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.

Metrics

  • 2,399
    Page views
  • 359
    Downloads
  • 7
    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. 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

Further reading

    1. Computational and Systems Biology
    2. Medicine
    Riku Klén et al.
    Research Article

    New SARS-CoV-2 variants, breakthrough infections, waning immunity, and sub-optimal vaccination rates account for surges of hospitalizations and deaths. There is an urgent need for clinically valuable and generalizable triage tools assisting the allocation of hospital resources, particularly in resource-limited countries. We developed and validate CODOP, a machine learning-based tool for predicting the clinical outcome of hospitalized COVID-19 patients. CODOP was trained, tested and validated with six cohorts encompassing 29223 COVID-19 patients from more than 150 hospitals in Spain, the USA and Latin America during 2020-22. CODOP uses 12 clinical parameters commonly measured at hospital admission for reaching high discriminative ability up to nine days before clinical resolution (AUROC: 0·90-0·96), it is well calibrated, and it enables an effective dynamic risk stratification during hospitalization. Furthermore, CODOP maintains its predictive ability independently of the virus variant and the vaccination status. To reckon with the fluctuating pressure levels in hospitals during the pandemic, we offer two online CODOP calculators, suited for undertriage or overtriage scenarios, validated with a cohort of patients from 42 hospitals in three Latin American countries (78-100% sensitivity and 89-97% specificity). The performance of CODOP in heterogeneous and geographically disperse patient cohorts and the easiness of use strongly suggest its clinical utility, particularly in resource-limited countries.

    1. Cancer Biology
    2. Computational and Systems Biology
    Gökçe Senger et al.
    Research Article

    Aneuploidy, a state of chromosome imbalance, is a hallmark of human tumors, but its role in cancer still remains to be fully elucidated. To understand the consequences of whole-chromosome-level aneuploidies on the proteome, we integrated aneuploidy, transcriptomic and proteomic data from hundreds of TCGA/CPTAC tumor samples. We found a surprisingly large number of expression changes happened on other, non-aneuploid chromosomes. Moreover, we identified an association between those changes and co-complex members of proteins from aneuploid chromosomes. This co-abundance association is tightly regulated for aggregation-prone aneuploid proteins and those involved in a smaller number of complexes. On the other hand, we observe that complexes of the cellular core machinery are under functional selection to maintain their stoichiometric balance in aneuploid tumors. Ultimately, we provide evidence that those compensatory and functional maintenance mechanisms are established through post-translational control and that the degree of success of a tumor to deal with aneuploidy-induced stoichiometric imbalance impacts the activation of cellular protein degradation programs and patient survival.