Abstract

The hippocampal dentate gyrus is an important relay conveying sensory information from the entorhinal cortex to the hippocampus proper. During exploration, the dentate gyrus has been proposed to act as a pattern separator. However, the dentate gyrus also shows structured activity during immobility and sleep. The properties of these activity patterns at cellular resolution, and their role in hippocampal-dependent memory processes have remained unclear. Using dual-color in-vivo two-photon Ca2+ imaging, we show that in immobile mice dentate granule cells generate sparse, synchronized activity patterns associated with entorhinal cortex activation. These population events are structured and modified by changes in the environment; and they incorporate place- and speed cells. Importantly, they are more similar than expected by chance to population patterns evoked during self-motion. Using optogenetic inhibition, we show that granule cell activity is not only required during exploration, but also during immobility in order to form dentate gyrus-dependent spatial memories.

Data availability

Binarized imaging traces of all cells from all experiment sessions are available on Dryad. https://doi.org/10.5061/dryad.mkkwh70z6.

The following data sets were generated

Article and author information

Author details

  1. Martin Pofahl

    Institute of Experimental Epileptology and Cognition Research, University of Bonn Medical Center, University of Bonn Medical Center, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9473-6195
  2. Negar Nikbakht

    Institute of Experimental Epileptology and Cognition Research, University of Bonn Medical Center, University of Bonn Medical Center, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. André N Haubrich

    Institute of Experimental Epileptology and Cognition Research, University of Bonn Medical Center, University of Bonn Medical Center, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7895-6203
  4. Theresa M Nguyen

    Institute of Experimental Epileptology and Cognition Research, University of Bonn Medical Center, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Nicola Masala

    Institute of Experimental Epileptology and Cognition Research, University of Bonn Medical Center, University of Bonn Medical Center, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Fabian J Distler

    Institute of Experimental Epileptology and Cognition Research, University of Bonn Medical Center, University of Bonn Medical Center, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Oliver Braganza

    Institute of Experimental Epileptology and Cognition Research, University of Bonn Medical Center, University of Bonn Medical Center, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8508-1070
  8. Jakob H Macke

    Excellence Cluster Machine Learning, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5154-8912
  9. Laura A Ewell

    Institute of Experimental Epileptology and Cognition Research, University of Bonn Medical Center, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Kurtulus Golcuk

    Institute of Experimental Epileptology and Cognition Research, University of Bonn Medical Center, University of Bonn Medical Center, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  11. Heinz Beck

    IEECR, University of Bonn Medical Center, Bonn, Germany
    For correspondence
    heinz.beck@ukbonn.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8961-998X

Funding

Deutsche Forschungsgemeinschaft (SFB 1089,Project C04)

  • Heinz Beck

Deutsche Forschungsgemeinschaft (EXC 2064/1 PN 390727645)

  • Jakob H Macke
  • Heinz Beck

Alexander von Humboldt-Stiftung (PSI)

  • Kurtulus Golcuk

Volkswagen Foundation

  • Oliver Braganza
  • Laura A Ewell

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Laura L Colgin, University of Texas at Austin, United States

Ethics

Animal experimentation: All animal experiments were conducted in accordance with European (2010/63/EU) and federal law (TierSchG, TierSchVersV) on animal care and use and approved by the county of North-Rhine Westphalia (LANUV AZ 84-02.04.2015.A524, AZ 81-02.04.2019.A216).

Version history

  1. Received: December 15, 2020
  2. Accepted: March 11, 2021
  3. Accepted Manuscript published: March 12, 2021 (version 1)
  4. Version of Record published: March 23, 2021 (version 2)

Copyright

© 2021, Pofahl et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Martin Pofahl
  2. Negar Nikbakht
  3. André N Haubrich
  4. Theresa M Nguyen
  5. Nicola Masala
  6. Fabian J Distler
  7. Oliver Braganza
  8. Jakob H Macke
  9. Laura A Ewell
  10. Kurtulus Golcuk
  11. Heinz Beck
(2021)
Synchronous activity patterns in the dentate gyrus during immobility
eLife 10:e65786.
https://doi.org/10.7554/eLife.65786

Share this article

https://doi.org/10.7554/eLife.65786

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