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P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila

Hoopfer, Eric D. and Jung, Yonil and Inagaki, Hidehiko K. and Rubin, Gerald M. and Anderson, David J. (2015) P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila. eLife, 4 . Art. No. 11346. ISSN 2050-084X. http://resolver.caltech.edu/CaltechAUTHORS:20160104-124804649

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[img] Video (MPEG) (Video 2. P1^a>dTrpA1 behavioral phenotype) - Supplemental Material
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[img] Video (MPEG) (Video 3. Activation of P1 neurons induces aggression between wingless males) - Supplemental Material
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[img] Video (MPEG) (Video 4. P1^a>CsChrimson phenotype in pairs of males during strong photostimulation) - Supplemental Material
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[img] Video (MPEG) (Video 5. P1^a>ReaChR males interacting following barrier removal 10 min after photostimulation) - Supplemental Material
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Abstract

How brains are hardwired to produce aggressive behavior, and how aggression circuits are related to those that mediate courtship, is not well understood. A large-scale screen for aggression-promoting neurons in Drosophila identified several independent hits that enhanced both inter-male aggression and courtship. Genetic intersections revealed that P1 interneurons, previously thought to exclusively control male courtship, were responsible for both phenotypes. The aggression phenotype was fly-intrinsic, and required male-specific chemosensory cues on the opponent. Optogenetic experiments indicated that P1 activation promoted aggression vs. wing extension at low vs. high thresholds, respectively. High frequency photostimulation promoted wing extension and aggression in an inverse manner, during light ON and OFF, respectively. P1 activation enhanced aggression by promoting a persistent internal state, which could endure for minutes prior to social contact. Thus P1 neurons promote an internal state that facilitates both aggression and courtship, and can control these social behaviors in a threshold-dependent manner.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.7554/eLife.11346DOIArticle
http://elifesciences.org/content/4/e11346PublisherArticle
Additional Information:© 2015, Hoopfer 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. Received September 3, 2015. Accepted December 15, 2015. Published December 29, 2015. We thank Barret Pfeiffer for design, construction, and gift of the Chrimson and OpGcamp lines, construction of the GAL4 collection and LexAop-Flp lines and for advice and discussions; Hui Chiu for contributions, discussions and for sharing her unpublished data; Heather Dionne and Christine Murphy for construction of split-GAL4 and LexA lines; Kenta Asahina, Stefanie Hampel, Andrew Seeds, Moriel Zelikowsky, Weizhe Hong and Allan Wong for advice and discussions; Richard Axel for critical comments on the manuscript; Pietro Perona and Eyrún Eyjólfsdótir for JCtrax software; Kristin Branson and Mayank Kabra for help with JAABA classifiers; Frank Midgley and Jinyang Liu for help modifying the tracking software for a computer cluster; Guss Lott for gVision software; Barry Dickson, Bruce Baker and Yufeng Pan for GAL4 lines; Sharon Low and Mary Phillips for technical assistance with behavioral assays; Karen Hibbard, Monti Mercer, James McMahon and Marcela Arenas-Sanchez for fly husbandry; Celine Chiu for laboratory management; Gina Mancuso, Crystal Sullivan, Sarah Moorehead and Emily Willis for administrative assistance; Kevin Moses, the Janelia Visiting Scientist Program and the Fly Olympiad Program for support. Author contributions: EDH, Conducted all experiments except for the functional imaging, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article YJ, Conducted the functional imaging experiment, Acquisition of data, Analysis and interpretation of data. HKI, Generated the ReaChR transgenic flies and established the optogenetic behavior system, Drafting or revising the article, Contributed unpublished essential data or reagents. GMR, Contributed to the design of genetic intersection strategies, Conception and design, Contributed unpublished essential data or reagents. DJA, Conception and design, Analysis and interpretation of data, Drafting or revising the article. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. COMPETING INTERESTS: The authors declare that no competing interests exist.
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Fly Olympiad ProgramUNSPECIFIED
NIH Predoctoral FellowshipUNSPECIFIED
Heiwa Nakajima FoundationUNSPECIFIED
NIHDA031389
Gordon and Betty Moore FoundationUNSPECIFIED
Record Number:CaltechAUTHORS:20160104-124804649
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20160104-124804649
Official Citation:P1 interneurons promote a persistent internal state that enhances inter-male aggression in Drosophila Eric D Hoopfer, Yonil Jung, Hidehiko K Inagaki, Gerald M Rubin, David J Anderson DOI: http://dx.doi.org/10.7554/eLife.11346 Published December 29, 2015 eLife 2015;10.7554/eLife.11346
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:63329
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:05 Jan 2016 19:27
Last Modified:13 Apr 2016 23:59

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