Intracranial EEG signals disentangle multi-areal neural dynamics of vicarious pain perception

Huixin Tan, Xiaoyu Zeng, Jun Ni, Kun Liang, Cuiping Xu, Yanyang Zhang, Jiaxin Wang, Zizhou Li, Jiaxin Yang, Chunlei Han, Yuan Gao, Xinguang Yu, Shihui Han, Fangang Meng () and Yina Ma ()
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Huixin Tan: State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University
Xiaoyu Zeng: State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University
Jun Ni: State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University
Kun Liang: Capital Medical University
Cuiping Xu: Capital Medical University
Yanyang Zhang: Chinese PLA General Hospital
Jiaxin Wang: State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University
Zizhou Li: State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University
Jiaxin Yang: State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University
Chunlei Han: Capital Medical University
Yuan Gao: Capital Medical University
Xinguang Yu: Chinese PLA General Hospital
Shihui Han: Peking University
Fangang Meng: Capital Medical University
Yina Ma: State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: Abstract Empathy enables understanding and sharing of others’ feelings. Human neuroimaging studies have identified critical brain regions supporting empathy for pain, including the anterior insula (AI), anterior cingulate (ACC), amygdala, and inferior frontal gyrus (IFG). However, to date, the precise spatio-temporal profiles of empathic neural responses and inter-regional communications remain elusive. Here, using intracranial electroencephalography, we investigated electrophysiological signatures of vicarious pain perception. Others’ pain perception induced early increases in high-gamma activity in IFG, beta power increases in ACC, but decreased beta power in AI and amygdala. Vicarious pain perception also altered the beta-band-coordinated coupling between ACC, AI, and amygdala, as well as increased modulation of IFG high-gamma amplitudes by beta phases of amygdala/AI/ACC. We identified a necessary combination of neural features for decoding vicarious pain perception. These spatio-temporally specific regional activities and inter-regional interactions within the empathy network suggest a neurodynamic model of human pain empathy.

Date: 2024
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DOI: 10.1038/s41467-024-49541-1

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