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A directional tuning map of Drosophila elementary motion detectors



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.


  1. Bausenwein, B., Dittrich, A. P. M. & Fischbach, K. F. The optic lobe of Drosophila melanogaster II. Sorting of retinotopic pathways in the medulla. Cell Tissue Res. 267, 17–28 (1992)

    Article  CAS  Google Scholar 

  2. Akerboom, J. et al. Optimization of a GCaMP calcium indicator for neural activity imaging. J. Neurosci. 32, 13819–13840 (2012)

    Article  CAS  Google Scholar 

  3. Cajal, S. R. & Sanchez, D. Contribucion al conocimiento de los centros nerviosos de los insectos (Imprenta de Hijos de Nicholas Moja, 1915)

    Book  Google Scholar 

  4. Strausfeld, N. J. Atlas of an Insect Brain (Springer, 1976)

    Book  Google Scholar 

  5. Fischbach, K. F. & Dittrich, A. P. M. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res. 258, 441–475 (1989)

    Article  Google Scholar 

  6. Reichardt, W. Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. In Sensory Communication (ed. Rosenblith, W. A. ) 303–317 (MIT Press and John Wiley & Sons, 1961)

    Google Scholar 

  7. Borst, A., Haag, J. & Reiff, D. F. Fly motion vision. Annu. Rev. Neurosci. 33, 49–70 (2010)

    Article  CAS  Google Scholar 

  8. Buchner, E., Buchner. S & Buelthoff, I. Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. 1. Wildtype. J. Comp. Physiol. 155, 471–483 (1984)

    Article  Google Scholar 

  9. Strausfeld, N. J. & Lee, J. K. Neuronal basis for parallel visual processing in the fly. Vis. Neurosci. 7, 13–33 (1991)

    Article  CAS  Google Scholar 

  10. Schnell, B., Raghu, V. S., Nern, A. & Borst, A. Columnar cells necessary for motion responses of wide-field visual interneurons in Drosophila. J. Comp. Physiol. A 198, 389–395 (2012)

    Article  Google Scholar 

  11. Douglass, J. K. & Strausfeld, N. J. Visual motion-detection circuits in flies: Parallel direction- and non-direction-sensitive pathways between the medulla and lobula plate. J. Neurosci. 16, 4551–4562 (1996)

    Article  CAS  Google Scholar 

  12. Franceschini, N., Riehle, A. & Le Nestour, A. Directionally selective motion detection by insect neurons. In Facets of Vision (ed. Stavenga, H. ) 360–390 (Springer, 1989)

    Book  Google Scholar 

  13. Joesch, M., Schnell, B., Raghu, S. V., Reiff, D. F. & Borst, A. ON and OFF pathways in Drosophila motion vision. Nature 468, 300–304 (2010)

    Article  ADS  CAS  Google Scholar 

  14. Pfeiffer, B. D. et al. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl Acad. Sci. USA 105, 9715–9720 (2008)

    Article  ADS  CAS  Google Scholar 

  15. Denk, W., Strickler, J. H. & Webb, W. W. Two-photon laser scanning fluorescence microscopy. Science 248, 73–76 (1990)

    Article  ADS  CAS  Google Scholar 

  16. Oyster, C. W. & Barlow, H. B. Direction-selective units in rabbit retina: distribution of preferred directions. Science 155, 841–842 (1967)

    Article  ADS  CAS  Google Scholar 

  17. Sweeney, S. T., Broadie, K., Keane, J., Niemann, H. & O’Kane, C. J. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14, 341–351 (1995)

    Article  CAS  Google Scholar 

  18. Seelig, J. D. et al. Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nature Methods 7, 535–540 (2010)

    Article  CAS  Google Scholar 

  19. Clark, D. A., Bursztyn, L., Horowitz, M. A., Schnitzer, M. J. & Clandinin, T. R. Defining the computational structure of the motion detector in Drosophila. Neuron 70, 1165–1177 (2011)

    Article  CAS  Google Scholar 

  20. Egelhaaf, M. & Borst, A. Calcium accumulation in visual interneurons of the fly: Stimulus dependence and relationship to membrane potential. J. Neurophysiol. 73, 2540–2552 (1995)

    Article  CAS  Google Scholar 

  21. Joesch, M., Plett, J., Borst, A. & Reiff, D. F. Response properties of motion-sensitive visual interneurons in the lobula plate of Drosophila melanogaster. Curr. Biol. 18, 368–374 (2008)

    Article  CAS  Google Scholar 

  22. Schnell, B. et al. Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. J. Neurophysiol. 103, 1646–1657 (2010)

    Article  CAS  Google Scholar 

  23. Borst, A. & Egelhaaf, M. Direction selectivity of fly motion-sensitive neurons is computed in a two-stage process. Proc. Natl Acad. Sci. USA 87, 9363–9367 (1990)

    Article  ADS  CAS  Google Scholar 

  24. Single, S., Haag, J. & Borst, A. Dendritic computation of direction selectivity and gain control in visual interneurons. J. Neurosci. 17, 6023–6030 (1997)

    Article  CAS  Google Scholar 

  25. Eichner, H., Joesch, M., Schnell, B., Reiff, D. F. & Borst, A. Internal structure of the fly elementary motion detector. Neuron 70, 1155–1164 (2011)

    Article  CAS  Google Scholar 

  26. Joesch, M., Weber, F., Eichner, H. & Borst, A. Functional specialization of parallel motion detection circuits in the fly. J. Neurosci. 33, 902–905 (2013)

    Article  CAS  Google Scholar 

  27. Egelhaaf, M. & Borst, A. Are there separate ON and OFF channels in fly motion vision? Vis. Neurosci. 8, 151–164 (1992)

    Article  CAS  Google Scholar 

  28. Takemura, S. Y., Lu, Z. & Meinertzhagen, I. A. Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J. Comp. Neurol. 509, 493–513 (2008)

    Article  Google Scholar 

  29. Euler, T., Detwiler, P. B. & Denk, W. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852 (2002)

    Article  ADS  CAS  Google Scholar 

  30. Pologruto, T. A., Sabatini, B. L. & Svoboda, K. ScanImage: Flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2, 13 (2003)

    Article  Google Scholar 

  31. Jenett, A. et al. A Gal4-driver line resource for Drosophila neurobiology. Cell Rep. 2, 991–1001 (2012)

    Article  CAS  Google Scholar 

  32. Reiff, D. F., Plett, J., Mank, M., Griesbeck, O. & Borst, A. Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila. Nature Neurosci. 13, 973–978 (2010)

    Article  CAS  Google Scholar 

  33. Euler, T. et al. Eyecup scope—optical recording of light stimulus-evoked fluorescence signals in the retina. Pfluger Arch. 457, 1393–1414 (2009)

    Article  CAS  Google Scholar 

  34. Reiser, M. B. & Dickinson, M. H. A modular display system for insect behavioral neuroscience. J. Neurosci. Methods 167, 127–139 (2008)

    Article  Google Scholar 

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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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Maisak, M., Haag, J., Ammer, G. et al. A directional tuning map of Drosophila elementary motion detectors. Nature 500, 212–216 (2013).

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