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