Global change in brain state during spontaneous and forced walk in Drosophila is composed of combined activity patterns of different neuron classes

  1. Sophie Aimon  Is a corresponding author
  2. Karen Y Cheng
  3. Julijana Gjorgjieva
  4. Ilona C Grunwald Kadow  Is a corresponding author
  1. Max Planck Institute for Biological Cybernetics, Germany
  2. University of Bonn, Germany
  3. Technical University of Munich, Germany

Abstract

Movement-correlated brain activity has been found across species and brain regions. Here, we used fast whole-brain lightfield imaging in adult Drosophila to investigate the relationship between walk and brain-wide neuronal activity. We observed a global change in activity that tightly correlated with spontaneous bouts of walk. While imaging specific sets of excitatory, inhibitory, and neuromodulatory neurons highlighted their joint contribution, spatial heterogeneity in walk- and turning-induced activity allowed parsing unique responses from subregions and sometimes individual candidate neurons. For example, previously uncharacterized serotonergic neurons were inhibited during walk. While activity onset in some areas preceded walk onset exclusively in spontaneously walking animals, spontaneous and forced walk elicited similar activity in most brain regions. These data suggest a major contribution of walk and walk-related sensory or proprioceptive information to global activity of all major neuronal classes.

Data availability

Time series of regional data are available on Dryad https://doi.org/10.5061/dryad.3bk3j9kpb, and small datasets of processed data used for generating figures are on github: https://github.com/sophie63/Aimon2022. Code to analyze the data is available on https://github.com/sophie63/Aimon2022 and https://github.com/sophie63/FlyLFM.Original data is very large (several tens of TB) and is available upon request to Ilona.grunwald@uni-bonn.de.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Sophie Aimon

    Kavli Institute for Brain and Mind, Max Planck Institute for Biological Cybernetics, tuebingen, Germany
    For correspondence
    aimon.sophie@gmail.com
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0990-0342
  2. Karen Y Cheng

    Institute of Physiology II, University of Bonn, Bonn, Germany
    Competing interests
    No competing interests declared.
  3. Julijana Gjorgjieva

    School of Life Sciences, Technical University of Munich, Freising, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7118-4079
  4. Ilona C Grunwald Kadow

    Institute of Physiology II, University of Bonn, Bonn, Germany
    For correspondence
    ilona.grunwald@ukbonn.de
    Competing interests
    Ilona C Grunwald Kadow, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9085-4274

Funding

European Research Council (ERCStG FlyContext)

  • Ilona C Grunwald Kadow

European Research Council (ERCStG NeuroDevo)

  • Julijana Gjorgjieva

Simons Foundation (Aimon - 414701)

  • Sophie Aimon

iiBehave network grant by the Ministry of Culture and Science of the State of North Rhine-Westphalia

  • Ilona C Grunwald Kadow

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

Reviewing Editor

  1. Damon A Clark, Yale University, United States

Version history

  1. Preprint posted: January 20, 2022 (view preprint)
  2. Received: November 27, 2022
  3. Accepted: April 13, 2023
  4. Accepted Manuscript published: April 17, 2023 (version 1)
  5. Version of Record published: May 9, 2023 (version 2)

Copyright

© 2023, Aimon 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. Sophie Aimon
  2. Karen Y Cheng
  3. Julijana Gjorgjieva
  4. Ilona C Grunwald Kadow
(2023)
Global change in brain state during spontaneous and forced walk in Drosophila is composed of combined activity patterns of different neuron classes
eLife 12:e85202.
https://doi.org/10.7554/eLife.85202

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https://doi.org/10.7554/eLife.85202

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