Release from the cone ribbon synapse under bright light conditions can be controlled by the opening of only a few Ca 2+ channels

Journal of Neurophysiology

Volumn 106, Issue 6, 2011, Pages 2922-2935

  Bartoletti, Theodore M ^a,b   Jackman, Skyler L ^c   Babai, Norbert ^a   Mercer, Aaron J ^a,b   Kramer, Richard H ^d   Thoreson, Wallace B ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Computer modeling; Electrophysiology; Retina; Synaptic transmission

Indexed keywords

CALCIUM CHANNEL; NEURONAL CALCIUM SENSOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CALCIUM TRANSPORT; CELL FUSION; CELL VACUOLE; CONTROLLED STUDY; DIFFUSION; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HYPERPOLARIZATION; LIGHT INTENSITY; MALE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE STIMULATION; NONHUMAN; PHOTORECEPTOR POTENTIAL; PRIORITY JOURNAL; RETINA; RETINA BIPOLAR GANGLION CELL; RETINA CONE; SALAMANDER; SYNAPSE; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP;

3-PYRIDINECARBOXYLIC ACID, 1,4-DIHYDRO-2,6-DIMETHYL-5-NITRO-4-(2-(TRIFLUOROMETHYL)PHENYL)-, METHYL ESTER; ANIMALS; BARIUM; BIOPHYSICAL PROCESSES; CALCIUM; CALCIUM CHANNEL AGONISTS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CHELATING AGENTS; COMPUTER SIMULATION; EGTAZIC ACID; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; ION CHANNEL GATING; LIGHT; MALE; MODELS, BIOLOGICAL; NIFEDIPINE; PATCH-CLAMP TECHNIQUES; PROBABILITY; RETINA; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL HORIZONTAL CELLS; SYNAPSES; URODELA;

EID: 83055161550     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00634.2011     Document Type: Article

References (76)

1. Ait-Haddou R, Kurachi Y, Nomura T. On calcium-buffer dynamics within the excess buffer regime. J Theor Biol 264: 55-65, 2010.
2. Augustine GJ, Adler EM, Charlton MP. The calcium signal for transmitter secretion from presynaptic nerve terminals. Ann NY Acad Sci 635: 365-681, 1991.
3. Babai N, Bartoletti TM, Thoreson WB. Calcium regulates vesicle replenishment at the cone ribbon synapse. J Neurosci 30: 15866-15877, 2010.
4. Bartoletti TM, Babai N, Thoreson WB. Vesicle pool size at the salamander cone ribbon synapse. J Neurophysiol 103: 419-423, 2010.
5. Beutner D, Voets T, Neher E, Moser T. Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29: 681-690, 2001.
6. Bollmann JH, Sakmann B, Borst JG. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289: 953-957, 2000.
7. Brandt A, Khimich D, Moser T. Few CaV1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 25: 11577-11585, 2005.
8. Brown AM, Kunze DL, Yatani A. The agonist effect of dihydropyridines on Ca channels. Nature 311: 570-572, 1984.
9. Brown AM, Kunze DL, Yatani A. Dual effects of dihydropyridines on whole cell and unitary calcium currents in single ventricular cells of guinea-pig. J Physiol 379: 495-514, 1986.
10. 2+ channels trigger transmitter release at a central GABAergic synapse. Nat Neurosci 13: 19-21, 2010.
11. Burrone J, Neves G, Gomis A, Cooke A, Lagnado L. Endogenous calcium buffers regulate fast exocytosis in the synaptic terminal of retinal bipolar cells. Neuron 33: 101-112, 2002.
12. Cadetti L, Bartoletti TM, Thoreson WB. Quantal mEPSCs and residual glutamate: how horizontal cell responses are shaped at the photoreceptor ribbon synapse. Eur J Neurosci 27: 2575-2586, 2008.
13. 2+ in the cone photoreceptor synaptic terminal. Vis Neurosci 25: 693-700, 2008.
14. Church PJ, Stanley EF. Single L-type calcium channel conductance with physiological levels of calcium in chick ciliary ganglion neurons. J Physiol 496: 59-68, 1996.
15. Coggins M, Zenisek D. Evidence that exocytosis is driven by calcium entry through multiple calcium channels in goldfish retinal bipolar cells. J Neurophysiol 101: 2601-2619, 2009.
16. 2+ current in mammalian cone photoreceptors. Neuron 32: 1107-1117, 2001.
17. Doering CJ, Hamid J, Simms B, McRory JE, Zamponi GW. Cav1.4 encodes a calcium channel with low open probability and unitary conductance. Biophys J 89: 3042-3048, 2005.
18. Duncan G, Rabl K, Gemp I, Heidelberger R, Thoreson WB. Quantitative analysis of synaptic release at the photoreceptor synapse. Biophys J 98: 2102-2110, 2010.
19. Fedchyshyn MJ, Wang LY. Developmental transformation of the release modality at the calyx of Held synapse. J Neurosci 25: 4131-4140, 2005.
20. Fenwick EM, Marty A, Neher E. Sodium and calcium channels in bovine chromaffin cells. J Physiol 331: 599-635, 1982.
21. Fox AP, Nowycky MC, Tsien RW. Single-channel recordings of three types of calcium channels in chick sensory neurones. J Physiol 394: 173-200, 1987.
22. Gollasch M, Hescheler J, Quayle JM, Patlak JB, Nelson MT. Single calcium channel currents of arterial smooth muscle at physiological calcium concentrations. Am J Physiol Cell Physiol 263: C948-C952, 1992.
23. Gray EG, Pease HL. On understanding the organisation of the retinal receptor synapses. Brain Res 35: 1-15, 1971.
24. Hagiwara S, Ohmori H. Studies of single calcium channel currents in rat clonal pituitary cells. J Physiol 336: 649-661, 1983.
25. Heidelberger R, Heinemann C, Neher E, Matthews G. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371: 513-515, 1994.
26. Heidelberger R, Thoreson WB, Witkovsky P. Synaptic transmission at retinal ribbon synapses. Prog Retin Eye Res 24: 682-720, 2005.
27. Hess P, Lansman JB, Tsien RW. Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists. Nature 311: 538-544, 1984.
28. 2+ channels. J Gen Physiol 122: 657-671, 2003.
29. Hosoi N, Arai I, Tachibana M. Group III metabotropic glutamate receptors and exocytosed protons inhibit L-type calcium currents in cones but not in rods. J Neurosci 25: 4062-4072, 2005.
30. Jackman SL, Choi SY, Thoreson WB, Rabl K, Bartoletti TM, Kramer RH. Role of the synaptic ribbon in transmitting the cone light response. Nat Neurosci 12: 303-310, 2009.
31. Jarsky T, Tian M, Singer JH. Nanodomain control of exocytosis is responsible for the signaling capability of a retinal ribbon synapse. J Neurosci 30: 11885-11895, 2010.
32. Kokubun S, Reuter H. Dihydropyridine derivatives prolong the open state of Ca channels in cultured cardiac cells. Proc Natl Acad Sci USA 81: 4824-4827, 1984.
33. Lasansky A. Organization of the outer synaptic layer in the retina of the larval tiger salamander. Philos Trans R Soc Lond B Biol Sci 265: 471-489, 1973.
34. Lisman JE, Raghavachari S, Tsien RW. The sequence of events that underlie quantal transmission at central glutamatergic synapses. Nat Rev Neurosci 8: 597-609, 2007.
35. LoGiudice L, Matthews G. The role of ribbons at sensory synapses. Neuroscientist 15: 380-391, 2009.
36. Lux HD, Brown AM. Patch and whole cell calcium currents recorded simultaneously in snail neurons. J Gen Physiol 83: 727-50, 1984.
37. McDonald TF, Pelzer S, Trautwein W, Pelzer DJ. Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol Rev 74: 365-507, 1994.
38. Mercer AJ, Rabl K, Riccardi GE, Brecha NC, Stella SL Jr, Thoreson WB. Location of release sites and calcium-activated chloride channels relative to calcium channel at the photoreceptor ribbon synapse. J Neurophysiol 105: 321-335, 2011.
39. Mercer AJ, Chen M, Thoreson WB. Lateral mobility of presynaptic L-type calcium channels at photoreceptor ribbon synapses. J Neurosci 31: 4397-4406, 2011.
40. Mintz IM, Sabatini BL, Regehr WG. Calcium control of transmitter release at a cerebellar synapse. Neuron 15: 675-688, 1995.
41. Morgans CW. Localization of the alpha1F calcium channel subunit in the rat retina. Invest Ophthalmol Vis Sci 42: 2414-2418, 2001.
42. Morgans CW, Bayley PR, Oesch NW, Ren G, Akileswaran L, Taylor WR. Photoreceptor calcium channels: insight from night blindness. Vis Neurosci 22: 561-568, 2005.
43. Nachman-Clewner M, St Jules R, Townes-Anderson E. L-type calcium channels in the photoreceptor ribbon synapse: localization and role in plasticity. J Comp Neurol 415: 1-16, 1999.
44. ++ signals. Cell Calcium 24: 345-357, 1998.
45. Pang JJ, Gao F, Barrow A, Jacoby RA, Wu SM. How do tonic glutamatergic synapses evade receptor desensitization? J Physiol 586: 2889-2902, 2008.
46. Prescott ED, Zenisek D. Recent progress towards understanding the synaptic ribbon. Curr Opin Neurobiol 15: 43143-43146, 2005.
47. Rabl K, Cadetti L, Thoreson WB. Kinetics of exocytosis is faster in cones than in rods. J Neurosci 25: 4633-4640, 2005.
48. Raviola E, Gilula NB. Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J Cell Biol 65: 192-222, 1975.
49. Raviola E, Raviola G. Structure of the synaptic membranes in the inner plexiform layer of the retina: a freeze-fracture study in monkeys and rabbits. J Comp Neurol 209: 233-248, 1982.
50. Rieke F, Schwartz EA. Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse. J Physiol 493: 1-8, 1996.
51. 2+ channels in hair cells from bullfrog saccule. J Physiol 538: 729-745, 2002.
52. Sanguinetti MC, Kass RS. Voltage-dependent block of calcium channel current in the calf cardiac Purkinje fiber by dihydropyridine calcium channel antagonists. Circ Res 55: 336-48, 1984.
53. Schmitz F. The making of synaptic ribbons: how they are built and what they do. Neuroscientist 15: 611-624, 2009.
54. Schneggenburger R, Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406: 889-893, 2000.
55. 2+ from one or two channels controls fusion of a single vesicle at the frog neuromuscular junction. J Neurosci 26: 13240-13249, 2006.
56. 2+ in darkness is lower in rods than cones, causing slower tonic release of vesicles. J Neurosci 27: 5033-5042, 2007.
57. Simon SM, Llinás RR. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys J 48: 485-498, 1985.
58. Snellman J, Mehta B, Babai N, Bartoletti TM, Akmentin W, Francis A, Matthews G, Thoreson WB, Zenisek D. Acute destruction of the synaptic ribbon reveals a role for the ribbon in vesicle priming. Nat Neurosci 14: 1135-1141, 2011.
59. Specht D, Wu SB, Turner P, Dearden P, Koentgen F, Wolfrum U, Maw M, Brandstätter JH, tom Dieck S. Effects of presynaptic mutations on a postsynaptic Cacna1s calcium channel colocalized with mGluR6 at mouse photoreceptor ribbon synapses. Invest Ophthalmol Vis Sci 50: 505-515, 2009.
60. Stanley EF. Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron 11: 1007-1011, 1993.
61. 2+ dynamics within the presynaptic terminals of salamander rod photoreceptors. J Neurophysiol 94: 4544-4553, 2005.
62. Sterling P, Matthews G. Structure and function of ribbon synapses. Trends Neurosci 28: 20-29, 2005.
63. Szikra T, Krizaj D. The dynamic range and domain-specific signals of intracellular calcium in photoreceptors. Neuroscience 141: 143-155, 2006.
64. 2+ currents and synaptic transmission in amphibian photoreceptors. J Neurophysiol 77: 2175-2190, 1997.
65. Thoreson WB, Nitzan R, Miller RF. Chloride efflux inhibits single calcium channel open probability in vertebrate photoreceptors: chloride imaging and cell-attached patch-clamp recordings. Vis Neurosci 17: 197-206, 2000.
66. Thoreson WB, Bryson EJ. Chloride equilibrium potential in salamander cones. BMC Neurosci 5: 53, 2004.
67. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42: 595-605, 2004.
68. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, Brauner D, Fejtová A, Bracko O, Gundelfinger ED, Brandstätter JH. 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, 2005.
69. Usukura J, Yamada E. Ultrastructure of the synaptic ribbons in photoreceptor cells of Rana catesbeiana revealed by freeze-etching and freeze-substitution. Cell Tissue Res 247: 483-488, 1987.
70. von Gersdorff H, Sakaba T, Berglund K, Tachibana M. Submillisecond kinetics of glutamate release from a sensory synapse. Neuron 21: 1177-1188, 1998.
71. Wheeler DB, Randall A, Tsien RW. Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science 264: 107-111, 1994.
72. Worley JF 3rd, Kotlikoff MI. Dihydropyridine-sensitive single calcium channels in airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 259: L468-L480, 1990.
73. Wu MM, Llobet A, Lagnado L. Loose coupling between calcium channels and sites of exocytosis in chromaffin cells. J Physiol 587: 5377-5391, 2009.
74. Xu JW, Slaughter MM. Large-conductance calcium-activated potassium channels facilitate transmitter release in salamander rod synapse. J Neurosci 25: 7660-7668, 2005.
75. 2+ channels expressed in mouse cochlear inner hair cells. J Physiol 588: 187-199, 2010.
76. 2+ currents in chicken embryo semicircular canal type I and type II hair cells. J Neurophysiol 96: 602-612, 2006.