Multiple redundant medulla projection neurons mediate color vision in drosophila

Journal of Neurogenetics

Volumn 28, Issue 3-4, 2014, Pages 374-388

  Melnattur, Krishna V ^a   Pursley, Randall ^b   Lin, Tzu Yang ^a   Ting, Chun Yuan ^a   Smith, Paul D ^c   Pohida, Thomas ^b   Lee, Chi Hon ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

Author keywords

Color discrimination; Medulla projection neurons; Neural substrate; Visual behavior

Indexed keywords

ORA TRANSIENTLESS PROTEIN; PHOSPHOLIPASE C; PROTEIN; RHODOPSIN; RHODOPSIN 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; AVERSIVE OPERANT CONDITIONING; BLUE; COLOR; COLOR DISCRIMINATION; COLOR VISION; CONTROLLED STUDY; DIMERIZATION; DROSOPHILA; ENHANCER REGION; GREEN; INSTRUMENTAL CONDITIONING; INTERNEURON; ISOLUMINANCE; LIGHT EMITTING DIODE; LUMINANCE; MEDULLA PROJECTION NEURON; NONHUMAN; PHENOTYPE; PHOTORECEPTOR; PHOTORECEPTOR R7; PHOTORECEPTOR R8; PROMOTER REGION; SPATIAL ORIENTATION; SPECTRAL SENSITIVITY; SYNAPSE; SYNAPTIC TRANSMISSION; VISUAL SYSTEM; WILD TYPE; ANIMAL; MEDULLA OBLONGATA; NERVE CELL; PERCEPTIVE DISCRIMINATION; PHOTORECEPTOR CELL; PHOTOSTIMULATION; PHYSIOLOGY;

ANIMALS; COLOR VISION; DISCRIMINATION (PSYCHOLOGY); DROSOPHILA; MEDULLA OBLONGATA; NEURONS; PHOTIC STIMULATION; PHOTORECEPTOR CELLS, INVERTEBRATE; SYNAPSES; VISUAL PATHWAYS;

EID: 84908617949     PISSN: 01677063     EISSN: 15635260     Source Type: Journal    
DOI: 10.3109/01677063.2014.891590     Document Type: Article

References (61)

1. Borst, A. (2009). Drosophila's view on insect vision. Curr Biol, 19, R36-R47
2. Bender, J. A., & Dickinson, M. H. (2006). Visual stimulation of saccades in magnetically tethered Drosophila. J Exp Biol, 209 (Pt 16), 3170-3182
3. Cajal, S. R., & Sanchez, D. (1915). Contribucion al conocimiento de los centros nerviosos del los insectos. Trab Lab Invest Biol, 13, 1-167
4. Calkins, D. J., & Sterling, P. (1999). Evidence that circuits for spatial and color vision segregate at the first retinal synapse. Neuron, 24, 313-321
5. Chen, S., & Li, W. (2012). A color-coding amacrine cell may provide a blue-off signal in a mammalian retina. Nat Neurosci, 15, 954-956
6. Chiappe, M. E., Seelig J. D., Reiser, M. B., & Jayaraman, V. (2010). Walking modulates speed sensitivity in Drosophila motion vision. Curr Biol, 20, 1470-1475
7. Clark, D. A., Bursztyn, L., Horowitz, M. A., Schnitzer, M. J., & Clandinin, T. R. (2011). Defi ning the computational structure of the motion detector in Drosophila. Neuron, 70, 1165-1177
8. Crane, J. (1955). Imaginal behavior of a Trinidad butterfly, Heliconius erato hydara Hewitson, with a special reference to the social use of color. Zoologica, 40, 167-196
9. Dacey, D. M. (2004). Origins of perception: Retinal ganglion cell diversity and the creation of parallel visual pathways. In M. S. Gazanniga (Ed.), The cognitive neurosciences (pp. 281-301). Cambridge, MA: MIT Press
10. Dacey, D. M., Crook, J. D., & Packer, O. S. (2013). Distinct synaptic mechanisms create parallel S-ON and S-OFF color opponent pathways in the primate retina. Vis Neurosci, 1-13
11. Duistermars, B. J., & Frye, M. A. (2008). A magnetic tether system to investigate visual and olfactory mediated flight control in Drosophila. J Vis Exp, 21, e1063
12. Dyer, A. G., Paulk, A. C., & Reser, D. H. (2011). Colour processing in complex environments: Insights from the visual system of bees. Proc Biol Sci, 278, 952-959
13. Feinberg, E. H., Vanhoven, M. K., Bendesky, A., Wang, G., Fetter, R. D., Shen, K., & Bargmann, C. I. (2008). GFP Reconstitution Across Synaptic Partners (GRASP) defi nes cell contacts and synapses in living nervous systems. Neuron, 57, 353-363
14. Field, G. D., & Chichilnisky, E. J. (2007). Information processing in the primate retina: Circuitry and coding. Annu Rev Neurosci, 30, 1-30
15. Fischbach, K. F. (1979). Simultaneous and successive color contrast expressed in slow phototactic behavior of walking Drosophila melanogaster. J Comp Physiol, 130, 161-171
16. Fischbach, K. F., & Dittrich, A. P. (1989). The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res, 258, 441-475
17. Gao, S., Takemura, S. Y., Ting, C. Y., Huang, S., Lu, Z., Luan, H., Rister, J., Thum, A. S., Yang, M., Hong, S. T., Wang, J. W., Odenwald, W. F., White, B. H., Meinertzhagen, I. A., & Lee, C. H. (2008). The neural substrate of spectral preference in Drosophila. Neuron, 60, 328-342
18. Goldsmith, T. H. (1991). The evolution of visual pigments and colour vision. In P. Gouras (Ed.), The perception of colour (pp. 62-89). London: Macmillan
19. Gordon, M. D., & Scott, K. (2009). Motor control in a Drosophila taste circuit. Neuron, 61, 373-384
20. Goyret, J., Pfaff, M., Raguso, R. A., & Kelber, A. (2008). Why do Manduca sexta feed from white flowers?. Innate and learnt colour preferences in a hawkmoth. Naturwissenschaften, 95, 569-576
21. Hardie, R. C. (1979). Electro-physiological analysis of fly retina.1. Comparative properties of R1-6 and R7 and R8. J Comp Physiol, 129, 19-33
22. Heisenberg, M., & Buchner, E. (1977). Role of retinula cell-types in visual behavior of Drosophila melanogaster. J Comp Physiol, 117, 127-162
23. Helmstaedter, M., Briggman, K. L., Turaga, S. C., Jain, V., Seung, H. S., & Denk, W. (2013). Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature, 500, 168-174
24. Hernández de Salomon, C., & Spatz, H. C. (1983). Colour vision in Drosophila melanogaster: Wavelength discrimination. J Comp Physiol, 150, 31-37
25. Jacobs, G. H. (2009). Evolution of colour vision in mammals. Phil Trans R Soc B, 364, 2957-2967
26. Joesch, M., Schnell, B., Raghu, S. V., Reiff, D. F., & Borst, A. (2010). ON and OFF pathways in Drosophil a motion vision. Nature, 468, 300-304
27. Karuppudurai, T., Lin, T. Z., Ting, C. Y., Pursley, R., Melnattur, K. V., Diao, F., White, B. H., Macpherson, L. J., Gallio, M., Pohida, T., & Lee, C. H. (2014). A hard-wired glutamatergic circuit pools and relays UV signals to a higher visual center to mediate spectral preference in Drosophila. Neuron, 81, 603-615
28. Kelber, A. (1996). Colour learning in the hawkmoth Macroglossum stellatarum. J Exp Biol, 199, 1127-1131
29. Kelber, A., Vorobyev, M., & Osorio, D. (2003). Animal colour vision - behavioural tests and physiological concepts. Biol Rev Camb Philos Soc, 78, 81-118
30. Koshitaka, H., Kinoshita, M., Vorobyev, M., & Arikawa, K. (2008). Tetrachromacy in a butterfly that has eight varieties of spectral receptors. Proc Biol Sci, 275, 947-954
31. Luan, H., Peabody, N. C., Vinson, C. R., & White, B. H. (2006). Refi ned spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron, 52, 425-436
32. Meinertzhagen, I. A., & Lee, C. H. (2012). The genetic analysis of functional connectomics in Drosophila. Adv Genet, 80, 99-151
33. Menne, D., & Spatz, H. C. (1977). Colour vision in Drosophila melanogaster. J Comp Physiol, 114, 301-312
34. Menzel, R. (1979). Spectral sensitivity and color vision in invertebrates. In H. Autrum (Ed.), Comparative physiology and evolution of vision in invertebrates. (Vol. 7/6/6 A, pp. 503-580). Berlin and Heidelberg: Springer
35. Menzel, R., & Greggers, U. (1985). Natural phototaxis and its relationship to colour vision in honeybees. J Comp Physiol, 157, 311-321
36. Mikeladze-Dvali, T., Wernet, M. F., Pistillo, D., Mazzoni, E. O., Teleman, A. A., Chen, Y. W., 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
37. Morante, J., & Desplan, C. (2008). The color-vision circuit in the medulla of Drosophila. Curr Biol, 18, 553-565
38. Nathans, J. (1999). The evolution and physiology of human color vision: Insights from molecular genetic studies of visual pigments. Neuron, 24, 299-312
39. Neitz, J., & Neitz, M. (2011). The genetics of normal and defective color vision. Vision Res, 51, 633-651
40. O'Tousa, J. E., Baehr, W., Martin, R. L., Hirsh, J., Pak, W. L., & Applebury, M. L. (1985). The Drosophila ninaE gene encodes an opsin. Cell, 40, 839-850
41. Packer, O. S., Verweij, J., Li, P. H., Schnapf, J. L., & Dacey, D. M. (2010). Blue-yellow opponency in primate S cone photoreceptors. J Neurosci, 30, 568-572
42. Rister, J., Pauls, D., Schnell, B., Ting, C. Y., Lee, C. H., Sinakevitch, I., Morante, J., Strausfeld, N. J., Ito, K., & Heisenberg, M. (2007). Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster. Neuron, 56, 155-170
43. Salcedo, E., Huber, A., Henrich, S., Chadwell, L. V., Chou, W. H., Paulsen, R., & Britt, S. G. (1999). Blue-and green-absorbing visual pigments of Drosophila : Ectopic expression and physiological characterization of the R8 photoreceptor cell-specifi c Rh5 and Rh6 rhodopsins. J Neurosci, 19, 10716-10726
44. Sanes, J. R., & Zipursky, S. L. (2010). Design principles of insect and vertebrate visual systems. Neuron, 66, 15-36
45. Schnaitmann, C., Garbers, C., Wachtler, T., & Tanimoto, H. (2013). Color discrimination with broadband photoreceptors. Curr Biol, 23, 2375-2382
46. Schnaitmann, C., Vogt, K., Triphan, T., & Tanimoto, H. (2010). Appetitive and aversive visual learning in freely moving Drosophila. Front Behav Neurosci, 4, 1-10
47. Srinivasan, M. V. (2010). Honey bees as a model for vision, perception, and cognition. Annu Rev Entomol, 55, 267-284
48. Smakman, J. G. J., & Stavenga D. G. (1986). Spctral sensitivity of blowfly photoreceptors: Dependence of waveguide effects and pigment concentration. Vision Res, 26, 1019-1025
49. Stockman, A., & Brainard, D. (2010). Color vision mechanisms. In M. Bass (Ed.), OSA handbook of optics (pp. 11.11-11.104). New York: McGraw Hill
50. Sweeney, S. T., Broadie, K., Keane, J., Niemann, H., & O'Kane, C. J. (1995). Targeted expression of tetanus toxin light chain in Drosophila specifi cally eliminates synaptic transmission and causes behavioral defects. Neuron, 14, 341-351
51. Takemura, S. Y., & Arikawa, K. (2006). Ommatidial type-specifi c interphotoreceptor connections in the lamina of the swallowtail butterfly, Papilio xuthus. J Comp Neurol, 494, 663-672
52. Takemura, S. Y., Lu, Z., & Meinertzhagen, I. A. (2008). Synaptic circuits of the Drosophila optic lobe: The input terminals to the medulla. J Comp Neurol, 509, 493-513
53. Takemura, S. Y., Bharioke, A., Lu, Z., Nern, A., Vitaladevuni, S., Rivlin, P. K, et al. (2013). A visual motion detection circuit suggested by Drosophila connectomics. Nature, 500, 175-181
54. Tang, S., Wolf, R., Xu, S., & Heisenberg, M. (2004). Visual pattern recognition in Drosophila is invariant for retinal position. Science, 305, 1020-1022
55. Ting, C. Y., Herman, T., Yonekura, S., Gao, S., Wang, J., Serpe, M., O'Connor, M. B., Zipursky, S. L., & Lee, C. H. (2007). Tiling of R7 axons in the Drosophila visual system is mediated both by transduction of an activin signal to the nucleus and by mutual repulsion. Neuron, 56, 793-806
56. Ting, C. Y., McQueen, P. G., Pandya, N., Lin, T. Z., Yang, M., Onteddu, V. R., O'Connor, M. B., McAuliffe, M., & Lee, C. H. (2014). Photoreceptor-derived Activin promotes dendritic termination and restricts the teceptive fi elds of first-order interneurons in Drosophila. Neuron, 81, 830-846
57. Troje, N. (1993). Spectral categories in the learning behaviour of blowflies. Z Naturforsch C, 48, 96-96
58. van Hateren, J. H. (1993). Spatial, temporal and spectral preprocessing for colour vision. Proc Biol Sci, 251, 61-68
59. Wyszecki, G., & Stiles, W. S. (1982). Color science. New York: Wiley
60. Yamaguchi, S., Desplan, C., & Heisenberg, M. (2010). Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila. Proc Natl Acad Sci U S A, 107, 5634-5639
61. Yamaguchi, S., Wolf, R., Desplan, C., & Heisenberg, M. (2008). Motion vision is independent of color in Drosophila. Proc Natl Acad Sci U S A, 105, 4910-4915