Transmission at the photoreceptor synapse

Progress in Brain Research

Volumn 131, Issue , 2001, Pages 145-159

  Witkovsky, Paul ^a   Thoreson, Wallace ^b   Tranchina, Daniel ^c  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE TRANSPORTER; GLUTAMIC ACID;

CALCIUM CURRENT; HUMAN; NEUROTRANSMISSION; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RETINA CONE; RETINA ROD; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 0035783953     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/s0079-6123(01)31013-0     Document Type: Review

References (80)

1. Akopian, A., Johnson, J., Gabriel, R., Brecha, N. and Witkovsky, P. (2000) Somatostatin modulates voltage-gated K and Ca currents in rod and cone photoreceptors of the salamander retina. J. Neurosci., 20: 929-936.
2. Arriza, J.L., Fairman, W.A., Wadiche, J.I., Murdoch, G.H., Kavanaugh, M.P. and Amara, S.G. (1994) Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J. Neurosci., 14: 5559-5569.
3. Artalejo, C., Mogul, D., Perlman, R.L. and Fox, A.P. (1991) Three types of bovine chromaffin cell Ca2+ channels: Facilitation increases the opening probability of a 27 pS channel. J. Physiol., 444: 213-240.
4. Attwell, D., Borges, S., Wu, S.M. and Wilson, M. (1987) Signal clipping by the rod output synapse. Nature, 328: 522-524.
5. Augustine, G.J., Adler, E.M. and Charlton, M.P. (1991) The calcium signal for transmitter secretion from presynaptic nerve terminals. NY Acad. Sci., 635: 365-381.
6. Augustine, G.J., Betz, H., Bommert, K., Charlton, M.P., deBello, W.M., Hans, M. and Swandulla, D. (1994) Molecular pathways for presynaptic calcium signaling. In: Stjarne, L., Greengard, P., Grillner, S., Hokfelt, T. and Ottoson, D. (Eds.), Molecular and Cellular Mechanisms of Neurotransmitter Release. Raven Press, NY.
7. Augustine, G.J. and Neher, E. (1992) Calcium requirements for secretion in bovine chromaffin cells. J. Physiol., 450: 247-271.
8. Bader, C.R., Bertrand, D. and Schwartz, E.A. (1982) Voltage- activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. J. Physiol., 331: 253-284.
9. Barbour, B., Brew, H. and Attwell, D. (1991) Electrogenic uptake of glutamate and aspartate into glial cells isolated from the salamander (Amblystoma) retina. J. Physiol., 436: 169-193.
10. Barnes, S., Merchant, V. and Mahmud, F. (1993) Modulation of transmission gain by protons at the photoreceptor output synapse. Proc. Natl. Acad. Sci., 90: 10081-10085.
11. Belgum, H.J. and Copenhagen, D.R. (1988) Synaptic transfer of rod signals to horizontal and bipolar cells in the retina of the toad (Bufo marinus). J. Physiol., 396: 225-245.
12. Brandstatter, J.H., Koulen, P., Kuhn, R., van der Putten, H. and Wassle, H. (1996) Compartmental localization of a metabotropic glutamate receptor (mGluR7): Two different active sites at a retinal synapse. J. Nezirosci. 16: 4749-4756.
13. Brandstatter, J.H., Koulen, P. and Wassle, H. (1998) Diversity of glutamate receptors in the mammalian retina. Vision Res., 38: 1385-1397.
14. Cahill, G.M. and Besharse,J.C. (1992) Light-sensitive melatonin synthesis by Xenopus photoreceptors after destruction of the inner retina. Vis. Neurosci., 8: 489-490.
15. Chapman, E.R., Hanson, P.I. and Jahn, R. (1995) The neuronal exocytotic fusion machine: Some new developments. Neuropharmacology, 34: 1343-1349.
16. Copenhagen, D.R. and Jahr, C.E. (1989) Release of endogenous excitatory amino acids from turtle photoreceptors. Nature, 342: 536-539.
17. Copenhagen, D.R. and Owen, W.G. (1976) Functional characteristics of lateral interactions between rods in the retina of the snapping turtle. J. Physiol., 259: 251-282.
18. Corey, D.P., Dubinsky, J.M. and Schwartz, E.A. (1984) The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. Physiol., 354: 557-575.
19. Derouiche, A. and Rauen, T. (1995) Coincidence of L-glutamate/L-aspartate transporter (GLAST) and glutamine synthetase (GS) immunoreactions in retinal glia: Evidence for coupling of GLAST and GS in transmitter clearance. J. Neurosci. Res., 42: 131-143.
20. DeVries, S.H. and Schwartz, E.A. (1999) Kainate receptors mediate synaptic transmission between cones and 'Off' bipolar cells in a mammalian retina. Nature, 397: 157-160.
21. Dowling, J.E. (1987) The Retina. An Approachable Part of the Brain. Belknap Press, Cambridge, MA.
22. Eliasof, S. and Jahr, C.E. (1997) Rapid AMPA receptor desensitization in catfish cone horizontal cells. Vis. Neurosci., 14: 13-18.
23. Fosse, V.M., Kolstad, J. and Fonnum, F. (1986) A bioluminescence method for the measurement of L-glutamate: Applications to the study of changes in the release of L-glutamate from lateral geniculate nucleus and superior colliculus after visual cortex ablation in rats. J. Neurochem., 47: 340-349.
24. Gaal, L., Roska, B., Picaud, S.A, Wu, S.M., Marc, R., and Werblin, F.S. (1998) Postsynaptic response kinetics are controlled by a glutamate transporter at cone photoreceptors. J. Neurophysiol., 79: 190-196.
25. Gold, G.H. and Dowling, J.E. (1979) Photoreceptor coupling in retina of the toad, Bufo marinus. I. Anatomy. J. Neurophysiol., 42: 292-310.
26. Grant, G.B. and Dowling, J.E. (1995) A glutamate-activated chloride current in cone-driven ON bipolar cells of the white perch retina, J. Neurosci., 15: 3852-3862.
27. Grant, G.B. and Werblin, F.S. (1996) A glutamate-elicited chloride current with transporter-like properties in rod photoreceptors of the tiger salamander. Vis. Neurosci., 13: 135-144.
28. Hamill, O.P., Marty, A., Neher, E., Sakmann, B. and Sigworth, F.J. (1981) Improved patch clamp technique for high resolution current recording from cell and cell-free membrane patches. Pflug. Arch., 391: 85-100.
29. Hayashi, Y., Shi, S.-H., Esteban, J.A., Piccini, A., Poncer, J.-C. and Malinow, R. (2000) Driving AMPA receptors into synapses by LTP and CAMKII: Requirement for GluR1 and PDZ domain interaction. Science, 287: 2262-2267.
30. Heuser, J.E. and Reese, T.S. (1973) Evidence for recycling of synaptic vesicles membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol., 57: 315-344.
31. Hollman, M. and Heinemann, S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci., 17: 31-108.
32. Koontz, M.A. and Hendrickson, A. (1993) Comparison of immunolocalization patterns for the synaptic vesicle proteins p65 and synapsin I in macaque monkey retina. Synapse, 14: 268-282.
33. Koulen, P., Fletcher, E.L., Craven, S.E., Bredt, D.S. and Wassle, H. (1998) Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina. J. Neurosci., 18: 10136-10149.
34. Koulen, P., Kuhn, R., Wassle, H. and Brandstatter, J.H. (1999) Modulation of the intracellular calcium concentration in photoreceptor terminals by a presynaptic metabotropic glutamate receptor. Proc. Natl. Acad. Sci., 96: 9909-9914.
35. Krizaj, D. and Copenhagen, D.R. (1998) Compartmentalization of calcium extrusion mechanisms in the outer and inner segments of photoreceptors. Neuron, 21: 249-256.
36. Krizaj, D., Gabriel, R., Owen, W.G. and Witkovsky, P. (1998) Dopamine D2 receptor-mediated modulation of rod-cone coupling in the Xenopus retina. J. Comp. Neur., 398: 529-538,
37. Krizaj, D., Bao, J-X., Schmitz, Y., Witkovsky, P. and Copenhagen, D.R. (1999) Caffeine-sensitive calcium stores regulate synaptic transmission from retinal rod photoreceptors. J. Neurosci., 19: 7249-7261.
38. Kurenny, D.E., Moroz, L.L., Turner, R.W., Sharkey, K.A. and Barnes, S. (1994) Modulation of ion channels in rod photoreceptors by nitric oxide. Neuron, 13: 315-324.
39. Lasansky, A. (1973) Organization of the outer synaptic layer in the retina of the larval tiger salamander. Phil. Trans. R. Soc. Lond. B, 265: 471-489.
40. Lasater, E. and Witkovsky, P. (1991) The calcium current of turtle photoreceptor axon terminals. Neurosci. Res., (Suppl. 15): S165-S173.
41. Linser, P. and Moscona, A.A. (1979) Induction of glutamine synthetase in embryonic neural retina: Localization in Muller fibers and dependence on cell interactions. Proc. Natl. Acad. Sci., 76: 6476-6480.
42. Mandell, J.W., Townes-Anderson, E., Czernik, A.J., Cameron, R., Greengard. P. and De Camilli, P. (1990) Synapsins in the vertebrate retina: Absence from ribbon synapses and heterogeneous distribution among conventional synapses. Neuron, 5: 19-33.
43. Maple, B.R., Gao, F. and Wu, S.M. (1999) Glutamate receptors differ in rod- and cone-dominated off-center bipolar cells. NeuroReport, 10: 3605-3610.
44. Maricq, A.V. and Korenbrot, J.I. (1988) Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors. Neuron, 1: 503-515.
45. McCarthy, S.T., Younger, J.P. and Owen, W.G. (1994) Free calcium concentrations in bullfrog rods determined in the presence of multiple forms of fura-2. Biophys. J., 67: 2076-2089.
46. Minami, N., Berglund, K., Sakaba, T., Kohmoto, H. and Tachibana, M. (1998) Potentiation of transmitter release by protein kinase C in goldfish retinal bipolar cells. J. Physiol., 512: 219-225.
47. Morgans, C.W., El Far, O., Berntson, A., Wassle, H. and Taylor, W.R. (1998) Calcium extrusion from mammalian photoreceptor terminals. J. Neurosci., 18: 2467-2474.
48. Nakajima, Y., Iwakabe, H., Akazawa, C., Nawa, H., Shigemoto, R., Mizuno, N. and Nakanishi, S. (1993) Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2amino-4-phosphonobutyrate. J. Biol. Chem., 268: 11368-11373.
49. Nawy, S. and Jahr, C.E. (1991) cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter. Neuron, 7: 677-683.
50. Neher, E. (1998) Vesicle pools and Ca2+ microdomains: New tools for understanding their roles in neurotransmitter release. Neuron, 20: 389-399.
51. Nelson, R. (1977) Cat cones have rod input: A comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. J. Comp. Neurol., 172: 109-136.
52. O'Dell, T.J. and Christensen, B.N. (1986) N-methyl-D-aspartate receptors coexist with kainate and quisqualate receptors on single isolated catfish horizontal cells. Brain Res., 381: 359-362.
53. Olivera, B.M., Miljanich, G.P., Ramachandran, J. and Adams, M.E. (1994) Calcium channel diversity and neurotransmitter release: The w-conotoxins and w-agatoxins. Ann. Rev. Biochem., 63: 823-867.
54. Rauen, T., Taylor, W.R., Kuhlbrodt, K. and Wiessner, M. (1998) High-affinity glutamate transporters in the rat retina: a major role of the glial glutamate transporter GLAST-1 in transmitter clearance. Cell Tiss. Res., 291: 19-31.
55. Rieke, F. and Schwartz, E.A. (1994) A cGMP-gated current can control exocytosis at cone synapses. Neuron, 13: 863-873.
56. Rieke, F. and Schwartz, E.A. (1996) Asynchronous transmitter release: Control of exocytosis and endocytosis at the salamander rod synapse. J. Physiol., 493: 1-8.
57. Ripps, H., Shakib, M. and MacDonald, E.D. (1976) Peroxidase uptake by photoreceptor terminals of the skate retina. J. Cell Biol., 70: 86-96.
58. Roska, B., Gaal, L. and Werblin, F.S. (1998) Voltage-dependent uptake is a major determinant of glutamate concentration at the cone synapse: An analytical study. J. Neurophysiol., 80: 1951-1960.
59. Sasaki, T. and Kaneko, A. (1996) L-glutamate-induced responses in OFF-type bipolar cells of the cat retina. Vision Res., 36: 787-795.
60. Schmitz, Y. and Witkovsky, P. (1996) Glutamate release by the intact light-responsive photoreceptor layer of the Xenopus retina. J. Neurosci. Meth., 68: 55-60.
61. Schmitz, Y. and Witkovsky, P. (1997) Dependence of photoreceptor glutamate release on a dihydropyridine-sensitive calcium channel. Neurosci., 78: 1209-1216.
62. Schneeweis, D.M. and Schnapf, J.L. (1995) Photovoltage of rods and cones in the macaque retina. Science, 268: 1053-1056.
63. Shichi, H. (1983) Biochemistry of Vision. Academic Press, NY.
64. Stella, S. and Thoreson, W.B. (2000) Differential modulation of rod and cone calcium currents in tiger salamander retina by D2 dopamine receptors and cAMP. Eur. J. Neurosci., 12: 3537-3548.
65. Stockton, R.A. and Slaughter, M.M. (1989) B-wave of the electroretinogram. A reflection of ON bipolar cell activity. J. Gen. Physiol., 93: 101-122.
66. Tachibana, M., Okada, T., Arimura, T., Kobayashi, K. and Piccolino, M. (1993) Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells of the goldfish retina. J. Neurosci., 13: 2898-2909.
67. Taylor, W.R. and Morgans, C. (1998) Localization and properties of voltage-gated calcium channels in cone photo-receptors of Tupaia belangeri. Vis. Neurosci., 15: 541-552.
68. Thoreson, W.B., Nitzan, R. and Miller, R.F. (1997) Reducing extracellular chloride suppresses dihydropyridine-sensitive calcium currents and synaptic transmission in amphibian photoreceptors. J. Neurophysiol., 77: 2175-2190.
69. Thoreson, W.B. and Witkovsky, P. (1999) Glutamate receptors and circuits in the vertebrate retina. Prog. Retinal and Eye Res., 18: 765-810.
70. Tran, M.N., Higgs, M.H. and Lukasiewicz, P.D. (1999) AMPA receptor kinetics limit retinal amacrine cell excitatory synaptic responses. Vis. Neurosci., 16: 835-842.
71. Vardi, N., Morigiwa, K., Wang, T.-L., Shi, Y.-J. and Sterling, P. (1998) Neurochemistry of the mammalian cone 'synaptic complex'. Vision Res., 38: 1359-1369.
72. Verweij, J., Kamennans, M. and Spekreijse, H. (1996) Horizontal cells feed back to cones by shifting the cone calcium-current activation range. Vision Res., 36: 3943-3953.
73. Von Gersdorff, H., Vardi, E., Matthews, G. and Sterling, P. (1996) Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron, 16: 1221-1227.
74. Wilkinson, M.F. and Barnes, S. (1996) The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors. J. Gen. Physiol., 107: 621-630.
75. Winkler, B.S., Kapousta-Bruneau, N., Arnold, M.J. and Green, D.G. (1999) Effects of inhibiting glutamine synthetase and blocking glutamate uptake on b-wave generation in the isolated rat retina. Vis. Neurosci., 16: 345-353.
76. Witkovsky, P. and Dearry, A. (1991) Functional roles of dopamine in the vertebrate retina. Prog. Ret. Res., 11: 242-292.
77. Witkovsky, P., Schmitz, Y., Akopian, A., Krizaj, D. and Tranchina, D. (1997) Gain of rod to horizontal cell synaptic transfer: Relation to glutamate release and a dihydropyridine-sensitive calcium current. J. Neurosci., 17: 7297-7306.
78. Wu, S.M. (1988) Synaptic transmission from rods to horizontal cells in dark-adapted tiger salamander retina. Vision Res., 28: 1-8.
79. Yang, J.-H., Maple, B., Gao, F., Maguire, G. and Wu, S.M. (1998) Postsynaptic responses of horizontal cells in the tiger salamander retina are mediated by AMPA-preferring receptors. Brain Res. 797: 125-134.
80. Ziff, E.B. (1997) Enlightening the postsynaptic density. Neuron, 19: 1163-1174.