Motion-detecting circuits in flies: Coming into view

Annual Review of Neuroscience

Volumn 37, Issue , 2014, Pages 307-327

  Silies, Marion ^a   Gohl, Daryl M ^a   Clandinin, Thomas R ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Behavior; Drosophila; Evolution; Motion computation; Neurogenetics; Vision

Indexed keywords

ANIMAL BEHAVIOR; DROSOPHILA MELANOGASTER; INTERNEURON; MATHEMATICAL COMPUTING; NERVOUS SYSTEM; NEUROANATOMY; NONHUMAN; OPTIC LOBE; PHOTORECEPTOR; PRIORITY JOURNAL; REVIEW; VERTEBRATE; VISUOMOTOR COORDINATION; ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL MODEL; BRAIN; EVOLUTION; MOVEMENT PERCEPTION; NERVE TRACT; PHYSIOLOGY; VISUAL SYSTEM;

ANIMALS; BIOLOGICAL EVOLUTION; BRAIN; DROSOPHILA MELANOGASTER; MODELS, ANIMAL; MOTION PERCEPTION; NEURAL PATHWAYS; OPTIC LOBE, NONMAMMALIAN; VISUAL PATHWAYS;

EID: 84904612403     PISSN: 0147006X     EISSN: 15454126     Source Type: Book Series    
DOI: 10.1146/annurev-neuro-071013-013931     Document Type: Review

References (127)

1. Adelson EH, Bergen JR. 1985. Spatiotemporal energy models for the perception of motion. J. Opt. Soc. Am. A 2:284-99
2. Baccus SA,Olveczky BP,ManuM,MeisterM. 2008. A retinal circuit that computes objectmotion. J. Neurosci. 28:6807-17
3. Bahl A, Ammer G, Schilling T, Borst A. 2013. Object tracking in motion-blind flies. Nat. Neurosci. 16:730-38
4. Barlow HB, Levick WR. 1965. The mechanism of directionally selective units in rabbits retina. J. Physiol. 178:477-504
5. BarthM,HirschHV, Meinertzhagen IA, Heisenberg M.1997. Experience-dependent developmental plasticity in the optic lobe of Drosophila melanogaster. J. Neurosci. 17:1493-504
6. BarthM, SchultzeM, Schuster CM, Strauss R. 2010. Circadian plasticity in photoreceptor cells controls visual coding efficiency in Drosophila melanogaster. PLoS ONE 5:e9217
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
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
9. Bishop LG, Keehn DG. 1966. Two types of neurones sensitive to motion in the optic lobe of the fly. Nature 212:1374-76
10. Born RT, Bradley DC. 2005. Structure and function of visual area MT. Annu. Rev. Neurosci. 28:157-89
11. Borst A, Euler T. 2011. Seeing things in motion: models, circuits, and mechanisms. Neuron 71:974-94
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
13. Borst A, Haag J, Reiff DF. 2010. Fly motion vision. Annu. Rev. Neurosci. 33:49-70
14. Braitenberg V. 1970. Order and orientation of elements in the visual system of the fly. Kybernetik 7:235-42
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
16. Briggman KL, Helmstaedter M, Denk W. 2011. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471:183-88
17. Buchner E. 1976. Elementary movement detectors in an insect visual system. Biol. Cybernetics 24:85-101
18. Buchner E. 1984. Behavioural analysis of spatial vision in insects. In Photoreception and Vision in Invertebrates, ed. MA Ali, pp. 561-621. New York: Plenum
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
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
21. Card G, Dickinson MH. 2008. Visually mediated motor planning in the escape response of Drosophila. Curr. Biol. 18:1300-7
22. Chiappe ME, Seelig JD, Reiser MB, Jayaraman V. 2010. Walking modulates speed sensitivity in Drosophila motion vision. Curr. Biol. 20:1470-75
23. Chklovskii DB, Schikorski T, Stevens CF. 2002. Wiring optimization in cortical circuits. Neuron 34:341-47
24. Choe KM,ClandininTR. 2005. Thinking about visual behavior; learning about photoreceptor function. Curr. Top. Dev. Biol. 69:187-213
25. Clandinin TR, Zipursky SL. 2002. Making connections in the fly visual system. Neuron 35:827-41
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
27. Clark DA, Fitzgerald JE,Ales JM, GohlDM,SiliesMA, et al. 2014. Flies and humans share a motion estimation strategy that exploits natural scene statistics. Nat. Neurosci. 17:296-303
28. Clifford CW, Ibbotson MR. 2002. Fundamental mechanisms of visual motion detection: models, cells and functions. Prog. Neurobiol. 68:409-37
29. de Vries SE, Clandinin TR. 2012. Loom-sensitive neurons link computation to action in the Drosophila visual system. Curr. Biol. 22:353-62
30. 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. 16:4551-62
31. Duistermars BJ, Frye MA. 2008. Crossmodal visual input for odor tracking during fly flight. Curr. Biol. 18:270-75
32. Eckert H. 1981. The horizontal cells in the lobula plate of the blowfly, Phaenicia sericata. J. Comp. Physiol. 143:511-26
33. Egelhaaf M, Borst A. 1992. Are there separate ON and OFF channels in fly motion vision? Vis. Neurosci. 8:151-64
34. Egelhaaf M, Kern R, KrappHG, Kretzberg J,Kurtz R, Warzecha AK. 2002. Neural encoding of behaviourally relevant visual-motion information in the fly. Trends Neurosci. 25:96-102
35. Eichner H, Joesch M, Schnell B, Reiff DF, Borst A. 2011. Internal structure of the fly elementary motion detector. Neuron 70:1155-64
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
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
38. Fei H, Chow DM, Chen A, Romero-Calderon R, OngWS, et al. 2010. Mutation of the Drosophila vesicular GABA transporter disrupts visual figure detection. J. Exp. Biol. 213:1717-30
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
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
41. FotowatH, Fayyazuddin A, BellenHJ, Gabbiani F. 2009. A novel neuronal pathway for visually guided escape in Drosophila melanogaster. J. Neurophysiol. 102:875-85
42. Franceschini N, Riehle A, Le Nestour A. 1989. Directionally selective motion detection by insect neurons. See Stavenga and Hardie 1989, pp. 360-90
43. Freifeld L, Clark DA, Schnitzer MJ,HorowitzMA, Clandinin TR. 2013. GABAergic lateral interactions tune the early stages of visual processing in Drosophila. Neuron 78:1075-89
44. Fry SN, RohrseitzN, Straw AD, DickinsonMH. 2009. Visual control of flight speed in Drosophila melanogaster. J. Exp. Biol. 212:1120-30
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
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
47. Gollisch T, Meister M. 2010. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 65:150-64
48. Gotz KG. 1964. Optomotorische untersuchung des visuellen systems einiger augenmutanten der fruchtfliege Drosophila. Kybernetik 2:77-92
49. Gotz KG, Wenking H. 1973. Visual control of locomotion in the walking fruitfly Drosophila. J. Comp. Physiol. A 85:235-66
50. Haag J, Borst A. 2004. Neural mechanism underlying complex receptive field properties of motion-sensitive interneurons. Nat. Neurosci. 7:628-34
51. 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 101:16333-38
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
53. Haag J, Wertz A, Borst A. 2010. Central gating of fly optomotor response. Proc. Natl. Acad. Sci. USA 107:20104-9
54. Haikala V, Joesch M, Borst A, Mauss AS. 2013. Optogenetic control of fly optomotor responses. J. Neurosci. 33:13927-34
55. Hassenstein B, Reichardt W.1956. Systemtheoretische analyse der zeit-, reihenfolgen- und vorzeichenauswertung bei der bewegungsperzeption des r usselkafers chlorophanus. Z. Naturforschung B 11:513-24
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
57. Hecht S,Wald G. 1934. The visual acuity and intensity discrimination of Drosophila. J. Gen. Physiol. 17:517-47
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
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
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
62. Hildreth EC, Koch C. 1987. The analysis of visual motion: from computational theory to neuronal mechanisms. Annu. Rev. Neurosci. 10:477-533
63. Huston SJ, Krapp HG. 2008. Visuomotor transformation in the fly gaze stabilization system. PLoS Biol. 6:e173
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
65. Joesch M, Schnell B, Raghu SV, Reiff DF, Borst A. 2010. ON and OFF pathways in Drosophila motion vision. Nature 468:300-4
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
67. Johns DC, Marx R, Mains RE, ORourke B, Marban E. 1999. Inducible genetic suppression of neuronal excitability. J. Neurosci. 19:1691-97
68. Kalmus H. 1943. The optomotor responses of some eye mutants of Drosophila. J. Genet. 45:206-13
69. Katsov AY, Clandinin TR. 2008. Motion processing streams in Drosophila are behaviorally specialized. Neuron 59:322-35
70. Kitamoto T. 2001. Conditionalmodification of behavior in Drosophila by targeted expression of a temperaturesensitive shibire allele in defined neurons. J. Neurobiol. 47:81-92
71. Kolodziejczyk A, Sun X, Meinertzhagen IA, Nassel DR. 2008. Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system. PLoS ONE 3:e2110
72. Lai S-L, Lee T. 2006. Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9:703-9
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
74. Longden KD, Krapp HG. 2010. Octopaminergic modulation of temporal frequency coding in an identified optic flow-processing interneuron. Front. Syst. Neurosci. 4:153
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
76. Maimon G, Straw AD, Dickinson MH. 2010. Active flight increases the gain of visual motion processing in Drosophila. Nat. Neurosci. 13:393-99
77. Maisak MS,Haag J,AmmerG, Serbe E, MeierM, et al. 2013.Adirectional tuning map of Drosophila elementary motion detectors. Nature 500:212-16
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
79. Masland RH. 2012. The neuronal organization of the retina. Neuron 76:266-80
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
81. Meinertzhagen IA, ONeil SD. 1991. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J. Comp. Neurol. 305:232-63
82. Mizunami M, Weibrecht JM, Strausfeld NJ. 1998. Mushroom bodies of the cockroach: their participation in place memory. J. Comp. Neurol. 402:520-37
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
84. Morante J, Desplan C. 2008. The color-vision circuit in the medulla of Drosophila. Curr. Biol. 18:553-65
85. Morante J, Desplan C, Celik A. 2007. Generating patterned arrays of photoreceptors. Curr. Opin. Genet. Dev. 17:314-19
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
87. Nakayama K. 1985. Biological image motion processing: a review. Vision Res. 25:625-60
88. OCarroll DC, Bidwell NJ, Laughlin SB,Warrant EJ. 1996. Insect motion detectorsmatched to visual ecology. Nature 382:63-66
89. Ofstad TA, Zuker CS, Reiser MB. 2011. Visual place learning in Drosophila melanogaster. Nature 474:204-7
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
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
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
93. Raghu SV, Borst A. 2011. Candidate glutamatergic neurons in the visual system of Drosophila. PLoS ONE 6:e19472
94. Ramon y Cajal S, Sanchez D. 1915. Contribucion 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. In Sensory Communication, ed. WA Rosenblith, pp. 303-17. New York/London: MIT Press/Wiley
96. Reichardt W, Poggio T. 1975. Theory of pattern induced flight orientation of fly Musca domestica 0.2. Biol. Cybernet. 18:69-80
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
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
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
100. Sanes JR, Zipursky SL. 2010. Design principles of insect and vertebrate visual systems. Neuron 66:15-36
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
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
103. Seelig JD, Jayaraman V. 2013. Feature detection and orientation tuning in the Drosophila central complex. Nature 503:262-66
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
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
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
107. Stavenga DG, Hardie RC, eds. 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 and Hardie 1989, pp. 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
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
111. Straw AD, Branson K,Neumann TR,DickinsonMH. 2011. Multi-camera real-time three-dimensional tracking of multiple flying animals. J. R. Soc. Interface 8:395-409
112. Straw AD, Lee S, Dickinson MH. 2010. Visual control of altitude in flying Drosophila. Curr. Biol. 20:1550-56
113. Suver MP, Mamiya A, Dickinson MH. 2012. Octopamine neurons mediate flight-induced modulation of visual processing in Drosophila. Curr. Biol. 22:2294-302
114. Sweeney ST, Broadie K, Keane J, Niemann H, OKane CJ. 1995. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14:341-51
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
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
117. Takemura S-Y,LuZ, Meinertzhagen IA. 2008. Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J. Comp. Neurol. 509:493-513
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
119. Tammero LF, Frye MA, Dickinson MH. 2004. Spatial organization of visuomotor reflexes in Drosophila. J. Exp. Biol. 207:113-22
120. Tuthill JC, Chiappe ME, ReiserMB. 2011. Neural correlates of illusory motion perception in Drosophila. Proc. Natl. Acad. Sci. USA 108:9685-90
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
122. van Santen JP, Sperling G. 1984. Temporal covariance model of human motion perception. J. Opt. Soc. Am. A 1:451-73
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
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
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
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
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