Human hippocampal reactivation of amygdala encoding-related gamma patterns during aversive memory retrieval

Manuela Costa (), Daniel Pacheco-Estefan, Antonio Gil-Nagel, Rafael Toledano, Lukas Imbach, Johannes Sarnthein and Bryan A. Strange ()
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Manuela Costa: University Politécnica de Madrid, IdISSC
Daniel Pacheco-Estefan: Autonomous University of Barcelona
Antonio Gil-Nagel: Hospital Ruber Internacional
Rafael Toledano: Hospital Ruber Internacional
Lukas Imbach: Klinik Lengg
Johannes Sarnthein: University of Zurich and ETH Zurich
Bryan A. Strange: University Politécnica de Madrid, IdISSC

Nature Communications, 2025, vol. 16, issue 1, 1-14

Abstract: Abstract Emotional memories require coordinated activity of the amygdala and hippocampus. Human intracranial recordings have shown that formation of aversive memories involves an amygdala theta-hippocampal gamma phase code. Yet, the mechanisms engaged during translation of aversive experiences into memories and subsequent retrieval remain unclear. Directly recording from human amygdala and hippocampus, here we show that hippocampal gamma activity increases for correctly remembered aversive scenes. Crucially, patterns of amygdala high amplitude gamma activity at encoding are reactivated in the hippocampus, but not amygdala, during both aversive encoding and retrieval. Trial-specific hippocampal gamma patterns showing highest representational similarity with amygdala activity at encoding are reactivated in the hippocampus during aversive retrieval. This reactivation process occurs against a background of gamma activity that is otherwise decorrelated between encoding and retrieval. Thus, phasic hippocampal gamma responses track the retrieval of aversive memories, with activity patterns apparently entrained by the amygdala during encoding.

Date: 2025
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DOI: 10.1038/s41467-025-61928-2

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