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Reverse replay of behavioural sequences in hippocampal place cells during the awake state

Author

Listed:
  • David J. Foster

    (Massachusetts Institute of Technology)

  • Matthew A. Wilson

    (Massachusetts Institute of Technology)

Abstract

Run that by me again... During sleep, neurons in the rat hippocampus are known to replay sequences of activity that took place when the rat was awake. A new study, in rats running around a track, eating and grooming, shows that replay also occurs repeatedly during the awake state, and that behavioural sequences are replayed in reverse order. Theories of spatial learning have previously suggested that reverse replay might be useful. Replay during the awake state might also explain in part why learning can be more effective if learning sessions are spaced out in time rather than clustered together, why hyperactivity causes learning problems, and why simply being awake and resting can help learning.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:nature:v:440:y:2006:i:7084:d:10.1038_nature04587
    DOI: 10.1038/nature04587
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    Cited by:

    1. 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.
    2. 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.
    3. Alpha Renner & Forrest Sheldon & Anatoly Zlotnik & Louis Tao & Andrew Sornborger, 2024. "The backpropagation algorithm implemented on spiking neuromorphic hardware," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. 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.
    5. Alex P. Vaz & John H. Wittig & Sara K. Inati & Kareem A. Zaghloul, 2023. "Backbone spiking sequence as a basis for preplay, replay, and default states in human cortex," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. 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.
    7. Qi Huang & Zhibing Xiao & Qianqian Yu & Yuejia Luo & Jiahua Xu & Yukun Qu & Raymond Dolan & Timothy Behrens & Yunzhe Liu, 2024. "Replay-triggered brain-wide activation in humans," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. 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.
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    10. 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.
    11. 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.
    12. Murphy, Roy E, 2006. "Information Theory and Knowledge-Gathering," MPRA Paper 16, University Library of Munich, Germany.
    13. 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.
    14. 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.
    15. 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.
    16. 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.
    17. Demetrio Ferro & Tyler Cash-Padgett & Maya Zhe Wang & Benjamin Y. Hayden & Rubén Moreno-Bote, 2024. "Gaze-centered gating, reactivation, and reevaluation of economic value in orbitofrontal cortex," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    18. Hannah Tarder-Stoll & Christopher Baldassano & Mariam Aly, 2024. "The brain hierarchically represents the past and future during multistep anticipation," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    19. 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.
    20. Caleb Kemere & Margaret F Carr & Mattias P Karlsson & Loren M Frank, 2013. "Rapid and Continuous Modulation of Hippocampal Network State during Exploration of New Places," PLOS ONE, Public Library of Science, vol. 8(9), pages 1-16, September.
    21. 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.
    22. Carina Curto & Vladimir Itskov, 2008. "Cell Groups Reveal Structure of Stimulus Space," PLOS Computational Biology, Public Library of Science, vol. 4(10), pages 1-13, October.
    23. Buddhika Bellana & Abhijit Mahabal & Christopher J. Honey, 2022. "Narrative thinking lingers in spontaneous thought," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

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