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Reverse-correlation analysis of navigation dynamics in Drosophila larva using optogenetics

  1. Luis Hernandez-Nunez
  2. Jonas Belina
  3. Mason Klein
  4. Guangwei Si
  5. Lindsey Claus
  6. John R Carlson
  7. Aravinthan D T Samuel  Is a corresponding author
  1. Harvard University, United States
  2. Yale University, United States
Research Article
  • Cited 42
  • Views 3,136
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Cite this article as: eLife 2015;4:e06225 doi: 10.7554/eLife.06225

Abstract

Neural circuits for behavior transform sensory inputs into motor outputs in patterns with strategic value. Determining how neurons along a sensorimotor circuit contribute to this transformation is central to understanding behavior. To do this, a quantitative framework to describe behavioral dynamics is needed. Here, we built a high-throughput optogenetic system for Drosophila larva to quantify the sensorimotor transformations underlying navigational behavior. We express CsChrimson, a red-shifted variant of Channelrhodopsin, in specific chemosensory neurons, and expose large numbers of freely moving animals to random optogenetic activation patterns. We quantify their behavioral responses and use reverse correlation analysis to uncover the linear and static nonlinear components of navigation dynamics as functions of optogenetic activation patterns of specific sensory neurons. We find that linear-nonlinear (LN) models accurately predict navigational decision-making for different optogenetic activation waveforms. We use our method to establish the valence and dynamics of navigation driven by optogenetic activation of different combinations of bitter sensing gustatory neurons. Our method captures the dynamics of optogenetically-induced behavior in compact, quantitative transformations that can be used to characterize circuits for sensorimotor processing and their contribution to navigational decision making.

Article and author information

Author details

  1. Luis Hernandez-Nunez

    Center for Systems Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jonas Belina

    Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Mason Klein

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Guangwei Si

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Lindsey Claus

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. John R Carlson

    Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Aravinthan D T Samuel

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    For correspondence
    samuel@physics.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Publication history

  1. Received: December 22, 2014
  2. Accepted: May 1, 2015
  3. Accepted Manuscript published: May 5, 2015 (version 1)
  4. Version of Record published: June 16, 2015 (version 2)

Copyright

© 2015, Hernandez-Nunez 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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