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Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila

Nature Neuroscience volume 13, pages 973–978 (2010)Cite this article

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Abstract

In the visual system of Drosophila, photoreceptors R1–R6 relay achromatic brightness information to five parallel pathways. Two of them, the lamina monopolar cells L1 and L2, represent the major input lines to the motion detection circuitry. We devised a new method for optical recording of visually evoked changes in intracellular Ca2+ in neurons using targeted expression of a genetically encoded Ca2+ indicator. Ca2+ in single terminals of L2 neurons in the medulla carried no information about the direction of motion. However, we found that brightness decrements (light-OFF) induced a strong increase in intracellular Ca2+ but brightness increments (light-ON) induced only small changes, suggesting that half-wave rectification of the input signal occurs. Thus, L2 predominantly transmits brightness decrements to downstream circuits that then compute the direction of image motion.

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Figure 1: Experimental approach used for the recording of visually evoked changes in Ca2+ in visual interneurons of Drosophila.
Figure 2: Visually evoked changes in Ca2+ in L2 axon terminals in the medulla of Drosophila.
Figure 3: Neural signature of drifting visual gratings.
Figure 4: Genetic interference with the circuitry suggests that signal processing in L2 neurons is largely, but not completely, independent of photoreceptor-to-lamina signaling in parallel processing pathways.

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References

  1. Tammero, L.F. & Dickinson, M.H. The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster. J. Exp. Biol. 205, 327–343 (2002).

    PubMed  Google Scholar 

  2. Heisenberg, M. & Wolf, R. On the structure of yaw torque in visual flight orientation of Drosophila melanogaster. J. Comp. Physiol. [A] 130, 113–130 (1979).

    Article  Google Scholar 

  3. Tammero, L.F. & Dickinson, M.H. Collision-avoidance and landing responses are mediated by separate pathways in the fruit fly, Drosophila melanogaster. J. Exp. Biol. 205, 2785–2798 (2002).

    Google Scholar 

  4. Mronz, M. & Lehmann, F.O. The free-flight response of Drosophila to motion of the visual environment. J. Exp. Biol. 211, 2026–2045 (2008).

    Article  Google Scholar 

  5. Borst, A. & Haag, J. Neural networks in the cockpit of the fly. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 188, 419–437 (2002).

    Article  CAS  Google Scholar 

  6. Clifford, C.W. & Ibbotson, M.R. Fundamental mechanisms of visual motion detection: models, cells and functions. Prog. Neurobiol. 68, 409–437 (2002).

    Article  CAS  Google Scholar 

  7. Rister, J. et al. Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster. Neuron 56, 155–170 (2007).

    Article  CAS  Google Scholar 

  8. Coombe, P.E. & Heisenberg, M. The structural brain mutant vacuolar medulla of Drosophila melanogaster with specific behavioral defects and cell degeneration in the adult. J. Neurogenet. 3, 135–158 (1986).

    Article  CAS  Google Scholar 

  9. Zhu, Y., Nern, A., Zipursky, S.L. & Frye, M.A. Peripheral visual circuits functionally segregate motion and phototaxis behaviors in the fly. Curr. Biol. 19, 613–619 (2009).

    Article  Google Scholar 

  10. Katsov, A.Y. & Clandinin, T.R. Motion processing streams in Drosophila are behaviorally specialized. Neuron 59, 322–335 (2008).

    Article  CAS  Google Scholar 

  11. Hassenstein, B. & Reichardt, W. Systemtheoretische Analyse einer Verhaltensweise (der Wechsel-Folgen-Reaktion des Rüsselkäfers Chlorophanus viridis). Verh. Dtsch. Zool. Ges. 7, 95–102 (1952).

    Google Scholar 

  12. Hassenstein, B. & Reichardt, W. Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus. Z. Naturforsch. [B] 11b, 513–524 (1956).

    Article  Google Scholar 

  13. Götz, K.G. Optomotorische Untersuchungen des visuellen Systems einiger Augenmutanten der Fruchtfliege Drosophila. Kybernetik 2, 77–92 (1964).

    Article  Google Scholar 

  14. van Doorn, A.J. & Koenderink, J.J. Temporal properties of the visual detectability of moving spatial white noise. Exp. Brain Res. 45, 179–188 (1982).

    Article  CAS  Google Scholar 

  15. Barlow, H.B. & Levick, W.R. The mechanism of directionally selective units in rabbit's retina. J. Physiol. (Lond.) 178, 477–504 (1965).

    Article  CAS  Google Scholar 

  16. van Santen, J.P.H. & Sperling, G. Temporal covariance model of human motion perception. J. Opt. Soc. Am. A 1, 451–473 (1984).

    Article  CAS  Google Scholar 

  17. Adelson, E.H. & Bergen, J.R. Spatiotemporal energy models for the perception of motion. J. Opt. Soc. Am. A 2, 284–299 (1985).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  19. 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 

  20. 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 

  21. 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 

  22. Franceschini, N., Riehle, A. & Le Nestour, A. Directionally selective motion detection by insect neurons. in Facets of Vision (eds. Stavenga, D.G. & Hardie, R.C.) Ch. 17, 360–390 (Springer-Verlag, Berlin, 1989).

  23. Riehle, A. & Franceschini, N. Motion detection in flies: parametric control over ON-OFF pathways. Exp. Brain Res. 54, 390–394 (1984).

    Article  CAS  Google Scholar 

  24. Ullman, S. The Interpretation of Visual Motion (MIT Press, Cambridge, Massachusetts, 1979).

  25. Anstis, S.M. & Rogers, B.J. Illusory reversals of visual depth and movement during changes in contrast. Vision Res. 15, 957–961 (1975).

    Article  CAS  Google Scholar 

  26. 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 

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

  28. 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 

  29. Meinertzhagen, I.A. & O'Neil, S.D. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J. Comp. Neurol. 305, 232–263 (1991).

    Article  CAS  Google Scholar 

  30. Gengs, C. et al. The target of Drosophila photoreceptor synaptic transmission is a histamine-gated chloride channel encoded by ort (hclA). J. Biol. Chem. 277, 42113–42120 (2002).

    Article  CAS  Google Scholar 

  31. Hardie, R.C. A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse. Nature 339, 704–706 (1989).

    Article  CAS  Google Scholar 

  32. Skingsley, D.R., Laughlin, S.B. & Hardie, R.C. Properties of histamine-activated chloride channels in the large monopolar cells of the dipteran compound eye: a comparative study. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 176, 611–623 (1995).

    Article  CAS  Google Scholar 

  33. Laughlin, S.B. & Osorio, D. Mechanism for neural signal enhancement in the blowfly compound eye. J. Exp. Biol. 144, 113–146 (1989).

    Google Scholar 

  34. Järvilehto, M. & Zettler, F. Electrophysiological-histological studies on some functional properties of visual cells and second order neurons of an insect retina. Z. Zellforsch. Mikrosk. Anat. 136, 291–306 (1973).

    Article  Google Scholar 

  35. Zettler, F. & Järvilehto, M. Lateral inhibition in an insect eye. Z. Vgl. Physiol. 76, 233–244 (1972).

    Article  Google Scholar 

  36. Zettler, F. & Järvilehto, M. Active and passive axonal propagation of non-spike signals in the retina of Calliphora. J. Comp. Physiol. 85, 89–104 (1973).

    Article  Google Scholar 

  37. Zettler, F. & Straka, H. Synaptic chloride channels generating hyperpolarizing on-responses in monopolar neurons of the blowfly visual system. J. Exp. Biol. 131, 435–438 (1987).

    Google Scholar 

  38. Zheng, L. et al. Feedback network controls photoreceptor output at the layer of first visual synapses in Drosophila. J. Gen. Physiol. 127, 495–510 (2006).

    Article  CAS  Google Scholar 

  39. Douglass, J.K. & Strausfeld, N.J. Visual motion detection circuits in flies: peripheral motion computation by identified small-field retinotopic neurons. J. Neurosci. 15, 5596–5611 (1995).

    Article  CAS  Google Scholar 

  40. 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 

  41. Buschbeck, E.K. & Strausfeld, N.J. Visual motion-detection circuits in flies: small-field retinotopic elements responding to motion are evolutionarily conserved across taxa. J. Neurosci. 16, 4563–4578 (1996).

    Article  CAS  Google Scholar 

  42. Mank, M. et al. A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat. Methods 5, 805–811 (2008).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  45. Wu, C.F. & Wong, F. Frequency characteristics in the visual system of Drosophila: genetic dissection of electroretinogram components. J. Gen. Physiol. 69, 705–724 (1977).

    Article  CAS  Google Scholar 

  46. Coombe, P.E. The large monopolar cells L1 and L2 are responsible for ERG transients in Drosophila. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 159, 655–665 (1986).

    Article  Google Scholar 

  47. Wässle, H. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5, 747–757 (2004).

    Article  Google Scholar 

  48. Molnar, A., Hsueh, H.A., Roska, B. & Werblin, F.S. Crossover inhibition in the retina: circuitry that compensates for nonlinear rectifying synaptic transmission. J. Comput. Neurosci. 27, 569–590 (2009).

    Article  Google Scholar 

  49. Rentería, R.C. et al. Intrinsic ON responses of the retinal OFF pathway are suppressed by the ON pathway. J. Neurosci. 26, 11857–11869 (2006).

    Article  Google Scholar 

  50. Chalasani, S.H. et al. Dissecting a circuit for olfactory behavior in Caenorhabditis elegans. Nature 450, 63–70 (2007).

    Article  CAS  Google Scholar 

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Acknowledgements

We are very grateful to W. Denk, M. Mueller and J. Tritthardt for supporting and troubleshooting 2PLSM; M. Joesch for providing Matlab code and discussion; J. Haag and B. Schnell for discussion and comments on the manuscript; W. Essbauer and C. Theile for technical assistance; T. Gollisch for comments on the manuscript; G. Miesenböck and L. Sjulsion for their input on the use of LEDs; and the members of the mechanics and electronics workshop of the MPI Martinsried for excellent support.

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Authors and Affiliations

  1. Max Planck Institute of Neurobiology, Martinsried, Germany

    Dierk F Reiff, Johannes Plett, Marco Mank, Oliver Griesbeck & Alexander Borst

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  1. Dierk F Reiff
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  3. Marco Mank
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Contributions

D.F.R. conceptualized the triggered stimulus presentation, J.P. designed and engineered the LED arena, M.M. and O.G. engineered TN-XXL, A.B. and D.F.R. designed experiments and wrote the manuscript, D.F.R. performed all of the fly work, imaging experiments and data analysis and prepared the figures.

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Correspondence to Dierk F Reiff.

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Reiff, D., Plett, J., Mank, M. et al. Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila. Nat Neurosci 13, 973–978 (2010). https://doi.org/10.1038/nn.2595

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