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

Author:

Burgos Anita1ORCID,Honjo Ken2,Ohyama Tomoko3,Qian Cheng Sam1ORCID,Shin Grace Ji-eun4,Gohl Daryl M5,Silies Marion6,Tracey W Daniel78ORCID,Zlatic Marta9,Cardona Albert9ORCID,Grueber Wesley B1410ORCID

Affiliation:

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

2. Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan

3. Department of Biology, McGill University, Montreal, Canada

4. Department of Physiology and Cellular Biophysics, Columbia University Medical Center, New York, United States

5. University of Minnesota Genomics Center, Minneapolis, United States

6. European Neuroscience Institute Göttingen, Göttingen, Germany

7. The Linda and Jack Gill Center for Biomolecular Science, Indiana University, Bloomington, United States

8. Department of Biology, Indiana University, Bloomington, United States

9. Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

10. Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, United States

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.

Funder

National Science Foundation

National Institutes of Health

Japan Society for the Promotion of Science

Thompson Family Foundation

Howard Hughes Medical Institute

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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