Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila
- Columbia University Medical Center, United States
- University of Tsukuba, Japan
- McGill University, Canada
- University of Minnesota Genomics Center, United States
- European Neuroscience Institute, Germany
- Indiana University, United States
- Janelia Research Campus, Howard Hughes Medical Institute, 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.
Article and author information
Author details
Funding
National Science Foundation (Graduate Research Fellowship)
- Anita Burgos
National Institutes of Health (NS090909-01)
- Anita Burgos
Howard Hughes Medical Institute
- Marta Zlatic
National Institutes of Health (NS061908)
- Wesley B Grueber
National Institutes of Health (GM086458)
- W Daniel Tracey
National Institutes of Health (NS086564)
- Wesley B Grueber
Howard Hughes Medical Institute
- Albert Cardona
Thompson Family Foundation (Innovation Award)
- Grace Ji-eun Shin
- Wesley B Grueber
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2018, Burgos et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 6,368
- views
-
- 809
- downloads
-
- 81
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila
eLife 7:e26016.
https://doi.org/10.7554/eLife.26016
Further reading
-
- Computational and Systems Biology
- Neuroscience
The basolateral amygdala (BLA) is a key site where fear learning takes place through synaptic plasticity. Rodent research shows prominent low theta (~3–6 Hz), high theta (~6–12 Hz), and gamma (>30 Hz) rhythms in the BLA local field potential recordings. However, it is not understood what role these rhythms play in supporting the plasticity. Here, we create a biophysically detailed model of the BLA circuit to show that several classes of interneurons (PV, SOM, and VIP) in the BLA can be critically involved in producing the rhythms; these rhythms promote the formation of a dedicated fear circuit shaped through spike-timing-dependent plasticity. Each class of interneurons is necessary for the plasticity. We find that the low theta rhythm is a biomarker of successful fear conditioning. The model makes use of interneurons commonly found in the cortex and, hence, may apply to a wide variety of associative learning situations.
-
- Neuroscience
Mice can generate a cognitive map of an environment based on self-motion signals when there is a fixed association between their starting point and the location of their goal.
