Dynamic interactions in human amygdala subregions support hierarchical processing of fearful faces
Abstract
Fearful-expression recognition is vital for survival, relying on rapid fear detection and fine-grained face encoding. However, how human amygdala subregions differentially implement these distinct cognitive components remains unclear. Here, we recorded intracranial EEG from lateral and medial amygdala in epilepsy patients performing an emotional face-matching task, and combined multivariate decoding, time-frequency and directed-connectivity analyses with intracranial stimulation. We found that the lateral subregion exhibited early, fear-specific theta/alpha-band (4-12 Hz) activity with higher decoding accuracy and directed transfer of fear-specific information to the medial subregion, which showed delayed and sustained activation. By contrast, the medial subregion encoded face-specific information at a later stage in the 2-16 Hz band with superior decoding accuracy, and then relayed this information back to the lateral subregion. Critically, intracranial stimulation yielded double-dissociable behavioural effects, with lateral stimulation disrupting early fear detection while medial stimulation accelerated neutral-face recognition. Together, our study delineates a hierarchically organized, temporally structured division of labour within the human amygdala and show that dynamic interactions underlie hierarchical processing of fearful expressions.
Significance Statement
Recognizing fearful expressions is critical for adaptive behavior, yet how human amygdala subregions support this complex process remains unclear. By recording and stimulating the amygdala directly in humans, we demonstrate that the lateral and medial amygdala function in a temporally structured hierarchical framework in which the lateral amygdala rapidly detects threats while the medial amygdala subsequently integrates detailed facial information. These findings extend our understanding of how the amygdala coordinates multiple aspects of fear processing, offering new insight into the neural mechanisms underlying human adaptive behavior.
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