A time-stamp mechanism may provide temporal information necessary for egocentric to allocentric spatial transformations

Abstract

Learning the spatial organization of the environment is essential for most animals' survival. This requires the animal to derive allocentric spatial information from egocentric sensory and motor experience. The neural mechanisms underlying this transformation are mostly unknown. We addressed this problem in electric fish, which can precisely navigate in complete darkness and whose brain circuitry is relatively simple. We conducted the first neural recordings in the preglomerular complex, the thalamic region exclusively connecting the optic tectum with the spatial learning circuits in the dorsolateral pallium. While tectal topographic information was mostly eliminated in preglomerular neurons, the time-intervals between object encounters were precisely encoded. We show that this reliable temporal information, combined with a speed signal, can permit accurate estimation of the distance between encounters, a necessary component of path-integration that enables computing allocentric spatial relations. Our results suggest that similar mechanisms are involved in sequential spatial learning in all vertebrates.

Data availability

Datasets and analysis files have been deposited in Columbia University's Academic Commons repository (https://doi.org/10.7916/D86Q3F7S).

The following data sets were generated

Article and author information

Author details

  1. Avner Wallach

    Department of Physics, University of Ottawa, Ottawa, Canada
    For correspondence
    aw3057@columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2345-2942
  2. Erik Harvey-Girard

    Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. James Jaeyoon Jun

    Department of Physics, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. André Longtin

    Department of Physics, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Len Maler

    Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7666-2754

Funding

Natural Sciences and Engineering Research Council of Canada (121891-2009)

  • André Longtin

Canadian Institutes of Health Research (49510)

  • André Longtin
  • Len Maler

Natural Sciences and Engineering Research Council of Canada (147489-2017)

  • Len Maler

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

Ethics

Animal experimentation: All procedures were approved by the University of Ottawa Animal Care and follow guidelines established by the Society for Neuroscience (approved protocol number:CMM-2897)

Reviewing Editor

  1. Catherine Emily Carr, University of Maryland, United States

Publication history

  1. Received: March 18, 2018
  2. Accepted: November 12, 2018
  3. Accepted Manuscript published: November 22, 2018 (version 1)
  4. Version of Record published: November 29, 2018 (version 2)

Copyright

© 2018, Wallach 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. Avner Wallach
  2. Erik Harvey-Girard
  3. James Jaeyoon Jun
  4. André Longtin
  5. Len Maler
(2018)
A time-stamp mechanism may provide temporal information necessary for egocentric to allocentric spatial transformations
eLife 7:e36769.
https://doi.org/10.7554/eLife.36769

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