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Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship

Inagaki, Hidehiko K. and Jung, Yonil and Hoopfer, Eric D. and Wong, Allan M. and Mishra, Neeli and Lin, John Y. and Tsien, Roger Y. and Anderson, David J. (2013) Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship. Nature Methods, 11 (3). pp. 325-332. ISSN 1548-7091. PMCID PMC4151318. http://resolver.caltech.edu/CaltechAUTHORS:20140110-131314050

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Abstract

Optogenetics allows the manipulation of neural activity in freely moving animals with millisecond precision, but its application in Drosophila melanogaster has been limited. Here we show that a recently described red activatable channelrhodopsin (ReaChR) permits control of complex behavior in freely moving adult flies, at wavelengths that are not thought to interfere with normal visual function. This tool affords the opportunity to control neural activity over a broad dynamic range of stimulation intensities. Using time-resolved activation, we show that the neural control of male courtship song can be separated into (i) probabilistic, persistent and (ii) deterministic, command-like components. The former, but not the latter, neurons are subject to functional modulation by social experience, which supports the idea that they constitute a locus of state-dependent influence. This separation is not evident using thermogenetic tools, a result underscoring the importance of temporally precise control of neuronal activation in the functional dissection of neural circuits in Drosophila.


Item Type:Article
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http://www.nature.com/nmeth/journal/vaop/ncurrent/full/nmeth.2765.htmlPublisherArticle
http://dx.doi.org/10.1038/nmeth.2765DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4151318/PubMed CentralArticle
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Additional Information:© 2013 Macmillan Publishers Limited. Received 03 August 2013; Accepted 18 November 2013; Published online 22 December 2013. We thank K. Deisseroth (Stanford University) and B. Pfeiffer (Janelia Farm Research Campus) for plasmids. Fly stocks were generously provided by the Bloomington Stock Center, A. Fiala (Georg-August-Universität Göttingen),G.M. Rubin, L.L. Looger, B.J. Dickson (Janelia Farm Research Campus) and P.A. Garrity (Brandeis University). We also thank members of the Anderson lab for helpful discussion and sharing of flies. H.K.I. was supported by the Nakajima Foundation. J.Y.L. was funded by Foundation of Research, Science and Technology New Zealand. The project was supported by grants from the US National Institutes of Health to R.Y.T. (NS027177) and to D.J.A. (R01DA031389-03). D.J.A. and R.Y.T. are supported by the Howard Hughes Medical Institute. Author Contributions: H.K.I. and D.J.A. designed the experiments. H.K.I., Y.J. and N.M. performed behavioral experiments. H.K.I. and A.M.W. created the transgenic flies. H.K.I. performed physiological experiments. E.D.H. provided P1-GAL4. J.Y.L. and R.Y.T. provided the ReaChR reagent and advice on its biophysical properties. H.K.I. and Y.J. performed the data analysis. H.K.I. and D.J.A. prepared the figures and wrote the paper. The authors declare no competing financial interests.
Funders:
Funding AgencyGrant Number
Nakajima FoundationUNSPECIFIED
Foundation of Research, Science and Technology (New Zealand)UNSPECIFIED
NIHNS0271777
NIHR01DA031389-03
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:Sexual behaviour; Gustatory system; Optogenetics; Drosophila
PubMed Central ID:PMC4151318
Record Number:CaltechAUTHORS:20140110-131314050
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20140110-131314050
Official Citation:Inagaki, H. K., Jung, Y., Hoopfer, E. D., Wong, A. M., Mishra, N., Lin, J. Y., ... Anderson, D. J. (2014). Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship. Nat Meth, 11(3), 325-332. doi: 10.1038/nmeth.2765
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:43315
Collection:CaltechAUTHORS
Deposited By: Juan Valdivia
Deposited On:19 Feb 2014 16:34
Last Modified:21 Jul 2017 22:39

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