Disruptions of salience network during uncertain anticipation of conflict control in anxiety

Shangfeng Han; Jie Gao; Jie Hu; Yanghua Ye; Huiya Huang; Jing Liu; Mingfang Liu; Hui Ai; Jianyin Qiu; Yuejia Luo; Pengfei Xu

doi:10.1016/j.ajp.2023.103721

Disruptions of salience network during uncertain anticipation of conflict control in anxiety

Asian J Psychiatr. 2023 Oct:88:103721. doi: 10.1016/j.ajp.2023.103721. Epub 2023 Aug 2.

Authors

Shangfeng Han¹, Jie Gao², Jie Hu², Yanghua Ye³, Huiya Huang³, Jing Liu⁴, Mingfang Liu⁵, Hui Ai⁶, Jianyin Qiu⁷, Yuejia Luo⁸, Pengfei Xu⁹

Affiliations

¹ Department of Psychology and Center for Brain and Cognitive Sciences, School of Education, Guangzhou University, Guangzhou, China; Shenzhen Key Laboratory of Affective and Social Neuroscience, Center for Brain Disorders and Cognitive Sciences, School of Psychology, Shenzhen University, Shenzhen, China.
² School of Psychology, Chengdu Medical College, Chengdu, China.
³ Shenzhen Key Laboratory of Affective and Social Neuroscience, Center for Brain Disorders and Cognitive Sciences, School of Psychology, Shenzhen University, Shenzhen, China.
⁴ The National Clinical Research Center for Mental Disorders & Beijing Key Laboratory of Mental Disorders, Beijing Anding Hospital, Capital Medical University, Beijing, China; Advanced Innovation Center for Human Brain Protection, Capital Medical University, Beijing, China.
⁵ Community Health Service Center of Beijing Normal University, China.
⁶ Institute of Applied Psychology, Tianjin University, Tianjin, China; Academy of Medical Engineering and Translational Medicine, Tianjin University, Tianjin, China.
⁷ Shanghai Mental Health Center, School of Medicine, Shanghai Jiao Tong University, Shanghai, China.
⁸ School of Psychology, Chengdu Medical College, Chengdu, China; Institute for Neuropsychological Rehabilitation, University of Health and Rehabilitation Sciences, Qingdao, China. Electronic address: luoyj@bnu.edu.cn.
⁹ The State Key Lab of Cognitive and Learning, Beijing Key Laboratory of Applied Experimental Psychology, National Demonstration Center for Experimental Psychology Education (BNU), Faculty of Psychology, Beijing Normal University, Beijing, China; Center for Emotion and Brain, Shenzhen Institute of Neuroscience, Shenzhen, China. Electronic address: pxu@bnu.edu.cn.

PMID: 37562270
DOI: 10.1016/j.ajp.2023.103721

Abstract

Background: Anxiety has been characterized by disrupted processing of conflict control, while little is known about anticipatory processing of conflicts in anxiety. Anticipation is the key factor in both anxiety and cognitive control, especially under uncertain conditions. The current study therefore examined neurocomputational mechanisms of uncertain anticipation of conflict control in anxiety.

Methods: Twenty-six participants with high-trait anxiety and twenty-nine low-trait anxiety participants completed a cue-flanker task with functional magnetic resonance imaging. The hierarchical drift diffusion model (HDDM) was used to measure the cognitive computations during the task. To identify the neurocomputational mechanism of anticipatory control in anxiety, mediation analysis and dynamic causal modelling (DCM) analysis were conducted to examine the relationship between functional connectivity of brain networks and the parameters of HDDM.

Results: We found influences of regulatory signals from the dorsolateral prefrontal cortex to dorsal anterior cingulate cortex on decision threshold in low-trait anxiety (LTA), but not in high-trait anxiety (HTA), especially for the condition with uncertain cues. The results indicate deficient top-down anticipatory control of upcoming conflicts in anxious individuals. DCM and HDDM analyses revealed that lower decision threshold was associated with higher intrinsic connectivity of salience network (SN) in anxious individuals, suggesting that dysfunctional SN disrupts anticipation of conflict control under uncertainty in anxiety.

Conclusions: Our results suggest hyperfunction of the SN underlies the deficient information accumulation during uncertain anticipation of upcoming conflicts in anxiety. Our findings shed new light on the mechanisms of anticipation processing and the psychopathology of anxiety.

Keywords: Anticipation; Anxiety; Cognitive control; Salience network; Uncertain.