Aversive memory formation in humans involves an amygdala-hippocampus phase code

• DOI: 10.1038/s41467-022-33828-2
• Publication Date: 2022-10-27T14:05:52Z
• Authors: Manuela Costa; Diego Lozano-Sold...; Antonio Gil-Nagel; Rafael Toledano; Carina R. Oehrn; Lukas Kunz; Mar Yebra; Costantino Mendez...; Lennart Stieglitz; Johannes Sarnthein; Nikolai Axmacher; Stephan Moratti; Bryan A. Strange
• Keywords: 0301 basic medicine; Science; Emotions; 610 Medicine & health; 1600 General Chemistry; Mental disorders; Hippocampus; Article; Recuerdo mental; 10180 Clinic for Neurosurgery; 03 medical and health sciences; Cognition; 1300 General Biochemistry, Genetics and Molecular Biology; Memory; Hipocampo; Memoria; Humans; 1000 Multidisciplinary; Q; Brain; Amígdala del cerebelo; Amygdala; 3100 General Physics and Astronomy; Emociones; Mental Recall; Memory disorders; Mental recall

AbstractMemory for aversive events is central to survival but can become maladaptive in psychiatric disorders. Memory enhancement for emotional events is thought to depend on amygdala modulation of hippocampal activity. However, the neural dynamics of amygdala-hippocampal communication during emotional memory encoding remain unknown. Using simultaneous intracranial recordings from both structures in human patients, here we show that successful emotional memory encoding depends on the 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 a time period that enables lagged coherence between amygdala and downstream hippocampal gamma. These results reveal a mechanism whereby amygdala theta phase coordinates transient amygdala -hippocampal gamma coherence to facilitate aversive memory encoding. Pacing of lagged gamma coherence via amygdala theta phase may represent a general mechanism through which the amygdala relays emotional content to distant brain regions to modulate other aspects of cognition, such as attention and decision-making.