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Coordinated representational reinstatement in the human hippocampus and lateral temporal cortex during episodic memory retrieval

Author

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  • D. Pacheco Estefan

    (Institute for Bioengineering of Catalonia (IBEC)
    Universitat Pompeu Fabra)

  • M. Sánchez-Fibla

    (Universitat Pompeu Fabra)

  • A. Duff

    (Institute for Bioengineering of Catalonia (IBEC))

  • A. Principe

    (Hospital del Mar
    Hospital del Mar Medical Research Institute)

  • R. Rocamora

    (Hospital del Mar
    Hospital del Mar Medical Research Institute
    Universitat Pompeu Fabra)

  • H. Zhang

    (Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum)

  • N. Axmacher

    (Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum)

  • P. F. M. J. Verschure

    (Institute for Bioengineering of Catalonia (IBEC)
    The Barcelona Institute of Science and Technology (BIST)
    Passeig de Lluís Companys, 23)

Abstract

Theoretical models of episodic memory have proposed that retrieval depends on interactions between the hippocampus and neocortex, where hippocampal reinstatement of item-context associations drives neocortical reinstatement of item information. Here, we simultaneously recorded intracranial EEG from hippocampus and lateral temporal cortex (LTC) of epilepsy patients who performed a virtual reality spatial navigation task. We extracted stimulus-specific representations of both item and item-context associations from the time-frequency patterns of activity in hippocampus and LTC. Our results revealed a double dissociation of representational reinstatement across time and space: an early reinstatement of item-context associations in hippocampus preceded a later reinstatement of item information in LTC. Importantly, reinstatement levels in hippocampus and LTC were correlated across trials, and the quality of LTC reinstatement was predicted by the magnitude of phase synchronization between hippocampus and LTC. These findings confirm that episodic memory retrieval in humans relies on coordinated representational interactions within a hippocampal-neocortical network.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-09569-0
    DOI: 10.1038/s41467-019-09569-0
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    Cited by:

    1. Sanne Ten Oever & Alexander T. Sack & Carina R. Oehrn & Nikolai Axmacher, 2021. "An engram of intentionally forgotten information," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    2. Luca D. Kolibius & Frederic Roux & George Parish & Marije Wal & Mircea Plas & Ramesh Chelvarajah & Vijay Sawlani & David T. Rollings & Johannes D. Lang & Stephanie Gollwitzer & Katrin Walther & Rüdige, 2023. "Hippocampal neurons code individual episodic memories in humans," Nature Human Behaviour, Nature, vol. 7(11), pages 1968-1979, November.
    3. Sandra Gattas & Myra Sarai Larson & Lilit Mnatsakanyan & Indranil Sen-Gupta & Sumeet Vadera & A. Lee Swindlehurst & Paul E. Rapp & Jack J. Lin & Michael A. Yassa, 2023. "Theta mediated dynamics of human hippocampal-neocortical learning systems in memory formation and retrieval," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Haoxin Zhang & Ivan Skelin & Shiting Ma & Michelle Paff & Lilit Mnatsakanyan & Michael A. Yassa & Robert T. Knight & Jack J. Lin, 2024. "Awake ripples enhance emotional memory encoding in the human brain," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Daniel Pacheco-Estefan & Marie-Christin Fellner & Lukas Kunz & Hui Zhang & Peter Reinacher & Charlotte Roy & Armin Brandt & Andreas Schulze-Bonhage & Linglin Yang & Shuang Wang & Jing Liu & Gui Xue & , 2024. "Maintenance and transformation of representational formats during working memory prioritization," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    6. 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.
    7. Huixin Tan & Xiaoyu Zeng & Jun Ni & Kun Liang & Cuiping Xu & Yanyang Zhang & Jiaxin Wang & Zizhou Li & Jiaxin Yang & Chunlei Han & Yuan Gao & Xinguang Yu & Shihui Han & Fangang Meng & Yina Ma, 2024. "Intracranial EEG signals disentangle multi-areal neural dynamics of vicarious pain perception," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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