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Effects of visual inputs on neural dynamics for coding of location and running speed in medial entorhinal cortex

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Cite this article as: eLife 2020;9:e62500 doi: 10.7554/eLife.62500

Abstract

Neuronal representations of spatial location and movement speed in the medial entorhinal cortex during the 'active' theta state of the brain are important for memory-guided navigation and rely on visual inputs. However, little is known about how visual inputs change neural dynamics as a function of running speed and time. By manipulating visual inputs in mice, we demonstrate that changes in spatial stability of grid cell firing correlate with changes in a proposed speed signal by local field potential theta frequency. In contrast, visual inputs do not alter the running speed-dependent gain in neuronal firing rates. Moreover, we provide evidence that sensory inputs other than visual inputs can support grid cell firing, though less accurately, in complete darkness. Finally, changes in spatial accuracy of grid cell firing on a 10 s time scale suggest that grid cell firing is a function of velocity signals integrated over past time.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Matlab code for Figure 4 is provided on the laboratory's GitHub page (https://github.com/hasselmonians/light-modulation and https://github.com/hasselmonians/mle_rhythmicity). Source data files have been provided for Figures 2, 3, 4, 5, and 6.

Article and author information

Author details

  1. Holger Dannenberg

    Psychological & Brain Sciences, Boston University, Boston, United States
    For correspondence
    hdannenb@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0340-0128
  2. Hallie Lazaro

    Psychological & Brain Sciences, Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Pranav Nambiar

    Psychological & Brain Sciences, Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Alec Hoyland

    Psychological & Brain Sciences, Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4732-5932
  5. Michael E. Hasselmo

    Psychological & Brain Sciences, Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9925-6377

Funding

National Institutes of Health (R01MH60013)

  • Holger Dannenberg
  • Hallie Lazaro
  • Pranav Nambiar
  • Alec Hoyland
  • Michael E. Hasselmo

National Institutes of Health (R01MH120073)

  • Holger Dannenberg
  • Hallie Lazaro
  • Pranav Nambiar
  • Alec Hoyland
  • Michael E. Hasselmo

National Institutes of Health (R01MH052090)

  • Holger Dannenberg
  • Hallie Lazaro
  • Pranav Nambiar
  • Alec Hoyland
  • Michael E. Hasselmo

National Institutes of Health (K99NS116129)

  • Holger Dannenberg

Office of Naval Research (MURI N00014-16-1-2832)

  • Holger Dannenberg
  • Hallie Lazaro
  • Pranav Nambiar
  • Alec Hoyland
  • Michael E. Hasselmo

Office of Naval Research (MURI N00014-19-1-2571)

  • Holger Dannenberg
  • Hallie Lazaro
  • Pranav Nambiar
  • Alec Hoyland
  • Michael E. Hasselmo

Office of Naval Research (DURIP N00014-17-1-2304)

  • Holger Dannenberg
  • Hallie Lazaro
  • Pranav Nambiar
  • Alec Hoyland
  • Michael E. Hasselmo

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All handling of animals and experimental procedures were approved by the Institutional Animal Care and Use Committee (IACUC) for the Charles River Campus at Boston University under protocol #16-008 . All surgery was performed under isoflurane anesthesia and buprenorphine analgesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. Adrien Peyrache, McGill University, Canada

Publication history

  1. Received: August 26, 2020
  2. Accepted: December 9, 2020
  3. Accepted Manuscript published: December 10, 2020 (version 1)
  4. Version of Record published: December 30, 2020 (version 2)

Copyright

© 2020, Dannenberg 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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