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A neural signature for the subjective experience of threat anticipation under uncertainty

Author

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  • Xiqin Liu

    (West China Hospital of Sichuan University
    University of Electronic Science and Technology of China
    University of Electronic Science and Technology of China)

  • Guojuan Jiao

    (University of Electronic Science and Technology of China
    The Second Xiangya Hospital of Central South University)

  • Feng Zhou

    (Southwest University
    MOE Key Laboratory of Cognition and Personality)

  • Keith M. Kendrick

    (University of Electronic Science and Technology of China)

  • Dezhong Yao

    (University of Electronic Science and Technology of China)

  • Qiyong Gong

    (West China Hospital of Sichuan University
    West China Xiamen Hospital of Sichuan University)

  • Shitong Xiang

    (Fudan University
    (Fudan University), Ministry of Education)

  • Tianye Jia

    (Fudan University
    (Fudan University), Ministry of Education
    Fudan University
    Psychology and Neuroscience, King’s College London)

  • Xiao-Yong Zhang

    (Fudan University
    (Fudan University), Ministry of Education)

  • Jie Zhang

    (Fudan University
    (Fudan University), Ministry of Education)

  • Jianfeng Feng

    (Fudan University
    (Fudan University), Ministry of Education
    Fudan University
    Zhangjiang Fudan International Innovation Center)

  • Benjamin Becker

    (The University of Hong Kong
    The University of Hong Kong)

Abstract

Uncertainty about potential future threats and the associated anxious anticipation represents a key feature of anxiety. However, the neural systems that underlie the subjective experience of threat anticipation under uncertainty remain unclear. Combining an uncertainty-variation threat anticipation paradigm that allows precise modulation of the level of momentary anxious arousal during functional magnetic resonance imaging (fMRI) with multivariate predictive modeling, we train a brain model that accurately predicts subjective anxious arousal intensity during anticipation and test it across 9 samples (total n = 572, both gender). Using publicly available datasets, we demonstrate that the whole-brain signature specifically predicts anxious anticipation and is not sensitive in predicting pain, general anticipation or unspecific emotional and autonomic arousal. The signature is also functionally and spatially distinguishable from representations of subjective fear or negative affect. We develop a sensitive, generalizable, and specific neuroimaging marker for the subjective experience of uncertain threat anticipation that can facilitate model development.

Suggested Citation

  • Xiqin Liu & Guojuan Jiao & Feng Zhou & Keith M. Kendrick & Dezhong Yao & Qiyong Gong & Shitong Xiang & Tianye Jia & Xiao-Yong Zhang & Jie Zhang & Jianfeng Feng & Benjamin Becker, 2024. "A neural signature for the subjective experience of threat anticipation under uncertainty," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45433-6
    DOI: 10.1038/s41467-024-45433-6
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    References listed on IDEAS

    as
    1. Choong-Wan Woo & Liane Schmidt & Anjali Krishnan & Marieke Jepma & Mathieu Roy & Martin A. Lindquist & Lauren Y. Atlas & Tor D. Wager, 2017. "Quantifying cerebral contributions to pain beyond nociception," Nature Communications, Nature, vol. 8(1), pages 1-14, April.
    2. Feng Zhou & Weihua Zhao & Ziyu Qi & Yayuan Geng & Shuxia Yao & Keith M. Kendrick & Tor D. Wager & Benjamin Becker, 2021. "A distributed fMRI-based signature for the subjective experience of fear," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    3. Philip A. Kragel & Michael T. Treadway & Roee Admon & Diego A. Pizzagalli & Evan C. Hahn, 2023. "A mesocorticolimbic signature of pleasure in the human brain," Nature Human Behaviour, Nature, vol. 7(8), pages 1332-1343, August.
    4. Choong-Wan Woo & Mathieu Roy & Jason T Buhle & Tor D Wager, 2015. "Distinct Brain Systems Mediate the Effects of Nociceptive Input and Self-Regulation on Pain," PLOS Biology, Public Library of Science, vol. 13(1), pages 1-14, January.
    5. Bowen J. Fung & Song Qi & Demis Hassabis & Nathaniel Daw & Dean Mobbs, 2019. "Slow escape decisions are swayed by trait anxiety," Nature Human Behaviour, Nature, vol. 3(7), pages 702-708, July.
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