From behavior to circuit modeling of light-seeking navigation in zebrafish larvae

  1. Sophia Karpenko
  2. Sebastien Wolf
  3. Julie Lafaye
  4. Guillaume Le Goc
  5. Thomas Panier
  6. Volker Bormuth
  7. Raphaël Candelier
  8. Georges Debrégeas  Is a corresponding author
  1. Laboratoire Jean Perrin, France
  2. Laboratoire de Physique de l'Ecole Normale Supérieure, France

Abstract

Bridging brain-scale circuit dynamics and organism-scale behavior is a central challenge in neuroscience. It requires the concurrent development of minimal behavioral and neural circuit models that can quantitatively capture basic sensorimotor operations. Here we focus on light-seeking navigation in zebrafish larvae. Using a virtual reality assay, we first characterize how motor and visual stimulation sequences govern the selection of discrete swim-bout events that subserve the fish navigation in the presence of a distant light source. These mechanisms are combined into a comprehensive Markov-chain model of navigation that quantitatively predict the stationary distribution of the fish's body orientation under any given illumination profile. We then map this behavioral description onto a neuronal model of the ARTR, a small neural circuit involved in the orientation-selection of swim bouts. We demonstrate that this visually-biased decision-making circuit can similarly capture the statistics of both spontaneous and contrast-driven navigation.

Data availability

Data and analysis codes are available at Dryad Digital: Data DOI: doi:10.5061/dryad.v9s4mw6qx

The following data sets were generated

Article and author information

Author details

  1. Sophia Karpenko

    IBPS, CNRS, Sorbonne Université, Laboratoire Jean Perrin, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Sebastien Wolf

    PSL, ENS, CNRS, IBENS, INSERM, Laboratoire de Physique de l'Ecole Normale Supérieure, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Julie Lafaye

    IBPS, CNRS, Sorbonne Université, Laboratoire Jean Perrin, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Guillaume Le Goc

    IBPS, CNRS, Sorbonne Université, Laboratoire Jean Perrin, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Thomas Panier

    IBPS, CNRS, Sorbonne Université, Laboratoire Jean Perrin, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Volker Bormuth

    IBPS, CNRS, Sorbonne Université, Laboratoire Jean Perrin, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Raphaël Candelier

    IBPS, CNRS, Sorbonne Université, Laboratoire Jean Perrin, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1523-6249
  8. Georges Debrégeas

    IBPS, CNRS, Sorbonne Université, Laboratoire Jean Perrin, Paris, France
    For correspondence
    georges.debregeas@upmc.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3698-4497

Funding

Human Frontier Science Program (RGP0060/2017)

  • Georges Debrégeas

H2020 European Research Council (71598)

  • Volker Bormuth

Agence Nationale de la Recherche (ANR-16-CE16-0017)

  • Raphaël Candelier
  • Georges Debrégeas

Fondation pour la Recherche Médicale (FDT201904008219)

  • Sophia Karpenko

ATIP-Avenir program

  • Volker Bormuth

Fondation pour la Recherche Médicale (SPF201809007064)

  • Sebastien Wolf

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 experiments were approved by Le Comité d'Éthique pour l'Expérimentation Animale Charles Darwin C2EA-05 (02601.01).

Reviewing Editor

  1. Gordon J Berman, Emory University, United States

Publication history

  1. Received: October 19, 2019
  2. Accepted: January 2, 2020
  3. Accepted Manuscript published: January 2, 2020 (version 1)
  4. Version of Record published: January 29, 2020 (version 2)

Copyright

© 2020, Karpenko 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. Sophia Karpenko
  2. Sebastien Wolf
  3. Julie Lafaye
  4. Guillaume Le Goc
  5. Thomas Panier
  6. Volker Bormuth
  7. Raphaël Candelier
  8. Georges Debrégeas
(2020)
From behavior to circuit modeling of light-seeking navigation in zebrafish larvae
eLife 9:e52882.
https://doi.org/10.7554/eLife.52882

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