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

Abstract

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.

Autoren

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

DOI

10.7554/elife.26016

eISSN

2050-084X

Zeitschrift

eLife

Sprache

en

Online publication date

2018

Status

Published online

Herausgeber

eLife Sciences Publications, Ltd

Herausgeber URL

http://dx.doi.org/10.7554/elife.26016

Datum der Datenerfassung

2023

Titel

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

Ausgabe der Zeitschrift

7

Datenquelle: Crossref

Abstract

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.

Addresses

Department of Neuroscience, Columbia University Medical Center, New York, United States.

Autoren

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

DOI

10.7554/elife.26016

eISSN

2050-084X

Externe Identifier

PubMed Identifier: 29528286
PubMed Central ID: PMC5869015

Funding acknowledgements

National Science Foundation: Graduate Research Fellowship
National Institutes of Health: NS090909-01
NINDS NIH HHS: R01 NS061908
NIH HHS: NS086564
NIH HHS: GM086458
Thompson Family Foundation: Innovation Award
National Institutes of Health: GM086458
Japan Society for the Promotion of Science: KAKENHI 26890025
NINDS NIH HHS: F31 NS090909
NIH HHS: NS061908
NIH HHS: NS090909-01
National Institutes of Health: NS061908
Howard Hughes Medical Institute:
National Institutes of Health: NS086564
NIGMS NIH HHS: R01 GM086458
NINDS NIH HHS: R24 NS086564

Open access

true

ISSN

2050-084X

Zeitschrift

eLife

Schlüsselwörter

Efferent Pathways
Interneurons
Nociceptors
Animals
Drosophila melanogaster
Behavior, Animal
Escape Reaction
Larva

Sprache

eng

Medium

Electronic

Online publication date

2018

Open access status

Open Access

Paginierung

e26016

Datum der Veröffentlichung

2018

Status

Published

Publisher licence

CC BY

Datum der Datenerfassung

2018

Titel

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

Sub types

Research Support, Non-U.S. Gov't
research-article
Research Support, U.S. Gov't, Non-P.H.S.
Journal Article
Research Support, N.I.H., Extramural

Ausgabe der Zeitschrift

7

Files

https://europepmc.org/articles/PMC5869015?pdf=render

Datenquelle: Europe PubMed Central

Abstract

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.

Date of acceptance

2018

Autoren

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

Autoren-URL

https://www.ncbi.nlm.nih.gov/pubmed/29528286

DOI

10.7554/eLife.26016

eISSN

2050-084X

Externe Identifier

PubMed Central ID: PMC5869015

Funding acknowledgements

NIH HHS: NS061908
NIH HHS: NS090909-01
NIGMS NIH HHS: R01 GM086458
NINDS NIH HHS: R01 NS061908
NIH HHS: GM086458
NIH HHS: NS086564
NINDS NIH HHS: F31 NS090909
NINDS NIH HHS: R24 NS086564
Howard Hughes Medical Institute:

Zeitschrift

Elife

Schlüsselwörter

D. melanogaster
behavior
interneuron
larva
neuroscience
nociception
sensory circuit
sensory neuron
Animals
Behavior, Animal
Drosophila melanogaster
Efferent Pathways
Escape Reaction
Interneurons
Larva
Nociceptors

Sprache

eng

Country

England

PII

26016

Datum der Veröffentlichung

2018

Status

Published online

Datum, an dem der Datensatz öffentlich gemacht wurde

2019

Titel

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

Sub types

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Ausgabe der Zeitschrift

7

Datenquelle: PubMed

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

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