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Active flight increases the gain of visual motion processing in Drosophila

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.

References

  1. Strausfeld, N.J. Atlas of an Insect Brain 214 (Springer-Verlag, 1976).

  2. Taylor, G.K. & Krapp, H.G. Sensory systems and flight stability: what do insects measure and why? in Insect Mechanics and Control: Advances in Insect Physiology, Vol. 34 (eds. Casas, J. & Simpson, S.J.) 231–316 (Academic Press, London, 2007).

  3. 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).

    CAS  Article  PubMed  Google Scholar 

  4. Hausen, K. Decoding of retinal image flow in insects. Rev. Oculomot. Res. 5, 203–235 (1993).

    CAS  PubMed  Google Scholar 

  5. Krapp, H.G. & Wicklein, M. in The Senses: a Comprehensive Reference (eds. Basbaum, A.I., Kaneko, A. & Shepherd, G.M.) 131–204 (Academic Press, London, 2008).

  6. Balint, C.N. & Dickinson, M.H. The correlation between wing kinematics and steering muscle activity in the blowfly Calliphora vicina. J. Exp. Biol. 204, 4213–4226 (2001).

    CAS  PubMed  Google Scholar 

  7. Frye, M.A. in Avances in Invertebrate Neurobiology (eds Greenspan, R. & North, G.) (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2007).

  8. Gotz, K.G. Flight control in Drosophila by visual perception of motion. Kybernetik 6, 199–208 (1968).

    Article  Google Scholar 

  9. 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).

    PubMed  Google Scholar 

  10. Budick, S.A. & Dickinson, M.H. Free-flight responses of Drosophila melanogaster to attractive odors. J. Exp. Biol. 209, 3001–3017 (2006).

    Article  PubMed  Google Scholar 

  11. Wilson, R.I., Turner, G.C. & Laurent, G. Transformation of olfactory representations in the Drosophila antennal lobe. Science 303, 366–370 (2004).

    CAS  Article  PubMed  Google Scholar 

  12. 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).

    CAS  Article  PubMed  Google Scholar 

  13. Turner, G.C., Bazhenov, M. & Laurent, G. Olfactory representations by Drosophila mushroom body neurons. J. Neurophysiol. 99, 734–746 (2008).

    Article  PubMed  Google Scholar 

  14. Ramirez, J.M. & Pearson, K.G. Alteration of bursting properties in interneurons during locust flight. J. Neurophysiol. 70, 2148–2160 (1993).

    CAS  Article  PubMed  Google Scholar 

  15. Treue, S. & Maunsell, J.H. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 382, 539–541 (1996).

    CAS  Article  PubMed  Google Scholar 

  16. Schmidt, M.F. & Konishi, M. Gating of auditory responses in the vocal control system of awake songbirds. Nat. Neurosci. 1, 513–518 (1998).

    CAS  Article  PubMed  Google Scholar 

  17. Rowell, C.H.F. Variable responsiveness of a visual interneurone in the free-moving locust and its relation to behaviour and arousal. J. Exp. Biol. 55, 727–747 (1971).

    Google Scholar 

  18. Rind, F.C., Santer, R.D. & Wright, G.A. Arousal facilitates collision avoidance mediated by a looming sensitive visual neuron in a flying locust. J. Neurophysiol. 100, 670–680 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Rosner, R., Egelhaaf, M. & Warzecha, A.K. Behavioural state affects motion-sensitive neurones in the fly visual system. J. Exp. Biol. 213, 331–338 (2010).

    CAS  Article  PubMed  Google Scholar 

  20. Tomioka, K. & Yamaguchi, T. Response modification of cricket sensory interneurons during flight. Zoolog. Sci. 1, 169–186 (1984).

    Google Scholar 

  21. Hengstenberg, R. Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora. J. Comp. Physiol. A. Neuroethol. Sens. Neural Behav. Physiol. 149, 179–193 (1982).

    Article  Google Scholar 

  22. Scott, E.K., Raabe, T. & Luo, L. Structure of the vertical and horizontal system neurons of the lobula plate in Drosophila. J. Comp. Physiol. 454, 470–481 (2002).

    Google Scholar 

  23. Haag, J. & Borst, A. Neural mechanism underlying complex receptive field properties of motion-sensitive interneurons. Nat. Neurosci. 7, 628–634 (2004).

    CAS  Article  PubMed  Google Scholar 

  24. Krapp, H.G. & Hengstenberg, R. Estimation of self-motion by optic flow processing in single visual interneurons. Nature 384, 463–466 (1996).

    CAS  Article  PubMed  Google Scholar 

  25. Hausen, K. The lobula-complex of the fly: structure, function and significance in visual behavior. in Photoreception and Vision in Invertebrates (ed. Ali, M.A.) (Plenum Press, New York, 1984).

    Chapter  Google Scholar 

  26. Hengstenberg, R. Spike responses of nonspiking visual inter-neurone. Nature 270, 338–340 (1977).

    CAS  Article  PubMed  Google Scholar 

  27. Haag, J., Theunissen, F. & Borst, A. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells. 2. Active membrane properties. J. Comput. Neurosci. 4, 349–369 (1997).

    CAS  Article  PubMed  Google Scholar 

  28. Gotz, K.G. Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster. J. Exp. Biol. 128, 35–46 (1987).

    Google Scholar 

  29. Graetzel, C.F., Fry, S.N. & Nelson, B.J. A 6,000-Hz computer vision system for real-time wing beat analysis of Drosophila. in BioRob. The First IEEE/RAS-EMBS Internation Conference on Biomdeical Robotics and Biomechatronics 1–6 (Institute of Electrical and Electronics Engineers, Pisa, Italy, 2006).

  30. Heisenberg, M., Wonneberger, R. & Wolf, R. Optomotor-blindH31—a Drosophila mutant of the lobula plate giant neurons. J. Comp. Physiol. A. Neuroethol. Sens. Neural Behav. Physiol. 124, 287–296 (1978).

    Article  Google Scholar 

  31. Gordon, S. & Dickinson, M.H. Role of calcium in the regulation of mechanical power in insect flight. Proc. Natl. Acad. Sci. USA 103, 4311–4315 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. North, R.A. & Uchimura, N. 5-Hydroxytryptamine acts at 5-HT2 receptors to decrease potassium conductance in rat nucleus accumbens neurones. J. Physiol. (Lond.) 417, 1–12 (1989).

    CAS  Article  Google Scholar 

  33. Krapp, H.G., Hengstenberg, B. & Hengstenberg, R. Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. J. Neurophysiol. 79, 1902–1917 (1998).

    CAS  Article  PubMed  Google Scholar 

  34. Longden, K.D. & Krapp, H.G. State-dependent performance of optic-flow processing interneurons. J. Neurophysiol. 102, 3606–3618 (2009).

    Article  PubMed  Google Scholar 

  35. Busch, S., Selcho, M., Ito, K. & Tanimoto, H. A map of octopaminergic neurons in the Drosophila brain. J. Comp. Neurol. 513, 643–667 (2009).

    Article  PubMed  Google Scholar 

  36. Orchard, I., Ramirez, J.M. & Lange, A.B. A multifunctional role for octopamine in locust flight. Annu. Rev. Entomol. 38, 227–249 (1993).

    CAS  Article  Google Scholar 

  37. Brembs, B., Christiansen, F., Pfluger, H.J. & Duch, C. Flight initiation and maintenance deficits in flies with genetically altered biogenic amine levels. J. Neurosci. 27, 11122–11131 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Harris, R.A., O'Carroll, D.C. & Laughlin, S.B. Contrast gain reduction in fly motion adaptation. Neuron 28, 595–606 (2000).

    CAS  Article  PubMed  Google Scholar 

  39. Niven, J.E. & Laughlin, S.B. Energy limitation as a selective pressure on the evolution of sensory systems. J. Exp. Biol. 211, 1792–1804 (2008).

    CAS  Article  PubMed  Google Scholar 

  40. Fetcho, J.R., Higashijima, S. & McLean, D.L. Zebrafish and motor control over the last decade. Brain Res. Rev. 57, 86–93 (2008).

    Article  PubMed  Google Scholar 

  41. Benzer, S. Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc. Natl. Acad. Sci. USA 58, 1112–1119 (1967).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Liu, G. et al. Distinct memory traces for two visual features in the Drosophila brain. Nature 439, 551–556 (2006).

    CAS  Article  PubMed  Google Scholar 

  43. Neuser, K., Triphan, T., Mronz, M., Poeck, B. & Strauss, R. Analysis of a spatial orientation memory in Drosophila. Nature 453, 1244–1247 (2008).

    CAS  Article  PubMed  Google Scholar 

  44. Strausfeld, N.J., Sinakevitch, I. & Okamura, J.Y. Organization of local interneurons in optic glomeruli of the dipterous visual system and comparisons with the antennal lobes. Dev. Neurobiol. 67, 1267–1288 (2007).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  46. Maimon, G., Straw, A.D. & Dickinson, M.H. A simple vision-based algorithm for decision making in flying Drosophila. Curr. Biol. 18, 464–470 (2008).

    CAS  Article  PubMed  Google Scholar 

  47. Fry, S.N., Sayaman, R. & Dickinson, M.H. The aerodynamics of free-flight maneuvers in Drosophila. Science 300, 495–498 (2003).

    CAS  Article  PubMed  Google Scholar 

  48. Straw, A.D. & Dickinson, M.H. Motmot, an open-source toolkit for real-time video acquisition and analysis. Source Code Biol. Med. 4, 5 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Wilson, R.I. & Laurent, G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J. Neurosci. 25, 9069–9079 (2005).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Barry, P.H. & Lynch, J.W. Liquid junction potentials and small-cell effects in patch-clamp analysis. J. Membr. Biol. 121, 101–117 (1991).

    CAS  Article  PubMed  Google Scholar 

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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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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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