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A directional tuning map of Drosophila elementary motion detectors

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Abstract

The extraction of directional motion information from changing retinal images is one of the earliest and most important processing steps in any visual system. In the fly optic lobe, two parallel processing streams have been anatomically described, leading from two first-order interneurons, L1 and L2, via T4 and T5 cells onto large, wide-field motion-sensitive interneurons of the lobula plate1. Therefore, T4 and T5 cells are thought to have a pivotal role in motion processing; however, owing to their small size, it is difficult to obtain electrical recordings of T4 and T5 cells, leaving their visual response properties largely unknown. We circumvent this problem by means of optical recording from these cells in Drosophila, using the genetically encoded calcium indicator GCaMP5 (ref. 2). Here we find that specific subpopulations of T4 and T5 cells are directionally tuned to one of the four cardinal directions; that is, front-to-back, back-to-front, upwards and downwards. Depending on their preferred direction, T4 and T5 cells terminate in specific sublayers of the lobula plate. T4 and T5 functionally segregate with respect to contrast polarity: whereas T4 cells selectively respond to moving brightness increments (ON edges), T5 cells only respond to moving brightness decrements (OFF edges). When the output from T4 or T5 cells is blocked, the responses of postsynaptic lobula plate neurons to moving ON (T4 block) or OFF edges (T5 block) are selectively compromised. The same effects are seen in turning responses of tethered walking flies. Thus, starting with L1 and L2, the visual input is split into separate ON and OFF pathways, and motion along all four cardinal directions is computed separately within each pathway. The output of these eight different motion detectors is then sorted such that ON (T4) and OFF (T5) motion detectors with the same directional tuning converge in the same layer of the lobula plate, jointly providing the input to downstream circuits and motion-driven behaviours.

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Figure 1: Directional tuning and layer-specific projection of T4 and T5 cells.
Figure 2: Local signals of T4 and T5 cells.
Figure 3: Comparison of visual response properties between T4 and T5 cells.
Figure 4: Voltage responses of lobula plate tangential cells and turning responses of walking flies to moving ON and OFF edges.

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Acknowledgements

We thank L. Looger, J. Simpson, V. Jayaraman and the Janelia GECI team for making and providing us with the GCaMP5 flies before publication; J. Plett for designing and engineering the LED arena; C. Theile, W. Essbauer and M. Sauter for fly work; and A. Mauss, F. Gabbiani and T. Bonhoeffer for critically reading the manuscript. This work was in part supported by the Deutsche Forschungsgemeinschaft (SFB 870). M.S.M., G.A., E.S., M.M., A.L., A.Ba and A.Bo are members of the Graduate School of Systemic Neurosciences.

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M.S.M. and J.H. jointly performed and, together with A.Bo., evaluated all calcium imaging experiments. G.A., E.S. and M.M. recorded from tangential cells. A.L., T.S. and A.Ba. performed the behavioural experiments. G.R., B.D. and A.N. generated the driver lines and characterized their expression pattern. D.F.R. performed preliminary imaging experiments. E.H. helped with programming and developed the PMT shielding for the two-photon microscope. A.Bo. designed the study and wrote the manuscript with the help of all authors.

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Correspondence to Alexander Borst.

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The authors declare no competing financial interests.

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Maisak, M., Haag, J., Ammer, G. et al. A directional tuning map of Drosophila elementary motion detectors. Nature 500, 212–216 (2013). https://doi.org/10.1038/nature12320

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