1932

Abstract

Visual motion cues provide animals with critical information about their environment and guide a diverse array of behaviors. The neural circuits that carry out motion estimation provide a well-constrained model system for studying the logic of neural computation. Through a confluence of behavioral, physiological, and anatomical experiments, taking advantage of the powerful genetic tools available in the fruit fly , an outline of the neural pathways that compute visual motion has emerged. Here we describe these pathways, the evidence supporting them, and the challenges that remain in understanding the circuits and computations that link sensory inputs to behavior. Studies in flies and vertebrates have revealed a number of functional similarities between motion-processing pathways in different animals, despite profound differences in circuit anatomy and structure. The fact that different circuit mechanisms are used to achieve convergent computational outcomes sheds light on the evolution of the nervous system.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-071013-013931
2014-07-08
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/neuro/37/1/annurev-neuro-071013-013931.html?itemId=/content/journals/10.1146/annurev-neuro-071013-013931&mimeType=html&fmt=ahah

Literature Cited

  1. Adelson EH, Bergen JR. 1985. Spatiotemporal energy models for the perception of motion. J. Opt. Soc. Am. A 2:284–99 [Google Scholar]
  2. Baccus SA, Ölveczky BP, Manu M, Meister M. 2008. A retinal circuit that computes object motion. J. Neurosci. 28:6807–17 [Google Scholar]
  3. Bahl A, Ammer G, Schilling T, Borst A. 2013. Object tracking in motion-blind flies. Nat. Neurosci. 16:730–38 [Google Scholar]
  4. Barlow HB, Levick WR. 1965. The mechanism of directionally selective units in rabbit's retina. J. Physiol. 178:477–504 [Google Scholar]
  5. Barth M, Hirsch HV, Meinertzhagen IA, Heisenberg M. 1997. Experience-dependent developmental plasticity in the optic lobe of Drosophila melanogaster. J. Neurosci. 17:1493–504 [Google Scholar]
  6. Barth M, Schultze M, Schuster CM, Strauss R. 2010. Circadian plasticity in photoreceptor cells controls visual coding efficiency in Drosophila melanogaster. PLoS ONE 5:e9217 [Google Scholar]
  7. Bausenwein B, Dittrich AP, Fischbach KF. 1992. The optic lobe of Drosophila melanogaster. II. Sorting of retinotopic pathways in the medulla. Cell Tissue Res. 267:17–28 [Google Scholar]
  8. Bausenwein B, Fischbach KF. 1992. Activity labeling patterns in the medulla of Drosophila melanogaster caused by motion stimuli. Cell Tissue Res. 270:25–35 [Google Scholar]
  9. Bishop LG, Keehn DG. 1966. Two types of neurones sensitive to motion in the optic lobe of the fly. Nature 212:1374–76 [Google Scholar]
  10. Born RT, Bradley DC. 2005. Structure and function of visual area MT. Annu. Rev. Neurosci. 28:157–89 [Google Scholar]
  11. Borst A, Euler T. 2011. Seeing things in motion: models, circuits, and mechanisms. Neuron 71:974–94 [Google Scholar]
  12. Borst A, Haag J. 2002. Neural networks in the cockpit of the fly. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 188:419–37 [Google Scholar]
  13. Borst A, Haag J, Reiff DF. 2010. Fly motion vision. Annu. Rev. Neurosci. 33:49–70 [Google Scholar]
  14. Braitenberg V. 1970. Order and orientation of elements in the visual system of the fly. Kybernetik 7:235–42 [Google Scholar]
  15. Branson K, Robie AA, Bender J, Perona P, Dickinson MH. 2009. High-throughput ethomics in large groups of Drosophila. Nat. Methods 6:451–57 [Google Scholar]
  16. Briggman KL, Helmstaedter M, Denk W. 2011. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471:183–88 [Google Scholar]
  17. Buchner E. 1976. Elementary movement detectors in an insect visual system. Biol. Cybernetics 24:85–101 [Google Scholar]
  18. Buchner E. 1984. Behavioural analysis of spatial vision in insects. Photoreception and Vision in Invertebrates MA Ali, pp. 561–621 New York: Plenum [Google Scholar]
  19. Buchner E, Buchner S, Hengstenberg R. 1979. 2-Deoxy-D-glucose maps movement-specific nervous activity in the second visual ganglion of Drosophila. Science 205:687–88 [Google Scholar]
  20. Budick SA, Reiser MB, Dickinson MH. 2007. The role of visual and mechanosensory cues in structuring forward flight in Drosophila melanogaster. J. Exp. Biol. 210:4092–103 [Google Scholar]
  21. Card G, Dickinson MH. 2008. Visually mediated motor planning in the escape response of Drosophila. Curr. Biol. 18:1300–7 [Google Scholar]
  22. Chiappe ME, Seelig JD, Reiser MB, Jayaraman V. 2010. Walking modulates speed sensitivity in Drosophila motion vision. Curr. Biol. 20:1470–75 [Google Scholar]
  23. Chklovskii DB, Schikorski T, Stevens CF. 2002. Wiring optimization in cortical circuits. Neuron 34:341–47 [Google Scholar]
  24. Choe KM, Clandinin TR. 2005. Thinking about visual behavior; learning about photoreceptor function. Curr. Top. Dev. Biol. 69:187–213 [Google Scholar]
  25. Clandinin TR, Zipursky SL. 2002. Making connections in the fly visual system. Neuron 35:827–41 [Google Scholar]
  26. Clark DA, Bursztyn L, Horowitz MA, Schnitzer MJ, Clandinin TR. 2011. Defining the computational structure of the motion detector in Drosophila. Neuron 70:1165–77 [Google Scholar]
  27. Clark DA, Fitzgerald JE, Ales JM, Gohl DM, Silies MA. et al. 2014. Flies and humans share a motion estimation strategy that exploits natural scene statistics. Nat. Neurosci. 17:296–303 [Google Scholar]
  28. Clifford CW, Ibbotson MR. 2002. Fundamental mechanisms of visual motion detection: models, cells and functions. Prog. Neurobiol. 68:409–37 [Google Scholar]
  29. de Vries SE, Clandinin TR. 2012. Loom-sensitive neurons link computation to action in the Drosophila visual system. Curr. Biol. 22:353–62 [Google Scholar]
  30. Douglass JK, Strausfeld NJ. 1996. Visual motion-detection circuits in flies: parallel direction- and non-direction-sensitive pathways between the medulla and lobula plate. J. Neurosci. 16:4551–62 [Google Scholar]
  31. Duistermars BJ, Frye MA. 2008. Crossmodal visual input for odor tracking during fly flight. Curr. Biol. 18:270–75 [Google Scholar]
  32. Eckert H. 1981. The horizontal cells in the lobula plate of the blowfly, Phaenicia sericata. J. Comp. Physiol. 143:511–26 [Google Scholar]
  33. Egelhaaf M, Borst A. 1992. Are there separate ON and OFF channels in fly motion vision?. Vis. Neurosci. 8:151–64 [Google Scholar]
  34. Egelhaaf M, Kern R, Krapp HG, Kretzberg J, Kurtz R, Warzecha AK. 2002. Neural encoding of behaviourally relevant visual-motion information in the fly. Trends Neurosci. 25:96–102 [Google Scholar]
  35. Eichner H, Joesch M, Schnell B, Reiff DF, Borst A. 2011. Internal structure of the fly elementary motion detector. Neuron 70:1155–64 [Google Scholar]
  36. Emerson RC, Bergen JR, Adelson EH. 1992. Directionally selective complex cells and the computation of motion energy in cat visual cortex. Vision Res. 32:203–18 [Google Scholar]
  37. Erclik T, Hartenstein V, McInnes RR, Lipshitz HD. 2009. Eye evolution at high resolution: the neuron as a unit of homology. Dev. Biol. 332:70–79 [Google Scholar]
  38. Fei H, Chow DM, Chen A, Romero-Calderón R, Ong WS. et al. 2010. Mutation of the Drosophila vesicular GABA transporter disrupts visual figure detection. J. Exp. Biol. 213:1717–30 [Google Scholar]
  39. Fischbach K-F, Dittrich APM. 1989. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res. 258:441–75 [Google Scholar]
  40. Fitzgerald JE, Katsov AY, Clandinin TR, Schnitzer MJ. 2011. Symmetries in stimulus statistics shape the form of visual motion estimators. Proc. Natl. Acad. Sci. USA 108:12909–14 [Google Scholar]
  41. Fotowat H, Fayyazuddin A, Bellen HJ, Gabbiani F. 2009. A novel neuronal pathway for visually guided escape in Drosophila melanogaster. J. Neurophysiol. 102:875–85 [Google Scholar]
  42. Franceschini N, Riehle A, Le Nestour A. 1989. Directionally selective motion detection by insect neurons. See Stavenga & Hardie 1989 360–90
  43. Freifeld L, Clark DA, Schnitzer MJ, Horowitz MA, Clandinin TR. 2013. GABAergic lateral interactions tune the early stages of visual processing in Drosophila. Neuron 78:1075–89 [Google Scholar]
  44. Fry SN, Rohrseitz N, Straw AD, Dickinson MH. 2009. Visual control of flight speed in Drosophila melanogaster. J. Exp. Biol. 212:1120–30 [Google Scholar]
  45. Frye MA, Dickinson MH. 2004. Motor output reflects the linear superposition of visual and olfactory inputs in Drosophila. J. Exp. Biol. 207:123–31 [Google Scholar]
  46. Gohl DM, Silies MA, Gao XJ, Bhalerao S, Luongo FJ. et al. 2011. A versatile in vivo system for directed dissection of gene expression patterns. Nat. Methods 8:231–37 [Google Scholar]
  47. Gollisch T, Meister M. 2010. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 65:150–64 [Google Scholar]
  48. Götz KG. 1964. Optomotorische untersuchung des visuellen systems einiger augenmutanten der fruchtfliege Drosophila. Kybernetik 2:77–92 [Google Scholar]
  49. Götz KG, Wenking H. 1973. Visual control of locomotion in the walking fruitfly Drosophila. J. Comp. Physiol. A 85:235–66 [Google Scholar]
  50. Haag J, Borst A. 2004. Neural mechanism underlying complex receptive field properties of motion-sensitive interneurons. Nat. Neurosci. 7:628–34 [Google Scholar]
  51. Haag J, Denk W, Borst A. 2004. Fly motion vision is based on Reichardt detectors regardless of the signal-to-noise ratio. Proc. Natl. Acad. Sci. USA 101:16333–38 [Google Scholar]
  52. Haag J, Wertz A, Borst A. 2007. Integration of lobula plate output signals by DNOVS1, an identified premotor descending neuron. J. Neurosci. 27:1992–2000 [Google Scholar]
  53. Haag J, Wertz A, Borst A. 2010. Central gating of fly optomotor response. Proc. Natl. Acad. Sci. USA 107:20104–9 [Google Scholar]
  54. Haikala V, Joesch M, Borst A, Mauss AS. 2013. Optogenetic control of fly optomotor responses. J. Neurosci. 33:13927–34 [Google Scholar]
  55. Hassenstein B, Reichardt W. 1956. Systemtheoretische analyse der zeit-, reihenfolgen- und vorzeichenauswertung bei der bewegungsperzeption des rüsselkäfers chlorophanus. Z. Naturforschung B 11:513–24 [Google Scholar]
  56. Hausen K. 1982. Motion sensitive interneurons in the optomotor system of the fly. I. The horizontal cells: structure and signals. Biol. Cybern. 45:143–56 [Google Scholar]
  57. Hecht S, Wald G. 1934. The visual acuity and intensity discrimination of Drosophila. J. Gen. Physiol. 17:517–47 [Google Scholar]
  58. Heisenberg M, Buchner E. 1977. The role of retinula cell types in visual behavior of Drosophila melanogaster. J. Comp. Physiol. A 187:127–62 [Google Scholar]
  59. Heisenberg M, Wolf R. 1984. Vision in Drosophila: Genetics of Microbehavior Berlin: Springer-Verlag
  60. Heisenberg M, Wonneberger R, Wolf R. 1978. Optomotor-blindH31—a Drosophila mutant of the lobula plate giant neurons. J. Comp. Physiol. A 124:287–96 [Google Scholar]
  61. Helmstaedter M, Briggman KL, Turaga SC, Jain V, Seung HS, Denk W. 2013. Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 500:168–74 [Google Scholar]
  62. Hildreth EC, Koch C. 1987. The analysis of visual motion: from computational theory to neuronal mechanisms. Annu. Rev. Neurosci. 10:477–533 [Google Scholar]
  63. Huston SJ, Krapp HG. 2008. Visuomotor transformation in the fly gaze stabilization system. PLoS Biol. 6:e173 [Google Scholar]
  64. Joesch M, Plett J, Borst A, Reiff DF. 2008. Response properties of motion-sensitive visual interneurons in the lobula plate of Drosophila melanogaster. Curr. Biol. 18:368–74 [Google Scholar]
  65. Joesch M, Schnell B, Raghu SV, Reiff DF, Borst A. 2010. ON and OFF pathways in Drosophila motion vision. Nature 468:300–4 [Google Scholar]
  66. Joesch M, Weber F, Eichner H, Borst A. 2013. Functional specialization of parallel motion detection circuits in the fly. J. Neurosci. 33:902–5 [Google Scholar]
  67. Johns DC, Marx R, Mains RE, O'Rourke B, Marbán E. 1999. Inducible genetic suppression of neuronal excitability. J. Neurosci. 19:1691–97 [Google Scholar]
  68. Kalmus H. 1943. The optomotor responses of some eye mutants of Drosophila. J. Genet. 45:206–13 [Google Scholar]
  69. Katsov AY, Clandinin TR. 2008. Motion processing streams in Drosophila are behaviorally specialized. Neuron 59:322–35 [Google Scholar]
  70. Kitamoto T. 2001. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol. 47:81–92 [Google Scholar]
  71. Kolodziejczyk A, Sun X, Meinertzhagen IA, Nässel DR. 2008. Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system. PLoS ONE 3:e2110 [Google Scholar]
  72. Lai S-L, Lee T. 2006. Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9:703–9 [Google Scholar]
  73. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451–61 [Google Scholar]
  74. Longden KD, Krapp HG. 2010. Octopaminergic modulation of temporal frequency coding in an identified optic flow-processing interneuron. Front. Syst. Neurosci. 4:153 [Google Scholar]
  75. Luan H, Peabody NC, Vinson CR, White BH. 2006. Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 52:425–36 [Google Scholar]
  76. Maimon G, Straw AD, Dickinson MH. 2010. Active flight increases the gain of visual motion processing in Drosophila. Nat. Neurosci. 13:393–99 [Google Scholar]
  77. Maisak MS, Haag J, Ammer G, Serbe E, Meier M. et al. 2013. A directional tuning map of Drosophila elementary motion detectors. Nature 500:212–16 [Google Scholar]
  78. Marmarelis PZ, McCann GD. 1973. Development and application of white-noise modeling techniques for studies of insect visual nervous system. Kybernetik 12:74–89 [Google Scholar]
  79. Masland RH. 2012. The neuronal organization of the retina. Neuron 76:266–80 [Google Scholar]
  80. Meier M, Serbe E, Maisak MS, Haag J, Dickson BJ, Borst A. 2014. Neural circuit components of the Drosophila OFF motion vision pathway. Curr. Biol. 24:385–92 [Google Scholar]
  81. Meinertzhagen IA, O'Neil SD. 1991. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J. Comp. Neurol. 305:232–63 [Google Scholar]
  82. Mizunami M, Weibrecht JM, Strausfeld NJ. 1998. Mushroom bodies of the cockroach: their participation in place memory. J. Comp. Neurol. 402:520–37 [Google Scholar]
  83. Morante J, Desplan C. 2004. Building a projection map for photoreceptor neurons in the Drosophila optic lobes. Semin. Cell Dev. Biol. 15:137–43 [Google Scholar]
  84. Morante J, Desplan C. 2008. The color-vision circuit in the medulla of Drosophila. Curr. Biol. 18:553–65 [Google Scholar]
  85. Morante J, Desplan C, Celik A. 2007. Generating patterned arrays of photoreceptors. Curr. Opin. Genet. Dev. 17:314–19 [Google Scholar]
  86. Mu L, Ito K, Bacon JP, Strausfeld NJ. 2012. Optic glomeruli and their inputs in Drosophila share an organizational ground pattern with the antennal lobes. J. Neurosci. 32:6061–71 [Google Scholar]
  87. Nakayama K. 1985. Biological image motion processing: a review. Vision Res. 25:625–60 [Google Scholar]
  88. O'Carroll DC, Bidwell NJ, Laughlin SB, Warrant EJ. 1996. Insect motion detectors matched to visual ecology. Nature 382:63–66 [Google Scholar]
  89. Ofstad TA, Zuker CS, Reiser MB. 2011. Visual place learning in Drosophila melanogaster. Nature 474:204–7 [Google Scholar]
  90. Pfeiffer BD, Jenett A, Hammonds AS, Ngo TT, Misra S. et al. 2008. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl. Acad. Sci. USA 105:9715–20 [Google Scholar]
  91. Pfeiffer BD, Ngo TT, Hibbard KL, Murphy C, Jenett A. et al. 2010. Refinement of tools for targeted gene expression in Drosophila. Genetics 186:735–55 [Google Scholar]
  92. Pflugfelder GO, Roth H, Poeck B, Kerscher S, Schwarz H. et al. 1992. The lethal(1)optomotor-blind gene of Drosophila melanogaster is a major organizer of optic lobe development: isolation and characterization of the gene. Proc. Natl. Acad. Sci. USA 89:1199–203 [Google Scholar]
  93. Raghu SV, Borst A. 2011. Candidate glutamatergic neurons in the visual system of Drosophila. PLoS ONE 6:e19472 [Google Scholar]
  94. Ramón y Cajal S, Sanchez D. 1915. Contribución al Conocimiento de los Centros Nerviosos de los Insectos Madrid: Imprenta de Hijos de Nicholas Moja
  95. Reichardt W. 1961. Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. Sensory Communication WA Rosenblith 303–17 New York/London: MIT Press/Wiley [Google Scholar]
  96. Reichardt W, Poggio T. 1975. Theory of pattern induced flight orientation of fly Musca domestica 0.2. Biol. Cybernet. 18:69–80 [Google Scholar]
  97. Reiff DF, Plett J, Mank M, Griesbeck O, Borst A. 2010. Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila. Nat. Neurosci. 13:973–78 [Google Scholar]
  98. Rister J, Pauls D, Schnell B, Ting CY, Lee CH. et al. 2007. Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster. Neuron 56:155–70 [Google Scholar]
  99. Rivera-Alba M, Vitaladevuni SN, Mischenko Y, Lu Z, Takemura SY. et al. 2011. Wiring economy and volume exclusion determine neuronal placement in the Drosophila brain. Curr. Biol. 21:2000–5 [Google Scholar]
  100. Sanes JR, Zipursky SL. 2010. Design principles of insect and vertebrate visual systems. Neuron 66:15–36 [Google Scholar]
  101. Schnell B, Joesch M, Forstner F, Raghu SV, Otsuna H. et al. 2010. Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. J. Neurophysiol. 103:1646–57 [Google Scholar]
  102. Schnell B, Raghu SV, Nern A, Borst A. 2012. Columnar cells necessary for motion responses of wide-field visual interneurons in Drosophila. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 198:389–95 [Google Scholar]
  103. Seelig JD, Jayaraman V. 2013. Feature detection and orientation tuning in the Drosophila central complex. Nature 503:262–66 [Google Scholar]
  104. Shinomiya K, Karuppudurai T, Lin T-Y, Lu Z, Lee C-H. et al. 2014. Candidate neural substrates for off-edge motion detection in Drosophila. Curr. Biol. 24:1062–70 [Google Scholar]
  105. Silies M, Gohl DM, Fisher YE, Freifeld L, Clark DA, Clandinin TR. 2013. Modular use of peripheral input channels tunes motion-detecting circuitry. Neuron 79:111–27 [Google Scholar]
  106. Sombati S, Hoyle G. 1984. Generation of specific behaviors in a locust by local release into neuropil of the natural neuromodulator octopamine. J. Neurobiol. 15:481–506 [Google Scholar]
  107. Stavenga DG, Hardie RC. 1989. Facets of Vision Berlin: Springer-Verlag
  108. Strausfeld NJ. 1989. Beneath the compound eye: neuroanatomical analysis and physiological correlates in the study of insect vision. See Stavenga & Hardie 1989 317–59
  109. Strausfeld NJ, Campos-Ortega JA. 1973. The L4 monopolar neurone: a substrate for lateral interaction in the visual system of the fly Musca domestica (L.). Brain Res. 59:97–117 [Google Scholar]
  110. Strausfeld NJ, Gronenberg W. 1990. Descending neurons supplying the neck and flight motor of Diptera: organization and neuroanatomical relationships with visual pathways. J. Comp. Neurol. 302:954–72 [Google Scholar]
  111. Straw AD, Branson K, Neumann TR, Dickinson MH. 2011. Multi-camera real-time three-dimensional tracking of multiple flying animals. J. R. Soc. Interface 8:395–409 [Google Scholar]
  112. Straw AD, Lee S, Dickinson MH. 2010. Visual control of altitude in flying Drosophila. Curr. Biol. 20:1550–56 [Google Scholar]
  113. Suver MP, Mamiya A, Dickinson MH. 2012. Octopamine neurons mediate flight-induced modulation of visual processing in Drosophila. Curr. Biol. 22:2294–302 [Google Scholar]
  114. Sweeney ST, Broadie K, Keane J, Niemann H, O'Kane CJ. 1995. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14:341–51 [Google Scholar]
  115. Takemura S-Y, Bharioke A, Lu Z, Nern A, Vitaladevuni S. et al. 2013. A visual motion detection circuit suggested by Drosophila connectomics. Nature 500:175–81 [Google Scholar]
  116. Takemura S-Y, Karuppudurai T, Ting CY, Lu Z, Lee CH, Meinertzhagen IA. 2011. Cholinergic circuits integrate neighboring visual signals in a Drosophila motion detection pathway. Curr. Biol. 21:2077–84 [Google Scholar]
  117. Takemura S-Y, Lu Z, Meinertzhagen IA. 2008. Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J. Comp. Neurol. 509:493–513 [Google Scholar]
  118. Tammero LF, Dickinson MH. 2002. The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster. J. Exp. Biol. 205:327–43 [Google Scholar]
  119. Tammero LF, Frye MA, Dickinson MH. 2004. Spatial organization of visuomotor reflexes in Drosophila. J. Exp. Biol. 207:113–22 [Google Scholar]
  120. Tuthill JC, Chiappe ME, Reiser MB. 2011. Neural correlates of illusory motion perception in Drosophila. Proc. Natl. Acad. Sci. USA 108:9685–90 [Google Scholar]
  121. Tuthill JC, Nern A, Holtz SL, Rubin GM, Reiser MB. 2013. Contributions of the 12 neuron classes in the fly lamina to motion vision. Neuron 79:128–40 [Google Scholar]
  122. van Santen JP, Sperling G. 1984. Temporal covariance model of human motion perception. J. Opt. Soc. Am. A 1:451–73 [Google Scholar]
  123. Venken KJT, Simpson JH, Bellen HJ. 2011. Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron 72:202–30 [Google Scholar]
  124. Wardill TJ, List O, Li X, Dongre S, McCulloch M. et al. 2012. Multiple spectral inputs improve motion discrimination in the Drosophila visual system. Science 336:925–31 [Google Scholar]
  125. Wertz A, Borst A, Haag J. 2008. Nonlinear integration of binocular optic flow by DNOVS2, a descending neuron of the fly. J. Neurosci. 28:3131–40 [Google Scholar]
  126. Yonehara K, Farrow K, Ghanem A, Hillier D, Balint K. et al. 2013. The first stage of cardinal direction selectivity is localized to the dendrites of retinal ganglion cells. Neuron 79:1078–85 [Google Scholar]
  127. Zhu Y, Nern A, Zipursky SL, Frye MA. 2009. Peripheral visual circuits functionally segregate motion and phototaxis behaviors in the fly. Curr. Biol. 19:613–19 [Google Scholar]
/content/journals/10.1146/annurev-neuro-071013-013931
Loading
/content/journals/10.1146/annurev-neuro-071013-013931
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error