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.

Reviewing Editor

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

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)

Version 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.

Metrics

  • 1,368
    views
  • 187
    downloads
  • 24
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. 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

Share this article

https://doi.org/10.7554/eLife.36769

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.