Neurons with cholinergic phenotype in the visual system of Drosophila

Journal of Comparative Neurology

Volumn 519, Issue 1, 2011, Pages 162-176

  Varija Raghu, Shamprasad ^a   Reiff, Dierk F ^a   Borst, Alexander ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

Cha; Cholinergic; Drosophila; Insects; MARCM; Visual system

Indexed keywords

ACETYLCHOLINE; TRANSCRIPTION FACTOR GAL4;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN REGION; BUSHY T CELL; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCATION; GOLGI COMPLEX; IMMUNOREACTIVITY; LOBULA COLUMNAR CELL; LOBULA TANGENTIAL CELL; MEDULLA INTRINSIC CELL; MEDULLA OBLONGATA; MEDULLA TANGENTIAL CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; OPTIC LOBE; PHENOTYPE; PRIORITY JOURNAL; TRANS LOBULA PLATE CELL; TRANSMEDULLARY Y CELL; VISUAL SYSTEM;

ACETYLCHOLINE; ANIMALS; BRAIN MAPPING; DROSOPHILA; FEMALE; IMMUNOHISTOCHEMISTRY; NEURONS; OPTIC LOBE, NONMAMMALIAN; PHENOTYPE; VISUAL PATHWAYS;

EID: 78649695146     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22512     Document Type: Article

References (79)

1. Banghart M, Borges K, Isacoff E, Trauner D, Kramer RH. 2004. Light-activated ion channels for remote control of neuronal firing. Nat Neurosci 7: 1381-1386.
2. 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.
3. 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.
4. Borst A. 2009. Drosophila's view on insect vision. Curr Biol 19: 36-47.
5. Borst A, Egelhaaf M. 1992. In vivo imaging of calcium accumulation in fly interneurons as elicited by visual motion stimulation. Proc Natl Acad Sci U S A 89: 4139-4143.
6. Borst A, Haag J. 1996. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells. I. Passive membrane properties. J Comput Neurosci 3: 313-336.
7. Borst A, Haag J. 2002. Neural networks in the cockpit of the fly. J Comp Physiol A 188: 419-437.
8. Borst A, Haag J, Reiff DF. 2010. Fly motion vision. Annu Rev Neurosci 33: 49-70.
9. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
10. Brotz TM, Borst A. 1996. Cholinergic and GABAergic receptors on fly tangential cells and their role in visual motion detection. J Neurophysiol 76: 1786-1799.
11. Brotz TM, Gundelfinger ED, Borst A. 2001. Cholinergic and GABAergic pathways in fly motion vision. BMC Neurosci 2: 1.
12. Buchner E, Buchner S, Bulthoff I. 1984. Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. J Comp Physiol A 155: 471-483.
13. 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.
14. Busch S, Selcho M, Ito K, Tanimoto H. 2009. A map of octopaminergic neurons in the Drosophila brain. J Comp Neurol 513: 643-67.
15. 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.
16. Cajal SR, Sanchez D. 1915. Contribución al conocimiento de los centras nerviosos de los insectos. Trab Lab Invest Biol, Univ Madr 13: 1-168.
17. Campos-Ortega JA, Strausfeld NJ. 1972. The columnar organization of the second synaptic region of the visual system of Musca domestica. L. I. Receptor terminals in the medulla. Z Zellforsch Mikrosk Anat 124: 561-585.
18. Douglass JK, Strausfeld NJ. 1995. Visual motion detection circuits in flies: peripheral motion computation by identified small-field retinotopic neurons. J Neurosci 15: 5596-5611.
19. Douglass JK, Strausfeld NJ. 1996. Visual motion-detection circuits in flies: parallel direction- and non-direction-sensitive pathways between the medulla and lobula plate. J Neurosci 16: 4551-4562.
20. Douglass JK, Strausfeld NJ. 2003a. Anatomical organization of retinotopic motion sensitive pathways in the optic lobes of flies. Microsc Res Tech 62: 132-150.
21. Douglass JK, Strausfeld NJ. 2003b. Retinotopic pathways providing motion-selective information to the lobula from peripheral elementary motion-detecting circuits. J Comp Neurol 457: 326-344.
22. 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.
23. 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.
24. Gilbert C, Strausfeld NJ. 1991. The functional organization of male-specific visual neurons in flies. J Comp Physiol A 169: 395-411.
25. Haag J, Borst A. 1996. Amplification of high-frequency synaptic inputs by active dendritic membrane processes. Nature 379: 639-641.
26. Haag J, Vermeulen A, Borst A. 1999. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells. III. Visual response properties. J Comput Neurosci 7: 213-234.
27. Haag J, Denk W, Borst A. 2004. Fly motion vision is based on Reichardt detectors regardless of the signal-to-noise ratio. Proc Natl Acad Sci U S A 101: 16333-16338.
28. 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.
29. Hamanaka Y, Meinertzhagen IA. 2010. Immunocytochemical localization of synaptic proteins to photoreceptor synapses of Drosophila melanogaster. J Comp Neurol 518: 1133-1155.
30. Hardie RC. 1987. Is histamine a neurotransmitter in insect photoreceptors? J Comp Physiol A 161: 201-213.
31. Hardie RC. 1989. Neurotransmitters in the compound eye. In: Stavenga DG, Hardie RC, editors. Facets of vision. Berlin: Springer. p 235-256.
32. 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.
33. 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.
34. 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.
35. Hendel T, Mank M, Schnell B, Griesbeck O, Borst A, Reiff DF. 2008. Fluorescence changes of genetic calcium indicators and OGB-1 correlated with neural activity and calcium in vivo and in vitro. J Neurosci 28: 7399-7411.
36. 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.
37. Homberg U, Hildebrand JG. 1989. Serotonin-immunoreactive neurons in the median protocerebrum and subesophageal ganglion of the sphinx moth Manduca sexta. Cell Tissue Res 258: 1-24.
38. 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.
39. Kitamoto T. 2001. Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47: 81-92.
40. Kitamoto T, Wang W, Salvaterra PM. 1998. Structure and organization of the Drosophila cholinergic locus. J Biol Chem 273: 2706-13.
41. Klemm N. 1976. Histochemistry of putative transmitter substances in the insect brain. Prog Neurobiol 7: 99-169.
42. 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: e2110.
43. 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
44. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451-61.
45. Lima SQ, Miesenboeck G. 2005. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121: 141-152.
46. Luo L, Callaway EM, Svoboda K. 2008. Genetic dissection of neural circuits. Neuron 57: 634-660.
47. Mank M, Santos AF, Direnberger S, Mrsic-Flogel TD, Hofer SB, Stein V, Hendel T, Reiff DF, Levelt C, Borst A, Bonhoeffer T, Hübener M, Griesbeck O. 2008. A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat Methods 5: 805-811.
48. 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.
49. Meyer EP, Matute C, Streit P, Nässel DR. 1986. Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemie 84: 207-216.
50. 2+ based on green fluorescent proteins and calmodulin. Nature 388: 882-887.
51. Morante J, Desplan C. 2008. The color-vision circuit in the medulla of Drosophila. Curr Biol 18: 553-565.
52. 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.
53. 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.
54. 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.
55. Pollack I, Hofbauer A. 1991. Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster. Cell Tissue Res 266: 391-398.
56. 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.
57. 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.
58. 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.
59. Salvaterra PM, Kitamoto T. 2001. Drosophila cholinergic neurons and processes visualized with Gal4/UAS-GFP. Brain Res Gene Expr Patterns 1: 73-82.
60. 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.
61. 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.
62. Schürmann FW, Elekes K, Geffard M. 1989. Dopamine-like immunoreactivity in the bee brain. Cell Tissue Res 256: 399-410.
63. Schuster R, Phannavong P, Schröder C, Gundelfinger ED. 1993. Immunohistochemical localization of a ligand-binding and a structural subunit of nicotinic acetylcholine receptors in the central nervous system of Drosophila melanogaster. J Comp Neurol 335: 149-162.
64. 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.
65. Sinakevitch I, Strausfeld NJ. 2004. Chemical neuroanatomy of the fly's movement detection pathway. J Comp Neurol 468: 6-23.
66. Single S, Borst A. 1998. Dendritic integration and its role in computing image velocity. Science 281: 1848-1850.
67. Strausfeld NJ. 1976a. Atlas of an insect brain. Berlin: Springer.
68. Strausfeld NJ. 1976b. Mosaic organization, layers and visual pathways in the insect brain. In: Zettler F, Weiler R, editors. Neural principles of vision. Berlin: Springer. p 245-279.
69. Strausfeld NJ. 1984. Functional anatomy of the blowfly visual system. In: Ali MA, editor. Photoreception and vision in invertebrates. New York: Plenum Press. p 483-522.
70. Strausfeld NJ, Lee JK. 1991. Neuronal basis for parallel visual processing in the fly. Vis Neurosci 7: 13-33
71. Stuart AE, Borycz J, Meinertzhagen IA. 2007. The dynamics of signaling at the histaminergic photoreceptor synapse of arthropods. Prog Neurobiol 82: 202-207.
72. Takagawa K, Salvaterra P. 1996. Analysis of choline acetyltransferase protein in temperature sensitive mutant flies using newly generated monoclonal antibody. Neurosci Res 24: 237-243.
73. Wertz A, Borst A, Haag J. 2008. Nonlinear integration of binocular optic flow by DNOVS2, a descending neuron of the fly. J Neurosci 28: 3131-3140.
74. Wertz A, Gaub B, Plett J, Haag J, Borst A. 2009a. Robust coding of ego-motion in descending neurons of the fly. J Neurosci 29: 14993-15000.
75. Wertz A, Haag J, Borst A. 2009b. Local and global motion preferences in descending neurons of the fly. J Comp Physiol 195: 1107-1120.
76. Yasuyama K, Salvaterra PM. 1999. Localization of choline acetyltransferase expressing neurons in Drosophila nervous system. Microsc Res Tech 45: 65-79.
77. Yasuyama K, Kitamoto T, Salvaterra PM. 1995. Immunocytochemical study of choline acetyltransferase in Drosophila melanogaster: an analysis of cis-regulatory regions controlling expression in the brain of cDNA-transformed flies. J Comp Neurol 361: 25-37.
78. Zhang F, Aravanis AM, Adamantidis A, de Lecea L, Deisseroth K. 2007. Circuit-breakers: optical technologies for probing neural signals and systems. Nat Rev Neurosci 8: 577-581.
79. Zhu Y, Nern A, Zipursky SL, Frye MA. 2009. Peripheral visual circuits functionally segregate motion and phototaxis behaviors. Curr Biol 19: 613-619.