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Synaptic vesicle dynamics in mouse rod bipolar cells

Published online by Cambridge University Press:  01 July 2008

QUN-FANG WAN ,
ALEJANDRO VILA ,
ZHEN-YU ZHOU  and
RUTH HEIDELBERGER
QUN-FANG WAN
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School at Houston, Houston, Texas
ALEJANDRO VILA
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School at Houston, Houston, Texas
ZHEN-YU ZHOU
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
*
*Address correspondence and reprint requests to: Ruth Heidelberger, Department of Neurobiology and Anatomy, University of Texas Medical School at Houston, 6431 Fannin Street, MSB 7.046, Houston, TX 77025. E-mail: ruth.heidelberger@uth.tmc.edu
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Abstract

To better understand synaptic signaling at the mammalian rod bipolar cell terminal and pave the way for applying genetic approaches to the study of visual information processing in the mammalian retina, synaptic vesicle dynamics and intraterminal calcium were monitored in terminals of acutely isolated mouse rod bipolar cells and the number of ribbon-style active zones quantified. We identified a releasable pool, corresponding to a maximum of ≈35 vesicles/ribbon-style active zone. Following depletion, this pool was refilled with a time constant of ≈7 s. The presence of a smaller, rapidly releasing pool and a small, fast component of refilling was also suggested. Following calcium channel closure, membrane surface area was restored to baseline with a time constant that ranged from 2 to 21 s depending on the magnitude of the preceding Ca2+ transient. In addition, a brief, calcium-dependent delay often preceded the start of onset of membrane recovery. Thus, several aspects of synaptic vesicle dynamics appear to be conserved between rod-dominant bipolar cells of fish and mammalian rod bipolar cells. A major difference is that the number of vesicles available for release is significantly smaller in the mouse rod bipolar cell, both as a function of the total number per neuron and on a per active zone basis.

Keywords

ExocytosisEndocytosisRibbon synapseRetinaVesicle

Information

Type
Research Articles
Information
Visual Neuroscience , Volume 25 , Issue 4 , July 2008 , pp. 523 - 533
Copyright
Copyright © Cambridge University Press 2008

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References

Abercrombie, M. (1946). Estimation of nuclear population from microtome sections. Anatomical Record 94, 239–247.CrossRefGoogle ScholarPubMed
Artalejo, C.R., Elhamdani, A. & Palfrey, H.C. (2002). Sustained stimulation shifts the mechanism of endocytosis from dynamin-1-dependent rapid endocytosis to clathrin- and dynamin-2-mediated slow endocytosis in chromaffin cells. Proceedings of the National Academy of Sciences of the United States of America 99, 6358–6363.CrossRefGoogle ScholarPubMed
Bieda, M.C. & Copenhagen, D.R. (2000). Inhibition is not required for the production of transient spiking responses from retinal ganglion cells. Visual Neuroscience 17, 243–254.CrossRefGoogle Scholar
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retinal and 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. Journal of Physiology 523(Pt 3), 771–783.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.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. European Journal of Neuroscience 10, 317–323.CrossRefGoogle ScholarPubMed
Edmonds, B.W., Gregory, F.D. & Schweizer, F.E. (2004). Evidence that fast exocytosis can be predominantly mediated by vesicles not docked at active zones in frog saccular hair cells. Journal of Physiology 560, 439–450.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
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, ed. Sakmann, B. & Neher, E., pp. 155–198. New York and London: 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. Journal of Neuroscience 19, 6309–6317.CrossRefGoogle ScholarPubMed
Heidelberger, R. (1998). Adenosine triphosphate and the late steps in calcium-dependent exocytosis at a ribbon synapse. 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. 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. (1992). Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. 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 and 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
Horrigan, F.T. & Bookman, R.J. (1994). Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron 13, 1119–1129.CrossRefGoogle ScholarPubMed
Hsu, S.F. & Jackson, M.B. (1996). Rapid exocytosis and endocytosis in nerve terminals of the rat posterior pituitary. Journal of Physiology 494(Pt 2), 539–553.CrossRefGoogle ScholarPubMed
Hull, C., Studholme, K., Yazulla, S. & von, G.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
Ishida, A.T., Stell, W.K. & Lightfoot, D.O. (1980). Rod and cone inputs to bipolar cells in goldfish retina. 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
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301–312.CrossRefGoogle ScholarPubMed
Kreft, M., Krizaj, D., Grilc, S. & Zorec, R. (2003). Properties of exocytotic response in vertebrate photoreceptors. Journal of Neurophysiology 90, 218–225.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. Journal of Neuroscience 26, 1366–1377.CrossRefGoogle ScholarPubMed
LoGiudice, L., Sterling, P. & Matthews, G. (2008). Mobility and turnover of vesicles at the synaptic ribbon. Journal of Neuroscience 28, 3150–3158.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
Messler, P., Harz, H. & Uhl, R. (1996). Instrumentation for multiwavelengths excitation imaging. Journal of Neuroscience Methods 69, 137–147.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
Naraghi, M., Muller, T.H. & Neher, E. (1998). Two-dimensional determination of the cellular Ca2+ binding in bovine chromaffin cells. Biophysical Journal 75, 1635–1647.CrossRefGoogle ScholarPubMed
Neher, E. (1998). Vesicle pools and Ca2+ microdomains: New tools for understanding their roles in neurotransmitter release. Neuron 20, 389–399.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., Gomis, A. & Lagnado, L. (2001). Calcium influx selects the fast mode of endocytosis in the synaptic terminal of retinal bipolar cells. Proceedings of the National Academy of Sciences of the United States of America 98, 15282–15287.CrossRefGoogle ScholarPubMed
Neves, G. & Lagnado, L. (1999). The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. Journal of Physiology 515(Pt 1), 181–202.CrossRefGoogle ScholarPubMed
Paillart, C., Li, J., Matthews, G. & Sterling, P. (2003). Endocytosis and vesicle recycling at a ribbon synapse. Journal of Neuroscience 23, 4092–4099.CrossRefGoogle Scholar
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. & 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. 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
Pyott, S.J. & Rosenmund, C. (2002). The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. 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. Journal of Neuroscience 25, 4633–4640.CrossRefGoogle ScholarPubMed
Renden, R. & von Gersdorff, H. (2007). Synaptic vesicle endocytosis at a CNS nerve terminal: Faster kinetics at physiological temperatures and increased endocytotic capacity during maturation. Journal of Neurophysiology 98, 3349–3359.CrossRefGoogle Scholar
Richards, D.A., Guatimosim, C., Rizzoli, S.O. & Betz, W.J. (2003). Synaptic vesicle pools at the frog neuromuscular junction. Neuron 39, 529–541.CrossRefGoogle ScholarPubMed
Rouze, N.C. & Schwartz, E.A. (1998). Continuous and transient vesicle cycling at a ribbon synapse. Journal of Neuroscience 18, 8614–8624.CrossRefGoogle Scholar
Saito, T. & Kujiraoka, T. (1982). Physiological and morphological identification of two types of on-center bipolar cells in the carp retina. Journal of Comparative Neurology 205, 161–170.CrossRefGoogle ScholarPubMed
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
Schmitz, F., Konigstorfer, A. & Sudhof, T.C. (2000). RIBEYE, a component of synaptic ribbons: A protein’s journey through evolution provides insight into synaptic ribbon function. Neuron 28, 857–872.CrossRefGoogle ScholarPubMed
Singer, J.H. & Diamond, J.S. (2003). Sustained Ca2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. 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
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
Sun, J.Y. & Wu, L.G. (2001). Fast kinetics of exocytosis revealed by simultaneous measurements of presynaptic capacitance and postsynaptic currents at a central synapse. Neuron 30, 171–182.CrossRefGoogle Scholar
Thoreson, W.B., Rabl, K., Townes-Anderson, E. & Heidelberger, R. (2004). A highly Ca2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42, 595–605.CrossRefGoogle ScholarPubMed
tom Dieck, S., Altrock, W.D., Kessels, M.M., Qualmann, B., Regus, H., Brauner, D., Fejtova, A., Bracko, O., Gundelfinger, E.D. & Brandstatter, 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. Journal of Cell Biology 168, 825–836.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. 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. Journal of Neuroscience 22, 10558–10566.CrossRefGoogle ScholarPubMed
Veruki, M.L., Morkve, S.H. & Hartveit, E. (2003). Functional properties of spontaneous EPSCs and non-NMDA receptors in rod amacrine (AII) cells in the rat retina. Journal of Physiology 549, 759–774.CrossRefGoogle ScholarPubMed
von Gersdorff, H. (2001). Synaptic ribbons: Versatile signal transducers. Neuron 29, 7–10.CrossRefGoogle ScholarPubMed
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. 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. 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, 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
Wadel, K., Neher, E. & Sakaba, T. (2007). The coupling between synaptic vesicles and Ca2+ channels determines fast neurotransmitter release. Neuron 53, 563–575.CrossRefGoogle ScholarPubMed
Wang, M.M., Janz, R., Belizaire, R., Frishman, L.J. & Sherry, D.M. (2003). Differential distribution and developmental expression of synaptic vesicle protein 2 isoforms in the mouse retina. Journal of Comparative Neurology 460, 106–122.CrossRefGoogle ScholarPubMed
Witkovsky, P. & Dowling, J.E. (1969). Synaptic relationships in the plexiform layers of carp retina. Zeitschrift für Zellforschung und Mikroskopische Anatomie 100, 60–82.CrossRefGoogle ScholarPubMed
Wu, L.G. (2004). Kinetic regulation of vesicle endocytosis at synapses. Trends in Neuroscience 27, 548–554.CrossRefGoogle ScholarPubMed
Wu, L.G. & Betz, W.J. (1996). Nerve activity but not intracellular calcium determines the time course of endocytosis at the frog neuromuscular junction. Neuron 17, 769–779.CrossRefGoogle Scholar
Zenisek, D., Horst, N.K., Merrifield, C., Sterling, P. & Matthews, G. (2004). Visualizing synaptic ribbons in the living cell. Journal of Neuroscience 24, 9752–9759.CrossRefGoogle ScholarPubMed
Zenisek, D., Steyer, J.A. & Almers, W. (2000). Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406, 1849–854.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