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.

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.

Metrics

  • 2,584
    views
  • 290
    downloads
  • 20
    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. 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

Share this article

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

Further reading

    1. Neuroscience
    Agnieszka Glica, Katarzyna Wasilewska ... Katarzyna Jednoróg
    Research Article

    The neural noise hypothesis of dyslexia posits an imbalance between excitatory and inhibitory (E/I) brain activity as an underlying mechanism of reading difficulties. This study provides the first direct test of this hypothesis using both electroencephalography (EEG) power spectrum measures in 120 Polish adolescents and young adults (60 with dyslexia, 60 controls) and glutamate (Glu) and gamma-aminobutyric acid (GABA) concentrations from magnetic resonance spectroscopy (MRS) at 7T MRI scanner in half of the sample. Our results, supported by Bayesian statistics, show no evidence of E/I balance differences between groups, challenging the hypothesis that cortical hyperexcitability underlies dyslexia. These findings suggest that alternative mechanisms must be explored and highlight the need for further research into the E/I balance and its role in neurodevelopmental disorders.

    1. Neuroscience
    David C Williams, Amanda Chu ... Michael A McDannald
    Research Advance

    Recognizing and responding to threat cues is essential to survival. Freezing is a predominant threat behavior in rats. We have recently shown that a threat cue can organize diverse behaviors beyond freezing, including locomotion (Chu et al., 2024). However, that experimental design was complex, required many sessions, and had rats receive many foot shock presentations. Moreover, the findings were descriptive. Here, we gave female and male Long Evans rats cue light illumination paired or unpaired with foot shock (8 total) in a conditioned suppression setting, using a range of shock intensities (0.15, 0.25, 0.35, or 0.50 mA). We found that conditioned suppression was only observed at higher foot shock intensities (0.35 mA and 0.50 mA). We constructed comprehensive temporal ethograms by scoring 22,272 frames across 12 behavior categories in 200-ms intervals around cue light illumination. The 0.50 mA and 0.35 mA shock-paired visual cues suppressed reward seeking, rearing, and scaling, as well as light-directed rearing and light-directed scaling. The shock-paired visual cue further elicited locomotion and freezing. Linear discriminant analyses showed that ethogram data could accurately classify rats into paired and unpaired groups. Using complete ethogram data produced superior classification compared to behavior subsets, including an Immobility subset featuring freezing. The results demonstrate diverse threat behaviors – in a short and simple procedure – containing sufficient information to distinguish the visual fear conditioning status of individual rats.