Neurons with GABAergic phenotype in the visual system of Drosophila

Journal of Comparative Neurology

Volumn 521, Issue 1, 2013, Pages 252-265

  Raghu, Shamprasad Varija ^a   Claussen, Jing ^a   Borst, Alexander ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

Drosophila; dVGAT Gal4; Flp FRT; GABA; GABAergic; Insects; Visual system

Indexed keywords

4 AMINOBUTYRIC ACID; NEUROTRANSMITTER;

ANIMAL CELL; ARTICLE; BUSHY T CELL; CELL TYPE; CENTRAL NERVOUS SYSTEM; DROSOPHILA; FEMALE; GABAERGIC SYSTEM; GOLGI STAIN; LAMINA MONOPOLAR CELL; LOBULA COLUMNAR NEURON; LOBULA COMPLEX; LOBULA PLATE INTRINSIC CELL; LOBULA TANGENTIAL CELL; MEDULLA INTRINSIC CELL; MEDULLA OBLONGATA; MEDULLA TANGENTIAL CELL; NERVE CELL; NEUROANATOMY; NONHUMAN; OPTIC LOBE; PHENOTYPE; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; TRANSMEDULLARY CELL; TRANSMEDULLARY Y AND Y CELL; VISUAL SYSTEM;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BRAIN MAPPING; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; MALE; NEURONS; OPTIC LOBE, NONMAMMALIAN; PHENOTYPE; TRANSCRIPTION FACTORS; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS; VISUAL PATHWAYS;

EID: 84870021414     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23208     Document Type: Article

References (63)

1. 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.
2. Bicker G, Schäfer S, Ottersen OP, Storm-Mathisen J. 1988. Glutamate-like immunoreactivity in identified neuronal populations of insect nervous systems. J Neurosci 8: 2108-2122.
3. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
4. Brotz TM, Gundelfinger ED, Borst A. 2001. Cholinergic and GABAergic pathways in fly motion vision. BMC Neurosci 2: 1.
5. Buchner E, Buchner S, Crawford G, Mason WT, Salvaterra PM, Sattelle DB. 1986. Choline acetyltransferase-like immunoreactivity in the brain of Drosophila melanogaster. Cell Tissue Res 246: 57-62.
6. Buijs RM, Vvan Vulpen EHS, Geffard M. 1987. Ultrastructural localization of GABA in the supraoptic nucleus and neural lobe. Neuroscience 20: 347-355.
7. Busch S, Selcho M, Ito K, Tanimoto H. 2009. A map of octopaminergic neurons in the Drosophila brain. J Comp Neurol 513: 643-667.
8. Buschbeck EK, Strausfeld NJ. 1996. Visual motion-detection circuits in flies: small-field retinotopic elements responding to motion are evolutionarily conserved across taxa. J Neurosci 16: 4563-4578.
9. Datum KH, Weiler R, Zettler F. 1986. Immunocytochemical demonstration of g-amino butyric acid and glutamic acid decarboxylase in R7 photoreceptors and C2 centrifugal fibers in the blowfly visual system. J Comp Physiol A 159: 241-249.
10. Douglass JK, Strausfeld NJ. 2003. Retinotopic pathways providing motion-selective information to the lobula from peripheral elementary motion-detecting circuits. J Comp Neurol 457: 326-344.
11. Duarte CB, Santos PF, Carvalho AP. 1999. Corelease of two functionally opposite neurotransmitters by retinal amacrine cells: experimental evidence and functional significance. J Neurosci Res 58: 475-479.
12. Eichner H, Joesch M, Schnell B, Reiff DF, Borst A. 2011. Internal structure of the fly elementary motion detector. Neuron 70: 1155-1164.
13. Fei H, Chow DM, Chen A, Calderón RR, Ong WS, Ackerson LY, Maidment NT, Simpson JH, Frye MA, Krantz DE. 2010. Mutation of the Drosophila vesicular GABA transporter disrupts visual figure detection. J Exp Biol 213: 1717-1730.
14. 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.
15. Gao S, Takemura S, Ting C, Huang S, Lu Z, Luan H, Rister J, Thum AS, Yang M, Hong S, Wang JW, Odenwald WF, White BH, Meinertzhagen IA, Lee C. 2008. The neural substrate of spectral preference in Drosophila. Neuron 60: 328-342.
16. Gasnier B. 2004. The SLC32 transporter, a key protein for the synaptic release of inhibitory amino acids. Pflugers Arch 447: 756-759.
17. Hamanaka Y, Meinertzhagen IA. 2010. Immunocytochemical localization of synaptic proteins to photoreceptor synapses of Drosophila melanogaster. J Comp Neurol 518: 1133-1155.
18. Hardie RC. 1987. Is histamine a neurotransmitter in insect photoreceptors? J Comp Physiol A 161: 201-213.
19. Hardie RC. 1989. Neurotransmitters in the compound eye. In: Stavenga DG, Hardie RC, editors. Facets of vision. Berlin: Springer. p 235-256.
20. 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.
21. 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.
22. Hausen K. 1984. The lobula-complex of the fly: structure, function and significance in visual behaviour. In: Ali MA, editor. Photoreception and vision in invertebrates. New York: Plenum Press. p 523-559.
23. 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.
24. 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.
25. Joesch M, Schnell B, Raghu SV, Reiff DF, Borst A. 2010. ON and OFF pathways in Drosophila motion vision. Nature 468: 300-304.
26. Kanner BI. 2006. Structure and function of sodium-coupled GABA and glutamate transporters. J Membr Biol 213: 89-100.
27. Kitamoto T, Wang W, Salvaterra PM. 1998. Structure and organization of the Drosophila cholinergic locus. J Biol Chem 273: 2706-2713.
28. Kleinfeld D, Bharioke A, Blinder P, Bock DD, Briggman KL, Chklovskii DB, Denk W, Helmstaedter M, Kaufhold JP, Lee WA, Meyer HS, Micheva KD, Oberlaender M, Prohaska S, Reid RC, Smith SJ, Takemura S, Tsai PS, Sakmann B. 2011. Large-scale automated histology in the pursuit of connectomes. J Neurosci 31: 16125-16138.
29. Kolodziejczyk A, Sun X, Meinertzhagen IA, Nässel DR. 2008. Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system. PLoS One 3: 2110.
30. Lahey T, Gorczyca M, Jia XX, Budnik V. 1994. The Drosophila tumor suppressor gene dlg is required for normal synaptic bouton structure. Neuron 13: 823-835.
31. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451-461.
32. Lee S, Kim Z. 2010. Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron 68: 1159-1172.
33. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM. 1997. Identification and characterization of the vesicular GABA transporter. Nature 389: 870-876.
34. 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.
35. Meyer EP, Matute C, Streit P, Nässel DR. 1986. Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemie 84: 207-216.
36. Morante J, Desplan C. 2008. The color-vision circuit in the medulla of Drosophila. Curr Biol 18: 553-565.
37. Nässel DR. 1988. Serotonin and serotonin-immunoreactive neurons in the insect nervous system. Progr Neurobiol 30: 1-85.
38. Nässel DR, Laxmyr L. 1983. Quantitative determination of biogenic amines and dopa in the CNS of adult and larval blowflies, Calliphora erythrocephala. Comp Biochem Physiol 75: 259-265.
39. Nässel DR, Ohlsson L, Sivasubramanian P. 1987. Differentiation of serotonin-immunoreactive neurons in fly optic lobes developing in situ or cultured in vivo without eye discs. J Comp Neurol 255: 327-340.
40. Nässel DR, Elekes K, Johansson KUI. 1988. Dopamine-immunoreactive neurons in the blowfly visual system: light and electronmicroscopic immunocytochemistry. J Chem Neuroanat 1: 311-325.
41. Neal MJ, Cunningham JR, Hutson H, Semark JE. 1992. Calcium dependent release of acetylcholine and γ-aminobutyric acid from the rabbit retina. Neurochem Int 20: 43-53.
42. O'Malley DM, Sandell JH, Masland RH. 1992. Co-release of acetylcholine and GABA by the starburst amacrine cells. J Neurosci 12: 1394-1408.
43. Otsuna H, Ito K. 2006. Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways. J Comp Neurol 497: 928-958.
44. Parnas D, Haghighi AP, Fetter RD, Kim SW, Goodman CS. 2001. Regulation of postsynaptic structure and protein localization by the Rho-type guanine nucleotide exchange factor dPix. Neuron 32: 415-424.
45. Pollack I, Hofbauer A. 1991. Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster. Cell Tissue Res 266: 391-398.
46. Raghu SV, Borst A. 2011. Candidate glutamatergic neurons in the visual system of Drosophila. PLoS ONE 6: e19472.
47. Raghu SV, Joesch M, Borst A, Reiff DF. 2007. Synaptic organization of lobula plate tangential cells in Drosophila: gamma-aminobutyric acid receptors and chemical release sites. J Comp Neurol 502: 598-610.
48. Raghu SV, Joesch M, Sigrist SJ, Borst A, Reiff DF. 2009. Synaptic organization of lobula plate tangential cells in Drosophila: Dalpha7 cholinergic receptors. J Neurogenet 23: 200-209.
49. Raghu SV, Reiff DF, Borst A. 2011. Neurons with cholinergic phenotype in the visual system of Drosophila. J Comp Neurol 519: 162-176.
50. Schäfer S, Bicker G, Ottersen OP, Storm-Mathisen J. 1988. Taurine-like immunoreactivity in the brain of the honey bee. J Comp Neurol 268: 60-70.
51. Schnell B, Joesch M, Foerstner F, Raghu SV, Otsuna H, Ito K, Borst A, Reiff DF. 2010. Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. J Neurophysiol 103: 1646-1657.
52. Schousboe A. 2000. Pharmacological and functional characterization of astrocytic GABA transport: a short review. Neurochem Res 25: 1241-1244.
53. Schürmann FW, Elekes K, Geffard M. 1989. Dopamine-like immunoreactivity in the bee brain. Cell Tissue Res 256: 399-410.
54. 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.
55. Sinakevitch I, Strausfeld NJ. 2004. Chemical neuroanatomy of the fly's movement detection pathway. J Comp Neurol 468: 6-23.
56. Strausfeld NJ. 1976a. Atlas of an insect brain. Berlin: Springer.
57. Strausfeld NJ. 1976b. Mosaic organization, layers and visual pathways in the insect brain. In: Neural principles of vision. Zettler F, Weiler R, editors. Berlin: Springer. p 245-279.
58. Strausfeld NJ. 1984. Functional anatomy of the blowfly visual system. In: Photoreception and vision in invertebrates. In: Ali MA, editor. New York: Plenum Press. p 483-522.
59. Stuart AE, Borycz J, Meinertzhagen IA. 2007. The dynamics of signaling at the histaminergic photoreceptor synapse of arthropods. Prog Neurobiol 82: 202-207.
60. 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.
61. Takemura SY, Karuppudurai T, Ting C-Y, Lu Z, Lee C-H, Meinertzhagen IA. 2011. Cholinergic circuits integrate neighboring visual signals in a Drosophila motion detection pathway. Curr Biol 21: 2077-2084.
62. Wojcik SM, Katsurabayashi S, Guillemin I, Friauf E, Rosenmund C, Brose N, Rhee JS. 2006. A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50: 575-587.
63. Wong AM, Wang JW, Axel R. 2002. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109: 229-241.