Optogenetic dissection of descending behavioral control in Drosophila
- Janelia Research Campus, Howard Hughes Medical Institute, United States
- Emory University, United States
- Princeton University, United States
Abstract
In most animals, the brain makes behavioral decisions that are transmitted by descending neurons to the nerve cord circuitry that produces behaviors. In insects, only a few descending neurons have been associated with specific behaviors. To explore how descending neurons control an insect's movements, we developed a novel method to systematically assay the behavioral effects of activating individual neurons on freely behaving terrestrial D. melanogaster. We calculated a two-dimensional representation of the entire behavior space explored by these flies and we associated descending neurons with specific behaviors by identifying regions of this space that were visited with increased frequency during optogenetic activation. Applying this approach across a large collection of descending neurons, we found that (1) activation of most of the descending neurons drove stereotyped behaviors, (2) in many cases multiple descending neurons activated similar behaviors, and (3) optogenetically-activated behaviors were often dependent on the behavioral state prior to activation.
Data availability
Videos including one second before until one second after activation for all flies during all treatments have been uploaded to Dryad (doi:10.5061/dryad.fr89c0c). We slowed down these movies 4X to allow easier examination.
-
Data from: Optogenetic dissection of descending behavioral control in DrosophilaAvailable at Dryad Digital Repository under a CC0 Public Domain Dedication.
Article and author information
Author details
Funding
Howard Hughes Medical Institute
- Jessica Cande
- Shigehiro Namiki
- Wyatt Korff
- Gwyneth M Card
- David L Stern
National Institutes of Health
- Josh W Shaevitz
- Gordon J Berman
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Kristin Scott, University of California, Berkeley, Berkeley, United States
Version history
- Received: December 12, 2017
- Accepted: June 3, 2018
- Accepted Manuscript published: June 26, 2018 (version 1)
- Version of Record published: July 4, 2018 (version 2)
Copyright
© 2018, Cande 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
-
- 7,073
- views
-
- 914
- downloads
-
- 125
- 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)
Optogenetic dissection of descending behavioral control in Drosophila
eLife 7:e34275.
https://doi.org/10.7554/eLife.34275
Further reading
-
- Neuroscience
The neurons that connect the brain and ventral nerve cord in fruit flies have been mapped in unprecedented detail.
-
- Neuroscience
Pavlovian fear conditioning has been extensively used to study the behavioral and neural basis of defensive systems. In a typical procedure, a cue is paired with foot shock, and subsequent cue presentation elicits freezing, a behavior theoretically linked to predator detection. Studies have since shown a fear conditioned cue can elicit locomotion, a behavior that – in addition to jumping, and rearing – is theoretically linked to imminent or occurring predation. A criticism of studies observing fear conditioned cue-elicited locomotion is that responding is non-associative. We gave rats Pavlovian fear discrimination over a baseline of reward seeking. TTL-triggered cameras captured 5 behavior frames/s around cue presentation. Experiment 1 examined the emergence of danger-specific behaviors over fear acquisition. Experiment 2 examined the expression of danger-specific behaviors in fear extinction. In total, we scored 112,000 frames for nine discrete behavior categories. Temporal ethograms show that during acquisition, a fear conditioned cue suppresses reward seeking and elicits freezing, but also elicits locomotion, jumping, and rearing – all of which are maximal when foot shock is imminent. During extinction, a fear conditioned cue most prominently suppresses reward seeking, and elicits locomotion that is timed to shock delivery. The independent expression of these behaviors in both experiments reveals a fear conditioned cue to orchestrate a temporally organized suite of behaviors.
