IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43254-7.html
   My bibliography  Save this article

Cortical reactivation of spatial and non-spatial features coordinates with hippocampus to form a memory dialogue

Author

Listed:
  • HaoRan Chang

    (University of Lethbridge)

  • Ingrid M. Esteves

    (University of Lethbridge)

  • Adam R. Neumann

    (University of Lethbridge)

  • Majid H. Mohajerani

    (University of Lethbridge
    McGill University)

  • Bruce L. McNaughton

    (University of Lethbridge
    University of California)

Abstract

Episodic memories comprise diverse attributes of experience distributed across neocortical areas. The hippocampus is integral to rapidly binding these diffuse representations, as they occur, to be later reinstated. However, the nature of the information exchanged during this hippocampal-cortical dialogue remains poorly understood. A recent study has shown that the secondary motor cortex carries two types of representations: place cell-like activity, which were impaired by hippocampal lesions, and responses tied to visuo-tactile cues, which became more pronounced following hippocampal lesions. Using two-photon Ca2+ imaging to record neuronal activities in the secondary motor cortex of male Thy1-GCaMP6s mice, we assessed the cortical retrieval of spatial and non-spatial attributes from previous explorations in a virtual environment. We show that, following navigation, spontaneous resting state reactivations convey varying degrees of spatial (trajectory sequences) and non-spatial (visuo-tactile attributes) information, while reactivations of non-spatial attributes tend to precede reactivations of spatial representations surrounding hippocampal sharp-wave ripples.

Suggested Citation

  • HaoRan Chang & Ingrid M. Esteves & Adam R. Neumann & Majid H. Mohajerani & Bruce L. McNaughton, 2023. "Cortical reactivation of spatial and non-spatial features coordinates with hippocampus to form a memory dialogue," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43254-7
    DOI: 10.1038/s41467-023-43254-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43254-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43254-7?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. Dun Mao & Steffen Kandler & Bruce L. McNaughton & Vincent Bonin, 2017. "Sparse orthogonal population representation of spatial context in the retrosplenial cortex," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    2. N. K. Logothetis & O. Eschenko & Y. Murayama & M. Augath & T. Steudel & H. C. Evrard & M. Besserve & A. Oeltermann, 2012. "Hippocampal–cortical interaction during periods of subcortical silence," Nature, Nature, vol. 491(7425), pages 547-553, November.
    3. Alessio Attardo & James E. Fitzgerald & Mark J. Schnitzer, 2015. "Impermanence of dendritic spines in live adult CA1 hippocampus," Nature, Nature, vol. 523(7562), pages 592-596, July.
    4. Simon P. Fisher & Nanyi Cui & Laura E. McKillop & Jessica Gemignani & David M. Bannerman & Peter L. Oliver & Stuart N. Peirson & Vladyslav V. Vyazovskiy, 2016. "Stereotypic wheel running decreases cortical activity in mice," Nature Communications, Nature, vol. 7(1), pages 1-12, December.
    5. Christopher D. Harvey & Philip Coen & David W. Tank, 2012. "Choice-specific sequences in parietal cortex during a virtual-navigation decision task," Nature, Nature, vol. 484(7392), pages 62-68, April.
    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. Weilun Sun & Ilseob Choi & Stoyan Stoyanov & Oleg Senkov & Evgeni Ponimaskin & York Winter & Janelle M. P. Pakan & Alexander Dityatev, 2021. "Context value updating and multidimensional neuronal encoding in the retrosplenial cortex," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    2. Luis M. Franco & Michael J. Goard, 2024. "Differential stability of task variable representations in retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. A. Barri & M. T. Wiechert & M. Jazayeri & D. A. DiGregorio, 2022. "Synaptic basis of a sub-second representation of time in a neural circuit model," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. Rodrigo Ordoñez Sierra & Lizeth Katherine Pedraza & Lívia Barcsai & Andrea Pejin & Qun Li & Gábor Kozák & Yuichi Takeuchi & Anett J. Nagy & Magor L. Lőrincz & Orrin Devinsky & György Buzsáki & Antal B, 2023. "Closed-loop brain stimulation augments fear extinction in male rats," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    9. Adeeti Aggarwal & Connor Brennan & Jennifer Luo & Helen Chung & Diego Contreras & Max B. Kelz & Alex Proekt, 2022. "Visual evoked feedforward–feedback traveling waves organize neural activity across the cortical hierarchy in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    10. Kaushik J. Lakshminarasimhan & Eric Avila & Xaq Pitkow & Dora E. Angelaki, 2023. "Dynamical latent state computation in the male macaque posterior parietal cortex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    11. John Palmer & Adam Keane & Pulin Gong, 2017. "Learning and executing goal-directed choices by internally generated sequences in spiking neural circuits," PLOS Computational Biology, Public Library of Science, vol. 13(7), pages 1-23, July.
    12. Xunda Wang & Alex T. L. Leong & Shawn Z. K. Tan & Eddie C. Wong & Yilong Liu & Lee-Wei Lim & Ed X. Wu, 2023. "Functional MRI reveals brain-wide actions of thalamically-initiated oscillatory activities on associative memory consolidation," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    13. David Kappel & Bernhard Nessler & Wolfgang Maass, 2014. "STDP Installs in Winner-Take-All Circuits an Online Approximation to Hidden Markov Model Learning," PLOS Computational Biology, Public Library of Science, vol. 10(3), pages 1-22, March.
    14. Yalin Yu & Yue Qiu & Gen Li & Kaiwei Zhang & Binshi Bo & Mengchao Pei & Jingjing Ye & Garth J. Thompson & Jing Cang & Fang Fang & Yanqiu Feng & Xiaojie Duan & Chuanjun Tong & Zhifeng Liang, 2023. "Sleep fMRI with simultaneous electrophysiology at 9.4 T in male mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    15. Shinichiro Kira & Houman Safaai & Ari S. Morcos & Stefano Panzeri & Christopher D. Harvey, 2023. "A distributed and efficient population code of mixed selectivity neurons for flexible navigation decisions," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    16. Amelia J. Christensen & Jonathan W. Pillow, 2022. "Reduced neural activity but improved coding in rodent higher-order visual cortex during locomotion," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    17. Ryan C Williamson & Benjamin R Cowley & Ashok Litwin-Kumar & Brent Doiron & Adam Kohn & Matthew A Smith & Byron M Yu, 2016. "Scaling Properties of Dimensionality Reduction for Neural Populations and Network Models," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-27, December.
    18. Ege Altan & Sara A Solla & Lee E Miller & Eric J Perreault, 2021. "Estimating the dimensionality of the manifold underlying multi-electrode neural recordings," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-23, November.
    19. Xu Han & Ben Vermaercke & Vincent Bonin, 2022. "Diversity of spatiotemporal coding reveals specialized visual processing streams in the mouse cortex," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    20. Haoxin Zhang & Ivan Skelin & Shiting Ma & Michelle Paff & Lilit Mnatsakanyan & Michael A. Yassa & Robert T. Knight & Jack J. Lin, 2024. "Awake ripples enhance emotional memory encoding in the human brain," Nature Communications, Nature, vol. 15(1), pages 1-13, 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_s41467-023-43254-7. 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.