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Functional specialization and interaction in the amygdala-hippocampus circuit during working memory processing

Author

Listed:
  • Jin Li

    (Chinese Academy of Sciences)

  • Dan Cao

    (Chinese Academy of Sciences)

  • Shan Yu

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xinyu Xiao

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Lukas Imbach

    (Klinik Lengg
    ETH and University of Zurich)

  • Lennart Stieglitz

    (University Hospital Zurich, University of Zurich)

  • Johannes Sarnthein

    (University Hospital Zurich, University of Zurich
    ETH Zurich)

  • Tianzi Jiang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    Zhejiang Lab)

Abstract

Both the hippocampus and amygdala are involved in working memory (WM) processing. However, their specific role in WM is still an open question. Here, we simultaneously recorded intracranial EEG from the amygdala and hippocampus of epilepsy patients while performing a WM task, and compared their representation patterns during the encoding and maintenance periods. By combining multivariate representational analysis and connectivity analyses with machine learning methods, our results revealed a functional specialization of the amygdala-hippocampal circuit: The mnemonic representations in the amygdala were highly distinct and decreased from encoding to maintenance. The hippocampal representations, however, were more similar across different items but remained stable in the absence of the stimulus. WM encoding and maintenance were associated with bidirectional information flow between the amygdala and the hippocampus in low-frequency bands (1–40 Hz). Furthermore, the decoding accuracy on WM load was higher by using representational features in the amygdala during encoding and in the hippocampus during maintenance, and by using information flow from the amygdala during encoding and that from the hippocampus during maintenance, respectively. Taken together, our study reveals that WM processing is associated with functional specialization and interaction within the amygdala-hippocampus circuit.

Suggested Citation

  • Jin Li & Dan Cao & Shan Yu & Xinyu Xiao & Lukas Imbach & Lennart Stieglitz & Johannes Sarnthein & Tianzi Jiang, 2023. "Functional specialization and interaction in the amygdala-hippocampus circuit during working memory processing," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38571-w
    DOI: 10.1038/s41467-023-38571-w
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    References listed on IDEAS

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    1. Serra E. Favila & Avi J. H. Chanales & Brice A. Kuhl, 2016. "Experience-dependent hippocampal pattern differentiation prevents interference during subsequent learning," Nature Communications, Nature, vol. 7(1), pages 1-10, April.
    2. Maria Sol Fustiñana & Tobias Eichlisberger & Tewis Bouwmeester & Yael Bitterman & Andreas Lüthi, 2021. "State-dependent encoding of exploratory behaviour in the amygdala," Nature, Nature, vol. 592(7853), pages 267-271, April.
    3. D. Pacheco Estefan & M. Sánchez-Fibla & A. Duff & A. Principe & R. Rocamora & H. Zhang & N. Axmacher & P. F. M. J. Verschure, 2019. "Coordinated representational reinstatement in the human hippocampus and lateral temporal cortex during episodic memory retrieval," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    4. Jie Zheng & Kristopher L. Anderson & Stephanie L. Leal & Avgusta Shestyuk & Gultekin Gulsen & Lilit Mnatsakanyan & Sumeet Vadera & Frank P. K. Hsu & Michael A. Yassa & Robert T. Knight & Jack J. Lin, 2017. "Amygdala-hippocampal dynamics during salient information processing," Nature Communications, Nature, vol. 8(1), pages 1-11, April.
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    Cited by:

    1. Biao Zhang & Shuqin Zhang & Shihua Zhang, 2024. "Whole brain alignment of spatial transcriptomics between humans and mice with BrainAlign," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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