Adaptive shifts in amygdala–hippocampal theta coupling govern aversive learning and extinction

Abstract

Adaptive behaviour relies on the flexible encoding and suppression of aversive associations often underpinned by amygdala-hippocampal interactions. Yet the spectral and directional dynamics underlying these interactions in humans remain poorly understood. Using intracranial EEG recordings from the amygdala and the hippocampus acquired during a two-day aversive learning and extinction task, we identified frequency-specific shifts: amygdala theta (3–8 Hz) and gamma (30–45 Hz) power increased during conditioning and decreased during extinction, while hippocampal alpha and gamma activity gave way to theta and gamma during extinction. Directional phase connectivity, results showed frequency-specific reversals: amygdala-to-hippocampus dominance at 3-5 Hz during conditioning and hippocampus-to-amygdala predominance in extinction, while 6-8 Hz showed the opposite pattern, a reconfiguration validated by computational modelling. These findings uncover distinct theta sub-bands coordinating dynamic, bidirectional communication in the human amygdala–hippocampal circuit, elucidating a neural mechanism for the flexible regulation of emotional memory.