A Hard-Wired Glutamatergic Circuit Pools and Relays UV Signals to Mediate Spectral Preference in Drosophila

Neuron

Volumn 81, Issue 3, 2014, Pages 603-615

  Karuppudurai, Thangavel ^a   Lin, Tzu Yang ^a   Ting, Chun Yuan ^a   Pursley, Randall ^b   Melnattur, Krishna V ^a   Diao, Fengqiu ^c   White, Benjamin H ^c   Macpherson, Lindsey J ^d   Gallio, Marco ^d,e   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 MENTAL HEALTH   (United States)

^d Och Spine at New York Presbyterian Hospitals   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; IONOTROPIC RECEPTOR; KAINIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DROSOPHILA; ELECTRON MICROSCOPY; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; IMMUNOHISTOCHEMISTRY; MORPHOLOGY; NEUROTRANSMISSION; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BRAIN MAPPING; COLOR VISION; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; LIGHT SIGNAL TRANSDUCTION; NERVE NET; OPTOMETRY; PHOTORECEPTOR CELLS, INVERTEBRATE; RECEPTORS, GLUTAMATE; RNA INTERFERENCE; ULTRAVIOLET RAYS; VISUAL PATHWAYS;

EID: 84893486384     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.12.010     Document Type: Article

References (47)

1. Abuin L., Bargeton B., Ulbrich M.H., Isacoff E.Y., Kellenberger S., Benton R. Functional architecture of olfactory ionotropic glutamate receptors. Neuron 2011, 69:44-60.
2. Borst A. Drosophila's view on insect vision. Curr. Biol. 2009, 19:R36-R47.
3. Chaudhry C., Plested A.J., Schuck P., Mayer M.L. Energetics of glutamate receptor ligand binding domain dimer assembly are modulated by allosteric ions. Proc. Natl. Acad. Sci. USA 2009, 106:12329-12334.
4. Clark D.A., Freifeld L., Clandinin T.R. Mapping and cracking sensorimotor circuits in genetic model organisms. Neuron 2013, 78:583-595.
5. Crane J. Imaginal behavior of a Trinidad butterfly, Heliconius erato hydara Hewitson, with a special reference to the social use of color. Zoologica 1955, 40:167-196.
6. Denk W., Briggman K.L., Helmstaedter M. Structural neurobiology: missing link to a mechanistic understanding of neural computation. Nat. Rev. Neurosci. 2012, 13:351-358.
7. Diao F., White B.H. A novel approach for directing transgene expression in Drosophila: T2A-Gal4 in-frame fusion. Genetics 2012, 190:1139-1144.
8. Feinberg E.H., Vanhoven M.K., Bendesky A., Wang G., Fetter R.D., Shen K., Bargmann C.I. GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 2008, 57:353-363.
9. Fischbach K.-F., Dittrich A.P.M. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res. 1989, 258:441-475.
10. Gao S.Y., Takemura S.Y., Ting C.Y., Huang S.L., Lu Z.Y., Luan H.J., Rister J., Thum A.S., Yang M.L., Hong S.T., et al. The neural substrate of spectral preference in Drosophila. Neuron 2008, 60:328-342.
11. Gordon M.D., Scott K. Motor control in a Drosophila taste circuit. Neuron 2009, 61:373-384.
12. Goyret J., Pfaff M., Raguso R.A., Kelber A. Why do Manduca sexta feed from white flowers? Innate and learnt colour preferences in a hawkmoth. Naturwissenschaften 2008, 95:569-576.
13. Hardie R.C. Electrophysiological analysis of fly retina. I: Comparative properties of R1-6 and R7 and 8. J.Comp. Physiol. [A] 1979, 129:19-33.
14. Heisenberg M., Buchner E. Role of retinula cell-types in visual behavior of Drosophila melanogaster. J.Comp. Physiol. [A] 1977, 117:127-162.
15. Hu K.G., Stark W.S. Specific receptor input into spectral preference in Drosophila. J.Comp. Physiol. [A] 1977, 121:241-252.
16. Ilse D., Vaidya V.G. Spontaneous feeding response to colours in Papilio demoleus L. Proc. Indiana Acad. Sci. 1956, 43:23-31.
17. Kelber A. Colour learning in the hawkmoth Macroglossum stellatarum. J.Exp. Biol. 1996, 199:1127-1131.
18. Kitamoto T. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J.Neurobiol. 2001, 47:81-92.
19. Koshitaka H., Kinoshita M., Vorobyev M., Arikawa K. Tetrachromacy in a butterfly that has eight varieties of spectral receptors. Proc. Biol. Sci. 2008, 275:947-954.
20. Kumar J., Schuck P., Mayer M.L. Structure and assembly mechanism for heteromeric kainate receptors. Neuron 2011, 71:319-331.
21. Littleton J.T., Ganetzky B. Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 2000, 26:35-43.
22. Luan H., Peabody N.C., Vinson C.R., White B.H. Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 2006, 52:425-436.
23. Mayer M.L. Structure and mechanism of glutamate receptor ion channel assembly, activation and modulation. Curr. Opin. Neurobiol. 2011, 21:283-290.
24. Meinertzhagen I.A. The organization of perpendicular fibre pathways in the insect optic lobe. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1976, 274:555-594.
25. Meinertzhagen I.A., Lee C.H. The genetic analysis of functional connectomics in Drosophila. Adv. Genet. 2012, 80:99-151.
26. Menne D., Spatz H.C. Color vision in Drosophila melanogaster. J.Comp. Physiol. [A] 1977, 114:301-312.
27. Menzel R. Spectral sensitivity and colour vision in invertebrates. Handbook of Sensory Physiology, Volume VII/6A: Vision in Invertebrates 1979, 503-580. Springer Verlag, New York. H. Autrum (Ed.).
28. Menzel R., Greggers U. Natural phototaxis and its relationship to color vision in honeybees. J.Comp. Physiol. [A] 1985, 157:311-321.
29. Mikeladze-Dvali T., Desplan C., Pistillo D. Flipping coins in the fly retina. Curr. Top. Dev. Biol. 2005, 69:1-15.
30. Morante J., Desplan C. The color-vision circuit in the medulla of Drosophila. Curr. Biol. 2008, 18:553-565.
31. Orger M.B., Baier H. Channeling of red and green cone inputs to the zebrafish optomotor response. Vis. Neurosci. 2005, 22:275-281.
32. O'Tousa J.E., Baehr W., Martin R.L., Hirsh J., Pak W.L., Applebury M.L. The Drosophila ninaE gene encodes an opsin. Cell 1985, 40:839-850.
33. Rister J., Pauls D., Schnell B., Ting C.Y., Lee C.H., Sinakevitch I., Morante J., Strausfeld N.J., Ito K., Heisenberg M. Dissection of the peripheral motion channel in the visual system of Drosophila melanogaster. Neuron 2007, 56:155-170.
34. Salcedo E., Huber A., Henrich S., Chadwell L.V., Chou W.H., Paulsen R., Britt S.G. Blue- and green-absorbing visual pigments of Drosophila: ectopic expression and physiological characterization of the R8photoreceptor cell-specific Rh5 and Rh6 rhodopsins. J.Neurosci. 1999, 19:10716-10726.
35. Schmid A., Hallermann S., Kittel R.J., Khorramshahi O., Frölich A.M., Quentin C., Rasse T.M., Mertel S., Heckmann M., Sigrist S.J. Activity-dependent site-specific changes of glutamate receptor composition invivo. Nat. Neurosci. 2008, 11:659-666.
36. Schnaitmann C., Vogt K., Triphan T., Tanimoto H. Appetitive andaversive visual learning in freely moving Drosophila. Front. Behav. Neurosci. 2010, 4:10.
37. Sobolevsky A.I., Rosconi M.P., Gouaux E. X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 2009, 462:745-756.
38. Sweeney S.T., Broadie K., Keane J., Niemann H., O'Kane C.J. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 1995, 14:341-351.
39. Takemura S.Y., Lu Z., Meinertzhagen I.A. Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J.Comp. Neurol. 2008, 509:493-513.
40. Takemura S.Y., Karuppudurai T., Ting C.Y., Lu Z., Lee C.H., Meinertzhagen I.A. Cholinergic circuits integrate neighboring visual signals in a Drosophila motion detection pathway. Curr. Biol. 2011, 21:2077-2084.
41. Takemura S.Y., Bharioke A., Lu Z., Nern A., Vitaladevuni S., Rivlin P.K., Katz W.T., Olbris D.J., Plaza S.M., Winston P., et al. A visual motion detection circuit suggested by Drosophila connectomics. Nature 2013, 500:175-181.
42. Ting C.Y., Herman T., Yonekura S., Gao S., Wang J., Serpe M., O'Connor M.B., Zipursky S.L., Lee C.H. 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 2007, 56:793-806.
43. Ting C.-Y., McQueen P.G., Pandya N., Lin T.-Y., Yang M., Reddy O.V., O'Connor M.B., McAuliffe M., Lee C.-H. Photoreceptor-derived activin promotes dendritic termination and restricts the receptive fields of first-order interneurons in Drosophila. Neuron 2014, Published online January 23, 2014. 10.1016/j.neuron.2013.12.012.
44. Weiss M.R. Innate colour preferences and flexible colour learning in the pipevine swallowtail. Anim. Behav. 1997, 53:1043-1052.
45. Wong A.M., Wang J.W., Axel R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 2002, 109:229-241.
46. Yamaguchi S., Desplan C., Heisenberg M. Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila. Proc. Natl. Acad. Sci. USA 2010, 107:5634-5639.
47. Young M., Salmon M., Forward R. Visual wavelength discrimination by the loggerhead turtle, Caretta caretta. Biol. Bull. 2012, 222:46-55.