Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviors

Deciphering how the brain regulates motor circuits to control complex behaviors is an important, long-standing challenge in neuroscience. In the fly, Drosophila melanogaster, this is coordinated by a population of ~ 1100 descending neurons (DNs). Activating only a few DNs is known to be sufficient t...

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Main Authors: Florian Aymanns, Chin-Lin Chen, Pavan Ramdya
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/81527
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author Florian Aymanns
Chin-Lin Chen
Pavan Ramdya
author_facet Florian Aymanns
Chin-Lin Chen
Pavan Ramdya
author_sort Florian Aymanns
collection DOAJ
description Deciphering how the brain regulates motor circuits to control complex behaviors is an important, long-standing challenge in neuroscience. In the fly, Drosophila melanogaster, this is coordinated by a population of ~ 1100 descending neurons (DNs). Activating only a few DNs is known to be sufficient to drive complex behaviors like walking and grooming. However, what additional role the larger population of DNs plays during natural behaviors remains largely unknown. For example, they may modulate core behavioral commands or comprise parallel pathways that are engaged depending on sensory context. We evaluated these possibilities by recording populations of nearly 100 DNs in individual tethered flies while they generated limb-dependent behaviors, including walking and grooming. We found that the largest fraction of recorded DNs encode walking while fewer are active during head grooming and resting. A large fraction of walk-encoding DNs encode turning and far fewer weakly encode speed. Although odor context does not determine which behavior-encoding DNs are recruited, a few DNs encode odors rather than behaviors. Lastly, we illustrate how one can identify individual neurons from DN population recordings by using their spatial, functional, and morphological properties. These results set the stage for a comprehensive, population-level understanding of how the brain’s descending signals regulate complex motor actions.
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spelling doaj.art-04ca228754004956b4a3272e3a198f492022-12-22T03:53:53ZengeLife Sciences Publications LtdeLife2050-084X2022-10-011110.7554/eLife.81527Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviorsFlorian Aymanns0https://orcid.org/0000-0003-4290-7244Chin-Lin Chen1https://orcid.org/0000-0002-4968-4920Pavan Ramdya2https://orcid.org/0000-0001-5425-4610Neuroengineering Laboratory, Brain Mind Institute & Interfaculty Institute of Bioengineering, EPFL, Lausanne, SwitzerlandNeuroengineering Laboratory, Brain Mind Institute & Interfaculty Institute of Bioengineering, EPFL, Lausanne, SwitzerlandNeuroengineering Laboratory, Brain Mind Institute & Interfaculty Institute of Bioengineering, EPFL, Lausanne, SwitzerlandDeciphering how the brain regulates motor circuits to control complex behaviors is an important, long-standing challenge in neuroscience. In the fly, Drosophila melanogaster, this is coordinated by a population of ~ 1100 descending neurons (DNs). Activating only a few DNs is known to be sufficient to drive complex behaviors like walking and grooming. However, what additional role the larger population of DNs plays during natural behaviors remains largely unknown. For example, they may modulate core behavioral commands or comprise parallel pathways that are engaged depending on sensory context. We evaluated these possibilities by recording populations of nearly 100 DNs in individual tethered flies while they generated limb-dependent behaviors, including walking and grooming. We found that the largest fraction of recorded DNs encode walking while fewer are active during head grooming and resting. A large fraction of walk-encoding DNs encode turning and far fewer weakly encode speed. Although odor context does not determine which behavior-encoding DNs are recruited, a few DNs encode odors rather than behaviors. Lastly, we illustrate how one can identify individual neurons from DN population recordings by using their spatial, functional, and morphological properties. These results set the stage for a comprehensive, population-level understanding of how the brain’s descending signals regulate complex motor actions.https://elifesciences.org/articles/81527population imagingtwo-photon microscopydescending neuronwalkinggroominglimb
spellingShingle Florian Aymanns
Chin-Lin Chen
Pavan Ramdya
Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviors
eLife
population imaging
two-photon microscopy
descending neuron
walking
grooming
limb
title Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviors
title_full Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviors
title_fullStr Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviors
title_full_unstemmed Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviors
title_short Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviors
title_sort descending neuron population dynamics during odor evoked and spontaneous limb dependent behaviors
topic population imaging
two-photon microscopy
descending neuron
walking
grooming
limb
url https://elifesciences.org/articles/81527
work_keys_str_mv AT florianaymanns descendingneuronpopulationdynamicsduringodorevokedandspontaneouslimbdependentbehaviors
AT chinlinchen descendingneuronpopulationdynamicsduringodorevokedandspontaneouslimbdependentbehaviors
AT pavanramdya descendingneuronpopulationdynamicsduringodorevokedandspontaneouslimbdependentbehaviors