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

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.

Metrics

  • 3,340
    views
  • 387
    downloads
  • 9
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. 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

Further reading

    1. Developmental Biology
    2. Neuroscience
    Ev L Nichols, Joo Lee, Kang Shen
    Research Article

    During development axons undergo long-distance migrations as instructed by guidance molecules and their receptors, such as UNC-6/Netrin and UNC-40/DCC. Guidance cues act through long-range diffusive gradients (chemotaxis) or local adhesion (haptotaxis). However, how these discrete modes of action guide axons in vivo is poorly understood. Using time-lapse imaging of axon guidance in C. elegans, we demonstrate that UNC-6 and UNC-40 are required for local adhesion to an intermediate target and subsequent directional growth. Exogenous membrane-tethered UNC-6 is sufficient to mediate adhesion but not directional growth, demonstrating the separability of haptotaxis and chemotaxis. This conclusion is further supported by the endogenous UNC-6 distribution along the axon’s route. The intermediate and final targets are enriched in UNC-6 and separated by a ventrodorsal UNC-6 gradient. Continuous growth through the gradient requires UNC-40, which recruits UNC-6 to the growth cone tip. Overall, these data suggest that UNC-6 stimulates stepwise haptotaxis and chemotaxis in vivo.

    1. Neuroscience
    Sainan Liu, Jiepin Huang ... Yan Yang
    Research Article

    Social relationships guide individual behavior and ultimately shape the fabric of society. Primates exhibit particularly complex, differentiated, and multidimensional social relationships, which form interwoven social networks, reflecting both individual social tendencies and specific dyadic interactions. How the patterns of behavior that underlie these social relationships emerge from moment-to-moment patterns of social information processing remains unclear. Here, we assess social relationships among a group of four monkeys, focusing on aggression, grooming, and proximity. We show that individual differences in social attention vary with individual differences in patterns of general social tendencies and patterns of individual engagement with specific partners. Oxytocin administration altered social attention and its relationship to both social tendencies and dyadic relationships, particularly grooming and aggression. Our findings link the dynamics of visual information sampling to the dynamics of primate social networks.