1. Neuroscience

Spatiotemporally precise optogenetic activation of sensory neurons in freely walking Drosophila

  1. Brian D DeAngelis
  2. Jacob A Zavatone-Veth
  3. Aneysis D Gonzalez-Suarez
  4. Damon A Clark  Is a corresponding author
  1. Yale University, United States
  2. Harvard University, United States
https://doi.org/10.7554/eLife.54183
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  1. Brian D DeAngelis
  2. Jacob A Zavatone-Veth
  3. Aneysis D Gonzalez-Suarez
  4. Damon A Clark
(2020)
Spatiotemporally precise optogenetic activation of sensory neurons in freely walking Drosophila
eLife 9:e54183.
https://doi.org/10.7554/eLife.54183
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Abstract

Previous work has characterized how walking Drosophila coordinate the movements of individual limbs (DeAngelis, Zavatone-Veth, and Clark, 2019). To understand the circuit basis of this coordination, one must characterize how sensory feedback from each limb affects walking behavior. However, it has remained difficult to manipulate neural activity in individual limbs of freely moving animals. Here, we demonstrate a simple method for optogenetic stimulation with body side-, body segment-, and limb-specificity that does not require real-time tracking. Instead, we activate at random, precise locations in time and space and use post hoc analysis to determine behavioral responses to specific activations. Using this method, we have characterized limb coordination and walking behavior in response to transient activation of mechanosensitive bristle neurons and sweet-sensing chemoreceptor neurons. Our findings reveal that activating these neurons has opposite effects on turning, and that activations in different limbs and body regions produce distinct behaviors.

Data availability

Source data were deposited on Dryad: https://doi.org/10.5061/dryad.nzs7h44nk.Analysis code is available here: https://github.com/ClarkLabCode/FlyLimbOptoCode.

The following data sets were generated

Article and author information

Author details

  1. Brian D DeAngelis

    Interdepartmental Neuroscience Program, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9418-7619

  2. Jacob A Zavatone-Veth

    Department of Physics, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4060-1738

  3. Aneysis D Gonzalez-Suarez

    Interdepartmental Neuroscience Program, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Damon A Clark

    Department of Molecular, Cellular, Developmental Biology, Yale University, New Haven, United States
    For correspondence
    damon.clark@yale.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8487-700X

Funding

National Institutes of Health (EY026555)

  • Brian D DeAngelis
  • Damon A Clark

National Institutes of Health (EY026878)

  • Brian D DeAngelis
  • Damon A Clark

Chicago Community Trust (Searle Scholar Award)

  • Damon A Clark

Alfred P. Sloan Foundation (Fellowship)

  • Damon A Clark

National Science Foundation (GRF)

  • Brian D DeAngelis

Smith Family Foundation (Scholar Award)

  • Brian D DeAngelis
  • Damon A Clark

National Science Foundation (IOS 1558103)

  • Jacob A Zavatone-Veth
  • Damon A Clark

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

Copyright

© 2020, DeAngelis 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. Brian D DeAngelis
  2. Jacob A Zavatone-Veth
  3. Aneysis D Gonzalez-Suarez
  4. Damon A Clark
(2020)
Spatiotemporally precise optogenetic activation of sensory neurons in freely walking Drosophila
eLife 9:e54183.
https://doi.org/10.7554/eLife.54183

Share this article

https://doi.org/10.7554/eLife.54183

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Further reading

    1. Neuroscience

    The manifold structure of limb coordination in walking Drosophila

    Brian D DeAngelis, Jacob A Zavatone-Veth, Damon A Clark
    Research Article

    Terrestrial locomotion requires animals to coordinate their limb movements to efficiently traverse their environment. While previous studies in hexapods have reported that limb coordination patterns can vary substantially, the structure of this variability is not yet well understood. Here, we characterized the symmetric and asymmetric components of variation in walking kinematics in the genetic model organism Drosophila. We found that Drosophila use a single continuum of coordination patterns without evidence for preferred configurations. Spontaneous symmetric variability was associated with modulation of a single control parameter—stance duration—while asymmetric variability consisted of small, limb-specific modulations along multiple dimensions of the underlying symmetric pattern. Commands that modulated walking speed, originating from artificial neural activation or from the visual system, evoked modulations consistent with spontaneous behavior. Our findings suggest that Drosophila employ a low-dimensional control architecture, which provides a framework for understanding the neural circuits that regulate hexapod legged locomotion.