IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-55833-x.html
   My bibliography  Save this article

Coordinated representations for naturalistic memory encoding and retrieval in hippocampal neural subspaces

Author

Listed:
  • Dasom Kwon

    (Sungkyunkwan University
    Institute for Basic Science)

  • Jungwoo Kim

    (Sungkyunkwan University
    Institute for Basic Science
    Sungkyunkwan University)

  • Seng Bum Michael Yoo

    (Sungkyunkwan University
    Institute for Basic Science
    Sungkyunkwan University
    Baylor College of Medicine)

  • Won Mok Shim

    (Sungkyunkwan University
    Institute for Basic Science
    Sungkyunkwan University)

Abstract

Our naturalistic experiences are organized into memories through multiple processes, including novelty encoding, memory formation, and retrieval. However, the neural mechanisms coordinating these processes remain elusive. Using fMRI data acquired during movie viewing and subsequent narrative recall, we examine hippocampal neural subspaces associated with distinct memory processes and characterized their relationships. We quantify novelty in character co-occurrences and the valence of relationships and estimate event memorability. Within the hippocampus, the novelty subspaces encoding each type exhibit partial overlap, and these overlapping novelty subspaces align with the subspace involved in memorability. Notably, following event boundaries, hippocampal states within these subspaces align inversely along a shared coding axis, predicting subsequent recall performance. This novelty-memorability alignment is selectively observed during encoding but not during retrieval. Finally, the identified functional subspaces reflect the intrinsic functional organization of the hippocampus. Our findings offer insights into how the hippocampus dynamically coordinates representations underlying memory encoding and retrieval at the population level to transform ongoing experiences into enduring memories.

Suggested Citation

  • Dasom Kwon & Jungwoo Kim & Seng Bum Michael Yoo & Won Mok Shim, 2025. "Coordinated representations for naturalistic memory encoding and retrieval in hippocampal neural subspaces," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-55833-x
    DOI: 10.1038/s41467-025-55833-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-55833-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-025-55833-x?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
    ---><---

    References listed on IDEAS

    as
    1. Anuck Sawangjit & Carlos N. Oyanedel & Niels Niethard & Carolina Salazar & Jan Born & Marion Inostroza, 2018. "The hippocampus is crucial for forming non-hippocampal long-term memory during sleep," Nature, Nature, vol. 564(7734), pages 109-113, December.
    2. Harrison Ritz & Amitai Shenhav, 2024. "Orthogonal neural encoding of targets and distractors supports multivariate cognitive control," Nature Human Behaviour, Nature, vol. 8(5), pages 945-961, May.
    3. Valerio Mante & David Sussillo & Krishna V. Shenoy & William T. Newsome, 2013. "Context-dependent computation by recurrent dynamics in prefrontal cortex," Nature, Nature, vol. 503(7474), pages 78-84, November.
    4. Gamaleldin F. Elsayed & Antonio H. Lara & Matthew T. Kaufman & Mark M. Churchland & John P. Cunningham, 2016. "Reorganization between preparatory and movement population responses in motor cortex," Nature Communications, Nature, vol. 7(1), pages 1-15, December.
    5. Zachariah M. Reagh & Charan Ranganath, 2023. "Flexible reuse of cortico-hippocampal representations during encoding and recall of naturalistic events," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Halle R. Dimsdale-Zucker & Maureen Ritchey & Arne D. Ekstrom & Andrew P. Yonelinas & Charan Ranganath, 2018. "CA1 and CA3 differentially support spontaneous retrieval of episodic contexts within human hippocampal subfields," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    7. Marius V. Peelen & Paul E. Downing, 2023. "Testing cognitive theories with multivariate pattern analysis of neuroimaging data," Nature Human Behaviour, Nature, vol. 7(9), pages 1430-1441, September.
    Full references (including those not matched with items on IDEAS)

    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. Pierre O. Boucher & Tian Wang & Laura Carceroni & Gary Kane & Krishna V. Shenoy & Chandramouli Chandrasekaran, 2023. "Initial conditions combine with sensory evidence to induce decision-related dynamics in premotor cortex," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    2. Nir Even-Chen & Blue Sheffer & Saurabh Vyas & Stephen I Ryu & Krishna V Shenoy, 2019. "Structure and variability of delay activity in premotor cortex," PLOS Computational Biology, Public Library of Science, vol. 15(2), pages 1-17, February.
    3. Javier G. Orlandi & Mohammad Abdolrahmani & Ryo Aoki & Dmitry R. Lyamzin & Andrea Benucci, 2023. "Distributed context-dependent choice information in mouse posterior cortex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. 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.
    5. Atsushi Kikumoto & Apoorva Bhandari & Kazuhisa Shibata & David Badre, 2024. "A transient high-dimensional geometry affords stable conjunctive subspaces for efficient action selection," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Georgia Koppe & Hazem Toutounji & Peter Kirsch & Stefanie Lis & Daniel Durstewitz, 2019. "Identifying nonlinear dynamical systems via generative recurrent neural networks with applications to fMRI," PLOS Computational Biology, Public Library of Science, vol. 15(8), pages 1-35, August.
    7. Jan Weber & Anne-Kristin Solbakk & Alejandro O. Blenkmann & Anais Llorens & Ingrid Funderud & Sabine Leske & Pål Gunnar Larsson & Jugoslav Ivanovic & Robert T. Knight & Tor Endestad & Randolph F. Helf, 2024. "Ramping dynamics and theta oscillations reflect dissociable signatures during rule-guided human behavior," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Eric A. Kirk & Keenan T. Hope & Samuel J. Sober & Britton A. Sauerbrei, 2024. "An output-null signature of inertial load in motor cortex," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Rishi Rajalingham & Aída Piccato & Mehrdad Jazayeri, 2022. "Recurrent neural networks with explicit representation of dynamic latent variables can mimic behavioral patterns in a physical inference task," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    10. Wan-Yu Shih & Hsiang-Yu Yu & Cheng-Chia Lee & Chien-Chen Chou & Chien Chen & Paul W. Glimcher & Shih-Wei Wu, 2023. "Electrophysiological population dynamics reveal context dependencies during decision making in human frontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    11. Wenyi Zhang & Yang Xie & Tianming Yang, 2022. "Reward salience but not spatial attention dominates the value representation in the orbitofrontal cortex," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    12. Yann Vanrobaeys & Utsav Mukherjee & Lucy Langmack & Stacy E. Beyer & Ethan Bahl & Li-Chun Lin & Jacob J. Michaelson & Ted Abel & Snehajyoti Chatterjee, 2023. "Mapping the spatial transcriptomic signature of the hippocampus during memory consolidation," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    13. Rishi Rajalingham & Hansem Sohn & Mehrdad Jazayeri, 2025. "Dynamic tracking of objects in the macaque dorsomedial frontal cortex," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    14. Joao Barbosa & Rémi Proville & Chris C. Rodgers & Michael R. DeWeese & Srdjan Ostojic & Yves Boubenec, 2023. "Early selection of task-relevant features through population gating," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    15. Nir Moneta & Mona M. Garvert & Hauke R. Heekeren & Nicolas W. Schuck, 2023. "Task state representations in vmPFC mediate relevant and irrelevant value signals and their behavioral influence," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    16. Huanyuan Zhou & KongFatt Wong-Lin & Da-Hui Wang, 2018. "Parallel Excitatory and Inhibitory Neural Circuit Pathways Underlie Reward-Based Phasic Neural Responses," Complexity, Hindawi, vol. 2018, pages 1-20, April.
    17. Benjamin R Cowley & Matthew A Smith & Adam Kohn & Byron M Yu, 2016. "Stimulus-Driven Population Activity Patterns in Macaque Primary Visual Cortex," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-31, December.
    18. Kiyohito Iigaya & Sanghyun Yi & Iman A. Wahle & Sandy Tanwisuth & Logan Cross & John P. O’Doherty, 2023. "Neural mechanisms underlying the hierarchical construction of perceived aesthetic value," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    19. Takuya Ito & Guangyu Robert Yang & Patryk Laurent & Douglas H. Schultz & Michael W. Cole, 2022. "Constructing neural network models from brain data reveals representational transformations linked to adaptive behavior," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    20. Eleanor Holton & Jan Grohn & Harry Ward & Sanjay G. Manohar & Jill X. O’Reilly & Nils Kolling, 2024. "Goal commitment is supported by vmPFC through selective attention," Nature Human Behaviour, Nature, vol. 8(7), pages 1351-1365, July.

    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:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-55833-x. 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.