A theory of joint attractor dynamics in the hippocampus and the entorhinal cortex accounts for artificial remapping and grid cell field-to-field variability

  1. Haggai Agmon
  2. Yoram Burak  Is a corresponding author
  1. Hebrew University of Jerusalem, Israel

Abstract

The representation of position in the mammalian brain is distributed across multiple neural populations. Grid cell modules in the medial entorhinal cortex (MEC) express activity patterns that span a low-dimensional manifold which remains stable across different environments. In contrast, the activity patterns of hippocampal place cells span distinct low-dimensional manifolds in different environments. It is unknown how these multiple representations of position are coordinated. Here we develop a theory of joint attractor dynamics in the hippocampus and the MEC. We show that the system exhibits a coordinated, joint representation of position across multiple environments, consistent with global remapping in place cells and grid cells. In addition, our model accounts for recent experimental observations that lack a mechanistic explanation: variability in the firing rate of single grid cells across firing fields, and artificial remapping of place cells under depolarization, but not under hyperpolarization, of layer II stellate cells of the MEC.

Data availability

This is a theoretical manuscript which does not contain data of our own. The rat trajectory used in Figure 4 to generate a distribution of velocities is taken from Fig.2c in (Hafting et al., 2005). It is available online at https://doi.org/10.11582/2014.00001.

The following previously published data sets were used
    1. Torkel Hafting
    (2014) Grid cell data Hafting et al 2005
    NIRD Research Data Archive, doi:10.11582/2014.00001.

Article and author information

Author details

  1. Haggai Agmon

    Edmond and Lily Safra Center for Brain Sciences, Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  2. Yoram Burak

    Racah Institute of Physics, Edmond and Lily Safra Center for Brain Sciences, Hebrew University of Jerusalem, Jerusalem, Israel
    For correspondence
    yoram.burak@elsc.huji.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1198-8782

Funding

Israel Science Foundation (1745/18 and 1978/13)

  • Haggai Agmon
  • Yoram Burak

German-Israeli Foundation for Scientific Research and Development (I-1477-421.13/2018)

  • Haggai Agmon
  • Yoram Burak

Gatsby Charitable Foundation (Gatsby Program in Theoretical Neuroscience at the Hebrew University)

  • Haggai Agmon
  • Yoram Burak

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

Reviewing Editor

  1. Rishidev Chaudhuri, UC Davis, United States

Publication history

  1. Received: March 13, 2020
  2. Accepted: August 7, 2020
  3. Accepted Manuscript published: August 11, 2020 (version 1)
  4. Version of Record published: August 25, 2020 (version 2)
  5. Version of Record updated: September 2, 2020 (version 3)

Copyright

© 2020, Agmon & Burak

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. Haggai Agmon
  2. Yoram Burak
(2020)
A theory of joint attractor dynamics in the hippocampus and the entorhinal cortex accounts for artificial remapping and grid cell field-to-field variability
eLife 9:e56894.
https://doi.org/10.7554/eLife.56894

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