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Abstract

The first synapses transmitting visual information contain an unusual organelle, the ribbon, which is involved in the transport and priming of vesicles to be released at the active zone. The ribbon is one of many design features that allow efficient refilling of the active zone, which in turn enables graded changes in membrane potential to be transmitted using a continuous mode of neurotransmitter release. The ribbon also plays a key role in supplying vesicles for rapid and transient bursts of release that signal fast changes, such as the onset of light. We increasingly understand how the physiological properties of ribbon synapses determine basic transformations of the visual signal and, in particular, how the process of refilling the active zone regulates the gain and adaptive properties of the retinal circuit. The molecular basis of ribbon function is, however, far from clear.

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2015-11-24
2024-04-16
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Literature Cited

  1. Abbott LF, Regehr WG. 2004. Synaptic computation. Nature 431:796–803 [Google Scholar]
  2. Alpadi K, Magupalli VG, Käppel S, Köblitz L, Schwarz K. et al. 2008. RIBEYE recruits Munc119, the mammalian ortholog of the Caenorhabditis elegans protein unc119 to synaptic ribbons of photoreceptor synapses. J. Biol. Chem. 283:26461–67 [Google Scholar]
  3. Asari H, Meister M. 2012. Divergence of visual channels in the inner retina. Nat. Neurosci. 15:1581–89 [Google Scholar]
  4. Baccus SA, Meister M. 2002. Fast and slow contrast adaptation in retinal circuitry. Neuron 36:909–19 [Google Scholar]
  5. Baden T, Berens P, Bethge M, Euler T. 2013a. Spikes in mammalian bipolar cells support temporal layering of the inner retina. Curr. Biol. 23:48–52 [Google Scholar]
  6. Baden T, Esposti F, Nikolaev A, Lagnado L. 2011. Spikes in retinal bipolar cells phase-lock to visual stimuli with millisecond precision. Curr. Biol. 21:1859–69 [Google Scholar]
  7. Baden T, Euler T, Weckstrom M, Lagnado L. 2013b. Spikes and ribbon synapses in early vision. Trends Neurosci. 36:480–88 [Google Scholar]
  8. Baden T, Nikolaev A, Esposti F, Dreosti E, Odermatt B, Lagnado L. 2014. A synaptic mechanism for temporal filtering of visual signals. PLOS Biol. 12:e1001972 [Google Scholar]
  9. Balasubramanian V, Sterling P. 2009. Receptive fields and functional architecture in the retina. J. Physiol. 587:2753–67 [Google Scholar]
  10. Ball SL, McEnery MW, Yunker AMR, Shin H-S, Gregg RG. 2011. Distribution of voltage gated calcium channel β-subunits in the mouse retina. Brain Res. 1412:1–8 [Google Scholar]
  11. Ball SL, Powers PA, Shin H-S, Morgans CW, Peachey NS, Gregg RG. 2002. Role of the β2 subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. Investig. Ophthalmol. Vis. Sci. 43:1595–603 [Google Scholar]
  12. Beaudoin DL, Borghuis BG, Demb JB. 2007. Cellular basis for contrast gain control over the receptive field center of mammalian retinal ganglion cells. J. Neurosci. 27:2636–45 [Google Scholar]
  13. Beaumont V, Llobet A, Lagnado L. 2005. Expansion of calcium microdomains regulates fast exocytosis at a ribbon synapse. PNAS 102:10700–5 [Google Scholar]
  14. Bech-Hansen NT, Naylor MJ, Maybaum TA, Sparkes RL, Koop B. et al. 2000. Mutations in NYX, encoding the leucine-rich proteoglycan nyctalopin, cause X-linked complete congenital stationary night blindness. Nat. Genet. 26:319–23 [Google Scholar]
  15. Benucci A, Saleem AB, Carandini M. 2013. Adaptation maintains population homeostasis in primary visual cortex. Nat. Neurosci. 16:724–29 [Google Scholar]
  16. Berglund K, Midorikawa M, Tachibana M. 2002. Increase in the pool size of releasable synaptic vesicles by the activation of protein kinase C in goldfish retinal bipolar cells. J. Neurosci. 22:4776–85 [Google Scholar]
  17. Boycott KM, Maybaum TA, Naylor MJ, Weleber RG, Robitaille J. et al. 2001. A summary of 20 CACNA1F mutations identified in 36 families with incomplete X-linked congenital stationary night blindness, and characterization of splice variants. Hum. Genet. 108:91–97 [Google Scholar]
  18. Buraei Z, Yang Y. 2010. The β-subunit of voltage-gated Ca2+ channels. Physiol. Rev. 90:1461–506 [Google Scholar]
  19. Burrone J, Lagnado L. 1997. Electrical resonance and Ca2+ influx in the synaptic terminal of depolarizing bipolar cells from the Goldfish retina. J. Physiol. 505:571–84 [Google Scholar]
  20. Burrone J, Lagnado L. 2000. Synaptic depression and the kinetics of exocytosis in retinal bipolar cells. J. Neurosci. 20:568–78 [Google Scholar]
  21. Burrone J, Neves G, Gomis A, Cooke A, Lagnado L. 2002. Endogenous calcium buffers regulate fast exocytosis in the synaptic terminal of retinal bipolar cells. Neuron 33:101–12 [Google Scholar]
  22. Burtscher V, Schicker K, Novikova E, Pöhn B, Stockner T. et al. 2014. Spectrum of Cav1.4 dysfunction in congenital stationary night blindness type 2. Biochim. Biophys. Acta 1838:2053–65 [Google Scholar]
  23. Busquet P, Nguyen NK, Schmid E, Tanimoto N, Seeliger MW. et al. 2010. CaV1.3 L-type Ca2+-channels modulate depression-like behaviour in mice independent of deaf phenotype. Int. J. Neuropsychopharmacol. 13:499–513 [Google Scholar]
  24. Catterall WA. 2011. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol. 3:a003947 [Google Scholar]
  25. Catterall WA, Perez-Reyes E, Snutch TP, Striessnig J. 2005. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol. Rev. 57:411–25 [Google Scholar]
  26. Cao Y, Posokhova E, Martemyanov KA. 2011. TRPM1 forms complexes with nyctalopin in vivo and accumulates in postsynaptic compartment of ON-bipolar neurons in mGluR6-dependent manner. J. Neurosci. 31:11521–26 [Google Scholar]
  27. Chang B, Heckenlively JR, Bayley PR, Brecha NC, Davisson MT. et al. 2006. The nob2 mouse, a null mutation in Cacna1f: anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses. Vis. Neurosci. 23:11–24 [Google Scholar]
  28. Chávez AE, Singer JH, Diamond JS. 2006. Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors. Nature 443:705–8 [Google Scholar]
  29. Chen M, Van Hook MJ, Zenisek D, Thoreson WB. 2013. Properties of ribbon and non-ribbon release from rod photoreceptors revealed by visualizing individual synaptic vesicles. J. Neurosci. 33:2071–86 [Google Scholar]
  30. Chinnadurai G. 2009. The transcriptional corepressor CtBP: a foe of multiple tumor suppressors. Cancer Res. 69:731–34 [Google Scholar]
  31. Choi SY, Jackman S, Thoreson WB, Kramer RH. 2008. Light regulation of Ca2+ in the cone photoreceptor synaptic terminal. Vis. Neurosci. 25:693–700 [Google Scholar]
  32. Connaughton VP, Graham D, Nelson R. 2004. Identification and morphological classification of horizontal, bipolar, and amacrine cells within the zebrafish retina. J. Comp. Neurol. 477:371–85 [Google Scholar]
  33. Cooper B, Hemmerlein M, Ammermüller J, Imig C, Reim K. et al. 2012. Munc13-independent vesicle priming at mouse photoreceptor ribbon synapses. J. Neurosci. 32:8040–52 [Google Scholar]
  34. Corda D, Colanzi A, Luini A. 2006. The multiple activities of CtBP/BARS proteins: the Golgi view. Trends Cell Biol. 16:167–73 [Google Scholar]
  35. Cui J, Pan Z-H. 2008. Two types of cone bipolar cells express voltage-gated Na+ channels in the rat retina. Vis. Neurosci. 25:635–45 [Google Scholar]
  36. Davydova D, Marini C, King C, Klueva J, Bischof F. et al. 2014. Bassoon specifically controls presynaptic P/Q-type Ca2+ channels via RIM-binding protein. Neuron 82:181–94 [Google Scholar]
  37. Dembla M, Wahl S, Katiyar R, Schmitz F. 2014. ArfGAP3 is a component of the photoreceptor synaptic ribbon complex and forms an NAD(H)-regulated, redox-sensitive complex with RIBEYE that is important for endocytosis. J. Neurosci. 34:5245–60 [Google Scholar]
  38. Deng L, Kaeser PS, Xu W, Südhof TC. 2011. RIM proteins activate vesicle priming by reversing autoinhibitory homodimerization of Munc13. Neuron 69:317–31 [Google Scholar]
  39. DeVries SH. 2000. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28:847–56 [Google Scholar]
  40. DeVries SH, Li W, Saszik S. 2006. Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 50:735–48 [Google Scholar]
  41. DeVries SH, Schwartz EA. 1999. Kainate receptors mediate synaptic transmission between cones and ‘Off’ bipolar cells in a mammalian retina. Nature 397:157–60 [Google Scholar]
  42. Dick O, Hack I, Altrock WD, Garner CC, Gundelfinger ED, Brandstätter JH. 2001. Localization of the presynaptic cytomatrix protein Piccolo at ribbon and conventional synapses in the rat retina: comparison with Bassoon. J. Comp. Neurol. 439:224–34 [Google Scholar]
  43. Dick O, tom Dieck S, Altrock WD, Ammermüller J, Weiler R. et al. 2003. The presynaptic active zone protein Bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37:775–86 [Google Scholar]
  44. Dobrunz LE, Stevens CF. 1999. Response of hippocampal synapses to natural stimulation patterns. Neuron 22:157–66 [Google Scholar]
  45. Doering CJ, Peloquin JB, McRory JE. 2007. The CaV1.4 calcium channel: more than meets the eye. Channels 1:4–11 [Google Scholar]
  46. Dowling JE, Ripps H. 1973. Effect of magnesium on horizontal cell activity in the skate retina. Nature 242:101–3 [Google Scholar]
  47. Dreosti E, Esposti F, Baden T, Lagnado L. 2011. In vivo evidence that retinal bipolar cells generate spikes modulated by light. Nat. Neurosci. 14:951–52 [Google Scholar]
  48. Dreosti E, Odermatt B, Dorostkar M, Lagnado L. 2009. A genetically encoded reporter of synaptic activity in vivo. Nat. Methods 6:883–89 [Google Scholar]
  49. Dunn FA, Rieke F. 2006. The impact of photoreceptor noise on retinal gain controls. Curr. Opin. Neurobiol. 16:363–70 [Google Scholar]
  50. Dunn FA, Rieke F. 2008. Single-photon absorptions evoke synaptic depression in the retina to extend the operational range of rod vision. Neuron 57:894–904 [Google Scholar]
  51. Esposti F, Johnston J, Rosa JM, Leung K-M, Lagnado L. 2013. Olfactory stimulation selectively modulates the OFF pathway in the retina of zebrafish. Neuron 79:97–110 [Google Scholar]
  52. Fenster SD, Chung WJ, Zhai R, Cases-Langhoff C, Voss B. et al. 2000. Piccolo, a presynaptic zinc-finger protein, structurally related to Bassoon. Neuron 25:203–14 [Google Scholar]
  53. Frank T, Khimich D, Neef A, Moser T. 2009. Mechanisms contributing to synaptic Ca2+ signals and their heterogeneity in hair cells. PNAS 106:4483–88 [Google Scholar]
  54. Frank T, Rutherford MA, Strenzke N, Neef A, Pangršič T. et al. 2010. Bassoon and the synaptic ribbon organize Ca2+ channels and vesicles to add release sites and promote refilling. Neuron 68:724–38 [Google Scholar]
  55. Gollisch T, Meister M. 2008. Modeling convergent ON and OFF pathways in the early visual system. Biol. Cybern. 99:263–78 [Google Scholar]
  56. Gollisch T, Meister M. 2010. Eye smarter than scientists believed: neural computations in circuits of the retina. Neuron 65:150–64 [Google Scholar]
  57. Gomis A, Burrone J, Lagnado L. 1999. Two actions of calcium regulate the supply of releasable vesicles at the ribbon synapse of retinal bipolar cells. J. Neurosci. 19:6309–17 [Google Scholar]
  58. Gray EG, Pease HL. 1971. On understanding the organization of the retinal receptor synapses. Brain Res. 35:1–15 [Google Scholar]
  59. Gregg RG, Kamermans M, Klooster J, Lukasiewicz PD, Peachey NS. et al. 2007. Nyctalopin expression in retinal bipolar cells restores visual function in a mouse model of complete X-linked congenital stationary night blindness. J. Neurophysiol. 98:3023–33 [Google Scholar]
  60. Gundelfinger ED, Fejtova A. 2012. Molecular organization and plasticity of the cytomatrix at the active zone. Curr. Opin. Neurobiol. 22:423–30 [Google Scholar]
  61. Han Y, Kaeser PS, Südhof TC, Schneggenburger R. 2011. RIM determines Ca2+ channel density and vesicle docking at the presynaptic active zone. Neuron 69:304–16 [Google Scholar]
  62. Heidelberger R, Matthews G. 1992. Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. J. Physiol. 447:235–56 [Google Scholar]
  63. Heidelberger R, Heinemann C, Neher E, Matthews G. 1994. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 37:513–15 [Google Scholar]
  64. Heidelberger R, Thoreson WB, Witkovsky P. 2005. Synaptic transmission at retinal ribbon synapses. Prog. Retin. Eye Res. 24:682–720 [Google Scholar]
  65. Hibino H, Pironkova R, Onwumere O, Vologodskaia M, Hudspeth AJ, Lesage F. 2002. RIM-binding proteins (RBPs) couple Rab3-interacting molecules (RIMs) to voltage-gated Ca2+ channels. Neuron 34:411–23 [Google Scholar]
  66. Hirokawa N. 2000. Stirring up development with heterotrimeric kinesin KIF3. Traffic 1:29–34 [Google Scholar]
  67. Hoda J-C, Zaghetto F, Koschak A, Striessnig J. 2005. Congenital stationary night blindness type 2 mutations S229P, G369D, L1068P, and W1440X alter channel gating or functional expression of CaV1.4 L-type Ca2+ channels. J. Neurosci. 25:252–59 [Google Scholar]
  68. Holt M, Cooke A, Neef A, Lagnado L. 2004. High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Curr. Biol. 14:173–83 [Google Scholar]
  69. Holt M, Cooke A, Wu MM, Lagnado L. 2003. Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells. J. Neurosci. 23:1329–39 [Google Scholar]
  70. Hu C, Bi A, Pan Z-H. 2009. Differential expression of three T-type calcium channels in retinal bipolar cells in rats. Vis. Neurosci. 26:177–87 [Google Scholar]
  71. Hull C, von Gersdorff H. 2004. Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal. Neuron 44:469–82 [Google Scholar]
  72. Jackman SL, Choi SY, Thoreson WB, Rabl K, Bartoletti TM, Kramer RH. 2009. Role of the synaptic ribbon in transmitting the cone light response. Nat. Neurosci. 12:303–10 [Google Scholar]
  73. Jarsky T, Cembrowski M, Logan SM, Kath WL, Riecke H. et al. 2011. A synaptic mechanism for retinal adaptation to luminance and contrast. J. Neurosci. 31:11003–15 [Google Scholar]
  74. Jockusch WJ, Praefcke GJK, McMahon HT, Lagnado L. 2005. Clathrin-dependent and clathrin-independent retrieval of synaptic vesicles in retinal bipolar cells. Neuron 46:869–78 [Google Scholar]
  75. Johnson S, Halford S, Morris AG, Patel RJ, Wilkie SE. et al. 2003. Genomic organisation and alternative splicing of human RIM1, a gene implicated in autosomal dominant cone-rod dystrophy (CORD7). Genomics 81:304–14 [Google Scholar]
  76. Juusola M, French AS, Uusitalo RO, Weckstrom M. 1996. Information processing by graded-potential transmission through tonically active synapses. Trends Neurosci. 19:292–97 [Google Scholar]
  77. Kaeser PS, Deng L, Wang Y, Dulubova I, Liu X. et al. 2011. RIM tethers Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 144:282–95 [Google Scholar]
  78. Kaur T, Nawy S. 2012. Characterization of Trpm1 desensitization in ON bipolar cells and its role in downstream signalling. J. Physiol. 590:1179–92 [Google Scholar]
  79. Kawai F, Horiguchi M, Ichinose H, Ohkuma M, Isobe R, Miyachi E. 2005. Suppression by an h current of spontaneous Na+ action potentials in human cone and rod photoreceptors. Investig. Ophthalmol. Vis. Sci. 46:390–97 [Google Scholar]
  80. Kawai F, Horiguchi M, Suzuki H, Miyachi E. 2001. Na+ action potentials in human photoreceptors. Neuron 30:451–58 [Google Scholar]
  81. Kiyonaka S, Nakajima H, Takada Y, Hida Y, Yoshioka T. et al. 2012. Physical and functional interaction of the active zone protein CAST/ERC2 and the β-subunit of the voltage-dependent Ca2+ channel. J. Biochem. 152:149–59 [Google Scholar]
  82. Kiyonaka S, Wakamori M, Miki T, Uriu Y, Nonaka M. et al. 2007. RIM1 confers sustained activity and neurotransmitter vesicle anchoring to presynaptic Ca2+ channels. Nat. Neurosci. 10:691–701 [Google Scholar]
  83. Lagnado L, Gomis A, Job C. 1996. Continuous vesicle cycling in the synaptic terminal of retinal bipolar cells. Neuron 17:957–67 [Google Scholar]
  84. Lenzi D, von Gersdorff H. 2001. Structure suggests function: the case for synaptic ribbons as exocytotic nanomachines. Bioessays 23:831–40 [Google Scholar]
  85. Limbach C, Laue MM, Wang X, Hu B, Thiede N. et al. 2011. Molecular in situ topology of Aczonin/Piccolo and associated proteins at the mammalian neurotransmitter release site. PNAS 108:392–401 [Google Scholar]
  86. Liu C, Bickford LS, Held RG, Nyitrai H, Südhof TC, Kaeser PS. 2014. The active zone protein family ELKS supports Ca2+ influx at nerve terminals of inhibitory hippocampal neurons. J. Neurosci. 34:12289–303 [Google Scholar]
  87. Liu X, Kerov V, Haeseleer F, Majumder A, Artemyev N. et al. 2013. Dysregulation of CaV1.4 channels disrupts the maturation of photoreceptor synaptic ribbons in congenital stationary night blindness type 2. Channels 7:514–23 [Google Scholar]
  88. Llobet A, Beaumont V, Lagnado L. 2003. Real-time measurement of exocytosis and endocytosis using interference of light. Neuron 40:1075–86 [Google Scholar]
  89. Llobet A, Gallop JL, Burden JJE, Camdere G, Chandra P. et al. 2011. Endophilin drives the fast mode of vesicle retrieval in a ribbon synapse. J. Neurosci. 31:8512–19 [Google Scholar]
  90. LoGiudice L, Matthews G. 2007. Endocytosis at ribbon synapses. Traffic 8:1123–28 [Google Scholar]
  91. LoGiudice L, Sterling P, Matthews G. 2008. Mobility and turnover of vesicles at the synaptic ribbon. J. Neurosci. 28:3150–58 [Google Scholar]
  92. Ma Y-P, Pan Z-H. 2003. Spontaneous regenerative activity in mammalian retinal bipolar cells: roles of multiple subtypes of voltage-dependent Ca2+ channels. Vis. Neurosci. 20:131–39 [Google Scholar]
  93. Magupalli VG, Schwarz K, Alpadi K, Natarajan S, Seigel GM, Schmitz F. 2008. Multiple RIBEYE–RIBEYE interactions create a dynamic scaffold for the formation of synaptic ribbons. J. Neurosci. 28:7954–67 [Google Scholar]
  94. Manookin MB, Demb JB. 2006. Presynaptic mechanism for slow contrast adaptation in mammalian retinal ganglion cells. Neuron 50:453–64 [Google Scholar]
  95. Masland RH. 2012. The neuronal organization of the retina. Neuron 76:266–80 [Google Scholar]
  96. Mattapallil MJ, Wawrousek EF, Chan C-C, Zhao H, Roychoudhury J. et al. 2012. The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. Investig. Ophthalmol. Vis. Sci. 53:2921–27 [Google Scholar]
  97. Matthews G, Fuchs P. 2010. The diverse role of ribbon synapses in sensory neurotransmission. Nat. Rev. Neurosci. 11:812–22 [Google Scholar]
  98. Matthews G, Sterling P. 2008. Evidence that vesicles undergo compound fusion on the synaptic ribbon. J. Neurosci. 28:5403–11 [Google Scholar]
  99. Mehalow AK, Kameya S, Smith RS, Hawes NL, Denegre JM. et al. 2003. CRB1 is essential for external limiting membrane integrity and photoreceptor morphogenesis in the mammalian retina. Hum. Mol. Genet. 12:2179–89 [Google Scholar]
  100. Mennerick S, Matthews G. 1996. Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17:1241–49 [Google Scholar]
  101. Mercer AJ, Chen M, Thoreson WB. 2011. Lateral mobility of presynaptic L-type calcium channels at photoreceptor ribbon synapses. J. Neurosci. 31:4397–406 [Google Scholar]
  102. Mercer AJ, Thoreson WB. 2011. The dynamic architecture of photoreceptor ribbon synapses: cytoskeletal, extracellular matrix, and intramembrane proteins. Vis. Neurosci. 28:453–71 [Google Scholar]
  103. Michaelides M, Holder GE, Hunt DM, Fitzke FW, Bird AC, Moore AT. 2005. A detailed study of the phenotype of an autosomal dominant cone-rod dystrophy (CORD7) associated with mutation in the gene for RIM1. Br. J. Ophthalmol. 89:198–206 [Google Scholar]
  104. Michalakis S, Shaltiel S, Sothilingam V, Koch S, Schludi V. et al. 2014. Mosaic synaptopathy and functional defects in Cav1.4 heterozygous mice and human carriers of CSNB2. Hum. Mol. Genet. 23:1538–50 [Google Scholar]
  105. Midorikawa M, Tsukamoto Y, Berglund K, Ishii M, Tachibana M. 2007. Different roles of ribbon-associated and ribbon-free active zones in retinal bipolar cells. Nat. Neurosci. 766:1268–76 [Google Scholar]
  106. Morgans CW, Bayley PR, Oesch N, Ren G, Akileswaran L, Taylor WR. 2005. Photoreceptor calcium channels: insight from night blindness. Vis. Neurosci. 22:561–68 [Google Scholar]
  107. Morgans CW, Ren G, Akileswaran L. 2006. Localization of nyctalopin in the mammalian retina. Eur. J. Neurosci. 23:1163–71 [Google Scholar]
  108. Moser T, Brandt A, Lysakowski A. 2006a. Hair cell ribbon synapses. Cell Tissue Res. 326:347–59 [Google Scholar]
  109. Moser T, Neef A, Khimich D. 2006b. Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. J. Physiol. 576:55–62 [Google Scholar]
  110. Muresan V, Lyass A, Schnapp BJ. 1999. The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors. J. Neurosci. 19:1027–37 [Google Scholar]
  111. Nakamura M, Sanuki R, Yasuma TR, Onishi A, Nishiguchi KM. et al. 2010. TRPM1 mutations are associated with the complete form of congenital stationary night blindness. Mol. Vis. 16:425–37 [Google Scholar]
  112. Neves G, Gomis A, Lagnado L. 2001. Calcium influx selects the fast mode of endocytosis in the synaptic terminal of retinal bipolar cells. PNAS 98:15282–87 [Google Scholar]
  113. Neves G, Lagnado L. 1999. The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. J. Physiol. 515:181–202 [Google Scholar]
  114. Nikolaev A, Leung K-M, Odermatt B, Lagnado L. 2013. Synaptic mechanisms of adaptation and sensitization. Nat. Neurosci. 16:934–41 [Google Scholar]
  115. Nouvian R, Beutner D, Parsons TD, Moser T. 2006. Structure and function of the hair cell ribbon synapse. J. Membr. Biol. 209:153–65 [Google Scholar]
  116. Odermatt B, Nikolaev A, Lagnado L. 2012. Encoding of luminance and contrast by linear and nonlinear synapses in the retina. Neuron 73:758–73 [Google Scholar]
  117. Oesch N, Diamond J. 2009. A night vision neuron gets a day job. Nat. Neurosci. 12:1209–11 [Google Scholar]
  118. Oesch NW, Diamond JS. 2011. Ribbon synapses compute temporal contrast and encode luminance in retinal rod bipolar cells. Nat. Neurosci. 14:1555–61 [Google Scholar]
  119. Ohtsuka T. 2013. CAST: functional scaffold for the integrity of the presynaptic active zone. Neurosci. Res. 76:10–15 [Google Scholar]
  120. Ozuysal Y, Baccus SA. 2012. Linking the computational structure of variance adaptation to biophysical mechanisms. Neuron 73:1002–15 [Google Scholar]
  121. Palmer MJ. 2006. Modulation of Ca2+-activated K+ currents and Ca2+-dependent action potentials by exocytosis in goldfish bipolar cell terminals. J. Physiol. 572:747–62 [Google Scholar]
  122. Pan Z-H, Hu H-J. 2000. Voltage-dependent Na+ currents in mammalian retinal cone bipolar cells. J. Neurophysiol. 84:2564–71 [Google Scholar]
  123. Pan Z-H, Hu H-J, Perring P, Andrade R. 2001. T-type Ca2+ channels mediate neurotransmitter release in retinal bipolar cells. Neuron 32:89–98 [Google Scholar]
  124. Parsons TD, Sterling P. 2003. Synaptic ribbon: conveyor belt or safety belt?. Neuron 37:379–82 [Google Scholar]
  125. Perge JA, Koch K, Miller R, Sterling P, Balasubramanian V. 2009. How the optic nerve allocates space, energy capacity, and information. J. Neurosci. 29:7917–28 [Google Scholar]
  126. Piatigorsky J. 2001. Dual use of the transcriptional corepressor (CtBP2)/ribbon synapse (RIBEYE) gene: How prevalent are multifunctional genes?. Trends Neurosci. 24:555–57 [Google Scholar]
  127. Protti DA, Flores-Herr N, von Gersdorff H. 2000. Light evokes Ca2+ spikes in the axon terminal of a retinal bipolar cell. Neuron 25:215–27 [Google Scholar]
  128. Pusch CM, Zeitz C, Brandau O, Pesch K, Achatz H. et al. 2000. The complete form of X-linked congenital stationary night blindness is caused by mutations in a gene encoding a leucine-rich repeat protein. Nat. Genet. 26:324–27 [Google Scholar]
  129. Rabl K, Cadetti L, Thoreson WB. 2005. Kinetics of exocytosis is faster in cones than in rods. J. Neurosci. 25:4633–40 [Google Scholar]
  130. Rea R, Li J, Dharia A, Levitan ES, Sterling P, Kramer RH. 2004. Streamlined synaptic vesicle cycle in cone photoreceptor terminals. Neuron 41:755–66 [Google Scholar]
  131. Regus-Leidig H, Fuchs M, Löhner M, Leist SR, Leal-Ortiz S. et al. 2014. In vivo knockdown of Piccolino disrupts presynaptic ribbon morphology in mouse photoreceptor synapses. Front. Cell. Neurosci. 8:259 [Google Scholar]
  132. Regus-Leidig H, Ott C, Löhner M, Atorf J, Fuchs M. et al. 2013. Identification and immuncytochemical characterization of Piccolino, a novel Piccolo splice variant selectively expressed at sensory ribbon synapses of the eye and ear. PLOS ONE 8:70373 [Google Scholar]
  133. Rieke F, Schwartz EA. 1996. Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse. J. Physiol. 493:1–8 [Google Scholar]
  134. Rizzoli SO, Betz WJ. 2005. Synaptic vesicle pools. Nat. Rev. Neurosci. 6:57–69 [Google Scholar]
  135. Rouze NC, Schwartz EA. 1998. Continuous and transient vesicle cycling at a ribbon synapse. J. Neurosci. 18:8614–24 [Google Scholar]
  136. Saszik S, DeVries SH. 2012. A mammalian retinal bipolar cell uses both graded changes in membrane voltage and all-or-nothing Na+ spikes to encode light. J. Neurosci. 32:297–307 [Google Scholar]
  137. Schoch S, Gundelfinger ED. 2006. Molecular organization of the presynaptic active zone. Cell Tissue Res. 326:379–91 [Google Scholar]
  138. Schmitz F. 2009. The making of synaptic ribbons: How they are built and what they do. Neuroscientist 15:611–24 [Google Scholar]
  139. Schmitz F. 2014. Presynaptic [Ca2+] and GCAPs: aspects on the structure and function of photoreceptor ribbon synapses. Front. Mol. Neurosci. 7:3 [Google Scholar]
  140. Schmitz F, Augustin I, Brose N. 2001. The synaptic vesicle priming protein Munc13-1 is absent from tonically active ribbon synapses of the rat retina. Brain Res. 895:258–63 [Google Scholar]
  141. 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 28:857–72 [Google Scholar]
  142. Schmitz F, Natarajan S, Venkatesan JK, Wahl S, Schwarz K, Grabner CP. 2012. EF hand-mediated Ca2+- and cGMP-signaling in photoreceptor synaptic terminals. Front. Mol. Neurosci. 5:26 [Google Scholar]
  143. Schwartz G, Rieke F. 2011. Nonlinear spatial encoding by retinal ganglion cells: when 1 + 1 ≠ 2. J. Gen. Physiol. 138:283–90 [Google Scholar]
  144. Schwarz K, Natarajan S, Kassas N, Vitale N, Schmitz F. 2011. . The synaptic ribbon is a site of phosphatidic acid generation in ribbon synapses. J. Neurosci. 31:15996–6011 [Google Scholar]
  145. Shaltiel L, Paparizos C, Fenske S, Hassan S, Gruner C. et al. 2012. Complex regulation of voltage-dependent activation and inactivation properties of retinal voltage-gated Cav1.4 L-type Ca2+ channels by Ca2+-binding protein 4 (CaBP4). J. Biol. Chem. 287:4336312–21 [Google Scholar]
  146. Sheets L, Hagen NW, Nicolson T. 2014. Ribeye subunits in zebrafish hair cells reveals that exogenous Ribeye B-domain and CtBP1 localize to the basal end of the synaptic ribbons. PLOS ONE 9:e107256 [Google Scholar]
  147. Sheets L, Kindt KS, Nicolson T. 2012. Presynaptic CaV1.3 channels regulate synaptic ribbon size and are required for synaptic maintenance in sensory hair cells. J. Neurosci. 32:17273–86 [Google Scholar]
  148. Sheets L, Trapani JG, Mo W, Obholzer N, Nicolson T. 2011. Ribeye is required for presynaptic CaV1.3a channel localization and afferent innervation of sensory hair cells. Development 138:1309–19 [Google Scholar]
  149. Shen Y, Rampino MA, Carroll RC, Nawy S. 2012. G-protein-mediated inhibition of the Trp channel (TRPM1) requires the Gbg dimer. PNAS 109:8752–57 [Google Scholar]
  150. Silver RA. 2010. Neuronal arithmetic. Nat. Rev. Neurosci. 11:474–89 [Google Scholar]
  151. Singer JH, Diamond JS. 2006. Vesicle depletion and synaptic depression at a mammalian ribbon synapse. J. Neurophysiol. 95:3191–98 [Google Scholar]
  152. Singh A, Hamedinger D, Hoda J-C, Gebhart M, Koschak A. et al. 2006. C-terminal modulator controls Ca2+-dependent gating of CaV1.4 L-type Ca2+ channels. Nat. Neurosci. 9:1108–16 [Google Scholar]
  153. Smirnakis SM, Berry MJ, Warland DK, Bialek W, Meister M. 1997. Adaptation of retinal processing to image contrast and spatial scale. Nature 386:69–73 [Google Scholar]
  154. Snellman J, Kaur T, Shen Y, Nawy S. 2008. Regulation of ON bipolar cell activity. Prog. Retin. Eye Res. 27:450–63 [Google Scholar]
  155. Snellman J, Mehta B, Babai N, Bartoletti TM, Akmentin W. et al. 2011. Acute destruction of the synaptic ribbon reveals a role for the ribbon in vesicle priming. Nat. Neurosci. 14:1135–41 [Google Scholar]
  156. Specht D, Wu SB, Turner P, Dearden P, Koentgen F. et al. 2009. Effects of presynaptic mutations on a postsynaptic Cacna1s calcium channel colocalized with mGluR6 at mouse photoreceptor ribbon synapses. Investig. Ophthalmol. Vis. Sci. 50:505–15 [Google Scholar]
  157. Sterling P, Matthews G. 2005. Structure and function of ribbon synapses. Trends Neurosci. 28:20–29 [Google Scholar]
  158. Striessnig J, Bolz HJ, Koschak A. 2010. Channelopathies in CaV1.1, CaV1.3, and CaV1.4 voltage-gated L-type Ca2+ channels. Pflügers Arch. 460:361–74 [Google Scholar]
  159. Südhof TC. 2012a. Calcium control of neurotransmitter release. Cold Spring Harb. Perspect. Biol. 4a011353
  160. Südhof TC. 2012b. The presynaptic active zone. Neuron 75:11–25 [Google Scholar]
  161. Südhof TC. 2013. A molecular machine for neurotransmitter release: synaptotagmin and beyond. Nat. Med. 19:1227–31 [Google Scholar]
  162. Südhof TC. 2014. The molecular machinery of neurotransmitter release (Nobel lecture). Angew. Chem. Int. Ed. 53:12696–717 [Google Scholar]
  163. Suh B, Baccus SA. 2014. Building blocks of temporal filters in retinal synapses. PLOS Biol. 12:e1001973 [Google Scholar]
  164. Takao-Rikitsu E, Mochida S, Inoue E, Deguchi-Tawarada M, Inoe M. et al. 2004. Physical and functional interaction of the active zone proteins, CAST, RIM1 and Bassoon, in neurotransmitter release. J. Cell Biol. 164:301–11 [Google Scholar]
  165. Tarr TB, Dittrich M, Meriney SD. 2013. Are unreliable release mechanisms conserved from NMJ to CNS?. Trends Neurosci. 36:14–22 [Google Scholar]
  166. Thoreson WB. 2007. Kinetics of synaptic transmission at ribbon synapses of rods and cones. Mol. Neurobiol. 36:205–23 [Google Scholar]
  167. Thoreson WB, Mercer AJ, Cork KM, Szalewski RJ. 2013. Lateral mobility of L-type calcium channels in synaptic terminals of retinal bipolar cells. Mol. Vis. 19:16–24 [Google Scholar]
  168. Thoreson WB, Rabl K, Townes-Anderson E, Heidelberger R. 2004. A highly Ca2+-sensitive pool of synaptic vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42:595–605 [Google Scholar]
  169. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H. et al. 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. 168:825–36 [Google Scholar]
  170. tom Dieck S, Brandstätter JH. 2006. Ribbon synapses of the retina. Cell Tissue Res. 326:339–46 [Google Scholar]
  171. tom Dieck S, Sanmarti-Vila L, Langnaese K, Richter K, Kindler S. et al. 1998. Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals. J. Cell Biol. 142:499–509 [Google Scholar]
  172. tom Dieck S, Specht D, Strenzke N, Hida Y, Krishnamoorthy V. et al. 2012. Deletion of the presynaptic scaffold CAST reduces active zone size in rod photoreceptors and impairs visual processing. J. Neurosci. 32:12192–203 [Google Scholar]
  173. Vaithianathan T, Akmentin W, Henry D, Matthews G. 2013. The ribbon-associated protein C-terminal-binding protein 1 is not essential for the structure and function of retinal ribbon synapses. Mol. Vis. 19:917–26 [Google Scholar]
  174. Vaithianathan T, Matthews G. 2014. Visualizing synaptic vesicle turnover and pool refilling driven by calcium nanodomains at presynaptic active zones of ribbon synapses. PNAS 111:8655–60 [Google Scholar]
  175. Van Hook MJ, Thoreson WB. 2012. Rapid synaptic vesicle endocytosis in cone photoreceptors of salamander retina. J. Neurosci. 32:18112–11123 [Google Scholar]
  176. Venkatesan JK, Natarajan S, Schwarz K, Mayer SI, Alpadi K. et al. 2010. Nicotinamide adenine dinucleotide-dependent binding of the neuronal Ca2+ sensor protein GCAP2 to photoreceptor synaptic ribbons. J. Neurosci. 30:6559–76 [Google Scholar]
  177. von Gersdorff H. 2001. Synaptic ribbons: versatile signal transducers. Neuron 29:7–10 [Google Scholar]
  178. von Gersdorff H, Matthews G. 1994. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367:735–39 [Google Scholar]
  179. von Gersdorff H, Sakaba T, Berglund K, Tachibana M. 1998. Submillisecond kinetics of glutamate release from a sensory synapse. Neuron 21:1177–88 [Google Scholar]
  180. Wahl S, Katiyar R, Schmitz F. 2013. A local, periactive zone endocytic machinery at photoreceptor synapses in close vicinity to synaptic ribbons. J. Neurosci. 33:10278–300 [Google Scholar]
  181. Wang X, Kibschull M, Laue MM, Lichte B, Petrasch-Parwez E, Kilimann MW. 1999. Aczonin, a 550-kD putative scaffolding protein of presynaptic active zones, shares homology regions with Rim and Bassoon and binds profilin. J. Cell Biol. 147:151–62 [Google Scholar]
  182. Wang Y, Okamoto M, Schmitz F, Hofmann K, Südhof TC. 1997. RIM is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 388:593–98 [Google Scholar]
  183. Wang Y, Liu X, Biederer T, Südhof TC. 2002. A family of RIM-binding proteins regulated by alternative splicing: implications for the genesis of synaptic active zones. PNAS 99:14464–69 [Google Scholar]
  184. Wark B, Lundstrom BN, Fairhall A. 2007. Sensory adaptation. Curr. Opin. Neurobiol. 17:423–29 [Google Scholar]
  185. Wässle H. 2004. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5:747–57 [Google Scholar]
  186. Wycisk KA, Budde B, Feil S, Skosyrski S, Buzzi F. et al. 2006. Structural and functional abnormalities of retinal ribbon synapses due to Cacna2d4 mutation. Investig. Ophthalmol. Vis. Sci. 47:3523–30 [Google Scholar]
  187. Zabouri N, Haverkamp S. 2013. Calcium channel-dependent molecular maturation of photoreceptor synapses. PLOS ONE 8:e63853 [Google Scholar]
  188. Zenisek D. 2008. Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals. PNAS 105:4922–27 [Google Scholar]
  189. Zenisek D, Henry D, Studholme K, Yazulla S, Matthews G. 2001. Voltage-dependent sodium channels are expressed in nonspiking retinal bipolar neurons. J. Neurosci. 21:4543–50 [Google Scholar]
  190. Zenisek D, Steyer JA, Almers W. 2000. Transport, capture and exocytosis of synaptic vesicles at active zones. Nature 406:849–54 [Google Scholar]
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