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Synaptic release at mammalian bipolar cell terminals

Published online by Cambridge University Press:  28 January 2011

QUN-FANG WAN  and
RUTH HEIDELBERGER
QUN-FANG WAN
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School at Houston, Houston, Texas
RUTH HEIDELBERGER*
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School at Houston, Houston, Texas Graduate School of Biomedical Sciences, University of Texas Health Science Center at Houston, Houston, Texas
*
*Address correspondence and reprint requests to: Dr. Ruth Heidelberger, Department of Neurobiology and Anatomy, MSB 7.046, University of Texas Medical School at Houston, 6431 Fannin Street, Houston, TX 77030. E-mail: [email protected]
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Abstract

Bipolar cells play a vital role in the transfer of visual information across the vertebrate retina. The synaptic output of these neurons is regulated by factors that are extrinsic and intrinsic. Relatively little is known about the intrinsic factors that regulate neurotransmitter exocytosis. Much of what we know about intrinsic presynaptic mechanisms that regulate glutamate release has come from the study of the unusually large and accessible synaptic terminal of the goldfish rod-dominant bipolar cell, the Mb1 bipolar cell. However, over the past several years, examination of presynaptic mechanisms governing neurotransmitter release has been extended to the mammalian rod bipolar cell. In this review, we discuss the recent advances in our understanding of synaptic vesicle dynamics and neurotransmitter release in rodent rod bipolar cells and consider how these properties help to shape the synaptic output of the mammalian retina.

Keywords

Rod bipolar cellExocytosisEndocytosisRibbon synapseSynaptic vesicle
Type
Review Article
Information
Visual Neuroscience , Volume 28 , Issue 1 , January 2011 , pp. 109 - 119
Copyright
Copyright © Cambridge University Press 2011

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References

Abercrombie, M. (1946). Estimation of nuclear population from microtome sections. Anatomical Record 94, 239–247.CrossRefGoogle ScholarPubMed
Adler, E.M., Augustine, G.J., Duffy, S.N. & Charlton, M.P. (1991). Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. The Journal of Neuroscience 11, 1496–1507.CrossRefGoogle ScholarPubMed
Alexander, K.R., Fishman, G.A., Peachey, N.S., Marchese, A.L. & Tso, M.O. (1992). ‘On’ response defect in paraneoplastic night blindness with cutaneous malignant melanoma. Investigative Ophthalmology & Visual Science 33, 477–483.Google ScholarPubMed
Baumann, L., Gerstner, A., Zong, X., Biel, M. & Wahl-Schott, C. (2004). Functional characterization of the L-type Ca2+ channel Cav1.4alpha1 from mouse retina. Investigative Ophthalmology & Visual Science 45, 708–713.CrossRefGoogle ScholarPubMed
Bech-Hansen, N.T., Naylor, M.J., Maybaum, T.A., Pearce, W.G., Koop, B., Fishman, G.A., Mets, M., Musarella, M.A. & Boycott, K.M. (1998). Loss-of-function mutations in a calcium-channel alpha1-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness. Nature Genetics 19, 264–267.CrossRefGoogle Scholar
Berntson, A., Smith, R.G. & Taylor, W.R. (2004). Transmission of single photon signals through a binary synapse in the mammalian retina. Visual Neuroscience 21, 693–702.CrossRefGoogle ScholarPubMed
Berntson, A., Taylor, W.R. & Morgans, C.W. (2003). Molecular identity, synaptic localization, and physiology of calcium channels in retinal bipolar cells. Journal of Neuroscience Research 71, 146–151.CrossRefGoogle ScholarPubMed
Berson, E.L. & Lessell, S. (1988). Paraneoplastic night blindness with malignant melanoma. American Journal of Ophthalmology 106, 307–311.CrossRefGoogle ScholarPubMed
Beutner, D., Voets, T., Neher, E. & Moser, T. (2001). Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29, 681–690.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retinal & Eye Research 20, 351–384.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Xin, D. (2000). Surround inhibition of mammalian AII amacrine cells is generated in the proximal retina. The Journal of Physiology 523(Pt 3), 771–783.CrossRefGoogle ScholarPubMed
Bollmann, J.H., Sakmann, B. & Borst, J.G. (2000). Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289, 953–957.CrossRefGoogle Scholar
Borst, J.G. & Sakmann, B. (1996). Calcium influx and transmitter release in a fast CNS synapse. Nature 383, 431–434.CrossRefGoogle Scholar
Burrone, J. & Lagnado, L. (1997). Electrical resonance and Ca2+ influx in the synaptic terminal of depolarizing bipolar cells from the goldfish retina. The Journal of Physiology 505(Pt 3), 571–584.CrossRefGoogle ScholarPubMed
Burrone, J., Neves, G., Gomis, A., Cooke, A. & Lagnado, L. (2002). Endogenous calcium buffers regulate fast exocystosis in the synaptic terminal of retinal bipolar cells. Neuron 33, 101–112.CrossRefGoogle Scholar
Chavez, A.E., Grimes, W.N. & Diamond, J.S. (2010). Mechanisms underlying lateral GABAergic feedback onto rod bipolar cells in rat retina. The Journal of Neuroscience 30, 2330–2339.CrossRefGoogle ScholarPubMed
Clayton, E.L., Sue, N., Smillie, K.J., O’Leary, T., Bache, N., Cheung, G., Cole, A.R., Wyllie, D.J., Sutherland, C., Robinson, P.J. & Cousin, M.A. (2010). Dynamin I phosphorylation by GSK3 controls activity-dependent bulk endocytosis of synaptic vesicles. Nature Neuroscience 13, 845–851.CrossRefGoogle ScholarPubMed
Coggins, M.R., Grabner, C.P., Almers, W. & Zenisek, D. (2007). Stimulated exocytosis of endosomes in goldfish retinal bipolar neurons. The Journal of Physiology 584, 853–865.CrossRefGoogle ScholarPubMed
Connaughton, V.P. (2011). This volume.Google Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. The Journal of Neuroscience 6, 331–345.CrossRefGoogle ScholarPubMed
Deans, M.R., Volgyi, B., Goodenough, D.A., Bloomfield, S.A. & Paul, D.L. (2002). Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36, 703–712.CrossRefGoogle ScholarPubMed
de la Villa, P., Vaquero, C.F. & Kaneko, A. (1998). Two types of calcium currents of the mouse bipolar cells recorded in the retinal slice preparation. The European Journal of Neuroscience 10, 317–323.CrossRefGoogle ScholarPubMed
Dinkelacker, V., Voets, T., Neher, E. & Moser, T. (2000). The readily releasable pool of vesicles in chromaffin cells is replenished in a temperature-dependent manner and transiently overfills at 37 degrees C. The Journal of Neuroscience 20, 8377–8383.CrossRefGoogle Scholar
Dittman, J.S. & Regehr, W.G. (1998). Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. The Journal of Neuroscience 18, 6147–6162.CrossRefGoogle ScholarPubMed
Dittman, J. & Ryan, T.A. (2009). Molecular circuitry of endocytosis at nerve terminals. Annual Review of Cell & Developmental Biology 25, 133–160.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, MA: Belknap Press of Harvard University Press.Google Scholar
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society of London. Series B 166, 80–111.Google ScholarPubMed
Dowling, J.E. & Werblin, F.S. (1969). Organization of retina of the mudpuppy, Necturus maculosus. I. Synaptic structure. Journal of Neurophysiology 32, 315–338.CrossRefGoogle ScholarPubMed
Duncan, G., Rabl, K., Gemp, I., Heidelberger, R. & Thoreson, W.B. (2010). Quantitative analysis of synaptic release at the photoreceptor synapse. Biophysical Journal 98, 2102–2110.CrossRefGoogle ScholarPubMed
Eggers, E.D. & Lukasiewicz, P.D. (2006). GABA(A), GABA(C) and glycine receptor-mediated inhibition differentially affects light-evoked signalling from mouse retinal rod bipolar cells. The Journal of Physiology 572, 215–225.CrossRefGoogle Scholar
Eisen, M.D., Spassova, M. & Parsons, T.D. (2004). Large releasable pool of synaptic vesicles in chick cochlear hair cells. Journal of Neurophysiology 91, 2422–2428.CrossRefGoogle ScholarPubMed
Euler, T. & Masland, R.H. (2000). Light-evoked responses of bipolar cells in a mammalian retina. Journal of Neurophysiology 83, 1817–1829.CrossRefGoogle Scholar
Fitzgerald, K.M., Cibis, G.W., Giambrone, S.A. & Harris, D.J. (1994). Retinal signal transmission in Duchenne muscular dystrophy: Evidence for dysfunction in the photoreceptor/depolarizing bipolar cell pathway. The Journal of Clinical Investigation 93, 2425–2430.CrossRefGoogle ScholarPubMed
Gaffield, M.A. & Betz, W.J. (2007). Synaptic vesicle mobility in mouse motor nerve terminals with and without synapsin. The Journal of Neuroscience 27, 13691–13700.CrossRefGoogle ScholarPubMed
Gentet, L.J., Stuart, G.J. & Clements, J.D. (2000). Direct measurement of specific membrane capacitance in neurons. Biophysical Journal 79, 314–320.CrossRefGoogle ScholarPubMed
Gillis, K.D. (1995). Techniques for membrane capacitance measurements. In Single Channel Recording (2nd ed.), ed. Neher, E. & Sakmann, B., pp. 155–198. New York: Plenum Press.CrossRefGoogle Scholar
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. The Journal of Neuroscience 19, 6309–6317.CrossRefGoogle ScholarPubMed
Hartveit, E. (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. Journal of Neurophysiology 81, 2923–2936.CrossRefGoogle ScholarPubMed
Heidelberger, R. (1998). Adenosine triphosphate and the late steps in calcium-dependent exocytosis at a ribbon synapse. The Journal of General Physiology 111, 225–241.CrossRefGoogle Scholar
Heidelberger, R. (2001). ATP is required at an early step in compensatory endocytosis in synaptic terminals. The Journal of Neuroscience 21, 6467–6474.CrossRefGoogle ScholarPubMed
Heidelberger, R., Heinemann, C., Neher, E. & Matthews, G. (1994). Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513–515.CrossRefGoogle Scholar
Heidelberger, R. & Matthews, G. (1991). Inhibition of calcium influx and calcium current by gamma-aminobutyric acid in single synaptic terminals. Proceedings of the National Academy of Sciences of the United States of America 88, 7135–7139.CrossRefGoogle ScholarPubMed
Heidelberger, R. & Matthews, G. (1992). Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. The Journal of Physiology 447, 235–256.CrossRefGoogle ScholarPubMed
Heidelberger, R., Sterling, P. & Matthews, G. (2002 a). Roles of ATP in depletion and replenishment of the releasable pool of synaptic vesicles. Journal of Neurophysiology 88, 98–106.CrossRefGoogle ScholarPubMed
Heidelberger, R., Thoreson, W.B. & Witkovsky, P. (2005). Synaptic transmission at retinal ribbon synapses. Progress in Retinal & Eye Research 24, 682–720.CrossRefGoogle ScholarPubMed
Heidelberger, R., Zhou, Z.Y. & Matthews, G. (2002 b). Multiple components of membrane retrieval in synaptic terminals revealed by changes in hydrostatic pressure. Journal of Neurophysiology 88, 2509–2517.CrossRefGoogle ScholarPubMed
Heinemann, C., Chow, R.H., Neher, E. & Zucker, R.S. (1994). Kinetics of the secretory response in bovine chromaffin cells following flash photolysis of caged Ca2+. Biophysical Journal 67, 2546–2557.CrossRefGoogle ScholarPubMed
Holt, M., Cooke, A., Neef, A. & Lagnado, L. (2004). High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Current Biology 14, 173–183.CrossRefGoogle Scholar
Holt, M., Cooke, A., Wu, M.M. & Lagnado, L. (2003). Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells. The Journal of Neuroscience 23, 1329–1339.CrossRefGoogle ScholarPubMed
Hu, C., Bi, A. & Pan, Z.H. (2009). Differential expression of three T-type calcium channels in retinal bipolar cells in rats. Visual Neuroscience 26, 177–187.CrossRefGoogle ScholarPubMed
Hull, C., Studholme, K., Yazulla, S. & von Gersdorff, H. (2006). Diurnal changes in exocytosis and the number of synaptic ribbons at active zones of an ON-type bipolar cell terminal. Journal of Neurophysiology 96, 2025–2033.CrossRefGoogle ScholarPubMed
Hull, C. & von Gersdorff, H. (2004). Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal. Neuron 44, 469–482.CrossRefGoogle Scholar
Innocenti, B. & Heidelberger, R. (2008). Mechanisms contributing to tonic release at the cone photoreceptor ribbon synapse. Journal of Neurophysiology 99(1), 25–36.CrossRefGoogle ScholarPubMed
Ishida, A.T., Stell, W.K. & Lightfoot, D.O. (1980). Rod and cone inputs to bipolar cells in goldfish retina. The Journal of Comparative Neurology 191, 315–335.CrossRefGoogle ScholarPubMed
Jockusch, W.J., Praefcke, G.J., McMahon, H.T. & Lagnado, L. (2005). Clathrin-dependent and clathrin-independent retrieval of synaptic vesicles in retinal bipolar cells. Neuron 46, 869–878.CrossRefGoogle ScholarPubMed
Joselevitch, C. & Kamermans, M. (2007). Interaction between rod and cone inputs in mixed-input bipolar cells in goldfish retina. Journal of Neuroscience Research 85, 1579–1591.CrossRefGoogle ScholarPubMed
Kamphuis, W. & Hendriksen, H. (1998). Expression patterns of voltage-dependent calcium channel alpha 1 subunits (alpha 1A-alpha 1E) mRNA in rat retina. Brain Res Mol Brain Res 55, 209–220.CrossRefGoogle ScholarPubMed
Kaneko, A. (1973). Receptive field organization of bipolar and amacrine cells in the goldfish retina. The Journal of Physiology 235, 133–153.CrossRefGoogle ScholarPubMed
Kaneko, A., Pinto, L.H. & Tachibana, M. (1989). Transient calcium current of retinal bipolar cells of the mouse. The Journal of Physiology 410, 613–629.CrossRefGoogle ScholarPubMed
Kaneko, A., Suzuki, S., Pinto, L.H. & Tachibana, M. (1991). Membrane currents and pharmacology of retinal bipolar cells: A comparative study on goldfish and mouse. Comparative Biochemistry & Physiology. C 98, 115–127.CrossRefGoogle ScholarPubMed
Koenig, J.H. & Ikeda, K. (1989). Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. The Journal of Neuroscience 9, 3844–3860.CrossRefGoogle ScholarPubMed
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295–329.CrossRefGoogle ScholarPubMed
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of cat retina. Science 186, 47–49.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301–312.CrossRefGoogle ScholarPubMed
Koschak, A., Reimer, D., Huber, I., Grabner, M., Glossmann, H., Engel, J. & Striessnig, J. (2001). Alpha 1D (Cav1.3) subunits can form L-type Ca2+ channels activating at negative voltages. The Journal of Biological Chemistry 276, 22100–22106.CrossRefGoogle ScholarPubMed
Koschak, A., Reimer, D., Walter, D., Hoda, J.C., Heinzle, T., Grabner, M. & Striessnig, J. (2003). Cav1.4alpha1 subunits can form slowly inactivating dihydropyridine-sensitive L-type Ca2+ channels lacking Ca2+-dependent inactivation. The Journal of Neuroscience 23, 6041–6049.CrossRefGoogle ScholarPubMed
Kushmerick, C., Renden, R. & von Gersdorff, H. (2006). Physiological temperatures reduce the rate of vesicle pool depletion and short-term depression via an acceleration of vesicle recruitment. The Journal of Neuroscience 26, 1366–1377.CrossRefGoogle ScholarPubMed
Lagnado, L., Gomis, A. & Job, C. (1996). Continuous vesicle cycling in the synaptic terminal of retinal bipolar cells. Neuron 17, 957–967.CrossRefGoogle ScholarPubMed
Lindau, M. & Neher, E. (1988). Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflügers Archiv 411, 137–146.CrossRefGoogle ScholarPubMed
Llobet, A., Beaumont, V. & Lagnado, L. (2003). Real-time measurement of exocytosis and endocytosis using interference of light. Neuron 40, 1075–1086.CrossRefGoogle ScholarPubMed
Logiudice, L., Henry, D. & Matthews, G. (2006). Identification of calcium channel alpha1 subunit mRNA expressed in retinal bipolar neurons. Molecular Vision 12, 184–189.Google ScholarPubMed
LoGiudice, L. & Matthews, G. (2007). Endocytosis at ribbon synapses. Traffic 8, 1123–1128.CrossRefGoogle ScholarPubMed
LoGiudice, L., Sterling, P. & Matthews, G. (2008). Mobility and turnover of vesicles at the synaptic ribbon. The Journal of Neuroscience 28, 3150–3158.CrossRefGoogle ScholarPubMed
Logiudice, L., Sterling, P. & Matthews, G. (2009). Vesicle recycling at ribbon synapses in the finely branched axon terminals of mouse retinal bipolar neurons. Neuroscience 164, 1546–1556.CrossRefGoogle ScholarPubMed
Lou, X., Paradise, S., Ferguson, S.M. & De Camilli, P. (2008). Selective saturation of slow endocytosis at a giant glutamatergic central synapse lacking dynamin 1. Proceedings of the National Academy of Sciences of the United States of America 105, 17555–17560.CrossRefGoogle Scholar
Ma, Y.P. & Pan, Z.H. (2003). Spontaneous regenerative activity in mammalian retinal bipolar cells: Roles of multiple subtypes of voltage-dependent Ca2+ channels. Visual Neuroscience 20, 131–139.CrossRefGoogle ScholarPubMed
Maguire, G., Maple, B., Lukasiewicz, P. & Werblin, F. (1989). Gamma-aminobutyrate type B receptor modulation of L-type calcium channel current at bipolar cell terminals in the retina of the tiger salamander. Proceedings of the National Academy of Sciences of the United States of America 86, 10144–10147.CrossRefGoogle ScholarPubMed
Mandell, J.W., Czernik, A.J., De Camilli, P., Greengard, P. & Townes-Anderson, E. (1992). Differential expression of synapsins I and II among rat retinal synapses. The Journal of Neuroscience 12, 1736–1749.CrossRefGoogle ScholarPubMed
Mandell, J.W., Townes-Anderson, E., Czernik, A.J., Cameron, R., Greengard, P. & De Camilli, P. (1990). Synapsins in the vertebrate retina: Absence from ribbon synapses and heterogeneous distribution among conventional synapses. Neuron 5, 19–33.CrossRefGoogle ScholarPubMed
Maple, B.R. & Wu, S.M. (1998). Glycinergic synaptic inputs to bipolar cells in the salamander retina. The Journal of Physiology 506(Pt 3), 731–744.CrossRefGoogle ScholarPubMed
Marks, B., Stowell, M.H., Vallis, Y., Mills, I.G., Gibson, A., Hopkins, C.R. & McMahon, H.T. (2001). GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410, 231–235.CrossRefGoogle ScholarPubMed
McRory, J.E., Hamid, J., Doering, C.J., Garcia, E., Parker, R., Hamming, K., Chen, L., Hildebrand, M., Beedle, A.M., Feldcamp, L., Zamponi, G.W. & Snutch, T.P. (2004). The CACNA1F gene encodes an L-type calcium channel with unique biophysical properties and tissue distribution. The Journal of Neuroscience 24, 1707–1718.CrossRefGoogle ScholarPubMed
Mennerick, S. & Matthews, G. (1996). Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17, 1241–1249.CrossRefGoogle ScholarPubMed
Mennerick, S. & Matthews, G. (1998). Rapid calcium-current kinetics in synaptic terminals of goldfish retinal bipolar neurons. Visual Neuroscience 15, 1051–1056.CrossRefGoogle ScholarPubMed
Mennerick, S., Zenisek, D. & Matthews, G. (1997). Static and dynamic membrane properties of large-terminal bipolar cells from goldfish retina: Experimental test of a compartment model. Journal of Neurophysiology 78, 51–62.CrossRefGoogle ScholarPubMed
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. Nature Neuroscience 10, 1268–1276.CrossRefGoogle ScholarPubMed
Miller, R.F., Gottesman, J., Henderson, D., Sikora, M. & Kolb, H. (2001). Pre- and postsynaptic mechanisms of spontaneous, excitatory postsynaptic currents in the salamander retina. Progress in Brain Research 131, 241–253.CrossRefGoogle ScholarPubMed
Morgans, C.W., Bayley, P.R., Oesch, N.W., Ren, G., Akileswaran, L. & Taylor, W.R. (2005). Photoreceptor calcium channels: Insight from night blindness. Visual Neuroscience 22(5), 561–568.CrossRefGoogle ScholarPubMed
Moser, T. & Beutner, D. (2000). Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proceedings of the National Academy of Sciences of the United States of America 97, 883–888.CrossRefGoogle ScholarPubMed
Nelson, R. (1982). AII amacrine cells quicken time course of rod signals in the cat retina. Journal of Neurophysiology 47, 928–947.CrossRefGoogle ScholarPubMed
Neves, G. & Lagnado, L. (1999). The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. The Journal of Physiology 515(Pt 1), 181–202.CrossRefGoogle ScholarPubMed
Oltedal, L. & Hartveit, E. (2010). Transient release kinetics of rod bipolar cells revealed by capacitance measurement of exocytosis from axon terminals in rat retinal slices. The Journal of Physiology 588, 1469–1487.CrossRefGoogle ScholarPubMed
Oltedal, L., Morkve, S.H., Veruki, M.L. & Hartveit, E. (2007). Patch-clamp investigations and compartmental modeling of rod bipolar axon terminals in an in vitro thin-slice preparation of the mammalian retina. Journal of Neurophysiology 97, 1171–1187.CrossRefGoogle Scholar
Paillart, C., Li, J., Matthews, G. & Sterling, P. (2003). Endocytosis and vesicle recycling at a ribbon synapse. The Journal of Neuroscience 23, 4092–4099.CrossRefGoogle Scholar
Palmer, M.J. (2006). Modulation of Ca2+-activated K+ currents and Ca2+-dependent action potentials by exocytosis in goldfish bipolar cell terminals. The Journal of Physiology 572, 747–762.CrossRefGoogle Scholar
Palmer, M.J., Hull, C., Vigh, J. & von Gersdorff, H. (2003). Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells. The Journal of Neuroscience 23, 11332–11341.CrossRefGoogle ScholarPubMed
Pan, Z.H. (2000). Differential expression of high- and two types of low-voltage-activated calcium currents in rod and cone bipolar cells of the rat retina. Journal of Neurophysiology 83, 513–527.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Pang, J.J., Gao, F., Lem, J., Bramblett, D.E., Paul, D.L. & Wu, S.M. (2010). Direct rod input to cone BCs and direct cone input to rod BCs challenge the traditional view of mammalian BC circuitry. Proceedings of the National Academy of Sciences of the United States of America 107, 395–400.CrossRefGoogle ScholarPubMed
Pang, J.J., Gao, F. & Wu, S.M. (2004). Light-evoked current responses in rod bipolar cells, cone depolarizing bipolar cells and AII amacrine cells in dark-adapted mouse retina. The Journal of Physiology 558, 897–912.CrossRefGoogle ScholarPubMed
Protti, D.A., Flores-Herr, N. & von Gersdorff, H. (2000). Light evokes Ca2+ spikes in the axon terminal of a retinal bipolar cell. Neuron 25, 215–227.CrossRefGoogle ScholarPubMed
Protti, D.A. & Llano, I. (1998). Calcium currents and calcium signaling in rod bipolar cells of rat retinal slices. The Journal of Neuroscience 18, 3715–3724.CrossRefGoogle ScholarPubMed
Pyott, S.J. & Rosenmund, C. (2002). The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. The Journal of Physiology 539, 523–535.CrossRefGoogle ScholarPubMed
Rabl, K., Cadetti, L. & Thoreson, W.B. (2005). Kinetics of exocytosis is faster in cones than in rods. The Journal of Neuroscience 25, 4633–4640.CrossRefGoogle ScholarPubMed
Rea, R., Li, J., Dharia, A., Levitan, E.S., Sterling, P. & Kramer, R.H. (2004). Streamlined synaptic vesicle cycle in cone photoreceptor terminals. Neuron 41, 755–766.CrossRefGoogle ScholarPubMed
Rizzoli, S.O. & Betz, W.J. (2005). Synaptic vesicle pools. Nature Reviews. Neuroscience 6, 57–69.CrossRefGoogle ScholarPubMed
Rouze, N.C. & Schwartz, E.A. (1998). Continuous and transient vesicle cycling at a ribbon synapse. The Journal of Neuroscience 18, 8614–8624.CrossRefGoogle Scholar
Royle, S.J. & Lagnado, L. (2010). Clathrin-mediated endocytosis at the synaptic terminal: Bridging the gap between physiology and molecules. Traffic 11, 1489–1497.CrossRefGoogle Scholar
Saito, T. & Kujiraoka, T. (1982). Physiological and morphological identification of two types of on-center bipolar cells in the carp retina. The Journal of Comparative Neurology 205, 161–170.CrossRefGoogle ScholarPubMed
Sakaba, T. & Neher, E. (2001). Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32(6), 1119–1131.CrossRefGoogle Scholar
Sakaba, T., Tachibana, M., Matsui, K. & Minami, N. (1997). Two components of transmitter release in retinal bipolar cells: Exocytosis and mobilization of synaptic vesicles. Neuroscience Research 27, 357–370.CrossRefGoogle ScholarPubMed
Satoh, H., Aoki, K., Watanabe, S.I. & Kaneko, A. (1998). L-type calcium channels in the axon terminal of mouse bipolar cells. Neuroreport 9, 2161–2165.CrossRefGoogle ScholarPubMed
Schmitz, F. (2009). The making of synaptic ribbons: How they are built and what they do. The Neuroscientist 15, 611–624.CrossRefGoogle Scholar
Schneggenburger, R. & Neher, E. (2000). Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406, 889–893.CrossRefGoogle Scholar
Shupliakov, O., Low, P., Grabs, D., Gad, H., Chen, H., David, C., Takei, K., De Camilli, P. & Brodin, L. (1997). Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276, 259–263.CrossRefGoogle ScholarPubMed
Singer, J.H. & Diamond, J.S. (2003). Sustained Ca2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. The Journal of Neuroscience 23, 10923–10933.CrossRefGoogle Scholar
Singer, J.H. & Diamond, J.S. (2006). Vesicle depletion and synaptic depression at a mammalian ribbon synapse. Journal of Neurophysiology 95, 3191–3198.CrossRefGoogle Scholar
Singer, J.H., Lassova, L., Vardi, N. & Diamond, J.S. (2004). Coordinated multivesicular release at a mammalian ribbon synapse. Nature Neuroscience 7, 826–833.CrossRefGoogle Scholar
Smith, S.M., Renden, R. & von Gersdorff, H. (2008). Synaptic vesicle endocytosis: Fast and slow modes of membrane retrieval. Trends in Neurosciences 31, 559–568.CrossRefGoogle ScholarPubMed
Snellman, J., Zenisek, D. & Nawy, S. (2009). Switching between transient and sustained signalling at the rod bipolar-AII amacrine cell synapse of the mouse retina. The Journal of Physiology 587, 2443–2455.CrossRefGoogle ScholarPubMed
Spiwoks-Becker, I., Vollrath, L., Seeliger, M.W., Jaissle, G., Eshkind, L.G. & Leube, R.E. (2001). Synaptic vesicle alterations in rod photoreceptors of synaptophysin-deficient mice. Neuroscience 107, 127–142.CrossRefGoogle ScholarPubMed
Stell, W.K., Ishida, A.T. & Lightfoot, D.O. (1977). Structural basis for on-and off-center responses in retinal bipolar cells. Science 198, 1269–1271.CrossRefGoogle ScholarPubMed
Sterling, P. & Matthews, G. (2005). Structure and function of ribbon synapses. Trends in Neurosciences 28, 20–29.CrossRefGoogle ScholarPubMed
Stevens, C.F. & Wesseling, J.F. (1998). Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron 21, 415–424.CrossRefGoogle ScholarPubMed
Strom, T.M., Nyakatura, G., Apfelstedt-Sylla, E., Hellebrand, H., Lorenz, B., Weber, B.H., Wutz, K., Gutwillinger, N., Ruther, K., Drescher, B., Sauer, C., Zrenner, E., Meitinger, T., Rosenthal, A. & Meindl, A. (1998). An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nature Genetics 19, 260–263.CrossRefGoogle ScholarPubMed
Sun, J., Pang, Z.P., Qin, D., Fahim, A.T., Adachi, R. & Sudhof, T.C. (2007). A dual-Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 450, 676–682.CrossRefGoogle Scholar
Tachibana, M. & Kaneko, A. (1987). gamma-Aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells: Evidence for negative feedback from amacrine cells. Proceedings of the National Academy of Sciences of the United States of America 84, 3501–3505.CrossRefGoogle ScholarPubMed
Tachibana, M. & Okada, T. (1991). Release of endogenous excitatory amino acids from ON-type bipolar cells isolated from the goldfish retina. The Journal of Neuroscience 11, 2199–2208.CrossRefGoogle ScholarPubMed
Tachibana, M., Okada, T., Arimura, T., Kobayashi, K. & Piccolino, M. (1993). Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells of the goldfish retina. The Journal of Neuroscience 13, 2898–2909.CrossRefGoogle ScholarPubMed
tom Dieck, S. & Brandstatter, J.H. (2006). Ribbon synapses of the retina. Cell & Tissue Research 326, 339–346.CrossRefGoogle ScholarPubMed
Trexler, E.B., Li, W. & Massey, S.C. (2005). Simultaneous contribution of two rod pathways to AII amacrine and cone bipolar cell light responses. Journal of Neurophysiology 93, 1476–1485.CrossRefGoogle ScholarPubMed
Tsukamoto, Y., Morigiwa, K., Ueda, M. & Sterling, P. (2001). Microcircuits for night vision in mouse retina. The Journal of Neuroscience 21, 8616–8623.CrossRefGoogle ScholarPubMed
Veruki, M.L. & Hartveit, E. (2002). Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. The Journal of Neuroscience 22, 10558–10566.CrossRefGoogle ScholarPubMed
Vigh, J. & von Gersdorff, H. (2005). Prolonged reciprocal signaling via NMDA and GABA receptors at a retinal synapse. The Journal of Neuroscience 25, 11412–11423.CrossRefGoogle Scholar
von Gersdorff, H. & Matthews, G. (1994 a). Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367, 735–739.CrossRefGoogle ScholarPubMed
von Gersdorff, H. & Matthews, G. (1994 b). Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 370, 652–655.CrossRefGoogle Scholar
von Gersdorff, H. & Matthews, G. (1996). Calcium-dependent inactivation of calcium current in synaptic terminals of retinal bipolar neurons. The Journal of Neuroscience 16, 115–122.CrossRefGoogle ScholarPubMed
von Gersdorff, H. & Matthews, G. (1997). Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. The Journal of Neuroscience 17, 1919–1927.CrossRefGoogle Scholar
von Gersdorff, H., Sakaba, T., Berglund, K. & Tachibana, M. (1998). Submillisecond kinetics of glutamate release from a sensory synapse. Neuron 21(5), 1177–1188.CrossRefGoogle ScholarPubMed
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. Neuron 16, 1221–1227.CrossRefGoogle ScholarPubMed
Von Kriegstein, K., Schmitz, F., Link, E. & Sudhof, T.C. (1999). Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses. The European Journal of Neuroscience 11, 1335–1348.CrossRefGoogle ScholarPubMed
von Ruden, L. & Neher, E. (1993). A Ca-dependent early step in the release of catecholamines from adrenal chromaffin cells. Science 262, 1061–1065.CrossRefGoogle ScholarPubMed
Wahl-Schott, C., Baumann, L., Cuny, H., Eckert, C., Griessmeier, K. & Biel, M. (2006). Switching off calcium-dependent inactivation in L-type calcium channels by an autoinhibitory domain. Proceedings of the National Academy of Sciences of the United States of America 103, 15657–15662.CrossRefGoogle ScholarPubMed
Wan, Q.F., Vila, A., Zhou, Z.Y. & Heidelberger, R. (2008). Synaptic vesicle dynamics in mouse rod bipolar cells. Visual Neuroscience 25, 523–533.CrossRefGoogle ScholarPubMed
Wan, Q.F., Zhou, Z.Y., Thakur, P., Vila, A., Sherry, D.M., Janz, R. & Heidelberger, R. (2010). SV2 acts via presynaptic calcium to regulate neurotransmitter release. Neuron 66, 884–895.CrossRefGoogle ScholarPubMed
Wang, L.Y. & Kaczmarek, L.K. (1998). High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394, 384–388.CrossRefGoogle ScholarPubMed
Wu, L.G., Ryan, T.A. & Lagnado, L. (2007). Modes of vesicle retrieval at ribbon synapses, calyx-type synapses, and small central synapses. The Journal of Neuroscience 27, 11793–11802.CrossRefGoogle ScholarPubMed
Xu, W. & Lipscombe, D. (2001). Neuronal Ca(V)1.3alpha(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. The Journal of Neuroscience 21, 5944–5951.CrossRefGoogle Scholar
Xu, J., McNeil, B., Wu, W., Nees, D., Bai, L. & Wu, L.-G. (2008). GTP-independent rapid and slow endocytosis at a central synase. Nature Neuroscience 11, 45–53.CrossRefGoogle Scholar
Xu, H.P., Zhao, J.W. & Yang, X.L. (2002). Expression of voltage-dependent calcium channel subunits in the rat retina. Neuroscience Letters 329, 297–300.CrossRefGoogle ScholarPubMed
Yamashita, T., Hige, T. & Takahashi, T. (2005). Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science 307, 124–127.CrossRefGoogle Scholar
Zanazzi, G. & Matthews, G. (2009). The molecular architecture of ribbon presynaptic terminals. Molecular Neurobiology 39, 130–148.CrossRefGoogle ScholarPubMed
Zenisek, D. (2008). Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals. Proceedings of the National Academy of Sciences of the United States of America 105, 4922–4927.CrossRefGoogle ScholarPubMed
Zenisek, D., Davila, V., Wan, L. & Almers, W. (2003). Imaging calcium entry sites and ribbon structures in two presynaptic cells. The Journal of Neuroscience 23, 2538–2548.CrossRefGoogle ScholarPubMed
Zenisek, D., Horst, N.K., Merrifield, C., Sterling, P. & Matthews, G. (2004). Visualizing synaptic ribbons in the living cell. The Journal of Neuroscience 24, 9752–9759.CrossRefGoogle ScholarPubMed
Zenisek, D. & Matthews, G. (1998). Calcium action potentials in retinal bipolar neurons. Visual Neuroscience 15, 69–75.CrossRefGoogle ScholarPubMed
Zenisek, D., Steyer, J.A. & Almers, W. (2000). Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406, 849–854.CrossRefGoogle ScholarPubMed
Zenisek, D., Steyer, J.A., Feldman, M.E. & Almers, W. (2002). A membrane marker leaves synaptic vesicles in milliseconds after exocytosis in retinal bipolar cells. Neuron 35, 1085–1097.CrossRefGoogle ScholarPubMed
Zhou, Z.Y., Wan, Q.F., Thakur, P. & Heidelberger, R. (2006). Capacitance measurements in the mouse rod bipolar cell identify a pool of releasable synaptic vesicles. Journal of Neurophysiology 96, 2539–2548.CrossRefGoogle ScholarPubMed