Synaptic vesicle pools and dynamics

Cold Spring Harbor Perspectives in Biology

Volumn 4, Issue 8, 2012, Pages

  Alabi, Abdul Rasheed A ^a   Tsien, Richard W ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; FLUORESCENT DYE; FM1 43; GREEN FLUORESCENT PROTEIN; PYRIDINIUM DERIVATIVE; QUANTUM DOT; QUATERNARY AMMONIUM DERIVATIVE;

ANIMAL; BIOLOGICAL MODEL; CLASSIFICATION; METABOLISM; NERVE CELL NETWORK; PHYSIOLOGY; REVIEW; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; MODELS, BIOLOGICAL; NERVE NET; NEUROTRANSMITTER AGENTS; PYRIDINIUM COMPOUNDS; QUANTUM DOTS; QUATERNARY AMMONIUM COMPOUNDS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 84865642204     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a013680     Document Type: Article

References (147)

1. Abbott LF, RegehrWG. 2004. Synaptic computation. Nature 431: 796-803.
2. Abbott LF, Varela JA, Sen K, Nelson SB. 1997. Synaptic depression and cortical gain control. Science 275: 220-224.
3. Ahmari SE, Buchanan J, Smith SJ. 2000. Assembly of presynaptic active zones fromcytoplasmic transport packets. Nat Neurosci 3: 445-451.
4. Allen C, Stevens CF. 1994. An evaluation of causes for unreliability of synaptic transmission. ProcNatl Acad Sci 91: 10380-10383.
5. Armitage BA, Siegelbaum SA. 1998. Presynaptic induction and expression of homosynaptic depression at Aplysia sensorimotor neuron synapses. J Neurosci 18: 8770-8779.
6. Atasoy D, Ertunc M, Moulder KL, Blackwell J, Chung C, Su J, Kavalali ET. 2008. Spontaneous and evoked glutamate release activates two populations of NMDA receptors with limited overlap. J Neurosci 28: 10151-10166.
7. Babai N, Bartoletti TM, Thoreson WB. 2010. Calcium regulates vesicle replenishment at the cone ribbon synapse. J Neurosci 30: 15866-15877.
8. Bielefeldt K, Jackson MB. 1993. A calcium-activated potassium channel causes frequency-dependent action-potential failures in a mammalian nerve terminal. J Neurophysiol 70: 284-298.
9. Birks R, Macintosh FC. 1961. Acetylcholine metabolism of a sympathetic ganglion. Can J Biochem Phys 39: 787.
10. Bittner GD, Kennedy D. 1970. Quantitative aspects of transmitter release. J Cell Biol 47: 585-592.
11. Blakely RD, Edwards RH. 2012. Vesicular and plasma membrane transporters for neurotransmitters. Cold Spring Harb Perspect Biol 4: a005595
12. Burrone J, Lagnado L. 2000. Synaptic depression and the kinetics of exocytosis in retinal bipolar cells. JNeurosci 20: 568-578.
13. Chung C, Barylko B, Leitz J, Liu X, Kavalali ET. 2010. Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission. J Neurosci 30: 1363-1376.
14. Darcy KJ, Staras K, Collinson LM, Goda Y. 2006. Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat Neurosci 9: 315-321.
15. Dekay JG, Chang TC, Mills N, Speed HE, Dobrunz LE. 2006. Responses of excitatory hippocampal synapses to natural stimulus patterns reveal a decrease in short-term facilitation and increase in short-term depression during postnatal development. Hippocampus 16: 66-79.
16. de Lange RP, de Roos AD, Borst JG. 2003. Two modes of vesicle recycling in the rat calyx of Held. J Neurosci 23: 10164-10173.
17. Del Castillo J, Katz B. 1954. Quantal components of the endplate potential. J Physiol 124: 560-573.
18. Del Castillo J, Katz B. 1956. Biophysical aspects of neuromuscular transmission. Prog. Biophys. Biophys. Chem. 6: 121-170.
19. Denker A, Bethani I, Krohnert K, Korber C, Horstmann H, Wilhelm BG, Barysch SV, Kuner T, Neher E, Rizzoli SO. 2011a. A small pool of vesicles maintains synaptic activity in vivo. Proc Natl Acad Sci 108: 17177-17182.
20. Denker A, Krohnert K, Buckers J, Neher E, Rizzoli SO. 2011b. The reserve pool of synaptic vesicles acts as a buffer for proteins involved in synaptic vesicle recycling. Proc Natl Acad Sci 108: 17183-17188.
21. De Robertis ED, Bennett HS. 1955. Some features of the submicroscopic morphology of synapses in frog and earthworm. J Biophys Biochem Cytol 1: 47-58.
22. Dobrunz LE, Stevens CF. 1997. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008.
23. Dobrunz LE, Stevens CF. 1999. Response of hippocampal synapses to natural stimulation patterns. Neuron 22: 157-166.
24. Dobrunz LE, Huang EP, Stevens CF. 1997. Very short-term plasticity in hippocampal synapses. ProcNatl Acad Sci 94: 14843-14847.
25. Elmqvist D, Quastel DM. 1965. A quantitative study of endplate potentials in isolated human muscle. J Physiol 178: 505-529.
26. Fatt P, Katz B. 1952. Spontaneous subthreshold activity at motor nerve endings. J Physiol 117: 109-128.
27. Fenton AA, Muller RU. 1998. Place cell discharge is extremely variable during individual passes of the rat through the firing field. Proc Natl Acad Sci 95: 3182-3187.
28. Fernandez-Alfonso T, Ryan TA. 2006. The efficiency of the synaptic vesicle cycle at central nervous system synapses. Trends Cell Biol 16: 413-420.
29. Fernandez-Alfonso T, Ryan TA. 2008. A heterogeneous "resting" pool of synaptic vesicles that is dynamically interchanged across boutons in mammalian CNS synapses. Brain Cell Biol 36: 87-100.
30. Fesce R, Grohovaz F, Valtorta F, Meldolesi F. 1994. Neurotransmitter release: fusion or "kiss-and-run?" Trends Cell Biol 4: 1-4.
31. Fioravante D, Chu Y, Myoga MH, Leitges M, Regehr WG. 2011. Calcium-dependent isoforms of protein kinase C mediate posttetanic potentiation at the calyx of Held. Neuron 70: 1005-1019.
32. Fisher-Lavie A, Zeidan A, Stern M, Garner CC, Ziv NE. 2011. Use dependence of presynaptic tenacity. J Neurosci 31: 16770-16780.
33. Fredj NB, Burrone J. 2009. A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat Neurosci 12: 751-758.
34. Gabriel T, Garcia-Perez E, Mahfooz K, Goni J, Martinez-Turrillas R, Perez-Otano I, Lo DC, Wesseling JF. 2011. A new kinetic framework for synaptic vesicle trafficking tested in synapsin knock-outs. J Neurosci 31: 11563-11577.
35. Garcia-Perez E, Lo DC, Wesseling JF. 2008. Kinetic isolation of a slowly recovering component of short-term depression during exhaustive use at excitatory hippocampal synapses. J Neurophysiol 100: 781-795.
36. + sensor for transmitter release at a central synapse. Cell 79: 717-727.
37. Goda Y, Stevens CF. 1998. Readily releasable pool size changes associated with long term depression. Proc Natl Acad Sci 95: 1283-1288.
38. 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. J Neurosci 19: 6309-6317.
39. Groemer TW, Klingauf J. 2007. Synaptic vesicles recycling spontaneously and during activity belong to the same vesicle pool. Nat Neurosci 10: 145-147.
40. Hallermann S, Pawlu C, Jonas P, Heckmann M. 2003. A large pool of releasable vesicles in a cortical glutamatergic synapse. Proc Natl Acad Sci 100: 8975-8980.
41. Hallermann S, Fejtova A, Schmidt H, Weyhersmuller A Silver RA, Gundelfinger ED, Eilers J. 2010. Bassoon speeds vesicle reloading at a central excitatory synapse. Neuron 68: 710-723.
42. Hanse E, Gustafsson B. 2001a. Factors explaining heterogeneity in short-term synaptic dynamics of hippocampal glutamatergic synapses in the neonatal rat. J Physiol 537: 141-149.
43. Hanse E, Gustafsson B. 2001b. Vesicle release probability and pre-primed pool at glutamatergic synapses in area CA1 of the rat neonatal hippocampus. J Physiol 531: 481-493.
44. Harata N, Pyle JL, Aravanis AM, Mozhayeva M, Kavalali ET Tsien RW. 2001a. Limited numbers of recycling vesicles in small CNS nerve terminals: Implications for neural signaling and vesicular cycling. Trends Neurosci 24: 637-643.
45. Harata N, Ryan TA, Smith SJ, Buchanan J, Tsien RW. 2001b. Visualizing recycling synaptic vesicles in hippocampal neurons by FM 1-43 photoconversion. Proc Natl Acad Sci 98: 12748-12753.
46. Harata NC, Aravanis AM, Tsien RW. 2006. Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion. J Neurochem 97: 1546-1570.
47. Harris KM, Sultan P. 1995. Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses. Neuropharmacology 34: 1387-1395.
48. +. Biophys J 67: 2546-2557.
49. Herzog E, Nadrigny F, Silm K, Biesemann C, Helling I, Bersot T, Steffens H, Schwartzmann R, Nagerl UV, El Mestikawy S, et al. 2011. In vivo imaging of intersynaptic vesicle exchange using VGLUT1 Venus knock-in mice. J Neurosci 31: 15544-15559.
50. Hessler NA, Shirke AM, Malinow R. 1993. The probability of transmitter release at a mammalian central synapse. Nature 366: 569-572.
51. Heuser JE, Reese TS. 1981. Structural changes after transmitter release at the frog neuromuscular junction. J Cell Biol 88: 564-580.
52. Hodgkin AL, Huxley AF. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500-544.
53. Hua Y, Sinha R, Martineau M, Kahms M, Klingauf J. 2010. A common origin of synaptic vesicles undergoing evoked and spontaneous fusion. Nat Neurosci 13: 1451-1453.
54. Hua Z, Leal-Ortiz S, Foss SM, Waites CL, Garner CC, Voglmaier SM, Edwards RH. 2011. v-SNARE composition distinguishes synaptic vesicle pools. Neuron 71: 474-487.
55. Ikeda K, Bekkers JM. 2009. Counting the number of releasable synaptic vesicles in a presynaptic terminal. Proc Natl Acad Sci 106: 2945-2950.
56. Kalla S, Stern M, Basu J, Varoqueaux F, Reim K, Rosenmund C, Ziv NE, Brose N. 2006. Molecular dynamics of a presynaptic active zone protein studied in Munc13-1-enhanced yellow fluorescent protein knock-in mutant mice. J Neurosci 26: 13054-13066.
57. Kamin D, Lauterbach MA, Westphal V, Keller J, Schonle A Hell SW, Rizzoli SO. 2010. High-and low-mobility stages in the synaptic vesicle cycle. Biophys J 99: 675-684.
58. Kim SH, Ryan TA. 2010. CDK5 serves as a major control point in neurotransmitter release. Neuron 67: 797-809.
59. Kraszewski K, Mundigl O, Daniell L, Verderio C, Matteoli M, De Camilli P. 1995. Synaptic vesicle dynamics in living cultured hippocampal neurons visualized with CY3-conjugated antibodies directed against the lumenal domain of synaptotagmin. J Neurosci 15: 4328-4342.
60. Kraushaar U, Jonas P. 2000. Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20: 5594-5607.
61. Krueger SR, Kolar A, Fitzsimonds RM. 2003. The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons. Neuron 40: 945-957.
62. Kuromi H, Kidokoro Y. 2005. Exocytosis and endocytosis of synaptic vesicles and functional roles of vesicle pools: Lessons from the Drosophila neuromuscular junction. Neuroscientist 11: 138-147.
63. Lee JS, Ho WK, Lee SH. 2010. Post-tetanic increase in the fast-releasing synaptic vesicle pool at the expense of the slowly releasing pool. J Gen Physiol 136: 259-272.
64. Li Z, Burrone J, Tyler WJ, Hartman KN, Albeanu DF, Murthy VN. 2005. Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proc Natl Acad Sci 102: 6131-6136.
65. Liley AW, North KA. 1953. An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction. J Neurophysiol 16: 509-527.
66. Liu G, Tsien RW. 1995. Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 375: 404-408.
67. + sensor for vesicle fusion. Nature 435: 497-501.
68. +-evoked transmitter release via acting on both Munc13 and protein kinase C. J Neurosci 28: 8257-8267.
69. Lundberg A, Quilisch H. 1953. Presynaptic potentiation and depression of neuromuscular transmission in frog and rat. Acta Physiol Scand Suppl 111: 111-120.
70. Matz J, Gilyan A, Kolar A, McCarvill T, Krueger SR. 2010. Rapid structural alterations of the active zone lead to sustained changes in neurotransmitter release. Proc Natl Acad Sci 107: 8836-8841.
71. Miesenbock G, De Angelis DA, Rothman JE. 1998. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394: 192-195.
72. + sensor proteins mediates short-term synaptic plasticity. Neuron 57: 210-216.
73. Moulder KL, Mennerick S. 2005. Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons. J Neurosci 25: 3842-3850.
74. Murthy VN, De Camilli P. 2003. Cell biology of the presynaptic terminal. Annu Rev Neurosci 26: 701-728.
75. Murthy VN, Stevens CF. 1998. Synaptic vesicles retain their identity through the endocytic cycle. Nature 392: 497-501.
76. Murthy VN, Stevens CF. 1999. Reversal of synaptic vesicle docking at central synapses. Nat Neurosci 2: 503-507.
77. Murthy VN, Sejnowski TJ, Stevens CF. 1997. Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18: 599-612.
78. Murthy VN, Schikorski T, Stevens CF, Zhu Y. 2001. Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32: 673-682.
79. Neher E. 2008. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59: 861-872.
80. Neher E, Sakaba T. 2001. Combining deconvolution and noise analysis for the estimation of transmitter release rates at the calyx of held. J Neurosci 21: 444-461.
81. Opazo F, Punge A, Buckers J, Hoopmann P, Kastrup L, Hell SW, Rizzoli SO. 2010. Limited intermixing of synaptic vesicle components upon vesicle recycling. Traffic 11: 800-812.
82. Otis T, Zhang S, Trussell LO. 1996. Direct measurement of AMPA receptor desensitization induced by glutamatergic synaptic transmission. J Neurosci 16: 7496-7504.
83. Palade GE. 1954. Electron microscope observations of interneuronal and neuromuscular synapses. Anat Rec 118: 335-336.
84. Palay SL. 1954. Electron microscope study of the cytoplasm of neurons. Anat Rec 118: 336.
85. Palay SL. 1956. Synapses in the central nervous system. J Biophys Biochem Cytol 2: 193-202.
86. +-triggered exocytosis. Curr Opin Cell Biol 22: 496-505.
87. Park H, Li Y, Tsien RW. 2012. Influence of synaptic vesicle position on release probability and exocytic fusion mode. Science doi: 10.1126/science.1216937.
88. Poskanzer KE, DavisGW. 2004. Mobilization and fusion of a non-recycling pool of synaptic vesicles under conditions of endocytic blockade. Neuropharmacology 47: 714-723.
89. Pyle JL, Kavalali ET, Piedras-Renteria ES, Tsien RW. 2000. Rapid reuse of readily releasable pool vesicles at hippocampal synapses. Neuron 28: 221-231.
90. Pyott SJ, Rosenmund C. 2002. The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. J Physiol 539: 523-535.
91. Ramirez DM, Khvotchev M, Trauterman B, Kavalali ET. 2012. Vti1a identifies a vesicle pool that preferentially recycles at rest and maintains spontaneous neurotransmission. Neuron 73: 121-134.
92. Ratnayaka A, MarraV, BushD, Burden JJ, Branco T, Staras K. 2012. Recruitment of resting vesicles into recycling pools supports NMDA-receptor dependent synaptic potentiation in cultured hippocampal neurons. J Physiol doi: 10.1113/jphysiol.2011.226688.
93. +-dependent neurotransmitter release. Cell 104: 71-81.
94. Ribrault C, Reingruber J, Petkovic M, Galli T, Ziv NE, Holcman D, Triller A. 2011. Syntaxin1A lateral diffusion reveals transient and local SNARE interactions. J Neurosci 31: 17590-17602.
95. Richards DA, Guatimosim C, Rizzoli SO, Betz WJ. 2003. Synaptic vesicle pools at the frog neuromuscular junction. Neuron 39: 529-541.
96. Rizzoli SO, Betz WJ. 2005. Synaptic vesicle pools. Nat Rev Neurosci 6: 57-69.
97. Rosenmund C, Stevens CF. 1996. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207.
98. Rosenmund C, Clements JD, Westbrook GL. 1993. Nonuniform probability of glutamate release at a hippocampal synapse. Science 262: 754-757.
99. Ruiz R, Cano R, Casanas JJ, Gaffield MA, Betz WJ, Tabares L. 2011. Active zones and the readily releasable pool of synaptic vesicles at the neuromuscular junction of the mouse. J Neurosci 31: 2000-2008.
100. Ryan TA, Ziv NE, Smith SJ. 1996. Potentiation of evoked vesicle turnover at individually resolved synaptic boutons. Neuron 17: 125-134.
101. Sakaba T, Neher E. 2001a. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyxtype synapse. Neuron 32: 1119-1131.
102. Sakaba T, Neher E. 2001b. Quantitative relationship between transmitter release and calcium current at the calyx of held synapse. J Neurosci 21: 462-476.
103. Sara Y, Virmani T, Deak F, Liu X, Kavalali ET. 2005. An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 45: 563-573.
104. Sara Y, Bal M, Adachi M, Monteggia LM, Kavalali ET. 2011. Use-dependent AMPA receptor block reveals segregation of spontaneous and evoked glutamatergic neurotransmission. J Neurosci 31: 5378-5382.
105. Saviane C, Silver RA. 2006. Fast vesicle reloading and a large pool sustain high bandwidth transmission at a central synapse. Nature 439: 983-987.
106. Schikorski T, Stevens CF. 1997. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17: 5858-5867.
107. Schikorski T, Stevens CF. 2001. Morphological correlates of functionality defined synaptic vesicle populations. Nature Neurosci 4: 391-395.
108. Schneggenburger R, Sakaba T, Neher E. 2002. Vesicle pools and short-term synaptic depression: Lessons from a large synapse. Trends Neurosci 25: 206-212.
109. + regulator of synaptic exocytosis. Nat Struct Mol Biol 17: 280-288.
110. Shtrahman M, Yeung C, Nauen DW, Bi GQ, Wu XL. 2005. Probing vesicle dynamics in single hippocampal synapses. Biophys J 89: 3615-3627.
111. Sjostrand FS. 1953. The ultrastructure of the inner segments of the retinal rods of the guinea pig eye as revealed by electron microscopy. J Cell Physiol 42: 45-70.
112. + acts by two separate pathways to modulate the supply of release-competent vesicles in chromaffin cells. Neuron 20: 1243-1253.
113. Staras K, Branco T, Burden JJ, Pozo K, Darcy K, Marra V Ratnayaka A, Goda Y. 2010. A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons. Neuron 66: 37-44.
114. Stevens CF, Sullivan JM. 1998. Regulation of the readily releasable vesicle pool by protein kinase C. Neuron 21: 885-893.
115. Stevens CF, Wang Y. 1994. Changes in reliability of synaptic function as a mechanism for plasticity. Nature 371: 704-707.
116. Stevens CF, Wang Y. 1995. Facilitation and depression at single central synapses. Neuron 14: 795-802.
117. Stevens CF, Wesseling JF. 1998. Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron 21: 415-424.
118. Stevens CF, Wesseling JF. 1999a. Augmentation is a potentiation of the exocytotic process. Neuron 22: 139-146.
119. Stevens CF, Wesseling JF. 1999b. Identification of a novel process limiting the rate of synaptic vesicle cycling at hippocampal synapses. Neuron 24: 1017-1028.
120. Stevens CF, Williams JH. 2000. "Kiss and run" exocytosis at hippocampal synapses. Proc Natl Acad Sci 97: 12828-12833.
121. Stevens CF, Williams JH. 2007. Discharge of the readily releasable pool with action potentials at hippocampal synapses. J Neurophysiol 98: 3221-3229.
122. Südhof TC. 2000. The synaptic vesicle cycle revisited. Neuron 28: 317-320.
123. Südhof TC. 2004. The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547.
124. Südhof TC. 2012. Calcium control of neurotransmitter release. Cold Spring Harb Perspect Biol 4: a011353.
125. Südhof TC, Rizo J. 2011. Synaptic vesicle exocytosis. Cold Spring Harb Perspect Biol 3: a005637.
126. Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, RiedelD, Urlaub H, Schenck S, Brugger B, Ringler P, et al. 2006. Molecular anatomy of a trafficking organelle. Cell 127: 831-846.
127. Thiagarajan TC, Lindskog M, Tsien RW. 2005. Adaptation to synaptic inactivity in hippocampal neurons. Neuron 47: 725-737.
128. Tsodyks MV, Markram H. 1997. The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci 94: 719-723.
129. Tsuriel S, Fisher A, Wittenmayer N, Dresbach T, Garner CC Ziv NE. 2009. Exchange and redistribution dynamics of the cytoskeleton of the active zone molecule bassoon. J Neurosci 29: 351-358.
130. von Gersdorff H, Matthews G. 1997. Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. J Neurosci 17: 1919-1927.
131. 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.
132. Waites CL, Garner CC. 2011. Presynaptic function in health and disease. Trends Neurosci 34: 326-337.
133. Wang LY, Kaczmarek LK. 1998. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394: 384-388.
134. Waters J, Smith SJ. 2000. Phorbol esters potentiate evoked and spontaneous release by different presynaptic mechanisms. J Neurosci 20: 7863-7870.
135. Waters J, Smith SJ. 2002. Vesicle pool partitioning influences presynaptic diversity and weighting in rat hippocampal synapses. J Physiol 541: 811-823.
136. Welzel O, Henkel AW, Stroebel AM, Jung J, Tischbirek CH Ebert K, Kornhuber J, Rizzoli SO, Groemer TW. 2011. Systematic heterogeneity of fractional vesicle pool sizes and release rates of hippocampal synapses. Biophys J 100: 593-601.
137. Wesseling JF, Lo DC. 2002. Limit on the role of activity in controlling the release-ready supply of synaptic vesicles. J Neurosci 22: 9708-9720.
138. Westphal V, Rizzoli SO, Lauterbach MA, Kamin D, Jahn R HellSW. 2008. Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320: 246-249.
139. Wilhelm BG, Groemer TW, Rizzoli SO. 2010. The same synaptic vesicles drive active and spontaneous release. Nat Neurosci 13: 1454-1456.
140. Willig KI, Rizzoli SO, Westphal V, Jahn R, Hell SW. 2006. STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature 440: 935-939.
141. Wu LG, Borst JG. 1999. The reduced release probability of releasable vesicles during recovery from short-term synaptic depression. Neuron 23: 821-832.
142. Wu LG, Saggau P. 1997. Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci 20: 204-212.
143. Wyatt RM, Balice-Gordon RJ. 2008. Heterogeneity in synaptic vesicle release at neuromuscular synapses of mice expressing synaptopHluorin. J Neurosci 28: 325-335.
144. Xu J, Wu LG. 2005. The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron 46: 633-645.
145. ZenisekD. 2008. Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals. Proc Natl Acad Sci 105: 4922-4927.
146. Zhang Q, Cao YQ, Tsien RW. 2007. Quantum dots provide an optical signal specific to full collapse fusion of synaptic vesicles. Proc Natl Acad Sci 104: 17843-17848.
147. Zucker RS, RegehrWG. 2002. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.