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

Author

Listed:
  • Manuela Costa

    (Universidad Politécnica de Madrid, IdISSC)

  • Diego Lozano-Soldevilla

    (Universidad Politécnica de Madrid, IdISSC)

  • Antonio Gil-Nagel

    (Hospital Ruber Internacional
    Fundación Iniciativa Para las Neurociencias (FINCE))

  • Rafael Toledano

    (Hospital Ruber Internacional
    Servicio de Neurología)

  • Carina R. Oehrn

    (University of California)

  • Lukas Kunz

    (Columbia University)

  • Mar Yebra

    (Universidad Politécnica de Madrid, IdISSC
    Cedars-Sinai Medical Center)

  • Costantino Mendez-Bertolo

    (Universidad Politécnica de Madrid, IdISSC
    Universidad de Cádiz, and Instituto de Investigación Biomédica de Cádiz (INIBICA))

  • Lennart Stieglitz

    (University Hospital Zurich, University of Zurich)

  • Johannes Sarnthein

    (University Hospital Zurich, University of Zurich)

  • Nikolai Axmacher

    (Ruhr University Bochum)

  • Stephan Moratti

    (Universidad Politécnica de Madrid, IdISSC
    Complutense University of Madrid)

  • Bryan A. Strange

    (Universidad Politécnica de Madrid, IdISSC
    Reina Sofia Centre for Alzheimer’s Research)

Abstract

Memory 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.

Suggested Citation

  • Manuela Costa & Diego Lozano-Soldevilla & Antonio Gil-Nagel & Rafael Toledano & Carina R. Oehrn & Lukas Kunz & Mar Yebra & Costantino Mendez-Bertolo & Lennart Stieglitz & Johannes Sarnthein & Nikolai , 2022. "Aversive memory formation in humans involves an amygdala-hippocampus phase code," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33828-2
    DOI: 10.1038/s41467-022-33828-2
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    References listed on IDEAS

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    1. Peide Zhang & Binbin Peng & Zhifu Mi & Zhongguo Lin & Huibin Du & Lu Cheng & Xiafei Zhou & Guozhi Cao, 2024. "The reduction of effective feedback reception due to negative emotions in appeals," Palgrave Communications, Palgrave Macmillan, vol. 11(1), pages 1-10, December.

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