Fly motion vision

Annual Review of Neuroscience

Volumn 33, Issue , 2010, Pages 49-70

  Borst, Alexander ^a   Haag, Juergen ^a   Reiff, Dierk F ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

ego motion; lobula plate; motion detection; optic flow; receptive field; tangential cell

Indexed keywords

DROSOPHILA; FLOW KINETICS; GANGLION; HEAD MOVEMENT; LOCOMOTION; MOTION ANALYSIS SYSTEM; MOTONEURON; MOVEMENT PERCEPTION; NECK MUSCLE; NONHUMAN; OPTIC LOBE; PHOTORECEPTOR; PRIORITY JOURNAL; RECEPTIVE FIELD; REVIEW; SIMULATION;

ANIMALS; DROSOPHILA MELANOGASTER; FLIGHT, ANIMAL; MOTION PERCEPTION; OPTIC LOBE, NONMAMMALIAN; PSYCHOMOTOR PERFORMANCE;

EID: 77955000408     PISSN: 0147006X     EISSN: 15454126     Source Type: Book Series    
DOI: 10.1146/annurev-neuro-060909-153155     Document Type: Review

References (165)

1. Bausenwein B, Fischbach KF. 1992. Activity labeling patterns in the medulla of Drosophila melanogaster caused by motion stimuli. Cell Tissue Res. 270:25-35
2. Borst A. 1991. Fly visual interneurons responsive to image expansion. Zool. Jb. Physiol. 95:305-313
3. Borst A. 2003. Noise, not stimulus entropy, determines neural information rate. J. Comput. Neurosci. 14:23-31
4. Borst A. 2007. Correlation versus gradient type motion detectors-the pros and cons. Phil. Trans. R. Soc. B 362:369-374
5. Borst A. 2009. Drosophila's view on insect vision. Curr. Biol. 19:36-47
6. Borst A, Bahde S. 1986. What kind of movement detector is triggering the landing response of the housefly? Biol. Cybern. 55:59-69
7. Borst A, Bahde S. 1988a. Spatio-temporal integration of motion: a simple strategy for safe landing in flies. Naturwiss 75:265-267
8. Borst A, Bahde S. 1988b. Visual information processing in the fly's landing system. J. Comp. Physiol. A 163:167-173
9. Borst A, Egelhaaf M. 1989. Principles of visual motion detection. Trends Neurosci. 12:297-306
10. Borst A, Egelhaaf M. 1990. Direction selectivity of fly motion-sensitive neurons is computed in a two-stage process. Proc. Natl. Acad. Sci. USA 87:9363-9367
11. Borst A, Egelhaaf M. 1992. In vivo imaging of calcium accumulation in fly interneurons as elicited by visual motion stimulation. Proc. Natl. Acad. Sci. USA 89:4139-4143
12. Borst A, Egelhaaf M, Haag J. 1995. Mechanisms of dendritic integration underlying gain control in flymotionsensitive interneurons. J. Comput. Neurosci. 2:5-18
13. Borst A, Flanagin V, Sompolinsky H. 2005. Adaptation without parameter change: dynamic gain control in motion detection. Proc. Natl. Acad. Sci. USA 102:6172-6176
14. Borst A, Haag J. 1996. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells. I. Passive membrane properties. J. Comput. Neurosci. 3:313-336
15. Borst A, Haag J. 2001. Effect of mean firing on neural information rate. J. Comput. Neurosci. 10:213-221
16. Borst A, Haag J. 2002. Neural networks in the cockpit of the fly. J. Comp. Physiol. 188:419-437
17. Borst A, Reisenman C, Haag J. 2003. Adaptation of response transients in fly motion vision. II: Model studies. Vision Res. 43:1309-1322
18. Borst A, Single S. 2000. Local current spread in electrically compact neurons of the fly. Neurosci. Lett. 285:123-126
19. Braitenberg V. 1967. Patterns of projection in visual system of fly. 1. Retina-Lamina projections. Exp. Brain. Res. 3:271-298
20. Braitenberg V. 1970. Order and orientation of elements in the visual system of the fly. Kybernetik 7:235-242
21. Braitenberg V, Taddei Ferretti C. 1966. Landing reaction of Musca domestica induced by visual stimuli. Naturwiss 6:155
22. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415
23. Brenner N, BialekW, de Ruyter van Steveninck R. 2000. Adaptive rescaling maximizes information transmission. Neuron 26:695-702
24. Brotz T, Borst A. 1996. Cholinergic and GABAergic receptors on fly tangential cells and their role in visual motion detection. J. Neurophysiol. 76:1786-1799
25. Brotz T, Gundelfinger E, Borst A. 2001. Cholinergic and GABAergic pathways in fly motion vision. Bio. Med. Cent. Neurosci. 2:1
26. Buchner E. 1976. Elementary movement detectors in an insect visual system. Biol. Cybern. 24:86-101
27. Buchner E, Buchner S, Bülthoff I. 1984. Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. J. Comp. Physiol. A 155:471-483
28. Cajal SR, Sanchez D. 1915. Contribucion al Conocimiento de los Centros Nerviosos de los Insectos.Madrid: Imprenta de Hijos de Nicholas Moja
29. Chan WP, Prete F, Dickinson MH. 1998. Visual input to the efferent control system of a fly's "gyroscope." Science 280:289-292
30. Coggshall JC, Boschek CB, Buchner SM. 1973. Preliminary investigations on a pair of giant fibers in the central nervous system of dipteran flies. Z. Naturforsch. 28c:783-784
31. Cuntz H, Foerstner F, Haag J, Borst A. 2008. The morphological identity of insect dendrites. PLoS Comp. Biol. 4: doi:10.1371/journal.pcbi.1000251
32. Cuntz H, Haag J, Borst A. 2003. Neural image processing by dendritic networks. Proc. Natl. Acad. Sci. USA 100:11082-11085
33. Cuntz H, Haag J, Foerstner F, Segev I, Borst A. 2007. Robust coding of flow-field parameters by axo-axonal gap junctions between fly visual interneurons. Proc. Natl. Acad. Sci. USA 104:10229-10233
34. DeVoe RD. 1980. Movement sensitivities of cells in the fly's medulla. J. Comp. Physiol. A 138:93-119
35. Douglass JK, Strausfeld NJ. 1995. Visual motion detection circuits in flies: peripheral motion computation by identified small-field retinotopic neurons. J. Neurosci. 15:5596-5611
36. Douglass JK, Strausfeld NJ. 1996. Visual motion-detection circuits in flies: parallel direction- and nondirection-sensitive pathways between the medulla and lobula plate. J. Neurosci. 16:4551-4562
37. Dror RO, O'Carroll DC, Laughlin SB. 2001. Accuracy of velocity estimation by Reichardt correlators. J. Opt. Soc. Am. A 18:241-252
38. Eckert H. 1973. Optomotorische untersuchungen am visuellen system der stubenfliege musca domestica L. Kybernetik 14:1-23
39. Eckert H, Dvorak DR. 1983. The centrifugal horizontal cells in the lobula plate of the blowfly Phaenicia sericata. J. Insect Physiol. 29:547-560
40. Egelhaaf M, Borst A. 1989. Transient and steady-state response properties of movement detectors. J. Opt. Soc. Am. A 6:116-127
41. Egelhaaf M, Borst A. 1995. Calcium accumulation in visual interneurons of the fly: stimulus dependence and relationship to membrane potential. J. Neurophysiol. 73:2540-2552
42. Egelhaaf M, Borst A, Pilz B. 1990. The role of GABA in detecting visual motion. Brain Res. 509:156-160
43. Egelhaaf M, Borst A, Reichardt W. 1989. Computational structure of a biological motion detection system as revealed by local detector analysis in the fly's nervous system. J. Opt. Soc. Am. A 6:1070-1087
44. Egelhaaf M, Borst A, Warzecha AK, Wildemann A, Flecks S. 1993. Neural circuit tuning fly visual neurons to motion of small objects. II. Input organization of inhibitory circuit elements revealed by electrophysiological and optical recording techniques. J. Neurophysiol. 69:340-351
45. Elyada Y, Haag J, Borst A. 2009. Different receptive fields in axons and dendrites underlie robust coding in motion-sensitive neurons. Nat. Neurosci. 12:327-333
46. Farrow K, Borst A, Haag J. 2005. Sharing receptive fields with your neighbors: tuning the vertical system cells to wide field motion. J. Neurosci. 25:3985-3993
47. Farrow K, Haag J, Borst A. 2003. Input organization of multifunctional motion sensitive neurons in the blowfly. J. Neurosci. 23:9805-9811
48. Farrow K, Haag J, Borst A. 2006. Nonlinear, binocular interactions underlying flow field selectivity of a motion-sensitive neuron. Nat. Neurosci. 9:1312-1320
49. Fermi G, Reichardt W. 1963. Optomotorische reaktionen der fliege Musca domestica. Kybernetik 2:15-28
50. Ffrench-Constant RH, Roush RT, Mortlock D, Dively GP. 1990. Isolation of dieldrin resistance from field populations of Drosophila melanogaster (Diptera: Drosophilidae). J. Econ. Entomol. 83:1733-1737
51. Fischbach KF, Dittrich APM. 1989. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res. 258:441-475
52. Franz MO, Krapp HG. 2000. Wide-field, motion-sensitive neurons and matched filters for optic flow fields. Biol. Cybern. 83:185-197
53. Gauck V, Egelhaaf M, Borst A. 1997. Synapse distribution on VCH, an inhibitory, motion-sensitive interneuron in the fly visual system. J. Comp. Neurol. 381:489-499
54. Geiger G, NässelDR. 1981. Visual orientation behavior of flies after selective laser beam ablation of interneurons. Nature 293:398-399
55. Gengs CX, Leung HT, Skingsley DR, Iovchev MI, Yin Z, et al. 2002. The target of Drosophila photoreceptor synaptic transmission is a histamine-gated chloride channel encoded of ort (hclA). J. Biol. Chem. 277:42113-42120
56. Gibson JJ. 1950. Perception of the Visual World. Boston: Houghton Mifflin
57. Gilbert C, PenistenDK, DeVoe RD. 1991. Discrimination of visual motion from flicker by identified neurons in the medulla of the fleshfly Sarcophaga bullata. J. Comp. Physiol. A 168:653-673
58. Goetz KG. 1964. Optomotorische untersuchung des visuellen systems einiger augenmutanten der fruchtfliege Drosophila. Kybernetik 2:77-92
59. Goetz KG. 1965. Die optischenübertragungseigenschaften der komplexaugen von Drosophila. Kybernetik 2:215-221
60. Goetz KG. 1987. Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster. J. Exp. Biol. 128:35-46
61. Gronenberg W, Milde JJ, Strausfeld NJ. 1995. Oculomotor control in Calliphorid flies-organization of descending neurons to neck motor-neurons responding to visual-stimuli. J. Comp. Neurol. 361:267-284
62. Guerrero G, Reiff DF, Agarwal G, Ball RW, Borst A, et al. 2005. Heterogeneity in synaptic transmission along a Drosophila larval motor axon. Nat. Neurosci. 8:1188-1196
63. Haag J, BorstA. 1996. Amplification of high-frequency synaptic inputs by active dendritic membrane processes. Nature 379:639-641
64. Haag J, Borst A. 1997. Encoding of visual motion information and reliability in spiking and graded potential neurons. J. Neurosci. 17:4809-4819
65. Haag J, Borst A. 1998. Active membrane characteristics and signal encoding in graded potential neurons. J. Neurosci. 18:7972-7986
66. Haag J, Borst A. 2000. Spatial distribution and characteristics of voltage-gated calcium currents within visual interneurons. J. Neurophysiol. 83:1039-1051
67. Haag J, Borst A. 2001. Recurrent network interactions underlying flow-field selectivity of visual interneurons. J. Neurosci. 21:5685-5692
68. Haag J, Borst A. 2002. Dendro-dendritic interactions between motion-sensitive large-field neurons in the fly. J. Neurosci. 22:3227-3233
69. Haag J, Borst A. 2003. Orientation tuning of motion-sensitive neurons shaped by vertical-horizontal network interactions. J. Comp. Physiol. A 189:363-370
70. Haag J, Borst A. 2004. Neural mechanism underlying complex receptive field properties of motion-sensitive interneurons. Nat. Neurosci. 7:628-634
71. Haag J, Borst A. 2005. Dye-coupling visualizes networks of large-field motion-sensitive neurons in the fly. J. Comp. Physiol. A 191:445-454
72. Haag J, Borst A. 2007. Reciprocal inhibitory connections within a neural network for rotational optic-flow processing. Front. Neurosci. 1:111-121
73. Haag J, Borst A. 2008. Electrical coupling of lobula plate tangential cells to a heterolateral motion-sensitive neuron in the fly. J. Neurosci. 28:14435-14442
74. Haag J, Denk W, Borst A. 2004. Fly motion vision is based on Reichardt detectors regardless of the signalto- noise ratio. Proc. Natl. Acad. Sci. USA 101:16333-16338
75. Haag J, Egelhaaf M, Borst A. 1992. Dendritic integration of motion information in visual interneurons of the blowfly. Neurosci. Lett. 140:173-176
76. Haag J, Theunissen F, Borst A. 1997. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells. II. Active membrane properties. J. Comput. Neurosci. 4:349-369
77. Haag J, Vermeulen A, Borst A. 1999. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells. III. Visual response properties. J. Comput. Neurosci. 7:213-234
78. 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
79. Hardie RC. 1986. The photoreceptor array of the dipteran retina. Trends Neurosci. 9:419-423
80. Hardie RC. 1989. A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse. Nature 339:704-706
81. Hardie RC, Raghu P. 2001. Visual transduction in Drosophila. Nature 413:186-193
82. Hassenstein B. 1991. Freiburger Universitaetsblaetter. Freiburg, Germ.: Rombach
83. Hassenstein B, Reichardt W. 1956. Systemtheoretische analyze der zeit-, reihenfolgen- und vorzeichenauswertung bei der bewegungsperzeption des rüsselkäfers chlorophanus. Z. Naturforsch. 11b:513-524
84. Hatsopoulos N, Gabbiani F, Laurent G. 1995. Elementary computation of object approach by a wide-field neuron. Science 270:1000-1003
85. Hausen K. 1982a. Motion sensitive interneurons in the optomotor system of the fly. I. The horizontal cells: structure and signals. Biol. Cybern. 45:143-156
86. Hausen K. 1982b. Motion sensitive interneurons in the optomotor system of the fly. II. The horizontal cells: receptive field organization and response characteristics. Biol. Cybern. 46:67-79
87. Hausen K. 1984. The lobula-complex of the fly: structure, function and significance in visual behavior. In Photoreception and Vision in Invertebrates, ed. MA Ali, pp. 523-559 New York/London: Plenum
88. Hausen K, Wehrhahn C. 1983. Microsurgical lesion of horizontal cells changes optomotor yaw response in the blowfly Calliphora erythocephala. Proc. R. Soc. London Ser. B 219:211-216
89. Heisenberg M, Buchner E. 1977. The role of retinula cell types in visual behavior of Drosophila melanogaster. J. Comp. Physiol. A 117:127-162
90. Heisenberg M, Wolf R. 1984. Vision in Drosophila. Berlin, Heidelberg: Springer
91. Heisenberg M, Wonneberger R, Wolf R. 1978. Optomotor-blind (H31): a Drosophila mutant of the lobula plate giant neurons. J. Comp. Physiol. A 124:287-296
92. Hendel T, Mank M, Schnell B, Griesbeck O, Borst A, Reiff DF. 2008. Fluorescence changes of genetic calcium indicators and OGB-1 correlated with neural activity and calcium in vivo and in vitro. J. Neurosci. 28:7399-7411
93. Hengstenberg R. 1977. Spike response of "nonspiking" visual interneurone. Nature 270:338-340
94. Hengstenberg R. 1982. Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora. J. Comp. Physiol. A 149:179-193
95. Hengstenberg R, Hausen K, Hengstenberg B. 1982. The number and structure of giant vertical cells (VS) in the lobula plate of the blowfly Calliphora erytrocephala. J. Comp. Physiol. A 149:163-177
96. HorstmannW, Egelhaaf M, Warzecha AK. 2000. Synaptic interactions increase optic flow specificity. Eur. J. Neurosci. 12:2157-2165
97. Huston SJ., KrappHG. 2008. Visuomotor transformation in the fly gaze stabilization system. PLoS Biol. 6:e173
98. Jaervilehto M, Zettler F. 1971. Localized intracellular potentials from pre-and postsynaptic components in the external plexiform layer of an insect retina. Z. Vergl. Physiol. 75:422-440
99. 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. 18:368-374
100. Johansson G. 1973. Visual perception of biological motion and a model of its analysis. Percept. Psychophys. 14:201-211
101. Kalb J, Egelhaaf M, Kurtz R. 2006. Robust integration of motion information in the fly visual system revealed by single cell photoablation. J. Neurosci. 26:7898-7906
102. Karmeier K, Krapp HG, Egelhaaf M. 2005. Population coding of self-motion: applying Bayesian analysis to a population of visual interneurons in the fly. J. Neurophysiol. 94:2182-2194
103. Karmeier K, van Hateren JH, Kern R, Egelhaaf M. 2006. Encoding of naturalistic optic flow by a population of blowfly motion-sensitive neurons. J. Neurophysiol. 96:1602-1614
104. Katsov AY, Clandinin TR. 2008. Motion processing streams in Drosophila are behaviorally specialized. Neuron 59:322-335
105. Kirschfeld K. 1967. Die projektion der optischen umwelt auf das raster der rhabdomere im komplexauge von MUSCA. Exp. Brain Res. 3:248-270
106. Koenderink JJ, van Doorn AJ. 1987. Facts on optic flow. Biol. Cybern. 56:247-254
107. Krapp HG, Hengstenberg B, Hengstenberg R. 1998. Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. J. Neurophysiol. 79:1902-1917
108. Krapp HG, Hengstenberg R. 1996. Estimation of self-motion by optic flow processing in single visual interneurons. Nature 384:463-466
109. Kurtz R,Warzecha AK, Egelhaaf M. 2001. Transfer of visual motion information via graded synapses operates linearly in the natural activity range. J. Neurosci. 21:6957-6966
110. Laughlin SB, Hardie RC. 1978. Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J. Comp. Physiol. A 128:319-340
111. Laughlin SB, Howard J, Blakeslee B. 1987. Synaptic limitations to contrast coding in the retina of the blowfly Calliphora. Proc. R. Soc. London B 231:437-467
112. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461
113. Maimon G, Straw AD, Dickinson MH. 2010. Active flight increases the gain of visual motion processing in Drosophila. Nat. Neurosci. 13:393-399
114. Mank M, Ferr̃ao Santos A, Direnberger S, Mrsic-Flogel TD, Hofer SB, et al. 2008. A genetically encoded calcium indicator for chronic in vivo two photon imaging. Nat. Methods 5:805-811
115. Mank M, Reiff DF, Heim N, Friedrich MW, Borst A, et al. 2006. A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change. Biophys. J. 90:1790-1796
116. Mayer M, Vogtmann K, Bausenwein B, Wolf R, Heisenberg M. 1988. Flight control during free yaw turns' in Drosophila melanogaster. J. Comp. Physiol. A 163:389-399
117. Meinertzhagen IA, O'Neil SD. 1991. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J. Comp. Neurol. 305:232-263
118. Milde JJ, Seyan HS, Strausfeld NJ. 1987. The neckmotor system of the fly Calliphora erythrocephala. 2. Sensory organization. J. Comp. Physiol. A 160:225-238
119. Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, et al. 1997. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388:882-887
120. Moffat KG, Gould JH, Smith HK, O'Kane CJ. 1992. Inducible cell ablation in Drosophila by cold-sensitive Ricin A chain. Development 114:681-687
121. Mronz M, Lehmann FO. 2008. The free-flight response of Drosophila to motion of the visual environment. J. Exp. Biol. 211:2026-2045
122. Nalbach G, Hengstenberg R. 1994. The halteres of the blowflyCalliphora. II. Three-dimensional organization of compensatory reactions to real and simulated rotations. J. Comp. Physiol. A 175:695-708
123. OertnerTG, BrotzT, Borst A. 2001. Mechanisms of dendritic calcium signaling in fly neurons. J. Neurophysiol. 85:439-447
124. O'Tousa JE, Leonard DS, Pack WL. 1989. Morphological defects in oraJK84 photoreceptors caused by mutation in R1-6 opsin gene of Drosophila. J. Neurogenetics 6:14-52
125. Pfeiffer BD, Jenett A, Hammonds AS, Ngo TB, Misra S, et al. 2008. Tools for neuroanatomy and neurogenetics in Drosophila. Proc. Natl. Acad. Sci. USA 105:9715-9720
126. Raghu SV, Joesch M, Borst A, Reiff DF. 2007. Synaptic organization of lobula plate tangential cells in Drosophila: GABA-receptors and chemical release sites. J. Comp. Neurol. 502:598-610
127. Raghu SV, Joesch M, Sigrist S, Borst A, Reiff DF. 2009. Synaptic organization of lobula plate tangential cells in Drosophila: Dα7 cholinergic receptors. J. Neurogenetics 23:200-209
128. Reichardt W. 1961. Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. In Sensory Communication, ed. WA Rosenblith, pp. 303-317 New York/London: MIT Press/Wiley
129. Reichardt W. 1987. Evaluation of optical motion information by movement detectors. J. Comp. Physiol. A 161:533-547
130. Reichardt W, Poggio T. 1979. Figure-ground discrimination by relative movement in the visual system of the fly. Part I: Experimental results. Biol. Cybern. 35:81-100
131. Reiff DF, Ihring A, Guerrero G, Isacoff EY, Joesch M, et al. 2005. In vivo performance of genetically encoded indicators of neural activity in flies. J. Neurosci. 25:4766-4778
132. Reisenman C, Haag J, Borst A. 2003. Adaptation of response transients in fly motion vision. I: Experiments. Vision Res. 43:1291-1307
133. Rind FC, Simmons PJ. 1992. Orthopteran DCMD neuron-a reevaluation of responses to moving objects. 1. Selective responses to approaching objects. J. Neurophysiol. 5:1654-1666
134. 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 56:155-170
135. Safran M, Flanagin V, Borst A, Sompolinsky H. 2007. Adaptation and information transmission in fly motion detection. J. Neurophysiol. 98:3309-3320
136. Sanchez-SorianoN, BottenbergW, Fiala A, Haessler U, Kerassoviti A, et al. 2005. Are dendrites in Drosophila homologous to vertebrate dendrites? Dev. Biol. 288:126-138
137. Schilstra C, van Hateren JH. 1999. Blowfly flight and optic flow. II. Head movement during flight. J. Exp. Biol. 202:1491-1500
138. Schnell B, Joesch M, Foerstner F, Raghu SV, Otsuna H, et al. 2010. Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. J. Neurophysiol. 103:1646-1657
139. Scott EK, Raabe T, Luo L. 2002. Structure of the vertical and horizontal system neurons of the lobula plate in Drosophila. J. Comp. Neurol. 454:470-481
140. Sherman A, Dickinson MH. 2002. A comparison of visual and haltere-mediated equilibrium reflexes in the fruit fly Drosophila melanogaster. J. Exp. Biol. 206:295-302
141. Shi L, Borst A. 2006. Propagation of photon noise and information transfer in motion vision. J. Comput. Neurosci. 20:167-178
142. Single S, Borst A. 1998. Dendritic integration and its role in computing image velocity. Science 281:1848-1850
143. Single S, Borst A. 2002. Different mechanisms of calcium entry within different dendritic compartments. J. Neurophysiol. 87:1616-1624
144. Single S, Haag J, Borst A. 1997. Dendritic computation of direction selectivity and gain control in visual interneurons. J. Neurosci. 17:6023-6030
145. Straka H, Ammermüller J. 1991. Temporal resolving power of blowfly visual system: effects of decamethonium and hyperpolarization on responses of laminar monopolar neurons. J. Comp. Physiol. A 168:129-139
146. Strausfeld NJ. 1970. Golgi studies on insects. 2. Optic lobes of diptera. Phil.Trans. R. Soc. London B 258:135-223
147. Strausfeld NJ. 1976. Atlas of an Insect Brain. Berlin/Heidelberg: Springer
148. Strausfeld NJ, BassemirUK. 1985. Lobula plate and ocellar interneurons converge onto a cluster of descending neurons leading to neck and leg motor neuropil in Calliphora-Erythrocephala. Cell Tissue Res. 240:617-640
149. Strausfeld NJ, Lee JK. 1991. Neuronal basis for parallel visual processing in the fly. Vis. Neurosci. 7:13-33
150. Strausfeld NJ, Seyan HS. 1985. Convergence of visual, haltere and prosternal inputs at neck motor neurons of Calliphora erythrocephala. Cell Tissue Res. 240:601-615
151. Strausfeld NJ, Seyan HS,Milde JJ. 1987. The neckmotor system of the fly Calliphora erythrocephala. 1. Muscles and motor neurons. J. Comp. Physiol. A 160:205-224
152. Straw AD, RainsfordT,O'Carroll DC. 2008. Contrast sensitivity of insectmotion detectors to natural images. J. Vision 8:1-9
153. Takemura SY, Lu Z,Meinertzhagen IA. 2008. Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J. Comp. Neurol. 509:493-513
154. Trujillo-Cenoz O, Melamed J. 1966. Compound eye of dipterans: anatomical basis for integration-an electron microscopic study. J. Ultrastruct. Res. 16:395-398
155. van der Bliek AM, Meyerowitz EM. 1991. Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351:411-414
156. Vigier P. 1908. Mecanisme de la synthese des impressions lumineuses receuellies par les yeux compose des Diptereres. C. R. Soc. Biol. Paris 64:1221-1223
157. WangT, MontellC. 2007. Phototransduction and retinal degeneration in Drosophila. PflugersArch. 454:821-847
158. Weber F, Eichner H, Cuntz H, Borst A. 2008. Eigenanalysis of a neural network for optic flow processing. New J. Phys. 10:1-21
159. Wernet MF,Mazzoni EO, Celik A, Duncan DM, Duncan I, Desplan C. 2006. Stochastic spikeless expression creates the retinal mosaic for color vision. Nature 440:174-180
160. Wertz A, Borst A, Haag J. 2008. Nonlinear integration of binocular optic flow by DNOVS2, a descending neuron of the fly. J. Neurosci. 28:3131-3140
161. Wertz A, Gaub B, Plett J, Haag J, Borst A. 2009. Robust coding of ego-motion in descending neurons of the fly. J. Neurosci. 29:14993-15000
162. Wertz A, Haag J, Borst A. 2009. Local and global motion preferences in descending neurons of the fly. J. Comp. Physiol. A 195:1107-1120
163. Yamaguchi S, Wolf R, Desplan C, Heisenberg M. 2008. Motion vision is independent of color in Drosophila. Proc. Natl. Acad. Sci. USA 105:4910-4915
164. Zheng L, Nikolaev A, Wardill TJ, O'Kane CJ, de Polavieja GG, Juusola M. 2009. Network adaptation improves temporal representation of naturalistic stimuli in Drosophila eye: I. Dynamics. PLoS One 4(1):e4307
165. Zhu Y, Nem A, Zipursky SL, Frye MA. 2009. Peripheral visual circuits functionally segregate motion and phototaxis behaviors in the fly. Curr. Biol. 19:1-7