The critical mediating roles of the middle temporal gyrus and ventrolateral prefrontal cortex in the dynamic processing of interpersonal emotion regulation

• Published in: NeuroImage (Orlando, Fla.) Fla.), 2024-10, Vol.300, p.120789, Article 120789
• Main Authors: Wang, Jiazheng, Yang, Zhenzhen, Klugah-Brown, Benjamin, Zhang, Tao, Yang, Jiemin, Yuan, JiaJin, Biswal, Bharat B
• Format: Article
• Language: English
• Subjects: Affect (Psychology); Brain; Dynamic functional connectivity (DFC); Efficiency; Emotional behavior; Emotional regulation; Emotions; Functional magnetic resonance imaging; Information processing; Interpersonal emotion regulation (IER); Middle temporal gyrus (MTG); Neural networks; Prefrontal cortex; Questionnaires; Social interaction; Social organization; Temporal gyrus; Temporal lobe; Ventrolateral prefrontal cortex (VLPFC)
• ISSN: 1053-8119; 1095-9572; 1095-9572
• DOI: 10.1016/j.neuroimage.2024.120789

•Our work offer valuable insights into decompose the dynamic cognitive-neural mechanism processing of the interpersonal emotion regulation (IER).•Our findings reveal that the left middle temporal gyrus and ventrolateral prefrontal cortex serve as pivotal regions for enhancing one's tendency and efficiency in utilizing IER, while also augmenting its regulatory effects.•The findings hold significant clinical implications, providing a foundation for future clinicians to precisely target specific brain regions in individuals with impaired social context, encompassing those afflicted with social anxiety disorder, and depression disorder. Interpersonal emotion regulation (IER) is a crucial ability for effectively recovering from negative emotions through social interaction. It has been emphasized that the empathy network, cognitive control network, and affective generation network sustain the deployment of IER. However, the temporal dynamics of functional connectivity among these networks of IER remains unclear. This study utilized IER task-fMRI and sliding window approach to examine both the stationary and dynamic functional connectivity (dFC) of IER. Fifty-five healthy participants were recruited for the present study. Through clustering analysis, four distinct brain states were identified in dFC. State 1 demonstrated situation modification stage of IER, with strong connectivity between affective generation and visual networks. State 2 exhibited pronounced connectivity between empathy network and both cognitive control and affective generation networks, reflecting the empathy stage of IER. Next, a ‘top-down’ pattern is observed between the connectivity of cognitive control and affective generation networks during the cognitive control stage of state 3. The affective response modulation stage of state 4 mainly involved connections between empathy and affective generation networks. Specifically, the degree centrality of the left middle temporal gyrus (MTG) mediated the association between one's IER tendency and the regulatory effects in state 2. The betweenness centrality of the left ventrolateral prefrontal cortex (VLPFC) mediated the association between one's IER efficiency and the regulatory effects in state 3. Altogether, these findings revealed that dynamic connectivity transitions among empathy, cognitive control, and affective generation networks, with the left VLPFC and MTG playing dominant roles, evident across the IER processing.