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Active flight increases the gain of visual motion processing in Drosophila

Nature Neuroscience volume 13, pages 393–399 (2010)Cite this article

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Abstract

We developed a technique for performing whole-cell patch-clamp recordings from genetically identified neurons in behaving Drosophila. We focused on the properties of visual interneurons during tethered flight, but this technique generalizes to different cell types and behaviors. We found that the peak-to-peak responses of a class of visual motion–processing interneurons, the vertical-system visual neurons (VS cells), doubled when flies were flying compared with when they were at rest. Thus, the gain of the VS cells is not fixed, but is instead behaviorally flexible and changes with locomotor state. Using voltage clamp, we found that the passive membrane resistance of VS cells was reduced during flight, suggesting that the elevated gain was a result of increased synaptic drive from upstream motion-sensitive inputs. The ability to perform patch-clamp recordings in behaving Drosophila promises to help unify the understanding of behavior at the gene, cell and circuit levels.

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Figure 1: Patch-clamp recordings in tethered, flying Drosophila.
Figure 2: Behavioral measurements of wing stroke amplitude during tethered flight.
Figure 3: Visual responses of VS cells are boosted and the resting potential depolarizes during flight.
Figure 4: During flight, passive membrane-resistance decreases and membrane voltage and current fluctuations increase.
Figure 5: Other neurons in the central brain are not depolarized during flight.
Figure 6: The baseline depolarization and visual-response boost have different recovery dynamics at the cessation of flight.

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Acknowledgements

We thank J. Assad, V. Bhandawat, G. Card, C. Chiu, M. Do, T. Herrington, W. Korff, G. Laurent, M. Murthy, P. Polidoro, G. Turner and R. Wilson for helpful discussion, comments and aid in developing the preparation. We are grateful to L. Luo for the Gal4-3a fly line. This work was supported by a National Science Foundation Frontiers in Integrative Biological Research 0623527 award (M.H.D.) and a Caltech Della Martin fellowship (G.M.).

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Authors and Affiliations

  1. Divisions of Biology and Engineering and Applied Sciences, California Institute of Technology, Pasadena, California, USA

    Gaby Maimon, Andrew D Straw & Michael H Dickinson

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  1. Gaby Maimon
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Contributions

G.M., A.D.S. and M.H.D. designed the experiments. G.M. and M.H.D. wrote the paper. G.M. developed the preparation, conducted the experiments and analyzed the data. A.D.S. designed the software and hardware system for tracking wing beat amplitudes in real time.

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Correspondence to Gaby Maimon.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–4 (PDF 3624 kb)

Supplementary Video 1

Fly flying during a patch-clamp recording. This video shows footage of a flying fly during an electrophysiological recording session. The green lines represent the estimates of the left and right wingbeat amplitudes. (MOV 3741 kb)

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Maimon, G., Straw, A. & Dickinson, M. Active flight increases the gain of visual motion processing in Drosophila. Nat Neurosci 13, 393–399 (2010). https://doi.org/10.1038/nn.2492

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