Brain-wide mapping of neural activity controlling zebrafish exploratory locomotion

  1. Timothy W Dunn
  2. Yu Mu
  3. Sujatha Narayan
  4. Owen Randlett
  5. Eva A Naumann
  6. Chao-Tsung Yang
  7. Alexander F Schier
  8. Jeremy Freeman
  9. Florian Engert
  10. Misha B Ahrens  Is a corresponding author
  1. Harvard University, United States
  2. Janelia Research Campus, Howard Hughes Medical Institute, United States

Abstract

In the absence of salient sensory cues to guide behavior, animals must still execute sequences of motor actions in order to forage and explore. How such successive motor actions are coordinated to form global locomotion trajectories is unknown. We mapped the structure of larval zebrafish swim trajectories in homogeneous environments and found that trajectories were characterized by alternating sequences of repeated turns to the left and to the right. Using whole-brain light-sheet imaging, we identified activity relating to the behavior in specific neural populations that we termed the anterior rhombencephalic turning region (ARTR). ARTR perturbations biased swim direction and reduced the dependence of turn direction on turn history, indicating that the ARTR is part of a network generating the temporal correlations in turn direction. We also find suggestive evidence for ARTR mutual inhibition and ARTR projections to premotor neurons. Finally, simulations suggest the observed turn sequences may underlie efficient exploration of local environments.

Article and author information

Author details

  1. Timothy W Dunn

    Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Yu Mu

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Sujatha Narayan

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Owen Randlett

    Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Eva A Naumann

    Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Chao-Tsung Yang

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Alexander F Schier

    Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Jeremy Freeman

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Florian Engert

    Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Misha B Ahrens

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    ahrensm@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: All experiments presented in this study were conducted in accordance with the animal research guidelines from the National Institutes of Health and were approved by the Institutional Animal Care and Use Committee (#13-98) and Institutional Biosafety Committee of Janelia Research Campus.

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Version history

  1. Received: November 3, 2015
  2. Accepted: March 9, 2016
  3. Accepted Manuscript published: March 22, 2016 (version 1)
  4. Version of Record published: April 19, 2016 (version 2)

Copyright

© 2016, Dunn 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. Timothy W Dunn
  2. Yu Mu
  3. Sujatha Narayan
  4. Owen Randlett
  5. Eva A Naumann
  6. Chao-Tsung Yang
  7. Alexander F Schier
  8. Jeremy Freeman
  9. Florian Engert
  10. Misha B Ahrens
(2016)
Brain-wide mapping of neural activity controlling zebrafish exploratory locomotion
eLife 5:e12741.
https://doi.org/10.7554/eLife.12741

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https://doi.org/10.7554/eLife.12741

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