Aversive memory formation in humans is determined by an amygdala-hippocampus phase code
Costa, M.; Lozano-Soldevilla, D.; Gil-Nagel Rein, A.; Toledano, R.; Oehrn, C.; Kunz, L.; Yebra, M.; Mendez-Bertolo, C.; Stieglitz, L.; Sarnthein, J.; Axmacher, N.; Moratti, S.; Strange, B. A.
Show abstract
Memory for aversive events is central to survival, but can also become maladaptive in psychiatric disorders. Emotional memory relies on the amygdala and hippocampus, but the neural dynamics of their communication during emotional memory encoding remain unknown. Using simultaneous intracranial recordings from both structures in human patients, we show that in response to emotionally aversive, but not neutral, visual stimuli, the amygdala transmits unidirectional influence on the hippocampus through theta oscillations. Critically, successful emotional memory encoding depends on the precise amygdala theta phase to which hippocampal gamma activity and neuronal firing couple. The phase difference between subsequently remembered vs. not-remembered emotional stimuli translates to [~]25-45 milliseconds, a time period that enables lagged coherence between amygdala and downstream hippocampal gamma activity. These results reveal a mechanism whereby amygdala theta phase coordinates transient coherence between amygdala and hippocampal gamma activity to facilitate the encoding of aversive memories in humans.
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