So many pieces, one puzzle: Cell type specification and visual circuitry in flies and mice

Genes and Development

Volumn 28, Issue 23, 2014, Pages 2565-2584

  Wernet, Mathias F ^a,b,c   Huberman, Andrew D ^d,e   Desplan, Claude ^b,c  

^a STANFORD UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY ABU DHABI   (United Arab Emirates)

^c NEW YORK UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell types; Circuitry; Function; Vision

Indexed keywords

MUS;

ANIMAL; ANIMAL BEHAVIOR; ANIMAL MODEL; CELL DIFFERENTIATION; CYTOLOGY; DROSOPHILA; EMBRYOLOGY; GENETICS; MOUSE; PHYSIOLOGY; RETINA; VISION;

ANIMALS; BEHAVIOR, ANIMAL; CELL DIFFERENTIATION; DROSOPHILA; MICE; MODELS, ANIMAL; RETINA; VISION, OCULAR; VISUAL PERCEPTION;

EID: 84914125463     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.248245.114     Document Type: Review

References (176)

1. Applebury ML, Antoch MP, Baxter LC, Chun LL, Falk JD, Farhangfar F, Kage K, Krystolik MG, Lyass LA, Robbins JT. 2000. The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27: 513-523.
2. Badea TC, Cahill H, Hattar S, Nathans J. 2009. Distinct roles of transcription factors brn3a and brn3b in controlling the development, morphology, and function of retinal ganglion cells. Neuron 61: 852-864.
3. Baden T, Schubert T, Chang L, Wei T, Zaichuk M, Wissinger B, Euler T. 2013. A tale of two retinal domains: near-optimal sampling of achromatic contrasts in natural scenes through asymmetric photoreceptor distribution. Neuron 80: 1206-1217.
4. Baker M. 2013. Neuroscience: through the eyes of a mouse. Nature 502: 156-158.
5. Bausenwein B, Fischbach KF. 1992. Activity labeling patterns in the medulla of Drosophila melanogaster caused by motion stimuli. Cell Tissue Res 270: 25-35.
6. 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.
7. Bayraktar OA, Doe CQ. 2013. Combinatorial temporal patterning in progenitors expands neural diversity. Nature 498: 449- 455.
8. Behnia R, Clark DA, Carter AG, Clandinin TR, Desplan C. 2014. Processing properties of ON and OFF pathways for Drosophila motion detection. Nature 512: 427-430.
9. Berson DM, Dunn FA, Takao M. 2002. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295: 1070-1073.
10. Bertet C, Li X, Erclik T, Cavey M, Wells B, Desplan C. 2014. Temporal patterning of neuroblasts controls notch-mediated cell survival through regulation of Hid or Reaper. Cell 158: 1173-1186.
11. Borst A. 2014. Neural circuits for elementary motion detection. J Neurogenet 10: 1-13.
12. Borst A, Euler T. 2011. Seeing things in motion: models, circuits, and mechanisms. Neuron 71: 974-994.
13. Briggman KL, Helmstaedter M, Denk W. 2011. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471: 183-188.
14. Buchner E, Buchner S, Bülthoff I. 1984. Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 155: 471-483.
15. Busse L, Ayaz A, Dhruv NT, Katzner S, Saleem AB, Schölvinck ML, Zaharia AD, Carandini M. 2011. The detection of visual contrast in the behaving mouse. J Neurosci 31: 11351-11361.
16. Campos-Ortega A, Hofbauer A. 1990. Proliferation pattern and early differentiation of the optic lobes in Drosophila melanogaster. Rouxs Arch Dev Biol 198: 264-274.
17. Cepko C. 2014. Intrinsically different retinal progenitor cells produce specific types of progeny. Nat Rev Neurosci 15: 615-627.
18. Chalupa LM, Werner JS. 2004 The visual neurosciences, volumes 1 and 2. MIT Press, Cambridge.
19. Chen SK, Badea TC, Hattar S. 2011. Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature 476: 92-95.
20. Chou WH, Hall KJ, Wilson DB, Wideman CL, Townson SM, Chadwell LV, Britt SG. 1996. Identification of a novel Drosophila opsin reveals specific patterning of the R7 and R8 photoreceptor cells. Neuron 17: 1101-1115.
21. Chou WH, Huber A, Bentrop J, Schulz S, Schwab K, Chadwell LV, Paulsen R, Britt SG. 1999. Patterning of the R7 and R8 photoreceptor cells of Drosophila: evidence for induced and default cell-fate specification. Development 126: 607-616.
22. Clark DA, Bursztyn L, Horowitz MA, Schnitzer MJ, Clandinin TR. 2011. Defining the computational structure of the motion detector in Drosophila. Neuron 70: 1165-1177.
23. Colonques J, Ceron J, Tejedor FJ. 2007. Segregation of postembryonic neuronal and glial lineages inferred from a mosaic analysis of the Drosophila larval brain. Mech Dev 124: 327- 340.
24. Cruz-Martín A, El-Danaf RN, Osakada F, Sriram B, Dhande OS, Nguyen PL, Callaway EM, Ghosh A, Huberman AD. 2014. A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex. Nature 507: 358-361.
25. Delogu A, Sellers K, Zagoraiou L, Bacianowska-Zbrog A, Mandal S, Guimera J, Rubenstein JL, Sugden D, Jessell TM, Lumsden A. 2012. Subcortical visual shell nuclei targeted by ipRGCs develop from a Sox14-GABAergic progenitor and require Sox14 to regulate daily activity rhythms. Neuron 75: 648- 662.
26. Demb JB. 2007. Cellular mechanisms for direction selectivity in the retina. Neuron 55: 179-186.
27. de Vries SE, Clandinin TR. 2012. Loom-sensitive neurons link computation to action in the Drosophila visual system. Curr Biol 22: 353-362.
28. Dhande OS, Huberman AD. 2014. Retinal ganglion cell maps in the brain: implications for visual processing. Curr Opin Neurobiol 24: 133-142.
29. Dhande OS, Estevez ME, Quattrochi LE, El-Danaf RN, Nguyen PL, Berson DM, Huberman AD. 2013. Genetic dissection of retinal inputs to brainstem nuclei controlling image stabilization. J Neurosci 33: 17797-17813.
30. Douglass JK, Strausfeld NJ. 2000. Optic flow representation in the optic lobes of Diptera: modeling the role of T5 directional tuning properties. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 186: 783-797.
31. Douglass JK, Strausfeld NJ. 2003. Anatomical organization of retinotopic motion-sensitive pathways in the optic lobes of flies. Microsc Res Tech 62: 132-150.
32. Duan X, Krishnaswamy A, De la Huerta I, Sanes JR. 2014. Type II cadherins guide assembly of a direction-selective retinal circuit. Cell 158: 793-807.
33. Dyer MA, Livesey FJ, Cepko CL, Oliver G. 2003. Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina. Nat Genet 34: 53-58.
34. Ecker JL, Dumitrescu ON, Wong KY, Alam NM, Chen SK, LeGates T, Renna JM, Prusky GT, Berson DM, Hattar S. 2010. Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 67: 49-60.
35. Egger B, Gold KS, Brand AH. 2011. Regulating the balance between symmetric and asymmetric stem cell division in the developing brain. Fly (Austin) 5: 237-241.
36. Eichner H, Joesch M, Schnell B, Reiff DF, Borst A. 2011. Internal structure of the fly elementary motion detector. Neuron 70: 1155-1164.
37. Estevez ME, Fogerson PM, Ilardi MC, Borghuis BG, Chan E, Weng S, Auferkorte ON, Demb JB, Berson DM. 2012. Form and function of the M4 cell, an intrinsically photosensitive retinal ganglion cell type contributing to geniculocortical vision. J Neurosci 32: 13608-13620.
38. Euler T, Detwiler PB, Denk W. 2002. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418: 845-852.
39. Feng L, Xie X, Joshi PS, Yang Z, Shibasaki K, Chow RL, Gan L. 2006. Requirement for Bhlhb5 in the specification of amacrine and cone bipolar subtypes in the mouse retina. Development 133: 4815-4825.
40. Field GD, Chichilnisky EJ. 2007. Information processing in the retina: circuitry and coding. Annu Rev Neurosci 30: 1-30.
41. Field GD, Gauthier JL, Sher A, Greschner M, Machado TA, Jepson LH, Shlens J, Gunning DE, Matieson K, DabrowskiW, et al. 2010. Functional connectivity in the retina at the resolution of photoreceptors. Nature 467: 673-677.
42. 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.
43. Fischbach KF, Hiesinger PR. 2008. Optic lobe development. Adv Exp Med Biol 628: 115-136.
44. Franceschini N, Kirschfeld K, Minke B. 1981. Fluorescence of photoreceptor cells observed in vivo. Science 213: 1264- 1267.
45. 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- 1089.
46. Fried SI, Münch TA, Werblin FS. 2002. Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420: 411-414.
47. Fuerst PG, Koizumi A, Masland RH, Burgess RW. 2008. Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 451: 470-474.
48. Fuerst PG, Bruce F, Tian M, WeiW, Elstrott J, Feller MB, Erskine L, Singer JH, Burgess RW. 2009. DSCAM and DSCAML1 function in self-avoidance in multiple cell types in the developing mouse retina. Neuron 64: 484-497.
49. Fujitani Y, Fujitani S, Luo H, Burlison J, Long Q, Kawaguchi Y, Edlund H, MacDonal RJ, Furukawa T, Fujikado T, et al. 2006. Ptf1a determines horizontal and amacrine cell fates during mouse retinal development. Development 133: 4439-4450.
50. Gao S, Takemura SY, Ting CY, Huang S, Lu Z, Luan H, Rister J, Thum AS, Yang M, Hong ST, et al. 2008. The neural substrate of spectral preference in Drosophila. Neuron 60: 328-342.
51. Glickfield LL, Histed MH, Maunsell JH. 2013. Mouse primary visual cortex is used to detect both orientation and contrast changes. J Neurosci 33: 19416-19422.
52. Gordon JA, Stryker MP. 1996. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J Neurosci 16: 3274-3286.
53. Gohl DM, Silies MA, Gao XJ, Bhalerao S, Luongo FJ, Lin CC, Potter CJ, Clandinin TR. 2011. A versatile in vivo system for directed dissection of gene expression patterns. Nat Methods 8: 231-237.
54. Goz D, Studholme K, Lappi DA, Rollag MD, Provencio I, Morin LP. 2008. Targeted destruction of photosensitive retinal ganglion cells with a saporin conjugate alters the effects of light on mouse circadian rhythms. PLoS ONE 3: e3153.
55. Güler AD, Ecker JL, Lall GS, Haq S, Altimus CM, Liao HW, Barnard AR, Cahill H, Badea TC, Zhao H, et al. 2008. Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 453: 102-105.
56. Haikala V, Joesch M, Borst A, Mauss AS. 2013. Optogenetic control of fly optomotor responses. J Neurosci 33: 13927- 13934.
57. Hanesch U, Fischbach KF, Heisenberg M. 1989. Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 257: 343-366.
58. Hardie RC. 1985. Functional organization of the fly retina. In Progress in sensory physiology, (ed. H. Autrum, et al.), pp 1- 79. Springer, Berlin.
59. Hasegawa E, Kitada Y, Kaido M, Takayama R, Awasaki T, Tabata T, Sato M. 2011. Concentric zones, cell migration and neuronal circuits in the Drosophila visual center. Development 138: 983-993.
60. Hasegawa E, Kaido M, Takayama R, Sato M. 2013. Brainspecific- homeobox is required for the specification of neuronal types in the Drosophila optic lobe. Dev Biol 377: 90-99.
61. Hassenstein B, Reichardt W. 1956. Systemtheoretische analyse der zeit, reihenfolgen und vorzeichenauswertung bei der bewegungsperzeption des rüsselkiifers Chlorophanus. Z Naturforsch IIb: 513-524.
62. Hatori M, Le H, Vollmers C, Keding SR, Tanaka N, Buch T, Waisman A, Schmedt C, Jegla T, Panda S. 2008. Inducible ablation of melanopsin-expressing retinal ganglion cells reveals their central role in non-image forming visual responses. PLoS ONE 3: 1-10.
63. Hattar S, Liao HW, Takao M, Berson DM, Yau KW. 2002. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295: 1065-1070.
64. Hattar S, Lucas RJ, Mrosovsky N, Thompson S, Douglas RH, Hankins MW, Lem J, Biel M, Hofmann F, Foster RG, et al. 2003. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424: 76-81.
65. Hattori D, Millard SS, Wojtowicz WM, Zipursky SL. 2008. Dscam-mediated cell recognition regulates neural circuit formation. Annu Rev Cell Dev Biol 24: 597-620.
66. Haverkamp S, Wassle H, Duebel J, Kuner T, Augustine GJ, Feng G, Euler T. 2005. The primordial, blue-cone color system of the mouse retina. J Neurosci 25: 5438-5445.
67. Heisenberg M, Buchner E. 1977. The role of retinula cell types in visual behavior of Drosophila melanogaster. J Comp Physiol 117: 127-162.
68. 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: 168-174.
69. Hiesinger PR, Zhai RG, Zhou Y, Koh TW, Mehta SQ, Schulze KL, Cao Y, Verstreken P, Clandinin TR, Fischbach KF, et al. 2006. Activity-independent prespecification of synaptic partners in the visual map of Drosophila. Curr Biol 16: 1835- 1843.
70. Hobert O, Carrera I, Stefanakis N. 2010. The molecular and gene regulatory signature of a neuron. Trends Neurosci 33: 435- 445.
71. Huberman AD, Niell CM. 2011. What can mice tell us about how vision works? Trends Neurosci 34: 464-473.
72. Huberman AD, Manu M, Koch SM, Susman MW, Lutz AB, Ullian EM, Baccus SA, Barres BA. 2008. Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59: 425-438.
73. Huberman AD, Wei W, Elstrott J, Stafford BK, Feller MB, Barres BA. 2009. Genetic identification of an on-off directionselective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 62: 327-334.
74. Isshiki T, Pearson B, Holbrook S, Doe CQ. 2001. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106: 511-521.
75. Jacob J, Maurange C, Gould AP. 2008. Temporal control of neuronal diversity: common regulatory principles in insects and vertebrates? Development 135: 3481-3489.
76. Jagadish S, Barnea G, Clandinin TR, Axel R. 2014. Identifying functional connections of the inner photoreceptors in drosophila using Tango-Trace. Neuron 83: 630-644.
77. Jenett A, Rubin GM, Ngo TT, Shepherd D, Murphy C, Dionne H, Pfeiffer BD, Cavallaro A, Hall D, Jeter J, et al. 2012. A GAL4-driver line resource for Drosophila neurobiology. Cell Reports 2: 991-1001.
78. Joesch M, Schnell B, Raghu SV, Reiff DF, Borst A. 2010. ON and OFF pathways in Drosophila motion vision. Nature 468: 300-304.
79. Joesch M, Weber F, Eichner H, Borst A. 2013. Functional specialization of parallel motion detection circuits in the fly. J Neurosci 33: 902-905.
80. Johnston RJ Jr. 2013. Lessons about terminal differentiation from the specification of color-detecting photoreceptors in the Drosophila retina. Ann N Y Acad Sci 1293: 33-44.
81. Johnston RJ Jr, Desplan C. 2010. Stochastic mechanisms of cell fate specification that yield random or robust outcomes. Annu Rev Cell Dev Biol 26: 689-719.
82. Johnston RJ, Desplan C. 2014. Interchromosomal communication coordinates an intrinsically stochastic expression descision between alleles. Science 343: 661-665.
83. Jukam D, Desplan C. 2011. Binary regulation of Hippo pathway by Merlin/NF2, Kibra, Lgl, and Melted specifies and maintains postmitotic neuronal fate. Dev Cell 21: 874-887.
84. Jukam D, Xie B, Rister J, Terrell D, Charlton-Perkins M, Pistillo D, Gebelein B, Desplan C, Cook T. 2013. Opposite feedbacks in the Hippo pathway for growth control and neural fate. Science 342: 1238016.
85. Karuppudurai T, Lin TY, Ting CY, Pursley R, Melnattur KV, Diao F, White BH, Macpherson LJ, Gallio M, Pohida T, et al. 2014. A hard-wired glutamatergic circuit pools and relays UV signals to mediate spectral preference in Drosophila. Neuron 81: 603-615.
86. Kay JN, Voinescu PE, Chu MW, Sanes JR. 2011a. Neurod6 expression defines new retinal amacrine cell subtypes and regulates their fate. Nat Neurosci 14: 965-972.
87. Kay JN, De la Huerta I, Kim IJ, Zhang Y, Yamagata M, Chu MW, Meister M, Sanes JR. 2011b. Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. J Neurosci 31: 7753-7762.
88. Kay JN, Chu MW, Sanes JR. 2012. MEGF10 and MEGF11 mediate homotypic interactions required for mosaic spacing of retinal neurons. Nature 483: 465-469.
89. Kim IJ, Zhang Y, Yamagata M, Meister M, Sanes JR. 2008. Molecular identification of a retinal cell type that responds to upward motion. Nature 452: 478-482.
90. Kim JS, Greene MJ, Zlateski A, Lee K, Richardson M, Turaga SC, Purcaro M, Balkam M, Robinson A, Behababi BF, et al. 2014. Space-time wiring specificity supports direction selectivity in the retina. Nature 509: 331-336.
91. Krahe TE, El-Danaf RN, Dilger EK, Henderson SC, Guido W. 2011. Morphologically distinct classes of relay cells exhibit regional preferences in the dorsal lateral geniculate nucleus of the mouse. J Neurosci 31: 17437-17448.
92. Kvon EZ, Kazmar T, Stampfel G, YáɁez-Cuna JO, Pagani M, Schernhuber K, Dickson BJ, Stark A. 2014. Genome-scale functional characterization of Drosophila developmental enhancers in vivo. Nature 512: 91-95.
93. Lefebvre JL, Kostadinov D, Chen WV, Maniatis T, Sanes JR. 2012. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488: 517-521.
94. Lettvin JY, Maturana HR, McCullough WS, Pitts WH. 1968. What the frog's eye tells the frog's brain. In The mind: biological approaches to its functions (ed. Corning WM, Balaban M), pp 233-258. Intersciences Publishers, New York.
95. Li S, Mo Z, Yang X, Price SM, Shen MM, Xiang M. 2004. Foxn4 controls the genesis of amacrine and horizontal cells by retinal progenitors. Neuron 43: 795-807.
96. Li X, Erclik T, Bertet C, Chen Z, Voutev R, Venkatesh S, Morante J, Celik A, Desplan C. 2013a. Temporal patterning of Drosophila medulla neuroblasts controls neural fates. Nature 498: 456-462.
97. Li X, Chen Z, Desplan C. 2013b. Temporal patterning of neural progenitors in Drosophila. Curr Top Dev Biol 105: 69-96.
98. Lin B, Wang SW, Masland RH. 2004. Retinal ganglion cell type, size, and spacing can be specified independent of homotypic dendritic contacts. Neuron 43: 475-485.
99. Liu G, Seiler H, Wen A, Zars T, Ito K,Wolf R, Heisenberg M, Liu L. 2006. Distinct memory traces for two visual features in the Drosophila brain. Nature 439: 551-556.
100. Livesey FJ, Cepko CL. 2001. Vertebrate neural cell-fate determination: lessons from the retina. Nat Rev Neurosci 2: 109- 118.
101. Losick R, Desplan C. 2008. Stochasticity and cell fate. Science 320: 65-68.
102. Maisak MS, Haag J, Ammer G, Serbe E, Meier M, Leonhardt A, Schilling T, Bahl A, Rubin GM, Nern A, et al. 2013. A directional tuning map of Drosophila elementary motion detectors. Nature 500: 212-216.
103. Malone JH, Hobert O. 2011. Microarrays, deep sequencing and the true measure of the transcriptome. BMC Biol 9: 34.
104. Masland RH. 2012. The neuronal organization of the retina. Neuron 76: 266-280.
105. Matsuoka RL, Nguyen-Ba-Charvet KT, Parray A, Badea TC, Chédotal A, Kolodkin AL. 2011a. Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 470: 259-263.
106. Matsuoka RL, Chivatakarn O, Badea TC, Samuels IS, Cahill H, Katayama K, Kumar SR, Suto F, Chédotal A, Peachey NS, et al. 2011b. Class 5 transmembrane semaphorins control selective Mammalian retinal lamination and function. Neuron 71: 460-473.
107. Matsuoka RL, Jiang Z, Samuels IS, Nguyen-Ba-Charvet KT, Sun LO, Peachy NS, Chedotal A, Yau KW, Kolodkin AL. 2012. Guidance-cue control of horizontal cell morphology, lamination and synapse formation in the mammalian outer retina. J Neurosci 32: 6859-6868.
108. Mazzoni EO, Celik A, Wernet MF, Vasiliauskas D, Johnston RJ, Cook TA, Pichaud F, Desplan C. 2008. Iroquois complex genes induce co-expression of rhodopsins in Drosophila. PLoS Biol 6: e97.
109. 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: 385-392.
110. 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.
111. Meinertzhagen IA, Takemura SY, Lu Z, Huang S, Gao S, Ting CY, Lee CH. 2009. From form to function: the ways to know a neuron. J Neurogenet 23: 68-77.
112. Melnattur KV, Pursley R, Lin TY, Ting CY, Smith PD, Pohida T, Lee CH. 2014. Multiple redundant medulla projection neurons mediate color vision in Drosophila. J Neurogenet 28: 374-388.
113. Mikeladze-Dvali T, Wernet MF, Pistillo D, Mazzoni EO, Teleman AA, Chen YW, Cohen S, Desplan C. 2005. The growth regulators warts/lats and melted interact in a bistable loop to specify opposite fates in Drosophila R8 photoreceptors. Cell 122: 775-787.
114. Morante J, Desplan C. 2008. The color-vision circuit in the medulla of Drosophila. Curr Biol 18: 553-565.
115. Morante J, Erclik T, Desplan C. 2011. Cell migration in Drosophila optic lobe neurons is controlled by eyeless/ Pax6. Development 138: 687-693.
116. Morin LP, Studholme KM. 2014. Retinofugal projections in the mouse. J Comp Neurol 522: 3733-3753.
117. Mu X, Beremand PD, Zhao S, Pershad R, Sun H, Scarpa A, Liang S, Thomas TL, Klein WH. 2004. Discrete gene sets depend on POU domain transcription factor Brn3b/Brn-3.2/POU4f2 for their expression in the mouse embryonic retina. Development 131: 1197-1210.
118. Nakhai H, Sel S, Favor J, Mendoza-Torres L, Paulsen F, Duncker GI, Schmid RM. 2007. Ptf1a is essential for the differentiation of GABAergic and glycinergic amacrine cells and horizontal cells in the mouse retina. Development 134: 1151-1160.
119. Ofstad TA, Zuker CS, Reiser MB. 2011. Visual place learning in Drosophila melanogaster. Nature 474: 204-207.
120. Osterhout JA, Josten N, Yamada J, Pan F, Wu SW, Nguyen PL, Panagiotakos G, Inoue YU, Egusa SF, Volgyi B, et al. 2011. Cadherin-6 mediates axon-target matching in a non-imageforming visual circuit. Neuron 71: 632-639.
121. Otsuna H, Shinomiya K, Ito K. 2014. Parallel neural pathways in higher visual centers of the Drosophila brain that mediate wavelength-specific behavior. Front Neural Circuits 8: 1-12.
122. Panda S, Sato TK, Castrucci AM, Rollag MD, DeGrip WJ, Hogenesch JB, Provencio I, Kay SA. 2002. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298: 2213-2216.
123. Papatsenko D, Sheng G, Desplan C. 1997. A new rhodopsin in R8 photoreceptors of Drosophila: evidence for coordinate expression with Rh3 in R7 cells. Development 124: 1665-1673.
124. Park SJ, Kim IJ, Looger LL, Demb JB, Borghuis BG. 2014. Excitatory synaptic inputs to mouse on-off direction-selective retinal ganglion cells lack direction tuning. J Neurosci 34: 3976-3981.
125. Peichle L, Wassle H. 1979. Size, scatter and coverage of ganglion cell receptive field centres in the cat retina. J Physiol 291: 117-141.
126. Pfeiffer BD, Jenett A, Hammonds AS, Ngo TT, Misra S, Murphy C, Scully A, Carlson JW, Wan KH, Laverty TR, et al. 2008. Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci 105: 9715-9720.
127. Poché RA, Reese BE. 2006. Retinal horizontal cells: challenging paradigms of neural development and cancer biology. Development 136: 2141-2151.
128. Reese BE. 2011. Development of the retina and optic pathway. Vision Res 51: 613-632.
129. 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: 973-978.
130. Rister J, Desplan C. 2011. The retinal mosaics of opsin expression in invertebrates and vertebrates. Dev Neurobiol 71: 1212-1226.
131. Rister J, Pauls D, Schnell B, Ting CY, Lee CH, Sinakevitch I, Morante J, Strausfeld NJ, Ito K, Heisenberg M. 2007. Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster. Neuron 56: 155-170.
132. Rister J, Desplan C, Vasiliauskas D. 2013. Establishing and maintaining gene expression patterns: insights from sensory receptor patterning. Development 140: 493-503.
133. Rivlin-Etzion M, Zhou K, Wei W, Elstrott J, Nguyen PL, Barres BA, Huberman AD, Feller MB. 2011. Transgenic mice reveal unexpected diversity of on-off direction-selective retinal ganglion cell subtypes and brain structures involved in motion processing. J Neurosci 31: 8760-8769.
134. Roska B, Werblin F. 2001. Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410: 583-587.
135. Sanes JR, Zipursky SL. 2010. Design principles of insect and vertebrate visual systems. Neuron 66: 15-36.
136. Schnaitmann C, Garbers C, Wachtler T, Tanimoto H. 2013. Color discrimination with broadband photoreceptors. Curr Biol 23: 2375-2382.
137. Scott EK, Reuter JE, Luo L. 2003. Dendritic development of Drosophila high order visual system neurons is independent of sensory experience. BMC Neurosci 4: 14.
138. Shinomiya K, Karuppudurai T, Lin TY, Lu Z, Lee CH,Meinertzhagen IA. 2014. Candidate neural substrates for off-edge motion detection in Drosophila. Curr Biol 24: 1062-1070.
139. 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: 111-127.
140. Simpson JI. 1984. The accessory optic system. Annu Rev Neurosci 7: 13-41.
141. Soustelle L, Giangrande A. 2007. Novel gcm-dependent lineages in the postembryonic nervous system of Drosophila melanogaster. Dev Dyn 236: 2101-2108.
142. Strother JA, Nern A, Reiser MB. 2014. Direct observation of ON and OFF pathways in the Drosophila visual system. Curr Biol 24: 976-983.
143. Sun LO, Jiang Z, Rivlin-Etzion M, Hand R, Brady CM, Matsuoka RL, Yau KW, Feller MB, Kolodkin AL. 2013. On and off retinal circuit assembly by divergent molecular mechanisms. Science 342: 1241974.
144. Suzuki T, Kaido M, Takayama R, Sato M. 2013. A temporal mechanism that produces neuronal diversity in the Drosophila visual center. Dev Biol 380: 12-24.
145. Swaroop A, Kim D, Forrest D. 2010. Transcriptional regulation of photoreceptor development and homeostasis in the mammalian retina. Nat Rev Neurosci 11: 563-576.
146. Sweeney NT, Tierney H, Feldheim DA. 2014. Tbr2 is required to generate a neural mediating the pupillary light reflex. J Neurosci 34: 5447-5453.
147. Szél A, Röchlich P, Caffé AR, Juliusson B, Aguirre G, Van Veeen T. 1992. Unique topographic separation of two spectral classes of cones in the mouse retina. J Comp Neurol 325: 327-342.
148. 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.
149. Takemura SY, Bharioke A, Lu Z, Nern A, Vitaladevuni S, Rivlin PK, Katz WT, Olbris DJ, Plaza SM, Winston P, et al. 2013. A visual motion detection circuit suggested by Drosophila connectomics. Nature 500: 175-181.
150. Thanawala SU, Rister J, Goldberg GW, Zuskov A, Olesnicky EC, Flowers JM, Jukam D, Purugganan MD, Gavis ER, Desplan C, et al. 2013. Regional modulation of a stochastically expressed factor determines photoreceptor subtypes in the Drosophila retina. Dev Cell 25: 93-105.
151. Ting CY, McQueen PG, Pandya N, Lin TY, Yang M, Reddy OV, O'Connor MB, McAuliffe M, Lee CH. 2014. Photoreceptorderived activin promotes dendritic termination and restricts the receptive fields of first-order interneurons in Drosophila. Neuron 81: 830-846.
152. Tomlinson A. 2003. Patterning the peripheral retina of the fly: decoding a gradient. Dev Cell 5: 799-809.
153. 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: 128-140.
154. Tuthill JC, Nern A, Rubin GM, Reiser MB. 2014. Wide-field feedback neurons dynamically tune early visual processing. Neuron 82: 887-895.
155. Vaney DI, Sivyer B, Taylor WR. 2012. Direction selectivity in the rat retina: symmetry and asymmetry in structure and function. Nat Rev Neurosci 13: 194-208.
156. Velez MM, Gohl D, Clandinin TR, Wernet MF. 2014. Differences in neural circuitry guiding behavioral responses to polarized light presented to either the dorsal or ventral retina in Drosophila. J Neurogenet 8: 1-13.
157. Voinescu PE, Kay JN, Sanes JR. 2009. Birthdays of retinal amacrine cell subtypes are systematically related to their molecular identity and soma position. J Comp Neurol 517: 737-750.
158. Wardill TJ, List O, Li X, Dongre S, McCulloch M, Ting CY, O'Kane CJ, Tang S, Lee CH, Hardie RC, et al. 2012. Multiple spectral inputs improve motion discrimination in the Drosophila visual system. Science 336: 925-931.
159. Wehner R. 2001. Polarization vision-a uniform sensory capacity? J Exp Biol 204: 2589-2596.
160. Wei W, Feller MB. 2011. Organization and development of direction-selective circuits in the retina. Trends Neurosci 34: 638-645.
161. Wei W, Hamby AM, Zhou K, Feller MB. 2011. Development of asymmetric inhibition underlying direction selectivity in the retina. Nature 469: 402-406.
162. Weir PT, Dickinson MH. 2012. Flying Drosophila orient to sky polarization. Curr Biol 22: 21-27.
163. Wernet MF, Labhart T, Baumann F, Mazzoni EO, Pichaud F, Desplan C. 2003. Homothorax switches function of Drosophila photoreceptors from color to polarized light sensors. Cell 115: 267-279.
164. Wernet MF, Mazzoni EO, Celik A, Duncan DM, Duncan I, Desplan C. 2006. Stochastic spineless expression creates the retinal mosaic for colour vision. Nature 440: 174-180.
165. Wernet MF, Celik A, Mikeladze-Dvali T, Desplan C. 2007. Generation of uniform fly retinas. Curr Biol 17: R1002- R1003.
166. Wernet MF, Velez MM, Clark DA, Baumann-Klausener F, Brown JR, Klovstad M, Labhart T, Clandinin TR. 2012. Genetic dissection reveals two separate retinal substrates for polarization vision in Drosophila. Curr Biol 22: 12-20.
167. Wolf R, Gebhardt B, Gademann R, Heisenberg M. 1980. Polarization sensitivity of course control in Drosophila melanogaster. J Comp Physiol 139: 177-191.
168. Wolff T, Ready DF. 1993. Pattern formation in the Drosophila retina. In The development of Drosophila melanogaster (ed. Bate MMA), pp. 1277-1325. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
169. Yamagata M, Sanes JR. 2008. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451: 465-469.
170. Yamagata M, Sanes JR. 2012. Expanding the Ig superfamily code for laminar specificity in retina: expression and role of contactins. J Neurosci 32: 14402-14414.
171. Yamagata M, Weiner JA, Sanes JR. 2002. Sidekicks: synaptic adhesion molecules that promote lamina-specific connectivity in the retina. Cell 110: 649-660.
172. Yamaguchi S, Desplan C, Heisenberg M. 2010. Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila. Proc Natl Acad Sci 107: 5634-5639.
173. Yilmaz M, Meister M. 2013. Rapid innate defensive responses of mice to looming visual stimuli. Curr Biol 23: 2011-2015.
174. Yonehara K, Ishikane H, Sakuta H, Shintani T, Nakamura- Yonehara K, Kamiji NL, Usui S, Noda M. 2009. Identification of retinal ganglion cells and their projections involved in central transmission of information about upward and downward image motion. PLoS ONE 4: e4320.
175. Yonehara K, Farrow K, Ghanem A, Hillier D, Balint K, Teixeira M, Juttner J, Noda M, Neve RL, Conzelmann KK, et al. 2013. The first stage of cardinal direction selectivity is localized to the dendrites of retinal ganglion cells. Neuron 79: 1078- 1085.
176. Yoshida K, Watanabe D, Ishikane H, Tachibana M, Pastan I, Nakanishi S. 2001. A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30: 771-780.