IDEAS home Printed from https://ideas.repec.org/a/nat/nathum/v8y2024i3d10.1038_s41562-023-01799-z.html
   My bibliography  Save this article

A generative model of memory construction and consolidation

Author

Listed:
  • Eleanor Spens

    (University College London)

  • Neil Burgess

    (University College London
    University College London)

Abstract

Episodic memories are (re)constructed, share neural substrates with imagination, combine unique features with schema-based predictions and show schema-based distortions that increase with consolidation. Here we present a computational model in which hippocampal replay (from an autoassociative network) trains generative models (variational autoencoders) to (re)create sensory experiences from latent variable representations in entorhinal, medial prefrontal and anterolateral temporal cortices via the hippocampal formation. Simulations show effects of memory age and hippocampal lesions in agreement with previous models, but also provide mechanisms for semantic memory, imagination, episodic future thinking, relational inference and schema-based distortions including boundary extension. The model explains how unique sensory and predictable conceptual elements of memories are stored and reconstructed by efficiently combining both hippocampal and neocortical systems, optimizing the use of limited hippocampal storage for new and unusual information. Overall, we believe hippocampal replay training generative models provides a comprehensive account of memory construction, imagination and consolidation.

Suggested Citation

  • Eleanor Spens & Neil Burgess, 2024. "A generative model of memory construction and consolidation," Nature Human Behaviour, Nature, vol. 8(3), pages 526-543, March.
    • Handle: RePEc:nat:nathum:v:8:y:2024:i:3:d:10.1038_s41562-023-01799-z
    DOI: 10.1038/s41562-023-01799-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41562-023-01799-z
    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/s41562-023-01799-z?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. Shekoofeh Hedayati & Ryan E. O’Donnell & Brad Wyble, 2022. "A model of working memory for latent representations," Nature Human Behaviour, Nature, vol. 6(5), pages 709-719, May.
    2. Edward H. Nieh & Manuel Schottdorf & Nicolas W. Freeman & Ryan J. Low & Sam Lewallen & Sue Ann Koay & Lucas Pinto & Jeffrey L. Gauthier & Carlos D. Brody & David W. Tank, 2021. "Geometry of abstract learned knowledge in the hippocampus," Nature, Nature, vol. 595(7865), pages 80-84, July.
    3. 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.
    4. Albert Tsao & Jørgen Sugar & Li Lu & Cheng Wang & James J. Knierim & May-Britt Moser & Edvard I. Moser, 2018. "Integrating time from experience in the lateral entorhinal cortex," Nature, Nature, vol. 561(7721), pages 57-62, September.
    5. Gido M. Ven & Hava T. Siegelmann & Andreas S. Tolias, 2020. "Brain-inspired replay for continual learning with artificial neural networks," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    6. Torkel Hafting & Marianne Fyhn & Sturla Molden & May-Britt Moser & Edvard I. Moser, 2005. "Microstructure of a spatial map in the entorhinal cortex," Nature, Nature, vol. 436(7052), pages 801-806, August.
    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. Krishna Choudhary & Sven Berberich & Thomas T. G. Hahn & James M. McFarland & Mayank R. Mehta, 2024. "Spontaneous persistent activity and inactivity in vivo reveals differential cortico-entorhinal functional connectivity," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. 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.
    3. Isabella C. Wagner & Luise P. Graichen & Boryana Todorova & Andre Lüttig & David B. Omer & Matthias Stangl & Claus Lamm, 2023. "Entorhinal grid-like codes and time-locked network dynamics track others navigating through space," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Babak Shahbaba & Lingge Li & Forest Agostinelli & Mansi Saraf & Keiland W. Cooper & Derenik Haghverdian & Gabriel A. Elias & Pierre Baldi & Norbert J. Fortin, 2022. "Hippocampal ensembles represent sequential relationships among an extended sequence of nonspatial events," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Taylor J. Malone & Nai-Wen Tien & Yan Ma & Lian Cui & Shangru Lyu & Garret Wang & Duc Nguyen & Kai Zhang & Maxym V. Myroshnychenko & Jean Tyan & Joshua A. Gordon & David A. Kupferschmidt & Yi Gu, 2024. "A consistent map in the medial entorhinal cortex supports spatial memory," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    6. Kyerl Park & Yoonsoo Yeo & Kisung Shin & Jeehyun Kwag, 2024. "Egocentric neural representation of geometric vertex in the retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Noga Mosheiff & Haggai Agmon & Avraham Moriel & Yoram Burak, 2017. "An efficient coding theory for a dynamic trajectory predicts non-uniform allocation of entorhinal grid cells to modules," PLOS Computational Biology, Public Library of Science, vol. 13(6), pages 1-19, June.
    8. Wenqi Chen & Jiejunyi Liang & Qiyun Wu & Yunyun Han, 2024. "Anterior cingulate cortex provides the neural substrates for feedback-driven iteration of decision and value representation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    9. Balázs Ujfalussy & Tamás Kiss & Péter Érdi, 2009. "Parallel Computational Subunits in Dentate Granule Cells Generate Multiple Place Fields," PLOS Computational Biology, Public Library of Science, vol. 5(9), pages 1-16, September.
    10. Louis-Emmanuel Martinet & Denis Sheynikhovich & Karim Benchenane & Angelo Arleo, 2011. "Spatial Learning and Action Planning in a Prefrontal Cortical Network Model," PLOS Computational Biology, Public Library of Science, vol. 7(5), pages 1-21, May.
    11. P. Dylan Rich & Stephan Yves Thiberge & Benjamin B. Scott & Caiying Guo & D. Gowanlock R. Tervo & Carlos D. Brody & Alla Y. Karpova & Nathaniel D. Daw & David W. Tank, 2024. "Magnetic voluntary head-fixation in transgenic rats enables lifespan imaging of hippocampal neurons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    12. Florian Raudies & Michael E Hasselmo, 2012. "Modeling Boundary Vector Cell Firing Given Optic Flow as a Cue," PLOS Computational Biology, Public Library of Science, vol. 8(6), pages 1-17, June.
    13. Terra A. Schall & King-Lun Li & Xiguang Qi & Brian T. Lee & William J. Wright & Erin E. Alpaugh & Rachel J. Zhao & Jianwei Liu & Qize Li & Bo Zeng & Lirong Wang & Yanhua H. Huang & Oliver M. Schlüter , 2024. "Temporal dynamics of nucleus accumbens neurons in male mice during reward seeking," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    14. Avgar, Tal & Deardon, Rob & Fryxell, John M., 2013. "An empirically parameterized individual based model of animal movement, perception, and memory," Ecological Modelling, Elsevier, vol. 251(C), pages 158-172.
    15. Sabrina L. L. Maoz & Matthias Stangl & Uros Topalovic & Daniel Batista & Sonja Hiller & Zahra M. Aghajan & Barbara Knowlton & John Stern & Jean-Philippe Langevin & Itzhak Fried & Dawn Eliashiv & Nanth, 2023. "Dynamic neural representations of memory and space during human ambulatory navigation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    16. Qiming Shao & Ligu Chen & Xiaowan Li & Miao Li & Hui Cui & Xiaoyue Li & Xinran Zhao & Yuying Shi & Qiang Sun & Kaiyue Yan & Guangfu Wang, 2024. "A non-canonical visual cortical-entorhinal pathway contributes to spatial navigation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    17. Xiaxia Xu & Lingzhen Song & Rebecca Kringel & Ileana L. Hanganu-Opatz, 2021. "Developmental decrease of entorhinal-hippocampal communication in immune-challenged DISC1 knockdown mice," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    18. Fabian Kessler & Julia Frankenstein & Constantin A. Rothkopf, 2024. "Human navigation strategies and their errors result from dynamic interactions of spatial uncertainties," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    19. Alexander Thomas Keinath, 2016. "The Preferred Directions of Conjunctive Grid X Head Direction Cells in the Medial Entorhinal Cortex Are Periodically Organized," PLOS ONE, Public Library of Science, vol. 11(3), pages 1-11, March.
    20. Toon Van de Maele & Bart Dhoedt & Tim Verbelen & Giovanni Pezzulo, 2024. "A hierarchical active inference model of spatial alternation tasks and the hippocampal-prefrontal circuit," Nature Communications, Nature, vol. 15(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:8:y:2024:i:3:d:10.1038_s41562-023-01799-z. 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.