Experience, circuit dynamics and forebrain recruitment in larval zebrafish prey capture

  1. Claire S Oldfield
  2. Irene Grossrubatscher
  3. Mario Chávez
  4. Adam Hoagland
  5. Alex R Huth
  6. Elizabeth C Carroll
  7. Andrew Prendergast
  8. Tony Qu
  9. Jack L Gallant
  10. Claire Wyart  Is a corresponding author
  11. Ehud Y Isacoff  Is a corresponding author
  1. University of California, Berkeley, United States
  2. CNRS-UMR-7225, France
  3. Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, France
  4. Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, France

Abstract

Experience strongly influences behavior, but little is known about how experience is encoded in the brain, and how changes in neural activity are implemented at a network level to improve performance. Here we investigate how differences in experience impact brain circuitry and behavior in larval zebrafish prey capture. We find that experience of live prey compared to inert food increases capture success by boosting capture initiation. To explore the underlying neural basis, we studied the effects of prior experience of live prey on behavior and brain activity. In response to live prey, animals with and without prior experience of live prey all show activity in visual areas (pretectum and optic tectum) and motor areas (cerebellum and hindbrain), with similar visual area retinotopic maps of prey position. However, prey-experienced animals more readily initiate capture in response to visual area activity and also have greater visually-evoked activity in two forebrain areas: the telencephalon and the habenula. Consistent with the contribution of the forebrain to prey capture, disruption of neurons in the habenula reduced prey capture performance in prey-experienced fish. Together, our results suggest that experience of prey strengthens prey-associated visual drive to the forebrain, and that this lowers the threshold for prey-associated visual activity to trigger activity in motor areas, thereby improving capture performance.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures.

Article and author information

Author details

  1. Claire S Oldfield

    MCB, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  2. Irene Grossrubatscher

    MCB, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  3. Mario Chávez

    CNRS-UMR-7225, Paris, France
    Competing interests
    No competing interests declared.
  4. Adam Hoagland

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  5. Alex R Huth

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  6. Elizabeth C Carroll

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  7. Andrew Prendergast

    Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    Competing interests
    No competing interests declared.
  8. Tony Qu

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  9. Jack L Gallant

    Programs in Neuroscience, Bioengineering, Biophysics & Vision Science, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7273-1054
  10. Claire Wyart

    Neurophysiology & Systems neuroscience, Institut du Cerveau et la Moelle épinière, Hôpital Pitié-Salpêtrière, Sorbonne Universités, UPMC Univ Paris 06, Inserm, CNRS, Paris, France
    For correspondence
    claire.wyart@icm-institute.org
    Competing interests
    Claire Wyart, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1668-4975
  11. Ehud Y Isacoff

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    ehud@berkeley.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4775-9359

Funding

Defense Advanced Research Projects Agency (N66001-17-C-4015)

  • Ehud Y Isacoff

National Institutes of Health (2PN2EY018241)

  • Ehud Y Isacoff

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

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (ACUC) of the University of California, Berkeley.protocol ID: UP-2015-06-7705-1, last approval date 11/20/2019).

Reviewing Editor

  1. Yuichi Iino, University of Tokyo, Japan

Publication history

  1. Received: March 4, 2020
  2. Accepted: September 26, 2020
  3. Accepted Manuscript published: September 28, 2020 (version 1)
  4. Version of Record published: October 15, 2020 (version 2)
  5. Version of Record updated: October 20, 2020 (version 3)

Copyright

© 2020, Oldfield 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. Claire S Oldfield
  2. Irene Grossrubatscher
  3. Mario Chávez
  4. Adam Hoagland
  5. Alex R Huth
  6. Elizabeth C Carroll
  7. Andrew Prendergast
  8. Tony Qu
  9. Jack L Gallant
  10. Claire Wyart
  11. Ehud Y Isacoff
(2020)
Experience, circuit dynamics and forebrain recruitment in larval zebrafish prey capture
eLife 9:e56619.
https://doi.org/10.7554/eLife.56619
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