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

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Abstract

Fearful-expression recognition is vital for survival, yet how human amygdala subregions differentially support its distinct cognitive components, including rapid threat detection and fine-grained face processing, remains unclear. Here, we recorded intracranial EEG from lateral and medial amygdala in epilepsy patients performing an emotional face-matching task. Using multivariate decoding, time-frequency and directed-connectivity analyses with intracranial stimulation, we found that the lateral subregion exhibited early, fear-specific responses with higher decoding accuracy and elevated theta/alpha-band (4-12 Hz) power, and transmitted this fear-specific information to the medial subregion, which showed delayed and sustained activation. By contrast, the medial subregion encoded face-specific information at later stage in the 2-16 Hz band with superior decoding accuracy and power, and then relayed this information back to the lateral subregion to complete processing. Further, intracranial stimulation produced behaviorally selective effects, with lateral stimulation disrupting fear detection while medial stimulation accelerated face recognition. Together, our study reveals that functional specialization and frequency-specific dynamic interaction among human amygdala subregions underlie distinct cognitive components of fearful-expression recognition.

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