IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43939-z.html
   My bibliography  Save this article

The role of experience in prioritizing hippocampal replay

Author

Listed:
  • Marta Huelin Gorriz

    (University College London (UCL))

  • Masahiro Takigawa

    (University College London (UCL))

  • Daniel Bendor

    (University College London (UCL))

Abstract

During sleep, recent memories are replayed by the hippocampus, leading to their consolidation, with a higher priority given to salient experiences. To examine the role of replay in the selective strengthening of memories, we recorded large ensembles of hippocampal place cells while male rats ran repeated spatial trajectories on two linear tracks, differing in either their familiarity or number of laps run. We observed that during sleep, the rate of replay events for a given track increased proportionally with the number of spatial trajectories run by the animal. In contrast, the rate of sleep replay events decreased if the animal was more familiar with the track. Furthermore, we find that the cumulative number of awake replay events occurring during behavior, influenced by both the novelty and duration of an experience, predicts which memories are prioritized for sleep replay, providing a more parsimonious neural correlate for the selective strengthening of memories.

Suggested Citation

  • Marta Huelin Gorriz & Masahiro Takigawa & Daniel Bendor, 2023. "The role of experience in prioritizing hippocampal replay," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43939-z
    DOI: 10.1038/s41467-023-43939-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43939-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43939-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
    ---><---

    References listed on IDEAS

    as
    1. Lisa Marshall & Halla Helgadóttir & Matthias Mölle & Jan Born, 2006. "Boosting slow oscillations during sleep potentiates memory," Nature, Nature, vol. 444(7119), pages 610-613, November.
    2. Anna C. Schapiro & Elizabeth A. McDevitt & Timothy T. Rogers & Sara C. Mednick & Kenneth A. Norman, 2018. "Human hippocampal replay during rest prioritizes weakly learned information and predicts memory performance," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    3. Erin Kendall Braun & G. Elliott Wimmer & Daphna Shohamy, 2018. "Retroactive and graded prioritization of memory by reward," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    4. Brad E. Pfeiffer & David J. Foster, 2013. "Hippocampal place-cell sequences depict future paths to remembered goals," Nature, Nature, vol. 497(7447), pages 74-79, May.
    5. David J. Foster & Matthew A. Wilson, 2006. "Reverse replay of behavioural sequences in hippocampal place cells during the awake state," Nature, Nature, vol. 440(7084), pages 680-683, March.
    6. Robert Stickgold, 2005. "Sleep-dependent memory consolidation," Nature, Nature, vol. 437(7063), pages 1272-1278, October.
    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. J Matthew Mahoney & Ali S Titiz & Amanda E Hernan & Rod C Scott, 2016. "Short-Range Temporal Interactions in Sleep; Hippocampal Spike Avalanches Support a Large Milieu of Sequential Activity Including Replay," PLOS ONE, Public Library of Science, vol. 11(2), pages 1-25, February.
    2. Nicolas Cazin & Martin Llofriu Alonso & Pablo Scleidorovich Chiodi & Tatiana Pelc & Bruce Harland & Alfredo Weitzenfeld & Jean-Marc Fellous & Peter Ford Dominey, 2019. "Reservoir computing model of prefrontal cortex creates novel combinations of previous navigation sequences from hippocampal place-cell replay with spatial reward propagation," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-32, July.
    3. Zhewei Zhang & Yuji K. Takahashi & Marlian Montesinos-Cartegena & Thorsten Kahnt & Angela J. Langdon & Geoffrey Schoenbaum, 2024. "Expectancy-related changes in firing of dopamine neurons depend on hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Anli A. Liu & Simon Henin & Saman Abbaspoor & Anatol Bragin & Elizabeth A. Buffalo & Jordan S. Farrell & David J. Foster & Loren M. Frank & Tamara Gedankien & Jean Gotman & Jennifer A. Guidera & Kari , 2022. "A consensus statement on detection of hippocampal sharp wave ripples and differentiation from other fast oscillations," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Will D Penny & Peter Zeidman & Neil Burgess, 2013. "Forward and Backward Inference in Spatial Cognition," PLOS Computational Biology, Public Library of Science, vol. 9(12), pages 1-22, December.
    6. Lukas Grossberger & Francesco P Battaglia & Martin Vinck, 2018. "Unsupervised clustering of temporal patterns in high-dimensional neuronal ensembles using a novel dissimilarity measure," PLOS Computational Biology, Public Library of Science, vol. 14(7), pages 1-34, July.
    7. Hefei Guan & Steven J. Middleton & Takafumi Inoue & Thomas J. McHugh, 2021. "Lateralization of CA1 assemblies in the absence of CA3 input," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    8. Aurelio Cortese & Ryu Ohata & Maria Alemany-González & Norimichi Kitagawa & Hiroshi Imamizu & Ai Koizumi, 2024. "Time-dependent neural arbitration between cue associative and episodic fear memories," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. Johannes Holz & Hannah Piosczyk & Nina Landmann & Bernd Feige & Kai Spiegelhalder & Dieter Riemann & Christoph Nissen & Ulrich Voderholzer, 2012. "The Timing of Learning before Night-Time Sleep Differentially Affects Declarative and Procedural Long-Term Memory Consolidation in Adolescents," PLOS ONE, Public Library of Science, vol. 7(7), pages 1-10, July.
    10. Sabrina Camargo & Maik Riedl & Celia Anteneodo & Jürgen Kurths & Thomas Penzel & Niels Wessel, 2014. "Sleep Apnea-Hypopnea Quantification by Cardiovascular Data Analysis," PLOS ONE, Public Library of Science, vol. 9(9), pages 1-9, September.
    11. Megha Jhanji & Chintada Nageswara Rao & Jacob C. Massey & Marion C. Hope & Xueyan Zhou & C. Dirk Keene & Tao Ma & Michael D. Wyatt & Jason A. Stewart & Mathew Sajish, 2022. "Cis- and trans-resveratrol have opposite effects on histone serine-ADP-ribosylation and tyrosine induced neurodegeneration," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    12. Nozomu H. Nakamura & Hidemasa Furue & Kenta Kobayashi & Yoshitaka Oku, 2023. "Hippocampal ensemble dynamics and memory performance are modulated by respiration during encoding," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. Usman Farooq & George Dragoi, 2024. "Experience of Euclidean geometry sculpts the development and dynamics of rodent hippocampal sequential cell assemblies," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    14. Aaron V Berard & Matthew S Cain & Takeo Watanabe & Yuka Sasaki, 2015. "Frequent Video Game Players Resist Perceptual Interference," PLOS ONE, Public Library of Science, vol. 10(3), pages 1-10, March.
    15. Sergio Garbarino, 2020. "Sleep Disorders across the Lifespan: A Different Perspective," IJERPH, MDPI, vol. 17(23), pages 1-5, December.
    16. Jennifer E Ashton & Scott A Cairney, 2021. "Future-relevant memories are not selectively strengthened during sleep," PLOS ONE, Public Library of Science, vol. 16(11), pages 1-14, November.
    17. 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.
    18. Chaogan Yan & Dongqiang Liu & Yong He & Qihong Zou & Chaozhe Zhu & Xinian Zuo & Xiangyu Long & Yufeng Zang, 2009. "Spontaneous Brain Activity in the Default Mode Network Is Sensitive to Different Resting-State Conditions with Limited Cognitive Load," PLOS ONE, Public Library of Science, vol. 4(5), pages 1-11, May.
    19. Asako Noguchi & Roman Huszár & Shota Morikawa & György Buzsáki & Yuji Ikegaya, 2022. "Inhibition allocates spikes during hippocampal ripples," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    20. Hong Yu & Xinkuan Xiang & Zongming Chen & Xu Wang & Jiaqi Dai & Xinxin Wang & Pengcheng Huang & Zheng-dong Zhao & Wei L. Shen & Haohong Li, 2021. "Periaqueductal gray neurons encode the sequential motor program in hunting behavior of mice," Nature Communications, Nature, vol. 12(1), pages 1-15, 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:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43939-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.