Adult-born granule cells improve stimulus encoding and discrimination in the dentate gyrus

  1. Diego M Arribas
  2. Antonia Marin-Burgin  Is a corresponding author
  3. Luis G Morelli  Is a corresponding author
  1. Instituto de Investigación en Biomedicina de Buenos Aires - CONICET - Partner Institute of the Max Planck Society, Argentina

Abstract

Heterogeneity plays an important role in diversifying neural responses to support brain function. Adult neurogenesis provides the dentate gyrus with a heterogeneous population of granule cells (GCs) that were born and developed their properties at different times. Immature GCs have distinct intrinsic and synaptic properties than mature GCs and are needed for correct encoding and discrimination in spatial tasks. How immature GCs enhance the encoding of information to support these functions is not well understood. Here, we record the responses to fluctuating current injections of GCs of different ages in mouse hippocampal slices to study how they encode stimuli. Immature GCs produce unreliable responses compared to mature GCs, exhibiting imprecise spike timings across repeated stimulation. We use a statistical model to describe the stimulus-response transformation performed by GCs of different ages. We fit this model to the data and obtain parameters that capture GCs encoding properties. Parameter values from this fit re ect the maturational differences of the population and indicate that immature GCs perform a differential encoding of stimuli. To study how this age heterogeneity influences encoding by a population, we perform stimulus decoding using populations that contain GCs of different ages. We find that, despite their individual unreliability, immature GCs enhance the fidelity of the signal encoded by the population and improve the discrimination of similar time dependent stimuli. Thus, the observed heterogeneity confers the population with enhanced encoding capabilities.

Data availability

The data generated in this study is publicly available at Dryad,doi:10.5061/dryad.73n5tb309. Custom code produced and used in the study is available at Github, https://github.com/diegoarri91/iclamp-glm.

The following data sets were generated

Article and author information

Author details

  1. Diego M Arribas

    Instituto de Investigación en Biomedicina de Buenos Aires - CONICET - Partner Institute of the Max Planck Society, Buenos Aires, Argentina
    Competing interests
    The authors declare that no competing interests exist.
  2. Antonia Marin-Burgin

    Instituto de Investigación en Biomedicina de Buenos Aires - CONICET - Partner Institute of the Max Planck Society, Buenos Aires, Argentina
    For correspondence
    aburgin@ibioba-mpsp-conicet.gov.ar
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0684-9796
  3. Luis G Morelli

    Instituto de Investigación en Biomedicina de Buenos Aires - CONICET - Partner Institute of the Max Planck Society, Buenos Aires, Argentina
    For correspondence
    lmorelli@ibioba-mpsp-conicet.gov.ar
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5614-073X

Funding

Agencia Nacional de Promoción Científica y Tecnológica (PICT 2015 0634)

  • Antonia Marin-Burgin

Agencia Nacional de Promoción Científica y Tecnológica (PICT 2018 0880)

  • Antonia Marin-Burgin

Agencia Nacional de Promoción Científica y Tecnológica (PICT 2017 3753)

  • Luis G Morelli

Agencia Nacional de Promoción Científica y Tecnológica (PICT 2019 0445)

  • Luis G Morelli

International Development Research Centre (IDRC108878)

  • Antonia Marin-Burgin

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Open access funding provided by Max Planck Society.

Reviewing Editor

  1. Timothy E Behrens, University of Oxford, United Kingdom

Ethics

Animal experimentation: Experimental protocol (2020-03-NE) was evaluated by the Institutional Animal Care and Use Committee of the IBioBA-CONICET according to the Principles for Biomedical Research involving animals of the Council for International Organizations for Medical Sciences and provisions stated in the Guide for the Care and Use of Laboratory Animals.

Version history

  1. Preprint posted: May 13, 2022 (view preprint)
  2. Received: May 13, 2022
  3. Accepted: August 15, 2023
  4. Accepted Manuscript published: August 16, 2023 (version 1)
  5. Version of Record published: September 4, 2023 (version 2)

Copyright

© 2023, Arribas 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. Diego M Arribas
  2. Antonia Marin-Burgin
  3. Luis G Morelli
(2023)
Adult-born granule cells improve stimulus encoding and discrimination in the dentate gyrus
eLife 12:e80250.
https://doi.org/10.7554/eLife.80250

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https://doi.org/10.7554/eLife.80250

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