Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila

Rapid and efficient escape behaviors in response to noxious sensory stimuli are essential for protection and survival. Yet, how noxious stimuli are transformed to coordinated escape behaviors remains poorly understood. In Drosophila larvae, noxious stimuli trigger sequential body bending and corkscr...

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Main Authors: Anita Burgos, Ken Honjo, Tomoko Ohyama, Cheng Sam Qian, Grace Ji-eun Shin, Daryl M Gohl, Marion Silies, W Daniel Tracey, Marta Zlatic, Albert Cardona, Wesley B Grueber
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-03-01
Series:eLife
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Online Access:https://elifesciences.org/articles/26016
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author Anita Burgos
Ken Honjo
Tomoko Ohyama
Cheng Sam Qian
Grace Ji-eun Shin
Daryl M Gohl
Marion Silies
W Daniel Tracey
Marta Zlatic
Albert Cardona
Wesley B Grueber
author_facet Anita Burgos
Ken Honjo
Tomoko Ohyama
Cheng Sam Qian
Grace Ji-eun Shin
Daryl M Gohl
Marion Silies
W Daniel Tracey
Marta Zlatic
Albert Cardona
Wesley B Grueber
author_sort Anita Burgos
collection DOAJ
description Rapid and efficient escape behaviors in response to noxious sensory stimuli are essential for protection and survival. Yet, how noxious stimuli are transformed to coordinated escape behaviors remains poorly understood. In Drosophila larvae, noxious stimuli trigger sequential body bending and corkscrew-like rolling behavior. We identified a population of interneurons in the nerve cord of Drosophila, termed Down-and-Back (DnB) neurons, that are activated by noxious heat, promote nociceptive behavior, and are required for robust escape responses to noxious stimuli. Electron microscopic circuit reconstruction shows that DnBs are targets of nociceptive and mechanosensory neurons, are directly presynaptic to pre-motor circuits, and link indirectly to Goro rolling command-like neurons. DnB activation promotes activity in Goro neurons, and coincident inactivation of Goro neurons prevents the rolling sequence but leaves intact body bending motor responses. Thus, activity from nociceptors to DnB interneurons coordinates modular elements of nociceptive escape behavior.
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spelling doaj.art-7c7d91a80d1d4f9684a3d7e21c07ce0a2022-12-22T02:02:47ZengeLife Sciences Publications LtdeLife2050-084X2018-03-01710.7554/eLife.26016Nociceptive interneurons control modular motor pathways to promote escape behavior in DrosophilaAnita Burgos0https://orcid.org/0000-0003-4603-2086Ken Honjo1Tomoko Ohyama2Cheng Sam Qian3https://orcid.org/0000-0002-2456-3153Grace Ji-eun Shin4Daryl M Gohl5Marion Silies6W Daniel Tracey7https://orcid.org/0000-0003-4666-8199Marta Zlatic8Albert Cardona9https://orcid.org/0000-0003-4941-6536Wesley B Grueber10https://orcid.org/0000-0001-6751-256XDepartment of Neuroscience, Columbia University Medical Center, New York, United StatesFaculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanDepartment of Biology, McGill University, Montreal, CanadaDepartment of Neuroscience, Columbia University Medical Center, New York, United StatesDepartment of Physiology and Cellular Biophysics, Columbia University Medical Center, New York, United StatesUniversity of Minnesota Genomics Center, Minneapolis, United StatesEuropean Neuroscience Institute Göttingen, Göttingen, GermanyThe Linda and Jack Gill Center for Biomolecular Science, Indiana University, Bloomington, United States; Department of Biology, Indiana University, Bloomington, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, United StatesDepartment of Neuroscience, Columbia University Medical Center, New York, United States; Department of Physiology and Cellular Biophysics, Columbia University Medical Center, New York, United States; Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, United StatesRapid and efficient escape behaviors in response to noxious sensory stimuli are essential for protection and survival. Yet, how noxious stimuli are transformed to coordinated escape behaviors remains poorly understood. In Drosophila larvae, noxious stimuli trigger sequential body bending and corkscrew-like rolling behavior. We identified a population of interneurons in the nerve cord of Drosophila, termed Down-and-Back (DnB) neurons, that are activated by noxious heat, promote nociceptive behavior, and are required for robust escape responses to noxious stimuli. Electron microscopic circuit reconstruction shows that DnBs are targets of nociceptive and mechanosensory neurons, are directly presynaptic to pre-motor circuits, and link indirectly to Goro rolling command-like neurons. DnB activation promotes activity in Goro neurons, and coincident inactivation of Goro neurons prevents the rolling sequence but leaves intact body bending motor responses. Thus, activity from nociceptors to DnB interneurons coordinates modular elements of nociceptive escape behavior.https://elifesciences.org/articles/26016nociceptionsensory circuitsensory neuronbehaviorinterneuronlarva
spellingShingle Anita Burgos
Ken Honjo
Tomoko Ohyama
Cheng Sam Qian
Grace Ji-eun Shin
Daryl M Gohl
Marion Silies
W Daniel Tracey
Marta Zlatic
Albert Cardona
Wesley B Grueber
Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila
eLife
nociception
sensory circuit
sensory neuron
behavior
interneuron
larva
title Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila
title_full Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila
title_fullStr Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila
title_full_unstemmed Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila
title_short Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila
title_sort nociceptive interneurons control modular motor pathways to promote escape behavior in drosophila
topic nociception
sensory circuit
sensory neuron
behavior
interneuron
larva
url https://elifesciences.org/articles/26016
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