A functional anatomical shift from the lateral frontal pole to dorsolateral prefrontal cortex in emotion action control underpins elevated levels of anxiety: partial replication and generalization of Bramson, et al., 2023

Abstract

Background: Emotion control represents a promising intervention target for mental disorders. In a recent study Bramson, et al. (2023) demonstrate a functional-anatomical shift from the lateral frontal pole (FPl) to the dorsolateral prefrontal cortex (DLPFC) in anxious individuals during emotional action control. However, findings of neuroimaging experiments are often limited regarding generalizability and reproducibility. The present study examined the robustness of the reported functional shift across samples, cultures and paradigms.

Methods: We capitalized on large-scale task fMRI data (n = 250 participants) using an affective linguistic Go/NoGo paradigm to examine the anxiety-related shift between FPl and DLPFC during emotional action control. Additionally, context-dependent functional connectivity analyses were employed to examine anxiety-related differences and associations on the network level.

Results: Non-anxious individuals engaged the left FPl while highly anxious individuals specifically recruited the DLPFC, but non-significant between-group differences were found (see also Bramson, et al.). The secondary analyses revealed moderate evidence for the absence of left FPl activation in the high-anxious as well as for left DLPFC activation in the non-anxious group. Additionally, trait anxiety scores were positively correlated with left DLPFC activity but negatively correlated with left FPl activity across groups. Furthermore, we found a context-specific connectivity shift between the subgenual anterior cingulate cortex (sgACC) with the FPl and DLPFC specifically in highly anxious individuals.

Conclusion: The results partially confirmed the anxiety-related shift as reported by Bramson and colleagues across paradigms and samples. The findings provide further support for the functional shift in anxiety and can inform target-based interventions of persistent emotional control deficits in anxiety disorders.

Keywords

emotion / inhibition / anxiety / frontal pole / DLPFC / Go/NoGo task

Supplementary data

Supplementary data are available at PSYRAD Journal online.

Author contributions

Qian Zhuang (Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Visualization, Writing - original draft), Shuxia Yao (Methodology), Lei Xu (Data curation), Shuaiyu Chen (Methodology), Jialin Li (Data curation), Xiaoxiao Zheng (Data curation), Meina Fu (Data curation), Keith M. Kendrick (Funding acquisition, Supervision, Validation, Writing - review & editing), and Benjamin Becker (Conceptualization, Funding acquisition, Supervision, Validation, Writing - review & editing)

Conflicts of interests

K.M.K. holds the position of Editor-in-Chief, and B.B. is a member of the editorial board of Psychoradiology. They were blinded from the review process and making decisions on the manuscript. The other authors declare no competing interests.

Acknowledgements

National Natural Science Foundation of China (grant nos. 32200904—Q.Z., 82271583—B.B., 31530032—K.M.K.), Key Technological Projects of Guangdong Province (grant no. 2018B030335001—K..MK.), and Medical and Health Technology Project of Zhejiang Provincial Health Commission (2023RC236—Q. Z.).

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