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Hippocampal neurons code individual episodic memories in humans

Author

Listed:
  • Luca D. Kolibius

    (Columbia University
    University of Glasgow
    University of Birmingham)

  • Frederic Roux

    (University of Birmingham)

  • George Parish

    (University of Birmingham)

  • Marije Wal

    (University of Birmingham)

  • Mircea Plas

    (University of Glasgow
    University of Birmingham)

  • Ramesh Chelvarajah

    (University of Birmingham
    Queen Elizabeth Hospital Birmingham)

  • Vijay Sawlani

    (Queen Elizabeth Hospital Birmingham)

  • David T. Rollings

    (Queen Elizabeth Hospital Birmingham)

  • Johannes D. Lang

    (University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg)

  • Stephanie Gollwitzer

    (University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg)

  • Katrin Walther

    (University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg)

  • Rüdiger Hopfengärtner

    (University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg)

  • Gernot Kreiselmeyer

    (University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg)

  • Hajo Hamer

    (University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg)

  • Bernhard P. Staresina

    (University of Oxford
    University of Oxford)

  • Maria Wimber

    (University of Glasgow
    University of Birmingham)

  • Howard Bowman

    (University of Birmingham
    University of Kent)

  • Simon Hanslmayr

    (University of Glasgow
    University of Birmingham)

Abstract

The hippocampus is an essential hub for episodic memory processing. However, how human hippocampal single neurons code multi-element associations remains unknown. In particular, it is debated whether each hippocampal neuron represents an invariant element within an episode or whether single neurons bind together all the elements of a discrete episodic memory. Here we provide evidence for the latter hypothesis. Using single-neuron recordings from a total of 30 participants, we show that individual neurons, which we term episode-specific neurons, code discrete episodic memories using either a rate code or a temporal firing code. These neurons were observed exclusively in the hippocampus. Importantly, these episode-specific neurons do not reflect the coding of a particular element in the episode (that is, concept or time). Instead, they code for the conjunction of the different elements that make up the episode.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nathum:v:7:y:2023:i:11:d:10.1038_s41562-023-01706-6
    DOI: 10.1038/s41562-023-01706-6
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    References listed on IDEAS

    as
    1. R. Quian Quiroga & L. Reddy & G. Kreiman & C. Koch & I. Fried, 2005. "Invariant visual representation by single neurons in the human brain," Nature, Nature, vol. 435(7045), pages 1102-1107, June.
    2. Johannes Niediek & Jan Boström & Christian E Elger & Florian Mormann, 2016. "Reliable Analysis of Single-Unit Recordings from the Human Brain under Noisy Conditions: Tracking Neurons over Hours," PLOS ONE, Public Library of Science, vol. 11(12), pages 1-26, December.
    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.
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