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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Format: | Article |
Language: | English |
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eLife Sciences Publications Ltd
2018-03-01
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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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institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-12-10T04:08:00Z |
publishDate | 2018-03-01 |
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series | eLife |
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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