Functional specialization and dynamical interaction in human amygdala subregions support fearful-expression processing

Fearful-expression processing supports adaptive responses to potential threats, requiring both rapid threat evaluation and face-related information processing. However, how human amygdala subregions contribute to these complementary processes remains unclear. Here we record intracranial electroencephalography from twelve patients with epilepsy during an emotional face-matching task, sampling 58 amygdala contacts with balanced hemispheric distributions.

Condition-specific analyses reveal separable theta/alpha dynamics between the lateral and medial amygdala within fearful-face and neutral-face matching conditions, but not shape matching. Between-condition contrasts further reveal earlier lateral amygdala engagement and stronger lateral-to-medial directional interactions for fearful-face versus neutral-face matching, whereas later medial engagement and stronger medial-to-lateral interactions emerge for neutral-face versus shape matching. Control analyses preserve the main neural effects.

In a separate cohort of seven patients, intracranial stimulation produces dissociable behavioral effects, with lateral stimulation impairing fear matching and medial stimulation facilitating neutral-face matching. Together, these findings reveal a condition-dependent functional differentiation within the human amygdala during fearful-expression processing. This manuscript was prepared with the assistance of ChatGPT to improve linguistic readability.

The authors thoroughly reviewed and revised all content as necessary. This work received support from the following sources: National Natural Science Foundation of China (No. 32400883 to D.C.; No. 32271085 to J.L.; No. 82001798 to Y.Z.), Beijing Natural Science Foundation (No. 5244049 to D.C.; No. L256006 to J.L.), the Young Talent Project of Chinese PLA General Hospital (No. 20230403 to Y.Z.), and the Innovation Incubation Project of Chinese PLA General Hospital for the Department of Neurosurgery (No.

These authors contributed equally: Dan Cao, Jiachen Cui, Xinyuan Yan. School of Psychology, Capital Normal University, Beijing, China Department of Psychiatry, University of Minnesota Medical School, Minneapolis, MN, USA State Key Laboratory of Cognitive Neuroscience and Learning, and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China Department of Neurosurgery, Chinese PLA General Hospital, Beijing, China Yuanyuan Dang, Hulin Zhao, Jianning Zhang & Yanyang Zhang Neurosurgery Institute, Chinese PLA General Hospital, Beijing, China Correspondence to Jin Li, Jianning Zhang or Yanyang Zhang. The authors declare no competing interests.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it.