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ON and OFF pathways in Drosophila motion vision

Nature volume 468, pages 300–304 (2010)Cite this article

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Abstract

Motion vision is a major function of all visual systems, yet the underlying neural mechanisms and circuits are still elusive. In the lamina, the first optic neuropile of Drosophila melanogaster, photoreceptor signals split into five parallel pathways, L1–L51. Here we examine how these pathways contribute to visual motion detection by combining genetic block and reconstitution of neural activity in different lamina cell types with whole-cell recordings from downstream motion-sensitive neurons2,3. We find reduced responses to moving gratings if L1 or L2 is blocked; however, reconstitution of photoreceptor input to only L1 or L2 results in wild-type responses. Thus, the first experiment indicates the necessity of both pathways, whereas the second indicates sufficiency of each single pathway. This contradiction can be explained by electrical coupling between L1 and L2, allowing for activation of both pathways even when only one of them receives photoreceptor input. A fundamental difference between the L1 pathway and the L2 pathway is uncovered when blocking L1 or L2 output while presenting moving edges of positive (ON) or negative (OFF) contrast polarity: blocking L1 eliminates the response to moving ON edges, whereas blocking L2 eliminates the response to moving OFF edges. Thus, similar to the segregation of photoreceptor signals in ON and OFF bipolar cell pathways in the vertebrate retina4, photoreceptor signals segregate into ON-L1 and OFF-L2 channels in the lamina of Drosophila.

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Figure 1: Fly optic lobe and GAL4 driver lines.
Figure 2: Tangential cell responses to moving large field gratings of various contrasts.
Figure 3: Lamina cells L1 and L2 are electrically coupled.
Figure 4: Voltage responses of lobula plate tangential cells to moving edges of a single polarity (single example response

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Acknowledgements

We thank C.-H. Lee, J. Rister and C. Schnaitmann for providing flies. Shaking B antibody was provided by J. Bacon. We thank W. Essbauer and C. Theile for technical assistance, and R. Schorner for the artwork in Fig. 1a.

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Author notes

  1. Maximilian Joesch and Bettina Schnell: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Systems and Computational Neurobiology, MPI for Neurobiology, Am Klopferspitz 18, 82152 Martinsried, Germany,

    Maximilian Joesch, Bettina Schnell, Shamprasad Varija Raghu, Dierk F. Reiff & Alexander Borst

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  1. Maximilian Joesch
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  3. Shamprasad Varija Raghu
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Contributions

M.J. performed the blocking experiments and neurobiotin injections; B.S. did the rescue experiments; M.J. and B.S. did all fly work and data analysis; S.V.R. analysed expression patterns of the driver lines; D.F.R. and A.B. designed and supervised the study; and A.B. wrote the manuscript with the help of all authors.

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Correspondence to Alexander Borst.

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Joesch, M., Schnell, B., Raghu, S. et al. ON and OFF pathways in Drosophila motion vision. Nature 468, 300–304 (2010). https://doi.org/10.1038/nature09545

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