 2023.

Authors

Qian Zhuang^{1

2}, Lei Qiao³, Lei Xu^{1

4}, Shuxia Yao¹, Shuaiyu Chen², Xiaoxiao Zheng^{1

5}, Jialin Li¹, Meina Fu¹, Keshuang Li^{1

6}, Deniz Vatansever⁷, Stefania Ferraro¹, Keith M Kendrick^{1

7}, Benjamin Becker^{8

9}

Affiliations

¹ The Center of Psychosomatic Medicine, Sichuan Provincial Center for Mental Health, Sichuan Provincial People's Hospital, The University of Electronic Science and Technology of China, Chengdu, Sichuan Province 611731, China.
² Center for Cognition and Brain Disorders, The Affiliated Hospital of Hangzhou Normal University, Hangzhou, Zhejiang Province 311121, China.
³ School of Psychology, Shenzhen University, Shenzhen 518060, China.
⁴ Institute of Brain and Psychological Sciences, Sichuan Normal University, Chengdu, 610068, China.
⁵ Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.
⁶ School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China.
⁷ Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai 200433, China.
⁸ State Key Laboratory of Brain and Cognitive Sciences, The University of Hong Kong, Hong Kong 999077, China.
⁹ Department of Psychology, The University of Hong Kong, Hong Kong 999077, China.

Abstract

Background: The involvement of specific basal ganglia-thalamocortical circuits in response inhibition has been extensively mapped in animal models. However, the pivotal nodes and directed causal regulation within this inhibitory circuit in humans remains controversial.

Objective: The main aim of the present study was to determine the causal information flow and critical nodes in the basal ganglia-thalamocortical inhibitory circuits and also to examine whether these are modulated by biological factors (i.e. sex) and behavioral performance.

Methods: Here, we capitalize on the recent progress in robust and biologically plausible directed causal modeling (DCM-PEB) and a large response inhibition dataset (n = 250) acquired with concomitant functional magnetic resonance imaging to determine key nodes, their causal regulation and modulation via biological variables (sex) and inhibitory performance in the inhibitory circuit encompassing the right inferior frontal gyrus (rIFG), caudate nucleus (rCau), globus pallidum (rGP), and thalamus (rThal).

Results: The entire neural circuit exhibited high intrinsic connectivity and response inhibition critically increased causal projections from the rIFG to both rCau and rThal. Direct comparison further demonstrated that response inhibition induced an increasing rIFG inflow and increased the causal regulation of this region over the rCau and rThal. In addition, sex and performance influenced the functional architecture of the regulatory circuits such that women displayed increased rThal self-inhibition and decreased rThal to GP modulation, while better inhibitory performance was associated with stronger rThal to rIFG communication. Furthermore, control analyses did not reveal a similar key communication in a left lateralized model.

Conclusions: Together, these findings indicate a pivotal role of the rIFG as input and causal regulator of subcortical response inhibition nodes.

Keywords: DCM; basal ganglia; effective connectivity; inferior frontal gyrus; response inhibition.