Regular mosaic of synaptic contacts among three retinal neurons

Journal of Comparative Neurology

Volumn 519, Issue 2, 2011, Pages 341-357

  Koizumi, Amane ^a   Jakobs, Tatjana C ^b   Masland, Richard H ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b National Institute for Natural Sciences   (Japan)

Author keywords

Mosaic; Retina; Spacing; Synapse

Indexed keywords

GREEN FLUORESCENT PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; FEMALE; MALE; MOSAICISM; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RETINA AMACRINE CELL; RETINA BIPOLAR GANGLION CELL; RETINA INNER PLEXIFORM LAYER; RETINA NERVE CELL; SYNAPTIC TRANSMISSION;

AMACRINE CELLS; ANIMALS; MEMBRANE PROTEINS; RABBITS; RECOMBINANT FUSION PROTEINS; RETINA; RETINAL BIPOLAR CELLS; RETINAL GANGLION CELLS; SYNAPSES;

EID: 78650237930     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22522     Document Type: Article

References (89)

1. Amthor FR, Takahashi ES, Oyster CW. 1989a. Morphologies of rabbit retinal ganglion cells with complex receptive fields. J Comp Neurol 280: 97-121.
2. Amthor FR, Takahashi ES, Oyster CW. 1989b. Morphologies of rabbit retinal ganglion cells with concentric receptive fields. J Comp Neurol 280: 72-96.
3. Barlow H, Levick W. 1965. The mechanism of directionally selective units in rabbit's retina. J Physiol 178: 477-504.
4. Ben-Ari Y. 2002. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3: 728-739.
5. Blackshaw SE, Nicholls JG, Parnas I. 1982. Physiological responses, receptive fields and terminal arborizations of nociceptive cells in the leech. J Physiol 326: 251-260.
6. Brown SP, Masland RH. 1999. Costratification of a population of bipolar cells with the direction-selective circuitry of the rabbit retina. J Comp Neurol 408: 97-106.
7. Calkins DJ, Tsukamoto Y, Sterling P. 1998. Microcircuitry and mosaic of a blue-yellow ganglion cell in the primate retina. J Neurosci 18: 3373-3385.
8. Carnevale NT, Hines ML. 2006. The NEURON book. Cambridge, UK: Cambridge University Press.
9. Chakrarvarti IM, Laha RG, Roy J. 1967. Handbook of methods of applied statistics. New York: John Wiley & Sons.
10. Chen BL, Hall DH, Chklovskii DB. 2006. Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci U S A 103: 4723-4728.
11. Chklovskii DB, Schikorski T, Stevens CF. 2002. Wiring optimization in cortical circuits. Neuron 34: 341-347.
12. Cook JE. 1996. Spatial properties of retinal mosaics: an empirical evaluation of some existing measures. Vis Neurosci 13: 15-30.
13. Cook JE, Becker DL, Kapila R. 1992. Independent mosaics of large inner-and outer-stratified ganglion cells in the goldfish retina. J Comp Neurol 318: 355-366.
14. Dacey DM. 1993. Morphology of a small-field bistratified ganglion cell type in the macaque and human retina. Vis Neurosci 10: 1081-1098.
15. Dickman DK, Lu Z, Meinertzhagen IA, Schwarz TL. 2006. Altered synaptic development and active zone spacing in endocytosis mutants. Curr Biol 16: 591-598.
16. Engström K. 1963. Cone types and cone arrangements in teleost retinae. Acta Zool 44: 179-243.
17. Euler T, Detwiler PB, Denk W. 2002. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418: 845-852.
18. Famiglietti EV. 1992. Dendritic co-stratification of ON and ON-OFF directionally selective ganglion cells with starburst amacrine cells in rabbit retina. J Comp Neurol 324: 322-335.
19. Famiglietti EV. 2005. Synaptic organization of complex ganglion cells in rabbit retina: type and arrangement of inputs to directionally selective and local-edge-detector cells. J Comp Neurol 484: 357-391.
20. Freed MA, Sterling P. 1988. The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. J Neurosci 8: 2303-2320.
21. Fuerst PG, Koizumi A, Masland RH, Burgess RW. 2008. Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 451: 470-474.
22. Grueber WB, Graubard K, Truman JW. 2001. Tiling of the body wall by multidendritic sensory neurons in Manduca sexta. J Comp Neurol 440: 271-283.
23. Grueber WB, Jan LY, Jan YN. 2002. Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129: 2867-2878.
24. He S, Masland RH. 1998. ON direction-selective ganglion cells in the rabbit retina: dendritic morphology and pattern of fasciculation. Vis Neurosci 15: 369-375.
25. Hibbard E. 1971. Grid patterns in the retinal organization of the cichlid fish Astronotus ocellatus. Exp Eye Res 12: 175-180.
26. Hines ML, Carnevale NT. 1997. The NEURON simulation environment. Neural Comput 9: 1179-1209.
27. Hirano AA, Brandstatter JH, Vila A, Brecha NC. 2007. Robust syntaxin-4 immunoreactivity in mammalian horizontal cell processes. Vis Neurosci 24: 489-502.
28. Jacoby RA, Wiechmann AF, Amara SG, Leighton BH, Marshak DW. 2000. Diffuse bipolar cells provide input to OFF parasol ganglion cells in the macaque retina. J Comp Neurol 416: 6-18.
29. Jakobs TC, Ben Y, Masland RH. 2003. CD15 immunoreactive amacrine cells in the mouse retina. J Comp Neurol 465: 361-371.
30. Jakobs TC, Koizumi A, Masland RH. 2008. The spatial distribution of glutamatergic inputs to dendrites of retinal ganglion cells. J Comp Neurol 510: 221-236.
31. Jan YN, Jan LY. 2003. The control of dendrite development. Neuron 40: 229-242.
32. Jeon CJ, Kong JH, Strettoi E, Rockhill R, Stasheff SF, Masland RH. 2002. Pattern of synaptic excitation and inhibition upon direction-selective retinal ganglion cells. J Comp Neurol 449: 195-205.
33. Klyachko VA, Stevens CF. 2003. Connectivity optimization and the positioning of cortical areas. Proc Natl Acad Sci U S A 100: 7937-7941.
34. Koizumi A, Jakobs TC, Masland RH. 2004. Inward rectifying currents stabilize the membrane potential in dendrites of mouse amacrine cells: patch-clamp recordings and single-cell RT-PCR. Mol Vis 10: 328-340.
35. Koizumi A, Hayashida Y, Kiuchi T, Yamada Y, Fujii A, Yagi T, Kaneko A. 2005. The interdependence and independence of amacrine cell dendrites: patch-clamp recordings and simulation studies on cultured GABAergic amacrine cells. J Integr Neurosci 4: 363-380.
36. Koizumi A, Zeck G, Ben Y, Masland RH, Jakobs TC. 2007. Organotypic culture of physiologically functional adult Mammalian retinas. PLoS ONE 2: e221.
37. Levick WR. 1967. Receptive fields and trigger features of ganglion cells in the visual streak of the rabbits retina. J Physiol 188: 285-307.
38. Li W, Keung JW, Massey SC. 2004. Direct synaptic connections between rods and OFF cone bipolar cells in the rabbit retina. J Comp Neurol 474: 1-12.
39. Lin B, Masland RH. 2005. Synaptic contacts between an identified type of ON cone bipolar cell and ganglion cells in the mouse retina. Eur J Neurosci 21: 1257-1270.
40. Lin B, Masland RH, Strettoi E. 2009. Remodeling of cone photoreceptor cells after rod degeneration in rd mice. Exp Eye Res 88: 589-599.
41. Lo DC, McAllister AK, Katz LC. 1994. Neuronal transfection in brain slices using particle-mediated gene transfer. Neuron 13: 1263-1268.
42. Mack AF. 2007. Evidence for a columnar organization of cones, Muller cells, and neurons in the retina of a cichlid fish. Neuroscience 144: 1004-1014.
43. MacNeil MA, Heussy JK, Dacheux RF, Raviola E, Masland RH. 2004. The population of bipolar cells in the rabbit retina. J Comp Neurol 472: 73-86.
44. Macri J, Martin PR, Grünert U. 2000. Distribution of the alpha1 subunit of the GABA(A) receptor on midget and parasol ganglion cells in the retina of the common marmoset Callithrix jacchus. Vis Neurosci 17: 437-448.
45. Marquardt T, Gruss P. 2002. Generating neuronal diversity in the retina: one for nearly all. Trends Neurosci 25: 32-38.
46. Massey SC, Mills SL. 1996. A calbindin-immunoreactive cone bipolar cell type in the rabbit retina. J Comp Neurol 366: 15-33.
47. McArdle CB, Dowling JE, Masland RH. 1977. Development of outer segments and synapses in the rabbit retina. J Comp Neurol 175: 253-274.
48. McGillem GS, Dacheux RF. 2001. Rabbit cone bipolar cells: correlation of their morphologies with whole-cell recordings. Vis Neurosci 18: 675-685.
49. Megias M, Emri Z, Freund TF, Gulyas AI. 2001. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102: 527-540.
50. Meinertzhagen IA, Hu X. 1996. Evidence for site selection during synaptogenesis: the surface distribution of synaptic sites in photoreceptor terminals of the files Musca and Drosophila. Cell Mol Neurobiol 16: 677-698.
51. Meinertzhagen IA, Govind CK, Stewart BA, Carter JM, Atwood HL. 1998. Regulated spacing of synapses and presynaptic active zones at larval neuromuscular junctions in different genotypes of the flies Drosophila and Sarcophaga. J Comp Neurol 393: 482-492.
52. Milam AH, Dacey DM, Dizhoor AM. 1993. Recoverin immunoreactivity in mammalian cone bipolar cells. Vis Neurosci 10: 1-12.
53. Mills SL, Massey SC. 1992. Morphology of bipolar cells labeled by DAPI in the rabbit retina. J Comp Neurol 321: 133-149.
54. Morgan JL, Schubert T, Wong RO. 2008. Developmental patterning of glutamatergic synapses onto retinal ganglion cells. Neural Dev 3: 8.
55. Nicholls JG, Baylor DA. 1968. Specific modalities and receptive fields of sensory neurons in CNS of the leech. J Neurophysiol 31: 740-756.
56. O'Brien BJ, Isayama T, Richardson R, Berson DM. 2002. Intrinsic physiological properties of cat retinal ganglion cells. J Physiol 538( Pt 3): 787-802.
57. Oesch N, Euler T, Taylor WR. 2005. Direction-selective dendritic action potentials in rabbit retina. Neuron 47: 739-750.
58. Panico J, Sterling P. 1995. Retinal neurons and vessels are not fractal but space-filling. J Comp Neurol 361: 479-490.
59. Podugolnikova TA. 1985a. Inner plexiform layer of jack mackerel retina: participation of amacrine and ganglion cells in its spatial organization. Vision Res 25: 1853-1864.
60. Podugolnikova TA. 1985b. Morphology of bipolar cells and their participation in spatial organization of the inner plexiform layer of jack mackerel retina. Vision Res 25: 1843-1851.
61. Reese BE, Galli-Resta L. 2002. The role of tangential dispersion in retinal mosaic formation. Prog Retin Eye Res 21: 153-168.
62. Rockhill RL, Euler T, Masland RH. 2000. Spatial order within but not between types of retinal neurons. Proc Natl Acad Sci U S A 97: 2303-2307.
63. Rockhill RL, Daly FJ, MacNeil MA, Brown SP, Masland RH. 2002. The diversity of ganglion cells in a mammalian retina. J Neurosci 22: 3831-3843.
64. Rodieck RW. 1991. The density recovery profile: a method for the analysis of points in the plane applicable to retinal studies. Vis Neurosci 6: 95-111.
65. Roska B, Werblin F. 2001. Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410: 583-587.
66. Roska B, Molnar A, Werblin FS. 2006. Parallel processing in retinal ganglion cells: how integration of space-time patterns of excitation and inhibition form the spiking output. J Neurophysiol 95: 3810-3822.
67. Schmitz F, Königstorfer A, Südhof TC. 2000. RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28: 857-872.
68. Shepherd GM. 2003. The synaptic organization of the brain. Shepherd GM, editor. New York: Oxford University Press.
69. Shepherd GM, Raastad M. 2003. Axonal varicosity distributions along parallel fibers: a new angle on a cerebellar circuit. Cerebellum 2: 110-113.
70. Shepherd GM, Raastad M, Andersen P. 2002. General and variable features of varicosity spacing along unmyelinated axons in the hippocampus and cerebellum. Proc Natl Acad Sci U S A 99: 6340-6345.
71. Sivyer B, Taylor WR, Vaney DI. 2010. Uniformity detector retinal ganglion cells fire complex spikes and receive only light-evoked inhibition. Proc Natl Acad Sci U S A 107: 5628-5633.
72. Song S, Sjostrom PJ, Reigl M, Nelson S, Chklovskii DB. 2005. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol 3: e68.
73. Stevens JK, McGuire BA, Sterling P. 1980. Toward a functional architecture of the retina: serial reconstruction of adjacent ganglion cells. Science 207: 317-319.
74. Taylor WR, He S, Levick WR, Vaney DI. 2000. Dendritic computation of direction selectivity by retinal ganglion cells. Science 289: 2347-2350.
75. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, Brauner D, Fejtova A, Bracko O, Gundelfinger ED, Brandstätter JH. 2005. Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J Cell Biol 168: 825-836.
76. Trexler EB, Li W, Mills SL, Massey SC. 2001. Coupling from AII amacrine cells to ON cone bipolar cells is bidirectional. J Comp Neurol 437: 408-422.
77. Van Haesendonck E, Missotten L. 1983. Stratification and square pattern arrangements in the dorsal inner plexiform layer in the retina of Callionymus lyra L. J Ultrastruct Res 83: 296-302.
78. Van Haesendonck E, Missotten L. 1991. Patterns of glutamate-like immunoreactive bipolar cell axons in the retina of the marine teleost, the dragonet. Vision Res 31: 451-462.
79. Van Wyk M, Taylor WR, Vaney DI. 2006. Local edge detectors: a substrate for fine spatial vision at low temporal frequencies in rabbit retina. J Neurosci 26: 13250-13263.
80. Wagner HJ. 1976. The connectivity of cones and cone horizontal cells in a mosaic-type teleost retina. Cell Tissue Res 175: 85-100.
81. Wässle H. 2004. Parallel processing in the mammalian retina. Nat Rev Neurosci 5: 747-757.
82. Wässle H, Riemann HJ. 1978. The mosaic of nerve cells in the mammalian retina. Proc R Soc Lond B Biol Sci 200: 441-461.
83. Wässle H, Boycott BB, Illing RB. 1981. Morphology and mosaic of on-and off-beta cells in the cat retina and some functional considerations. Proc R Soc Lond B Biol Sci 212: 177-195.
84. Wässle H, Puller C, Muller F, Haverkamp S. 2009. Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J Neurosci 29: 106-117.
85. Werblin F, Roska B, Balya D. 2001. Parallel processing in the mammalian retina: lateral and vertical interactions across stacked representations. Prog Brain Res 131: 229-238.
86. Xu Y, Vasudeva V, Vardi N, Sterling P, Freed MA. 2008. Different types of ganglion cell share a synaptic pattern. J Comp Neurol 507: 1871-1878.
87. Young RW. 1985. Cell differentiation in the retina of the mouse. Anat Rec 212: 199-205.
88. Zhang J, Li W, Trexler EB, Massey SC. 2002. Confocal analysis of reciprocal feedback at rod bipolar terminals in the rabbit retina. J Neurosci 22: 10871-10882.
89. Zheng JJ, Lee S, Zhou ZJ. 2004. A developmental switch in the excitability and function of the starburst network in the mammalian retina. Neuron 44: 851-864.