Hippocampal neurons code individual episodic memories in humans

Luca D Kolibius; Frederic Roux; George Parish; Marije Ter Wal; Mircea Van Der Plas; Ramesh Chelvarajah; Vijay Sawlani; David T Rollings; Johannes D Lang; Stephanie Gollwitzer; Katrin Walther; Rüdiger Hopfengärtner; Gernot Kreiselmeyer; Hajo Hamer; Bernhard P Staresina; Maria Wimber; Howard Bowman; Simon Hanslmayr

doi:10.1038/s41562-023-01706-6

Hippocampal neurons code individual episodic memories in humans

Luca D Kolibius^*, Frederic Roux, George Parish, Marije Ter Wal, Mircea Van Der Plas, Ramesh Chelvarajah, Vijay Sawlani, David T Rollings, Johannes D Lang, Stephanie Gollwitzer, Katrin Walther, Rüdiger Hopfengärtner, Gernot Kreiselmeyer, Hajo Hamer, Bernhard P Staresina, Maria Wimber, Howard Bowman, Simon Hanslmayr

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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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.

Original language	English
Number of pages	15
Journal	Nature Human Behaviour
Early online date	5 Oct 2023
DOIs	https://doi.org/10.1038/s41562-023-01706-6
Publication status	E-pub ahead of print - 5 Oct 2023

Bibliographical note

© 2023. The Author(s).
This manuscript was supported by the following grants: European Research Council grant no. 647954 (S.H.), European Research Council grant no. 715714 (M.W.) and European Research Council grant no. 101001121 (B.P.S.). Epilepsy Center, Department of Neurology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany is a Full Member of ERN EpiCare. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. We thank all the patients who have participated in our study.

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10.1038/s41562-023-01706-6Licence: Creative Commons: Attribution (CC BY)

KolibiusL2023HippocampalFinal published version, 1.71 MBLicence: Creative Commons: Attribution (CC BY)

H2020_ERC_STREAM
Wimber, M.
European Commission
1/03/17 → 31/08/23
Project: EU
H2020_ERC_CODE4MEMORY
Hanslmayr, S.
European Commission
1/10/15 → 31/03/22
Project: EU

Cite this

Kolibius, L. D., Roux, F., Parish, G., Ter Wal, M., Van Der Plas, M., Chelvarajah, R., Sawlani, V., Rollings, D. T., Lang, J. D., Gollwitzer, S., Walther, K., Hopfengärtner, R., Kreiselmeyer, G., Hamer, H., Staresina, B. P., Wimber, M., Bowman, H., & Hanslmayr, S. (2023). Hippocampal neurons code individual episodic memories in humans. Nature Human Behaviour. Advance online publication. https://doi.org/10.1038/s41562-023-01706-6

@article{43dae11e8c134ea9ad71e2f12ab7c6e9,

title = "Hippocampal neurons code individual episodic memories in humans",

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.",

author = "Kolibius, {Luca D} and Frederic Roux and George Parish and {Ter Wal}, Marije and {Van Der Plas}, Mircea and Ramesh Chelvarajah and Vijay Sawlani and Rollings, {David T} and Lang, {Johannes D} and Stephanie Gollwitzer and Katrin Walther and R{\"u}diger Hopfeng{\"a}rtner and Gernot Kreiselmeyer and Hajo Hamer and Staresina, {Bernhard P} and Maria Wimber and Howard Bowman and Simon Hanslmayr",

note = "{\textcopyright} 2023. The Author(s). This manuscript was supported by the following grants: European Research Council grant no. 647954 (S.H.), European Research Council grant no. 715714 (M.W.) and European Research Council grant no. 101001121 (B.P.S.). Epilepsy Center, Department of Neurology, University Hospital Erlangen, Friedrich-Alexander-Universit{\"a}t Erlangen-N{\"u}rnberg, Erlangen, Germany is a Full Member of ERN EpiCare. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. We thank all the patients who have participated in our study.",

year = "2023",

month = oct,

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Kolibius, LD, Roux, F, Parish, G, Ter Wal, M, Van Der Plas, M, Chelvarajah, R, Sawlani, V, Rollings, DT, Lang, JD, Gollwitzer, S, Walther, K, Hopfengärtner, R, Kreiselmeyer, G, Hamer, H, Staresina, BP, Wimber, M, Bowman, H & Hanslmayr, S 2023, 'Hippocampal neurons code individual episodic memories in humans', Nature Human Behaviour. https://doi.org/10.1038/s41562-023-01706-6

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AU - Kolibius, Luca D

AU - Roux, Frederic

AU - Parish, George

AU - Ter Wal, Marije

AU - Van Der Plas, Mircea

AU - Chelvarajah, Ramesh

AU - Sawlani, Vijay

AU - Rollings, David T

AU - Lang, Johannes D

AU - Gollwitzer, Stephanie

AU - Walther, Katrin

AU - Hopfengärtner, Rüdiger

AU - Kreiselmeyer, Gernot

AU - Hamer, Hajo

AU - Staresina, Bernhard P

AU - Wimber, Maria

AU - Bowman, Howard

AU - Hanslmayr, Simon

N1 - © 2023. The Author(s). This manuscript was supported by the following grants: European Research Council grant no. 647954 (S.H.), European Research Council grant no. 715714 (M.W.) and European Research Council grant no. 101001121 (B.P.S.). Epilepsy Center, Department of Neurology, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany is a Full Member of ERN EpiCare. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. We thank all the patients who have participated in our study.

PY - 2023/10/5

Y1 - 2023/10/5

N2 - 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.

AB - 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.

U2 - 10.1038/s41562-023-01706-6

DO - 10.1038/s41562-023-01706-6

M3 - Article

C2 - 37798368

SN - 2397-3374

JO - Nature Human Behaviour

JF - Nature Human Behaviour

ER -

Hippocampal neurons code individual episodic memories in humans

Abstract

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Projects

H2020_ERC_STREAM

H2020_ERC_CODE4MEMORY

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