Replay as wavefronts and theta sequences as bump oscillations in a grid cell attractor network

  1. Louis Kang  Is a corresponding author
  2. Michael R DeWeese
  1. University of California, Berkeley, United States

Abstract

Grid cells fire in sequences that represent rapid trajectories in space. During locomotion, theta sequences encode sweeps in position starting slightly behind the animal and ending ahead of it. During quiescence and slow wave sleep, bouts of synchronized activity represent long trajectories called replays, which are well-established in place cells and have been recently reported in grid cells. Theta sequences and replay are hypothesized to facilitate many cognitive functions, but their underlying mechanisms are unknown. One mechanism proposed for grid cell formation is the continuous attractor network. We demonstrate that this established architecture naturally produces theta sequences and replay as distinct consequences of modulating external input. Driving inhibitory interneurons at the theta frequency causes attractor bumps to oscillate in speed and size, which gives rise to theta sequences and phase precession, respectively. Decreasing input drive to all neurons produces traveling wavefronts of activity that are decoded as replays.

Data availability

Source code for the simulations have been included as supporting files.

Article and author information

Author details

  1. Louis Kang

    Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States
    For correspondence
    louis.kang@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5702-2740
  2. Michael R DeWeese

    Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

Adolph C. and Mary Sprague Miller Institute for Basic Research in Science, University of California Berkeley (Postdoctoral fellowship)

  • Louis Kang

Army Research Office (W911NF-13-1-0390)

  • Michael R DeWeese

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

Reviewing Editor

  1. Sachin Deshmukh, Indian Institute of Science Bangalore, India

Publication history

  1. Received: March 1, 2019
  2. Accepted: November 15, 2019
  3. Accepted Manuscript published: November 18, 2019 (version 1)
  4. Version of Record published: December 9, 2019 (version 2)

Copyright

© 2019, Kang & DeWeese

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. Louis Kang
  2. Michael R DeWeese
(2019)
Replay as wavefronts and theta sequences as bump oscillations in a grid cell attractor network
eLife 8:e46351.
https://doi.org/10.7554/eLife.46351
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