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

  • 2,464
    views
  • 282
    downloads
  • 19
    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
    Mi-Seon Kong, Ethan Ancell ... Larry S Zweifel
    Research Article

    The central amygdala (CeA) has emerged as an important brain region for regulating both negative (fear and anxiety) and positive (reward) affective behaviors. The CeA has been proposed to encode affective information in the form of valence (whether the stimulus is good or bad) or salience (how significant is the stimulus), but the extent to which these two types of stimulus representation occur in the CeA is not known. Here, we used single cell calcium imaging in mice during appetitive and aversive conditioning and found that majority of CeA neurons (~65%) encode the valence of the unconditioned stimulus (US) with a smaller subset of cells (~15%) encoding the salience of the US. Valence and salience encoding of the conditioned stimulus (CS) was also observed, albeit to a lesser extent. These findings show that the CeA is a site of convergence for encoding oppositely valenced US information.

    1. Neuroscience
    Sharon Inberg, Yael Iosilevskii ... Benjamin Podbilewicz
    Research Article

    Dendrites are crucial for receiving information into neurons. Sensory experience affects the structure of these tree-like neurites, which, it is assumed, modifies neuronal function, yet the evidence is scarce, and the mechanisms are unknown. To study whether sensory experience affects dendritic morphology, we use the Caenorhabditis elegans' arborized nociceptor PVD neurons, under natural mechanical stimulation induced by physical contacts between individuals. We found that mechanosensory signals induced by conspecifics and by glass beads affect the dendritic structure of the PVD. Moreover, developmentally isolated animals show a decrease in their ability to respond to harsh touch. The structural and behavioral plasticity following sensory deprivation are functionally independent of each other and are mediated by an array of evolutionarily conserved mechanosensory amiloride-sensitive epithelial sodium channels (degenerins). Calcium imaging of the PVD neurons in a micromechanical device revealed that controlled mechanical stimulation of the body wall produces similar calcium dynamics in both isolated and crowded animals. Our genetic results, supported by optogenetic, behavioral, and pharmacological evidence, suggest an activity-dependent homeostatic mechanism for dendritic structural plasticity, that in parallel controls escape response to noxious mechanosensory stimuli.