Synaptic circuits of the Drosophila optic lobe: The input terminals to the medulla

Journal of Comparative Neurology

Volumn 509, Issue 5, 2008, Pages 493-513

  Takemura, Shin Ya ^a   Lu, Zhiyuan ^a   Meinertzhagen, Ian A ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Column; Fly; Photoreceptors; Tetrad; Triad; Visual pathway

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL POPULATION; CELL SHAPE; CELL STRUCTURE; CELL TYPE; DROSOPHILA; ELECTRON MICROSCOPY; GOLGI COMPLEX; MEDULLA OBLONGATA; NEUROPIL; NONHUMAN; OPTIC LOBE; PHOTORECEPTOR; PRIORITY JOURNAL; SYNAPSE; VISUAL SYSTEM;

ANIMALS; DROSOPHILA; MEDULLA OBLONGATA; NERVE NET; OPTIC LOBE, NONMAMMALIAN; SYNAPSES; VISUAL PATHWAYS;

EID: 41549110431     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21757     Document Type: Article

References (78)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Bausenwein B, Fischbach K-F. 1992. Activity labeling patterns in the medulla of Drosophila melanogaster caused by motion stimuli. Cell Tissue Res 270:25-35.
3. Bausenwein B, Dittrich APM, Fischbach K-F. 1992. The optic lobe of Drosophila melanogaster II. Sorting of retinotopic pathways in the medulla. Cell Tissue Res 267:17-28.
4. Bodian D. 1962. The generalized vertebrate neuron. Science 137:323-326.
5. Borst A. 2000. Models of motion detection. Nat Neurosci 3(suppl):1168.
6. Borst A, Egelhaaf M. 1989. Principles of visual motion detection. Trends Neurosci 12:297-306.
7. Borycz JA, Borycz J, Kubow A, Kostyleva R, Meinertzhagen IA. 2005. Histamine compartments of the Drosophila brain with an estimate of the quantum content at the photoreceptor synapse. J Neurophysiol 93:1611-1619.
8. Boschek CB. 1971. On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. Z Zeilforsch Mikrosk Anat 118:369-409.
9. Braitenberg V. 1967. Patterns of projection in the visual system of the fly. I. Retina-lamina projections. Exp Brain Res 3:271-298.
10. Braitenberg V. 1970. Ordnung und Orientierung der Elemente im Sehsystem der Fliege. Kybernetik 7:235-242
11. Braitenberg V, Debbage P. 1974. A regular net of reciprocal synapses in the visual system of the fly, Musca domestica. J Comp Physiol 90:25-31.
12. Braitenberg V, Hauser-Holschuh H. 1972. Patterns of projection in the visual system of the fly II. Quantitative aspects of second order neurons in relation to models of movement perception. Exp Brain Res 16:184-209.
13. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
14. Buchner E, Bader R, Buchner S, Cox J, Emson PC, Flory E, Heizmann CW, Hemm S, Hofbauer A, Oertel WH. 1988. Cell-specific immuno-probes for the brain of normal and mutant Drosophila melanogaster. I. Wildtype visual system. Cell Tissue Res 253:357-370.
15. Campos-Ortega JA, Strausfeld NJ. 1972. Columns and layers in the second synaptic region of the fly's visual system: the case for two superimposed neuronal architectures. In: Wehner R, editor. Information processing in the visual systems of arthropods. New York: Springer-Verlag. p 31-36.
16. 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.
17. Cohen E, Sterling P. 1990. Demonstration of cell types among cone bipolar neurons of cat retina. Philos Trans Biol Sci 330:305-321.
18. Cook T, Desplan C. 2001. Photoreceptor subtype specification: from flies to humans. Semin Cell Dev Biol 12:509-18.
19. 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.
20. Douglass JK, Strausfeld NJ. 1996. Visual motion detection circuits in flies: parallel direction- and non-direction-sensitive pathways between medulla and lobula plate. J Neurosci 16:4551-4562.
21. Dowling JE. 1987. The retina. Cambridge, MA: Harvard University Press.
22. Dowling, JE, Boycott BB. 1966. Organization of the primate retina: electron microscopy. Proc R Soc Lond B 166:80-111.
23. Fabian-Fine R, Verstreken P, Hiesinger PR, Horne JA, Kostyleva R, Zhou Y, Bellen HJ, Meinertzhagen IA. 2003. Endophilin promotes a late step in endocytosis at glial invaginations in Drosophila photoreceptor terminals. J Neurosci 23:10732-10744.
24. Fiala JC. 2005. Reconstruct: a free editor for serial section microscopy. J Microsc 218:52-61
25. Fiala JC, Harris KM. 2001. Extending unbiased stereology of brain ultrastructure to three-dimensional volumes. J Am Med Inform Assoc 8:1-16.
26. Fischbach K-F, Dittrich APM. 1989. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441-475.
27. Franceschini N, Kirschfeld K, Minke B. 1981. Fluorescence of photoreceptor cells observed in vivo. Science 213:1264-1267.
28. Hardie RC. 1984. Properties of photoreceptors R7 and R8 in dorsal marginal ommatidia in the compound eyes of Musca and Calliphora. J Comp Physiol A 154:157-165.
29. Hardie RC. 1985. Functional organization of the fly retina. In: Autrum H, Ottoson D, Perl ER, Schmidt RF, Shimazu H, Willis WD, editors. Progress in sensory physiology, vol 5. New York: Springer-Verlag. p 1-79.
30. Hardie RC. 1989. Neurotransmitters in compound eyes. In: Stavenga DG, Hardie RC, editors. Facets of vision. New York: Springer-Verlag. p 235-256.
31. Hardie RC, Kirschfeld K. 1983. Ultraviolet sensitivity of fly photoreceptor-R7 and photoreceptor-R8 - evidence for a sensitizing function. Biophys Struct Mech 9:171-180.
32. Hausen K. 1984. The lobula-complex of the fly: structure, function and significance in visual behavior. In: Ali, MA, editor. Photoreception and vision in invertebrates. New York: Plenum Press. p 523-559
33. Heisenberg M, Buchner E. 1977. The rôle of retinula cell types in visual behaviour of Drosophila melanogaster. J Comp Physiol 117:127-162.
34. Jack JJB, Noble D, Tsien RW. 1975. Electric current flow in excitable cells. Oxford: Clarendon Press.
35. Kolodziejczyk A, Sun X, Meinertzhagen, IA, Nässel DR. 2008. Glutamate, GABA and acetylcholine signaling components in the lamina of the fly's Drosophila visual system. PLoS ONE 3:e2110.
36. 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.
37. Langley K, Grant NJ. 1997. Are exocytosis mechanisms neurotransmitter specific? Neurochem Int 31:739-757.
38. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461.
39. Masland RH. 2004. Neuronal cell types. Curr Biol 14:R497-500.
40. Meinertzhagen IA. 1976. The organization of perpendicular fibre pathways in the insect optic lobe. Philos Trans R Soc Lond B 274:555-596.
41. Meinertzhagen IA. 1996. Ultrastructure and quantification of synapses in the insect nervous system. J Neurosci Methods 69:59-73.
42. Meinertzhagen IA. 2001. Plasticity in the insect nervous system. Adv Insect Physiol 28:84-167.
43. Meinertzhagen IA, O'Neil SD. 1991. The synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J Comp Neurol 305:232-263.
44. Meinertzhagen IA, Sorra KE. 2001. Synaptic organisation in the fly's optic lamina: few cells, many synapses and divergent microcircuits. Prog Brain Res 131:53-69.
45. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, Alon U. 2002. Network motifs: simple building blocks of complex networks. Science 298:824-827.
46. Morante J, Desplan C. 2004. Building a projection map for photoreceptor neurons in the Drosophila optic lobes. Semin Cell Dev Biol 15:137-43.
47. Morante J, Desplan C. 2008. The color-vision in the medulla of Drosophila. Curr Biol 18:553-565.
48. Nicol D, Meinertzhagen IA. 1982. An analysis of the number and composition of the synaptic populations formed by photoreceptors of the fly. J Comp Neurol 207:29-44.
49. 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.
50. Palay SF, Chan-Palay V. 1974. Cerebellar cortex: cytology and organization. New York: Springer-Verlag.
51. Pichaud F, Briscoe A, Desplan C. 1999. Evolution of color vision. Curr Opin Neurobiol 9:622-627.
52. Pollack I, Hofbauer A. 1991. Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster. Cell Tissue Res 266:391-398.
53. Rall W, Burke RE, Holmes WR, Jack JJ, Redman SJ, Segev I. 1992. Matching dendritic neuron models to experimental data. Physiol Rev 72(suppl):S159-186.
54. Ramón y Cajal S, Sánchez D. 1915. Contribution al conocimiento de los centros nerviosos de los insectos. Trab Lab Invest Biol (Madrid) 13:1-167.
55. Ready DF, Hanson TE, Benzer S. 1976. Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53:217-240.
56. Reichardt, W. 1961. Autocorrelation, a principle for the evaluation of sensory information by the central nervous system. In: Rosenblith, WA, editor. Sensory communication, Cambridge, MA: MIT Press. p 303-317.
57. Rein K, Zöckler M, Mader MT, Grübel C, Heisenberg M. 2002. The Drosophila standard brain. Curr Biol 12:227-231.
58. 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.
59. 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.
60. Shaw SR. 1984. Early visual processing in insects. J Exp Biol 112:225-251.
61. Sinakevitch I, Strausfeld NJ. 2004. Chemical neuroanatomy of the fly's movement detection pathway. J Comp Neurol 468:6-23.
62. Sinakevitch I, Douglass JK, Scholtz G, Loesel R, Strausfeld NJ. 2003. Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa. J Comp Neurol 467:150-172.
63. Stark WS, Carlson SD. 1986. Ultrastructure of capitate projections in the optic neuropil of Diptera. Cell Tissue Res 246:481-486.
64. Sterling P. 1998. Retina. In: Shepherd GM, editor. The synaptic organization of the brain, 4 ed. New York: Oxford University Press. p 205-253.
65. Strausfeld NJ. 1970. Golgi studies on insects. Part II: The optic lobes of Diptera. Philos Trans R Soc Lond B 258:135-223.
66. Strausfeld NJ. 1971. The organization of the insect visual system (light microscopy). I. Projections and arrangements of neurons in the lamina ganglionaris of Diptera. Z Zellforsch 121:377-441.
67. Strausfeld NJ. 1976. Atlas of an insect brain. Springer-Verlag, Berlin, Heidelberg.
68. Strausfeld NJ. 1984. Functional neuroanatomy of the blowfly's visual system. In: Ali MA, editor. Photoreception and vision in invertebrates. New York: Plenum. p 483-522.
69. Strausfeld NJ, Campos-Ortega JA. 1972. Some interrelationships between the first and second synaptic regions of the fly's (Musca domestica L.) visual system. In: Wehner R, editor. Information processing in the visual systems of arthropods. New York: Springer-Verlag. p 23-30.
70. Strausfeld NJ, Campos-Ortega JA. 1977. Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition. Science 195:894-897.
71. Strausfeld NJ, Lee JK. 1991. Neuronal basis for parallel visual processing in the fly. Vis Neurosci 7:13-33.
72. Takemura SY, Arikawa K. 2006. Ommatidial type-specific interphotoreceptor connections in the lamina of the swallowtail butterfly, Papilio xuthus. J Comp Neurol 494:663-672.
73. Troje N. 1993. Spectral categories in the learning behaviour of blowflies. Z Naturforsch C 48:96-104.
74. Trujillo-Cenóz O. 1965. Some aspects of the structural organization of the intermediate retina of dipterans. J Ultrastruct Res 13:1-33.
75. 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 115:267-79.
76. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B 314:1-340.
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. Zheng L, de Polavieja GG, Wolfram V, Asyali MH, Hardie RC, Juusola M. 2006. Feedback network controls photoreceptor output at the layer of first visual synapses in Drosophila. J Gen Physiol 127:495-510.