Structure and function of a complex sensory synapse

Acta Physiologica

Volumn 204, Issue 4, 2012, Pages 479-486

  Regus Leidig, H ^a   Brandstatter J H ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Bipolar cell; Glutamate receptor; Photoreceptor; Retina; Ribbon synapse; Signal processing

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; ISOPROTEIN; KAINIC ACID; KINESIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TRANSIENT RECEPTOR POTENTIAL CHANNEL M1;

CALCIUM CELL LEVEL; CENTRAL NERVOUS SYSTEM; COMPLEX SENSORY SYNAPSE; ELECTRORETINOGRAPHY; EXOCYTOSIS; HYDROLYSIS; LIGHT INTENSITY; NIGHT BLINDNESS; NONHUMAN; PHENOTYPE; PHOTOTRANSDUCTION; PRIORITY JOURNAL; RETINA; RETINA BIPOLAR GANGLION CELL; RETINA CONE; RETINA ROD; REVIEW; SIGNAL PROCESSING; SYNAPSE; SYNAPTIC TRANSMISSION; VISUAL SYSTEM; VISUAL THRESHOLD;

ANIMALS; HUMANS; PHOTORECEPTOR CELLS, VERTEBRATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84857507868     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2011.02355.x     Document Type: Review

References (77)

1. Bartoletti, T.M., Babai, N. & Thoreson, W.B. 2010. Vesicle pool size at the salamander cone ribbon synapse. J Neurophysiol103, 419-423.
2. Bellone, R.R., Brooks, S.A., Sandmeyer, L., Murphy, B.A., Forsyth, G., Archer, S., Bailey, E. & Grahn, B. 2008. Differential gene expression of TRPM1, the potential cause of congenital stationary night blindness and coat spotting patterns (LP) in the Appaloosa horse (Equus caballus). Genetics179, 1861-1870.
3. Boycott, B.B. & Wässle, H. 1999. Parallel processing in the mammalian retina: the Proctor Lecture. Inv Oph Vis Sci40, 1313-1327.
4. Brandstätter, J.H. 2002. Glutamate receptors in the retina: the molecular substrate for visual signal processing. Curr Eye Res25, 327-331.
5. Brandstätter, J.H. & Hack, I. 2001. Localization of glutamate receptors at a complex synapse. The mammalian photoreceptor synapse. Cell Tissue Res303, 1-14.
6. Brandstätter, J.H., Koulen, P. & Wässle, H. 1997. Selective synaptic distribution of kainate receptor subunits in the two plexiform layers of the rat retina. J Neurosci17, 9298-9307.
7. Brandstätter, J.H., Koulen, P. & Wässle, H. 1998. Diversity of glutamate receptors in the mammalian retina. Vision Res38, 1385-1397.
8. Burns, M.E. & Baylor, D.A. 2001. Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu Rev Neurosci24, 779-805.
9. Chun, M.H., Grünert, U., Martin, P.R. & Wässle, H. 1996. The synaptic complex of cones in the fovea and in the periphery of the macaque monkey retina. Vision Res36, 3383-3395.
10. DeVries, S.H. 2000. Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron28, 847-856.
11. DeVries, S.H. & Baylor, D.A. 1995. An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina. Proc Natl Acad Sci U S A92, 10658-10662.
12. DeVries, S.H. & Schwartz, E.A. 1999. Kainate receptors mediate synaptic transmission between cones and 'Off' bipolar cells in a mammalian retina. Nature397, 157-160.
13. DeVries, S.H., Li, W. & Saszik, S. 2006. Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron50, 735-748.
14. Dick, O., tom Dieck, S., Altrock, W.D., Ammermüller, J., Weiler, R., Garner, C.C., Gundelfinger, E.D. & Brandstätter, J.H. 2003. The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron37, 775-786.
15. tom Dieck, S. & Brandstätter, J.H. 2006. Ribbon synapses of the retina. Cell Tissue Res326, 339-346.
16. tom Dieck, S., Altrock, W.D., Kessels, M.M., Qualmann, B., Regus, H., Brauner, D., Fejtová, A., Bracko, O., Gundelfinger, E.D. & Brandstätter, J.H. 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 Biol168, 825-836.
17. Dowling, J.E. & Boycott, B.B. 1966. Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci166, 80-111.
18. Fain, G.L., Matthews, H.R., Cornwall, M.C. & Koutalos, Y. 2001. Adaptation in vertebrate photoreceptors. Physiol Rev81, 117-151.
19. Field, G.D. & Rieke, F. 2002. Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron34, 773-785.
20. von Gersdorff, H. 2001. Synaptic ribbons: versatile signal transducers. Neuron29, 7-10.
21. von Gersdorff, H., Vardi, E., Matthews, G. & Sterling, P. 1996. Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron16, 1221-1227.
22. von Gersdorff, H., Sakaba, T., Berglund, K. & Tachibana, M. 1998. Submillisecond kinetics of glutamate release from a sensory synapse. Neuron21, 1177-1188.
23. Gießl, A., Regus-Leidig, H. & Brandstätter, J.H. 2010. Signal transduction and signal transmission. The two faces of a photoreceptor. e-Neuroforum3, 60-69.
24. Hack, I., Peichl, L. & Brandstätter, J.H. 1999. An alternative pathway for rod signals in the rodent retina: rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. Proc Natl Acad Sci U S A96, 14130-14135.
25. Hack, I., Frech, M., Dick, O., Peichl, L. & Brandstätter, J.H. 2001. Heterogeneous distribution of AMPA glutamate receptor subunits at the photoreceptor synapses of rodent retina. Eur J Neurosci13, 15-24.
26. Haucke, V., Neher, E. & Sigrist, S.J. 2011. Protein scaffolds in the coupling of synaptic exocytosis and endocytosis. Nat Rev Neurosci12, 127-138.
27. Haverkamp, S., Grünert, U. & Wässle, H. 2000. The cone pedicle, a complex synapse in the retina. Neuron27, 85-95.
28. Heidelberger, R. 1998. Adenosine triphosphate and the late steps in calcium-dependent exocytosis at a ribbon synapse. J Gen Physiol111, 225-241.
29. Heidelberger, R., Heinemann, C., Neher, E. & Matthews, G. 1994. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature371, 513-515.
30. Heidelberger, R., Sterling, P. & Matthews, G. 2002. Roles of ATP in depletion and replenishment of the releasable pool of synaptic vesicles. J Neurophysiol88, 98-106.
31. Heidelberger, R., Thoreson, W.B. & Witkovsky, P. 2005. Synaptic transmission at retinal ribbon synapses. Prog Retin Eye Res24, 682-720.
32. Hollmann, M. & Heinemann, S. 1994. Cloned glutamate receptors. Annu Rev Neurosci17, 31-108.
33. Jackman, S.L., Choi, S.Y., Thoreson, W.B., Rabl, K., Bartoletti, T.M. & Kramer, R.H. 2009. Role of the synaptic ribbon in transmitting the cone light response. Nat Neurosci12, 303-310.
34. Koike, C., Obara, T., Uriu, Y., Numata, T., Sanuki, R., Miyata, K., Koyasu, T., Ueno, S., Funabiki, K., Tani, A., Ueda, H., Kondo, M., Mori, Y., Tachibana, M. & Furukawa, T. 2010. TRPM1 is a component of the retinal ON bipolar cell transduction channel in the mGluR6 cascade. Proc Natl Acad Sci U S A107, 332-337.
35. Kolb, H. & Famiglietti, E.V. 1974. Rod and cone pathways in the inner plexiform layer of cat retina. Science186, 47-49.
36. Kolb, H. & Nelson, R. 1995. The organization of photoreceptor to bipolar synapses in the outer plexiform layer. In: M.B.A.Djamgoz, S.N. Archer & S. Vallerga (eds) Neurobiology and Clinical Aspects of the Outer Retina, pp. 273-296. Hall, London.
37. Lenzi, D. & von Gersdorff, H. 2001. Structure suggests function: the case for synaptic ribbons as exocytotic nanomachines. Bioessays23, 831-840.
38. Li, W., Chen, S. & DeVries, S.H. 2010. A fast rod photoreceptor signaling pathway in the mammalian retina. Nat Neurosci13, 414-416.
39. LoGiudice, L. & Matthews, G. 2009. The role of ribbons at sensory synapses. Neuroscientist15, 380-391.
40. Magupalli, V.G., Schwarz, K., Alpadi, K., Natarajan, S., Seigel, G.M. & Schmitz, F. 2008. Multiple RIBEYE-RIBEYE interactions create a dynamic scaffold for the formation of synaptic ribbons. J Neurosci28, 7954-7967.
41. Masu, M., Iwakabe, H., Tagawa, Y., Miyoshi, T., Yamashita, M., Fukuda, Y., Sasaki, H., Hiroi, K., Nakamura, Y., Shigemoto, R., Takada, M., Nakamura, K., Nakao, K., Katsuki, M. & Nakanishi, S. 1995. Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell80, 757-765.
42. Matthews, G. & Fuchs, P. 2010. The diverse roles of ribbon synapses in sensory neurotransmission. Nat Rev Neurosci11, 812-822.
43. Matthews, G. & Sterling, P. 2008. Evidence that vesicles undergo compound fusion on the synaptic ribbon. J Neurosci28, 5403-5411.
44. Mennerick, S. & Matthews, G. 1996. Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron17, 1241-1249.
45. Morgans, C.W., Brandstätter, J.H., Kellerman, J., Betz, H. & Wässle, H. 1996. A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina. J Neurosci16, 6713-6721.
46. Morgans, C.W., Zhang, J., Jeffrey, B.G., Nelson, S.M., Burke, N.S., Duvoisin, R.M. & Brown, R.L. 2009. TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells. Proc Natl Acad Sci U S A106, 19174-19178.
47. Morgans, C.W., Brown, R.L. & Duvoisin, R.M. 2010. TRPM1: the endpoint of the mGluR6 signal transduction cascade in retinal ON-bipolar cells. Bioessays32, 609-614.
48. Morigiwa, K. & Vardi, N. 1999. Differential expression of ionotropic glutamate receptor subunits in the outer retina. J Comp Neurol405, 173-184.
49. Muresan, V., Lyass, A. & Schnapp, B.J. 1999. The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors. J Neurosci19, 1027-1037.
50. Nathans, J. 1999. The evolution and physiology of human color vision: insights from molecular genetic studies of visual pigments. Neuron24, 299-312.
51. Niswender, C.M. & Conn, P.J. 2010. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol50, 295-322.
52. Nomura, A., Shigemoto, R., Nakamura, Y., Okamoto, N., Mizuno, N. & Nakanishi, S. 1994. Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell77, 361-369.
53. Ozawa, S., Kamiya, H. & Tsuzuki, K. 1998. Glutamate receptors in the mammalian central nervous system. Prog Neurobiol54, 581-618.
54. Parsons, T.D. & Sterling, P. 2003. Synaptic ribbon. Conveyor belt or safety belt?Neuron37, 379-382.
55. Rabl, K., Cadetti, L. & Thoreson, W.B. 2005. Kinetics of exocytosis is faster in cones than in rods. J Neurosci25, 4633-4640.
56. Raviola, E. & Gilula, N.B. 1975. Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J Cell Biol65, 192-222.
57. Regus-Leidig, H., tom Dieck, S., Specht, D., Meyer, L. & Brandstätter, J.H. 2009. Early steps in the assembly of photoreceptor ribbon synapses in the mouse retina: the involvement of precursor spheres. J Comp Neurol512, 814-824.
58. Reim, K., Wegmeyer, H., Brandstätter, J.H., Xue, M., Rosenmund, C., Dresbach, T., Hofmann, K. & Brose, N. 2005. Structurally and functionally unique complexins at retinal ribbon synapses. J Cell Biol169, 669-680.
59. Rieke, F. & Rudd, M.E. 2009. The challenges natural images pose for visual adaptation. Neuron64, 605-616.
60. Schmitz, F., Königstorfer, A. & Südhof, T.C. 2000. RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron28, 857-872.
61. Schneeweis, D.M. & Schnapf, J.L. 1995. Photovoltage of rods and cones in the macaque retina. Science268, 1053-1056.
62. Seeburg, P.H. 1993. The TINS/TiPS Lecture. The molecular biology of mammalian glutamate receptor channels. Trends Neurosci16, 359-365.
63. Sharpe, L.T. & Stockman, A. 1999. Rod pathways: the importance of seeing nothing. Trends Neurosci22, 497-504.
64. Shen, Y., Heimel, J.A., Kamermans, M., Peachey, N.S., Gregg, R.G. & Nawy, S. 2009. A transient receptor potential-like channel mediates synaptic transmission in rod bipolar cells. J Neurosci29, 6088-6093.
65. Snellman, J., Kaur, T., Shen, Y. & Nawy, S. 2008. Regulation of ON bipolar cell activity. Prog Ret Eye Res27, 450-463.
66. Snellman, J., Mehta, B., Babai, N., Bartoletti, T.M., Akmentin, W., Francis, A., Matthews, G., Thoreson, W. & Zenisek, D. 2011. Acute destruction of the synaptic ribbon reveals a role for the ribbon in vesicle priming. Nat Neurosci, doi: [Epub ahead of print].
67. Soucy, E., Wang, Y., Nirenberg, S., Nathans, J. & Meister, M. 1998. A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina. Neuron21, 481-493.
68. Spiwoks-Becker, I., Glas, M., Lasarzik, I. & Vollrath, L. 2004. Mouse photoreceptor synaptic ribbons lose and regain material in response to illumination changes. Eur J Neurosci19, 1559-1571.
69. Sterling, P. & Matthews, G. 2005. Structure and function of ribbon synapses. Trends Neurosci28, 20-29.
70. Thoreson, W.B. 2007. Kinetics of synaptic transmission at ribbon synapses of rods and cones. Mol Neurobiol36, 205-223.
71. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron42, 595-605.
72. Tsukamoto, Y., Masarachia, P., Schein, S.J. & Sterling, P. 1992. Gap junctions between the pedicles of macaque foveal cones. Vision Res32, 1809-1815.
73. Tsukamoto, Y., Morigiwa, K., Ueda, M. & Sterling, P. 2001. Microcircuits for night vision in mouse retina. J Neurosci21, 8616-8623.
74. Vardi, N. & Morigiwa, K. 1997. ON cone bipolar cells in rat express the metabotropic receptor mGluR6. Vis Neurosci14, 789-794.
75. Vardi, N., Duvoisin, R., Wu, G. & Sterling, P. 2000. Localization of mGluR6 to dendrites of ON bipolar cells in primate retina. J Comp Neurol423, 402-412.
76. Wang, Y., Okamoto, M., Schmitz, F., Hofmann, K. & Südhof, T.C. 1997. Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature388, 593-598.
77. Wässle, H. 2004. Parallel processing in the mammalian retina. Nature Rev Neurosci5, 1-11.