Velocity coupling of grid modules enables stable embedding of a low dimensional variable in a high dimensional attractor

  1. Noga Mosheiff
  2. Yoram Burak  Is a corresponding author
  1. Hebrew University, Israel

Abstract

Grid cells in the medial entorhinal cortex (MEC) encode position using a distributed representation across multiple neural populations (modules), each possessing a distinct spatial scale. The modular structure of the representation confers the grid cell neural code with large capacity. Yet, the modularity poses significant challenges for the neural circuitry that maintains the representation, and updates it based on self motion. Small incompatible drifts in different modules, driven by noise, can rapidly lead to large, abrupt shifts in the represented position, resulting in catastrophic readout errors. Here we propose a theoretical model of coupled modules. The coupling suppresses incompatible drifts, allowing for a stable embedding of a two dimensional variable (position) in a higher dimensional neural attractor, while preserving the large capacity. We propose that coupling of this type may be implemented by recurrent synaptic connectivity within the mEC with a relatively simple and biologically plausible structure.

Data availability

This is a theoretical work. There are no data sets associated with it.

Article and author information

Author details

  1. Noga Mosheiff

    Racah Institute of Physics, Hebrew University, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3649-4183
  2. Yoram Burak

    Racah Institute of Physics, Hebrew University, 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)

  • Yoram Burak

Israel Science Foundation (1978/13)

  • Yoram Burak

Gatsby Charitable Foundation

  • Yoram Burak

Dalia and Dan Maydan Fellowship

  • Noga Mosheiff

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

Reviewing Editor

  1. Stephanie Palmer, University of Chicago, United States

Publication history

  1. Received: May 15, 2019
  2. Accepted: August 29, 2019
  3. Accepted Manuscript published: August 30, 2019 (version 1)
  4. Version of Record published: September 23, 2019 (version 2)

Copyright

© 2019, Mosheiff & 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.

Metrics

  • 1,491
    Page views
  • 268
    Downloads
  • 9
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Noga Mosheiff
  2. Yoram Burak
(2019)
Velocity coupling of grid modules enables stable embedding of a low dimensional variable in a high dimensional attractor
eLife 8:e48494.
https://doi.org/10.7554/eLife.48494

Further reading

    1. Neuroscience
    Rong Zhao, Stacy D Grunke ... Joanna L Jankowsky
    Research Article

    Neurodegenerative diseases are characterized by selective vulnerability of distinct cell populations; however, the cause for this specificity remains elusive. Here we show that entorhinal cortex layer 2 (EC2) neurons are unusually vulnerable to prolonged neuronal inactivity compared with neighboring regions of the temporal lobe, and that reelin+ stellate cells connecting EC with the hippocampus are preferentially susceptible within the EC2 population. We demonstrate that neuronal death after silencing can be elicited through multiple independent means of activity inhibition, and that preventing synaptic release, either alone or in combination with electrical shunting, is sufficient to elicit silencing-induced degeneration. Finally, we discovered that degeneration following synaptic silencing is governed by competition between active and inactive cells, which is a circuit refinement process traditionally thought to end early in postnatal life. Our data suggests that the developmental window for wholesale circuit plasticity may extend into adulthood for specific brain regions. We speculate that this sustained potential for remodeling by entorhinal neurons may support lifelong memory but renders them vulnerable to prolonged activity changes in disease.

    1. Neuroscience
    Nace Mikus, Sebastian Korb ... Christoph Mathys
    Research Article

    Human behaviour requires flexible arbitration between actions we do out of habit and actions that are directed towards a specific goal. Drugs that target opioid and dopamine receptors are notorious for inducing maladaptive habitual drug consumption; yet, how the opioidergic and dopaminergic neurotransmitter systems contribute to the arbitration between habitual and goal-directed behaviour is poorly understood. By combining pharmacological challenges with a well-established decision-making task and a novel computational model, we show that the administration of the dopamine D2/3 receptor antagonist amisulpride led to an increase in goal-directed or ‘model-based’ relative to habitual or ‘model-free’ behaviour, whereas the non-selective opioid receptor antagonist naltrexone had no appreciable effect. The effect of amisulpride on model-based/model-free behaviour did not scale with drug serum levels in the blood. Furthermore, participants with higher amisulpride serum levels showed higher explorative behaviour. These findings highlight the distinct functional contributions of dopamine and opioid receptors to goal-directed and habitual behaviour and support the notion that even small doses of amisulpride promote flexible application of cognitive control.