IDEAS home Printed from https://ideas.repec.org/a/nat/nathum/v7y2023i11d10.1038_s41562-023-01706-6.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41562-023-01706-6
    File Function: Abstract
    Download Restriction: Access to the full text of the articles in this series is restricted.

    File URL: https://libkey.io/10.1038/s41562-023-01706-6?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    As the access to this document is restricted, you may want to search for a different version of it.

    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. 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.
    3. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Eleanor Spens & Neil Burgess, 2024. "A generative model of memory construction and consolidation," Nature Human Behaviour, Nature, vol. 8(3), pages 526-543, March.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Sina Mackay & Thomas P. Reber & Marcel Bausch & Jan Boström & Christian E. Elger & Florian Mormann, 2024. "Concept and location neurons in the human brain provide the ‘what’ and ‘where’ in memory formation," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    2. Umut Güçlü & Marcel A J van Gerven, 2014. "Unsupervised Feature Learning Improves Prediction of Human Brain Activity in Response to Natural Images," PLOS Computational Biology, Public Library of Science, vol. 10(8), pages 1-12, August.
    3. Marcel Bausch & Johannes Niediek & Thomas P. Reber & Sina Mackay & Jan Boström & Christian E. Elger & Florian Mormann, 2021. "Concept neurons in the human medial temporal lobe flexibly represent abstract relations between concepts," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    4. 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.
    5. Rodrigo Quian Quiroga & Marta Boscaglia & Jacques Jonas & Hernan G. Rey & Xiaoqian Yan & Louis Maillard & Sophie Colnat-Coulbois & Laurent Koessler & Bruno Rossion, 2023. "Single neuron responses underlying face recognition in the human midfusiform face-selective cortex," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    6. Martinez-Saito, Mario, 2022. "Discrete scaling and criticality in a chain of adaptive excitable integrators," Chaos, Solitons & Fractals, Elsevier, vol. 163(C).
    7. Jakub Kopal & Kuldeep Kumar & Kimia Shafighi & Karin Saltoun & Claudia Modenato & Clara A. Moreau & Guillaume Huguet & Martineau Jean-Louis & Charles-Olivier Martin & Zohra Saci & Nadine Younis & Elis, 2024. "Using rare genetic mutations to revisit structural brain asymmetry," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    8. Layton Lamsam & Brett Gu & Mingli Liang & George Sun & Kamren J. Khan & Kevin N. Sheth & Lawrence J. Hirsch & Christopher Pittenger & Alfred P. Kaye & John H. Krystal & Eyiyemisi C. Damisah, 2024. "The human claustrum tracks slow waves during sleep," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    9. Rybalova, E. & Averyanov, V. & Lozi, R. & Strelkova, G., 2024. "Peculiarities of the spatio-temporal dynamics of a Hénon–Lozi map network in the presence of Lévy noise," Chaos, Solitons & Fractals, Elsevier, vol. 184(C).
    10. Nanyi Fei & Zhiwu Lu & Yizhao Gao & Guoxing Yang & Yuqi Huo & Jingyuan Wen & Haoyu Lu & Ruihua Song & Xin Gao & Tao Xiang & Hao Sun & Ji-Rong Wen, 2022. "Towards artificial general intelligence via a multimodal foundation model," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    11. Louis Kang & Taro Toyoizumi, 2024. "Distinguishing examples while building concepts in hippocampal and artificial networks," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    12. Sara Mahallati & James C Bezdek & Milos R Popovic & Taufik A Valiante, 2019. "Cluster tendency assessment in neuronal spike data," PLOS ONE, Public Library of Science, vol. 14(11), pages 1-29, November.
    13. Ahalya Prabhakar & Todd Murphey, 2022. "Mechanical intelligence for learning embodied sensor-object relationships," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    14. Thomas P. Reber & Sina Mackay & Marcel Bausch & Marcel S. Kehl & Valeri Borger & Rainer Surges & Florian Mormann, 2023. "Single-neuron mechanisms of neural adaptation in the human temporal lobe," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    15. Henning Sprekeler & Christian Michaelis & Laurenz Wiskott, 2007. "Slowness: An Objective for Spike-Timing–Dependent Plasticity?," PLOS Computational Biology, Public Library of Science, vol. 3(6), pages 1-13, June.
    16. Dock H. Duncan & Dirk Moorselaar & Jan Theeuwes, 2023. "Pinging the brain to reveal the hidden attentional priority map using encephalography," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    17. Annika Hagemann & Jens Wilting & Bita Samimizad & Florian Mormann & Viola Priesemann, 2021. "Assessing criticality in pre-seizure single-neuron activity of human epileptic cortex," PLOS Computational Biology, Public Library of Science, vol. 17(3), pages 1-18, March.
    18. David Balduzzi & Giulio Tononi, 2009. "Qualia: The Geometry of Integrated Information," PLOS Computational Biology, Public Library of Science, vol. 5(8), pages 1-24, August.
    19. 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.
    20. 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.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:nathum:v:7:y:2023:i:11:d:10.1038_s41562-023-01706-6. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.