Mechanisms contributing to tonic release at the cone photoreceptor ribbon synapse

Journal of Neurophysiology

Volumn 99, Issue 1, 2008, Pages 25-36

  Innocenti, Barbara ^a   Heidelberger, Ruth ^a,b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; EGTAZIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; COMPUTER SIMULATION; ENDOCYTOSIS; FLUORESCENCE; KINETICS; NEUROTRANSMISSION; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA CONE; SALAMANDER; SIGNAL TRANSDUCTION; SYNAPSE;

AMBYSTOMA; ANIMALS; CALCIUM SIGNALING; COMPUTER SIMULATION; CONES (RETINA); ELECTRIC STIMULATION; ENDOCYTOSIS; EXOCYTOSIS; GLUTAMIC ACID; MEMBRANE FUSION; PATCH-CLAMP TECHNIQUES; PHOTOTRANSDUCTION; REACTION TIME; RETINA; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; TIME FACTORS; VISION;

EID: 38349007082     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00737.2007     Document Type: Article

References (100)

1. Ashmore JF, Copenhagen DR. An analysis of transmission from cones to hyperpolarizing bipolar cells in the retina of the turtle. J Physiol 340: 569-597, 1983.
2. Attwell D, Borges S, Wu SM, Wilson M. Signal clipping by the rod output synapse. Nature 328: 522-524, 1987.
3. Attwell D, Wilson M, Wu SM. A quantitative analysis of interactions between photoreceptors in the salamander (Ambystoma) retina. J Physiol 352: 703-737, 1984.
4. Bader CR, Bertrand D. Effect of changes in intra- and extracellular sodium on the inward (anomalous) rectification in salamander photoreceptors. J Physiol 347: 611-631, 1984.
5. Bader CR, Bertrand D, Schwartz EA. Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. J Physiol 331: 253-284, 1982.
6. Barnes S, Deschenes MC. Contribution of Ca and Ca-activated Cl channels to regenerative depolarization and membrane bistability of cone photoreceptors. J Neurophysiol 68: 745-755, 1992.
7. Barnes S, Hille B. Ionic channels of the inner segment of tiger salamander cone photoreceptors. J Gen Physiol 94: 719-743, 1989.
8. Baylor DA, Fuortes MG. Electrical responses of single cones in the retina of the turtle. J Physiol 207: 77-92, 1970.
9. Baylor DA, Fuortes MG, O'Bryan PM. Receptive fields of cones in the retina of the turtle. J Physiol 214: 265-294, 1971.
10. Beaumont V, Llobet A, Lagnado L. Expansion of calcium microdomains regulates fast exocytosis at a ribbon synapse. Proc Natl Acad Sci USA 102: 10700-10705, 2005.
11. Betz WJ, Bewick GS. Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255: 200-203, 1992.
12. 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.
13. 2+ signal. Nat Neurosci 8: 426-434, 2005.
14. Buckley K, Kelly RB. Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J Cell Biol 100: 1284-1294, 1985.
15. 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.
16. Cadetti L, Bryson EJ, Ciccone CA, Rabl K, Thoreson WB. Calcium-induced calcium release in rod photoreceptor terminals boosts synaptic transmission during maintained depolarization. Eur J Neurosci 23: 2983-2990, 2006.
17. Cadetti L, Tranchina D, Thoreson WB. A comparison of release kinetics and glutamate receptor properties in shaping rod-cone differences in EPSC kinetics in the salamander retina. J Physiol 569: 773-788, 2005.
18. 2+ concentration triggering exocytosis in neuroendocrine cells. Proc Natl Acad Sci USA 91: 12765-12769, 1994.
19. Corey DP, Dubinsky JM, Schwartz EA. The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. J Physiol 354: 557-575, 1984.
20. Daly C, Sugimori M, Moreira JE, Ziff EB, Llinás R. Synaptophysin regulates clathrin-independent endocytosis of synaptic vesicles. Proc Natl Acad Sci USA 97: 6120-6125, 2000.
21. De Camilli P, Takei K, McPherson PS. The function of dynamin in endocytosis. Curr Opin Neurobiol 5: 559-565, 1995.
22. DeVries SH. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28: 847-856, 2000.
23. DeVries SH, Li W, Saszik S. Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 50: 735-748, 2006.
24. Fernandez-Alfonso TR, Ryan TA. The efficiency of the synaptic vesicle cycle at central nervous system synapses. Trends Cell Biol 16: 413-420, 2006.
25. Flynn GE, Islas LD, Zagotta WN. Niflumic acid is an allosteric modulator of the sea urchin hyperpolarization-activated cyclic nucleotide-modulated channel. Biophysical Society Meeting Abstracts. Biophys J 90: 1218-Pos, 2006.
26. Fuortes MG, Schwartz EA, Simon EJ. Colour-dependence of cone responses in the turtle retina. J Physiol 234: 199-216, 1973.
27. Gillis KD. Techniques for membrane capacitance measurements. In: Single Channel Recording (2nd ed.), edited by Neher E, Sakmann B. New York: Plenum Press, 1995, p. 155-198.
28. Gold GH, Dowling JE. Photoreceptor coupling in retina of the toad, Bufo marinus. I. Anatomy. J Neurophysiol 42: 292-310, 1979.
29. Gomis A, Burrone J, Lagnado L. Two actions of calcium regulate the supply of releasable vesicles at the ribbon synapse of retinal bipolar cells. J Neurosci 19: 6309-6317, 1999.
30. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
31. Heidelberger R. Electrophysiological approaches to the study of neuronal exocytosis and synaptic vesicle dynamics. Rev Physiol Biochem Pharmacol 143: 1-80, 2001a.
32. Heidelberger R. ATP is required at an early step in compensatory endocytosis in synaptic terminals. J Neurosci 21: 6467-6474, 2001b.
33. Heidelberger R, Matthews G. Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. J Physiol 447: 235-256, 1992.
34. Heidelberger R, Sterling P, Matthews G. Roles of ATP in depletion and replenishment of the releasable pool of synaptic vesicles. J Neurophysiol 88: 98-106, 2002a.
35. Heidelberger R, Thoreson WB, Witkovsky P. Synaptic transmission at retinal ribbon synapses. Prog Retinal Eye Res 24: 682-720, 2005.
36. Heidelberger R, Zhou ZY, Matthews G. Multiple components of membrane retrieval in synaptic terminals revealed by changes in hydrostatic pressure. J Neurophysiol 88: 2509-2517, 2002b.
37. Holt M, Cooke A, Neef A, Lagnado L. High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Curr Biol 14: 173-183, 2004.
38. Horrigan FT, Bookman RJ. Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron 13: 1119-1129, 1994.
39. Hsu SF, Augustine GJ, Jackson MB. Adaptation of Ca(2+)-triggered exocytosis in presynaptic terminals. Neuron 17: 501-512, 1996.
40. Joshi C, Fernandez JM. Capacitance measurements. An analysis of the phase detector technique used to study exocytosis and endocytosis. Biophys J 53: 885-892, 1988.
41. Kushmerick C, Renden R, von Gersdorff H. Physiological temperatures reduce the rate of vesicle pool depletion and short-term depression via an acceleration of vesicle recruitment. J Neurosci 26: 1366-1377, 2006.
42. 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.
43. Lenzi D, Crum J, Ellisman MH, Roberts WM. Depolarization redistributes synaptic membrane and creates a gradient of vesicles on the synaptic body at a ribbon synapse. Neuron 36: 649-659, 2002.
44. Lindau M, Neher E. Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pfluegers Arch 411: 137-146, 1988.
45. MacLeish PR, Barnstable CJ, Townes-Anderson E. Use of a monoclonal antibody as a substrate for mature neurons in vitro. Proc Natl Acad Sci USA 80: 7014-7018, 1983.
46. Mariani AP. Photoreceptors of the larval tiger salamander retina. Proc R Soc Lond B Biol Sci 227: 483-492, 1986.
47. Maricq AV, Korenbrot JI. Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors. Neuron 1: 503-515, 1988.
48. Matsui K, Jahr CE. Ectopic release of synaptic vesicles. Neuron 40: 1173-1183, 2003.
49. Matthews G. Synaptic exocytosis and endocytosis: capacitance measurements. Curr Opin Neurobiol 6: 358-364, 1996.
50. Mennerick S, Matthews G. Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17: 1241-1249, 1996.
51. Messler P, Harz H, Uhl R. Instrumentation for multiwavelengths excitation imaging. J Neurosci Methods 69: 137-147, 1996.
52. Midorikawa M, Tsukamoto Y, Berglund K, Ishii M, Tachibana M. Different roles of ribbon-associated and ribbon-free active zones in retinal bipolar cells. Nat Neurosci 10: 1268-1276, 2007.
53. Moser T, Beutner D. Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc Natl Acad Sci USA 97: 883-888, 2000.
54. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20: 389-399, 1998.
55. Neves G, Lagnado L. The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. J Physiol 515: 181-202, 1999.
56. O'Brien J, Nguyen HB, Mills SL. Cone photoreceptors in bass retina use two connexins to mediate electrical coupling. J Neurosci 24: 5632-5642, 2004.
57. O'Bryan PM. Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina. J Physiol 235: 207-223, 1973.
58. Parsons TD, Lenzi D, Almers W, Roberts WM. Time-resolved studies of calcium-triggered exo- and endocytosis in an isolated presynaptic cell. Neuron 13: 875-883, 1994.
59. Picaud S, Larsson HP, Wellis DP, Lecar H, Werblin F. Cone photoreceptors respond to their own glutamate release in the tiger salamander. Proc Natl Acad Sci USA 92: 9417-9421, 1995a.
60. Picaud SA, Larsson HP, Grant GB, Lecar H, Werblin FS. Glutamate-gated chloride channel with glutamate-transporter-like properties in cone photoreceptors of the tiger salamander. J Neurophysiol 74: 1760-1771, 1995b.
61. Rabl K, Cadetti L, Thoreson WB. Kinetics of exocytosis is faster in cones than in rods. J Neurosci 25: 4633-4640, 2005.
62. Rabl K, Cadetti L, Thoreson WB. Paired-pulse depression at photoreceptor synapses. J Neurosci 26: 2555-2563, 2006.
63. Rabl K, Thoreson WB. Calcium-dependent inactivation and depletion of synaptic cleft calcium ions combine to regulate rod calcium currents under physiological conditions. Eur J Neurosci 16: 2070-2077, 2002.
64. Rabl K, Thoreson WB. Calcium microdomains regulate exocytosis from rods and cones (E-Abstract). Invest Ophthalmol Vis Sci 48: 3224. 2007.
65. Raviola E, Gilula NB. Gap junctions between photoreceptor cells in the vertebrate retina. Proc Natl Acad Sci USA 70: 1677-1681, 1973.
66. Rieke F, Schwartz EA. A cGMP-gated current can control exocytosis at cone synapses. Neuron 13: 863-873, 1994.
67. Rosenmund C, Stevens CF. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207, 1996.
68. Rouze NC, Schwartz EA. Continuous and transient vesicle cycling at a ribbon synapse. J Neurosci 18: 8614-8624, 1998.
69. Sakaba T, Tachibana M, Matsui K, Minami N. Two components of transmitter release in retinal bipolar cells: exocytosis and mobilization of synaptic vesicles. Neurosci Res 27: 357-370, 1997.
70. Satzler K, Sohl LF, Bollmann JH, Borst JG, Frotscher M, Sakmann B, Lubke JH. Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J Neurosci 22: 10567-10579, 2002.
71. Savchenko A, Barnes S, Kramer RH. Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature 390: 694-698, 1997.
72. Saviane C, Silver RA. Fast vesicle reloading and a large pool sustain high bandwidth transmission at a central synapse. Nature 439: 983-987, 2006.
73. Schmitz F, Königstorfer A, Südhof TC. RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28: 857-872, 2000.
74. Schnee ME, Lawton DM, Furness DN, Benke TA, Ricci AJ. Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron 47: 243-254, 2005.
75. Sherry DM, Bui DD, Degrip WJ. Identification and distribution of photoreceptor subtypes in the neotenic tiger salamander retina. Vis Neurosci 15: 1175-1187, 1998.
76. Shupliakov O, Low P, Grabs D, Gad H, Chen H, David C, Takei K, De Camilli P, Brodin L. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276: 259-263, 1997.
77. Sikora MA, Gottesman J, Miller RF. A computational model of the ribbon synapse. J Neurosci Methods 145: 47-61, 2005.
78. 2 acts by two separate pathways to modulate the supply of release-competent vesicles in chromaffin cells. Neuron 20: 1243-1253, 1998.
79. Spassova MA, Avissar M, Furman AC, Crumling MA, Saunders JC, Parsons TD. Evidence that rapid vesicle replenishment of the synaptic ribbon mediates recovery from short-term adaptation at the hair cell afferent synapse. J Assoc Res Otolaryngol 5: 376-390, 2004.
80. Sterling P, Matthews G. Structure and function of ribbon synapses. Trends Neurosci 28: 20-29, 2005.
81. Stevens CF, Tsujimoto T. Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc Natl Acad Sci USA 92: 846-849, 1995.
82. Stevens CF, Wang Y. Facilitation and depression at single central synapses. Neuron 14: 795-802, 1995.
83. Stevens CF, Wesseling JF. Identification of a novel process limiting the rate of synaptic vesicle cycling at hippocampal synapses. Neuron 24: 1017-1028, 1999.
84. Sun JY, Wu LG. Fast kinetics of exocytosis revealed by simultaneous measurements of presynaptic capacitance and postsynaptic currents at a central synapse. Neuron 30: 171-182, 2001.
85. Suryanarayanan A, Slaughter MM. Synaptic transmission mediated by internal calcium stores in rod photoreceptors. J Neurosci 26: 1759-1766, 2006.
86. Taschenberger H, Leao RM, Rowland KC, Spirou GA, von Gersdorff H. Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 36: 1127-1143, 2002.
87. Taylor WR, Morgans C. Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangeri. Vis Neurosci 15: 541-552, 1998.
88. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42: 595-605, 2004.
89. Verweij J, Kamermans M, van den Aker EC, Spekreijse H. Modulation of horizontal cell receptive fields in the light adapted goldfish retina. Vision Res 36: 3913-3923, 1996.
90. von Gersdorff H, Matthews G. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367: 735-739, 1994a.
91. von Gersdorff H, Matthews G. Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 370: 652-655, 1994b.
92. von Gersdorff H, Matthews G. Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. J Neurosci 17: 1919-1927, 1997.
93. von Gersdorff H, Sakaba T, Berglund K, Tachibana M. Submillisecond kinetics of glutamate release from a sensory synapse. Neuron 21: 1177-1188, 1998.
94. von Gersdorff H, Schneggenburger R, Weis S, Neher E. Presynaptic depression at a calyx synapse: the small contribution of metabotropic glutamate receptors. J Neurosci 17: 8137-8146, 1997.
95. von Ruden L, Neher E. A Ca-dependent early step in the release of catecholamines from adrenal chromaffin cells. Science 262: 1061-1065, 1993.
96. Xu J, Wu LG. The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron 46: 633-645, 2005.
97. Yang XL, Wu SM. Response sensitivity and voltage gain of the rod- and cone-horizontal cell synapses in dark- and light-adapted tiger salamander retina. J Neurophysiol 76: 3863-3874, 1996.
98. Zenisek D, Davila V, Wan L, Almers W. Imaging calcium entry sites and ribbon structures in two presynaptic cells. J Neurosci 23: 2538-2548, 2003.
99. Zenisek D, Steyer JA, Almers W. Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406: 849-854, 2000.
100. Zhou ZY, Wan QF, Thakur P, Heidelberger R. Capacitance measurements in the mouse rod bipolar cell identify a pool of releasable synaptic vesicles. J Neurophysiol 96: 2539-2548, 2006.