CoChat
Sign Up
Cited by 61Neuroscience and Neuropharmacology ResearchCellular transport and secretionExtracellular vesicles in disease

The readily-releasable pool dynamically regulates multivesicular release.

Open access
Vaden, Jada H, Banumurthy, Gokulakrishna, Gusarevich, Eugeny S, Overstreet-Wadiche, Linda, Wadiche, Jacques I·2019·eLife
DOI 10.7554/elife.47434PMC PMC6716946
Open this paper in CoChat — free account

Abstract

The number of neurotransmitter-filled vesicles released into the synaptic cleft with each action potential dictates the reliability of synaptic transmission. Variability of this fundamental property provides diversity of synaptic function across brain regions, but the source of this variability is unclear. The prevailing view is that release of a single (univesicular release, UVR) or multiple vesicles (multivesicular release, MVR) reflects variability in vesicle release probability, a notion that is well-supported by the calcium-dependence of release mode. However, using mouse brain slices, we now demonstrate that the number of vesicles released is regulated by the size of the readily-releasable pool, upstream of vesicle release probability. Our results point to a model wherein protein kinase A and its vesicle-associated target, synapsin, dynamically control release site occupancy to dictate the number of vesicles released without altering release probability. Together these findings define molecular mechanisms that control MVR and functional diversity of synaptic signaling.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.7554/elife.47434

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 90

  1. Ariel P Hoppa MB Ryan TA 2012 Intrinsic variability in Pv, RRP size, Ca(2+) channel repertoire, and presynaptic potentiation in individual synaptic boutons Frontiers in Synaptic Neuroscience 4 9 10.3389/fnsyn.2012.00009 23335896 PMC3542534 · DOI
  2. Auger C Kondo S Marty A 1998 Multivesicular release at single functional synaptic sites in cerebellar stellate and basket cells The Journal of Neuroscience 18 4532 4547 10.1523/JNEUROSCI.18-12-04532.1998 9614230 PMC6792676 · DOI
  3. Baldelli P Fassio A Valtorta F Benfenati F 2007 Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses Journal of Neuroscience 27 13520 13531 10.1523/JNEUROSCI.3151-07.2007 18057210 PMC6673103 · DOI
  4. Bender VA Pugh JR Jahr CE 2009 Presynaptically expressed long-term potentiation increases multivesicular release at parallel fiber synapses Journal of Neuroscience 29 10974 10978 10.1523/JNEUROSCI.2123-09.2009 19726655 PMC2775459 · DOI
  5. Biró AA Holderith NB Nusser Z 2005 Quantal size is independent of the release probability at hippocampal excitatory synapses Journal of Neuroscience 25 223 232 10.1523/JNEUROSCI.3688-04.2005 15634785 PMC6725207 · DOI
  6. Ceccaldi PE Grohovaz F Benfenati F Chieregatti E Greengard P Valtorta F 1995 Dephosphorylated synapsin I anchors synaptic vesicles to actin cytoskeleton: an analysis by videomicroscopy The Journal of Cell Biology 128 905 912 10.1083/jcb.128.5.905 7876313 PMC2120389 · DOI
  7. Chen C Regehr WG 1997 The mechanism of cAMP-mediated enhancement at a cerebellar synapse The Journal of Neuroscience 17 8687 8694 10.1523/JNEUROSCI.17-22-08687.1997 9348337 PMC6573078 · DOI
  8. Chi P Greengard P Ryan TA 2001 Synapsin dispersion and reclustering during synaptic activity Nature Neuroscience 4 1187 1193 10.1038/nn756 11685225 · DOI
  9. Christie JM Jahr CE 2006 Multivesicular release at Schaffer collateral-CA1 hippocampal synapses Journal of Neuroscience 26 210 216 10.1523/JNEUROSCI.4307-05.2006 16399689 PMC2670931 · DOI
  10. Clements JD 1996 Transmitter timecourse in the synaptic cleft: its role in central synaptic function Trends in Neurosciences 19 163 171 10.1016/S0166-2236(96)10024-2 8723198 · DOI
  11. Cousin MA Evans GJ 2011 Activation of silent and weak synapses by cAMP-dependent protein kinase in cultured cerebellar granule neurons The Journal of Physiology 589 1943 1955 10.1113/jphysiol.2010.200477 21486806 PMC3090596 · DOI
  12. Dittman JS Kreitzer AC Regehr WG 2000 Interplay between facilitation, depression, and residual calcium at three presynaptic terminals The Journal of Neuroscience 20 1374 1385 10.1523/JNEUROSCI.20-04-01374.2000 10662828 PMC6772383 · DOI
  13. Dittman JS Regehr WG 1998 Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to purkinje cell synapse The Journal of Neuroscience 18 6147 6162 10.1523/JNEUROSCI.18-16-06147.1998 9698309 PMC6793194 · DOI
  14. Dobrunz LE Stevens CF 1997 Heterogeneity of release probability, facilitation, and depletion at central synapses Neuron 18 995 1008 10.1016/S0896-6273(00)80338-4 9208866 · DOI · Paper page
  15. Elmqvist D Quastel DM 1965 A quantitative study of end-plate potentials in isolated human muscle The Journal of Physiology 178 505 529 10.1113/jphysiol.1965.sp007639 5827910 PMC1357310 · DOI
  16. Esser L Wang CR Hosaka M Smagula CS Südhof TC Deisenhofer J 1998 Synapsin I is structurally similar to ATP-utilizing enzymes The EMBO Journal 17 977 984 10.1093/emboj/17.4.977 9463376 PMC1170447 · DOI
  17. Foster KA Crowley JJ Regehr WG 2005 The influence of multivesicular release and postsynaptic receptor saturation on transmission at granule cell to purkinje cell synapses Journal of Neuroscience 25 11655 11665 10.1523/JNEUROSCI.4029-05.2005 16354924 PMC6726039 · DOI
  18. Foster KA Regehr WG 2004 Variance-mean analysis in the presence of a rapid antagonist indicates vesicle depletion underlies depression at the climbing fiber synapse Neuron 43 119 131 10.1016/j.neuron.2004.06.022 15233922 · DOI
  19. Gitler D Takagishi Y Feng J Ren Y Rodriguiz RM Wetsel WC Greengard P Augustine GJ 2004a Different presynaptic roles of synapsins at excitatory and inhibitory synapses Journal of Neuroscience 24 11368 11380 10.1523/JNEUROSCI.3795-04.2004 15601943 PMC6730366 · DOI
  20. Gitler D Xu Y Kao HT Lin D Lim S Feng J Greengard P Augustine GJ 2004b Molecular determinants of synapsin targeting to presynaptic terminals Journal of Neuroscience 24 3711 3720 10.1523/JNEUROSCI.5225-03.2004 15071120 PMC6729754 · DOI
  21. Gitler D Cheng Q Greengard P Augustine GJ 2008 Synapsin IIa controls the reserve pool of glutamatergic synaptic vesicles Journal of Neuroscience 28 10835 10843 10.1523/JNEUROSCI.0924-08.2008 18945891 PMC2605971 · DOI
  22. Greengard P Valtorta F Czernik AJ Benfenati F 1993 Synaptic vesicle phosphoproteins and regulation of synaptic function Science 259 780 785 10.1126/science.8430330 8430330 · DOI
  23. Harrison J Jahr CE 2003 Receptor occupancy limits synaptic depression at climbing fiber synapses The Journal of Neuroscience 23 377 383 10.1523/JNEUROSCI.23-02-00377.2003 12533597 PMC6741881 · DOI
  24. Higley MJ Soler-Llavina GJ Sabatini BL 2009 Cholinergic modulation of multivesicular release regulates striatal synaptic potency and integration Nature Neuroscience 12 1121 1128 10.1038/nn.2368 19668198 PMC2733934 · DOI · Paper page
  25. Hilfiker S Schweizer FE Kao HT Czernik AJ Greengard P Augustine GJ 1998 Two sites of action for synapsin domain E in regulating neurotransmitter release Nature Neuroscience 1 29 35 10.1038/229 10195105 · DOI
  26. Hilfiker S Czernik AJ Greengard P Augustine GJ 2001 Tonically active protein kinase A regulates neurotransmitter release at the squid giant synapse The Journal of Physiology 531 141 146 10.1111/j.1469-7793.2001.0141j.x 11179398 PMC2278449 · DOI
  27. Hilfiker S Benfenati F Doussau F Nairn AC Czernik AJ Augustine GJ Greengard P 2005 Structural domains involved in the regulation of transmitter release by synapsins Journal of Neuroscience 25 2658 2669 10.1523/JNEUROSCI.4278-04.2005 15758176 PMC6725186 · DOI
  28. Hosaka M Hammer RE Südhof TC 1999 A phospho-switch controls the dynamic association of synapsins with synaptic vesicles Neuron 24 377 387 10.1016/S0896-6273(00)80851-X 10571231 · DOI
  29. Hosaka M Südhof TC 1998 Synapsins I and II are ATP-binding proteins with differential Ca2+ regulation The Journal of Biological Chemistry 273 1425 1429 10.1074/jbc.273.3.1425 9430678 · DOI
  30. Huang YY Li XC Kandel ER 1994 cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase Cell 79 69 79 10.1016/0092-8674(94)90401-4 7923379 · DOI · Paper page
  31. Indriati DW Kamasawa N Matsui K Meredith AL Watanabe M Shigemoto R 2013 Quantitative localization of Cav2.1 (P/Q-type) voltage-dependent calcium channels in Purkinje cells: somatodendritic gradient and distinct somatic coclustering with calcium-activated potassium channels Journal of Neuroscience 33 3668 3678 10.1523/JNEUROSCI.2921-12.2013 23426693 PMC4031662 · DOI
  32. Kerchner GA Nicoll RA 2008 Silent synapses and the emergence of a postsynaptic mechanism for LTP Nature Reviews Neuroscience 9 813 825 10.1038/nrn2501 18854855 PMC2819160 · DOI
  33. Korn H Triller A Mallet A Faber DS 1981 Fluctuating responses at a central synapse: n of binomial fit predicts number of stained presynaptic boutons Science 213 898 901 10.1126/science.6266015 6266015 · DOI
  34. Llinas R Bloedel JR Hillman DE 1969 Functional characterization of neuronal circuitry of frog cerebellar cortex Journal of Neurophysiology 32 847 870 10.1152/jn.1969.32.6.847 4310505 · DOI
  35. Llinás R Gruner JA Sugimori M McGuinness TL Greengard P 1991 Regulation by synapsin I and Ca(2+)-calmodulin-dependent protein kinase II of the transmitter release in squid giant synapse The Journal of Physiology 436 257 282 10.1113/jphysiol.1991.sp018549 1676419 PMC1181504 · DOI
  36. Malagon G Miki T Llano I Neher E Marty A 2016 Counting vesicular release events reveals binomial release statistics at single glutamatergic synapses The Journal of Neuroscience 36 4010 4025 10.1523/JNEUROSCI.4352-15.2016 27053208 PMC6705515 · DOI
  37. Midorikawa M Sakaba T 2015 Imaging exocytosis of single synaptic vesicles at a fast CNS presynaptic terminal Neuron 88 492 498 10.1016/j.neuron.2015.09.047 26539890 · DOI
  38. Midorikawa M Sakaba T 2017 Kinetics of releasable synaptic vesicles and their plastic changes at hippocampal mossy fiber synapses Neuron 96 1033 1040 10.1016/j.neuron.2017.10.016 29103807 · DOI · Paper page
  39. Miki T Malagon G Pulido C Llano I Neher E Marty A 2016 Actin- and Myosin-Dependent Vesicle Loading of Presynaptic Docking Sites Prior to Exocytosis Neuron 91 808 823 10.1016/j.neuron.2016.07.033 27537485 · DOI
  40. Milovanovic D Wu Y Bian X De Camilli P 2018 A liquid phase of synapsin and lipid vesicles Science 361 604 607 10.1126/science.aat5671 29976799 PMC6191856 · DOI
  41. Moulder KL Meeks JP Shute AA Hamilton CK de Erausquin G Mennerick S 2004 Plastic elimination of functional glutamate release sites by depolarization Neuron 42 423 435 10.1016/S0896-6273(04)00184-9 15134639 · DOI
  42. Moulder KL Jiang X Chang C Taylor AA Benz AM Conti AC Muglia LJ Mennerick S 2008 A specific role for Ca2+-dependent adenylyl cyclases in recovery from adaptive presynaptic silencing Journal of Neuroscience 28 5159 5168 10.1523/JNEUROSCI.5317-07.2008 18480272 PMC2684782 · DOI
  43. Moulder KL Mennerick S 2005 Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons Journal of Neuroscience 25 3842 3850 10.1523/JNEUROSCI.5231-04.2005 15829636 PMC6724923 · DOI
  44. Murphy GJ Glickfeld LL Balsen Z Isaacson JS 2004 Sensory neuron signaling to the brain: properties of transmitter release from olfactory nerve terminals Journal of Neuroscience 24 3023 3030 10.1523/JNEUROSCI.5745-03.2004 15044541 PMC6729835 · DOI
  45. Nahir B Jahr CE 2013 Activation of Extrasynaptic NMDARs at individual parallel fiber-molecular layer interneuron synapses in cerebellum Journal of Neuroscience 33 16323 16333 10.1523/JNEUROSCI.1971-13.2013 24107963 PMC3792467 · DOI
  46. Napper RM Harvey RJ 1988 Number of parallel fiber synapses on an individual purkinje cell in the cerebellum of the rat The Journal of Comparative Neurology 274 168 177 10.1002/cne.902740204 3209740 · DOI
  47. Neher E 2010 What is rate-limiting during sustained synaptic activity: vesicle supply or the availability of release sites Frontiers in Synaptic Neuroscience 2 1 6 10.3389/fnsyn.2010.00144 21423530 PMC3059671 · DOI
  48. Neher E 2015 Merits and limitations of vesicle pool models in view of heterogeneous populations of synaptic vesicles Neuron 87 1131 1142 10.1016/j.neuron.2015.08.038 26402599 · DOI · Paper page
  49. Neher E Brose N 2018 Dynamically primed synaptic vesicle states: key to understand synaptic Short-Term plasticity Neuron 100 1283 1291 10.1016/j.neuron.2018.11.024 30571941 · DOI
  50. Neher E Sakaba T 2008 Multiple roles of calcium ions in the regulation of neurotransmitter release Neuron 59 861 872 10.1016/j.neuron.2008.08.019 18817727 · DOI
  51. Nusser Z 2018 Creating diverse synapses from the same molecules Current Opinion in Neurobiology 51 8 15 10.1016/j.conb.2018.01.001 29353084 · DOI
  52. Oertner TG Sabatini BL Nimchinsky EA Svoboda K 2002 Facilitation at single synapses probed with optical quantal analysis Nature Neuroscience 5 657 664 10.1038/nn867 12055631 · DOI
  53. Pan B Zucker RS 2009 A general model of synaptic transmission and short-term plasticity Neuron 62 539 554 10.1016/j.neuron.2009.03.025 19477155 PMC3035647 · DOI
  54. Pelkey KA Topolnik L Yuan XQ Lacaille JC McBain CJ 2008 State-dependent cAMP sensitivity of presynaptic function underlies metaplasticity in a hippocampal feedforward inhibitory circuit Neuron 60 980 987 10.1016/j.neuron.2008.11.018 19109906 PMC2630456 · DOI · Paper page
  55. Pulido C Trigo FF Llano I Marty A 2015 Vesicular release statistics and unitary postsynaptic current at single GABAergic synapses Neuron 85 159 172 10.1016/j.neuron.2014.12.006 25543456 · DOI
  56. Pulido C Marty A 2017 Quantal fluctuations in central mammalian synapses: functional role of vesicular docking sites Physiological Reviews 97 1403 1430 10.1152/physrev.00032.2016 28835509 · DOI
  57. Redman S 1990 Quantal analysis of synaptic potentials in neurons of the central nervous system Physiological Reviews 70 165 198 10.1152/physrev.1990.70.1.165 2404288 · DOI
  58. Rizzoli SO Betz WJ 2004 The structural organization of the readily releasable pool of synaptic vesicles Science 303 2037 2039 10.1126/science.1094682 15044806 · DOI
  59. Rosahl TW Spillane D Missler M Herz J Selig DK Wolff JR Hammer RE Malenka RC Südhof TC 1995 Essential functions of synapsins I and II in synaptic vesicle regulation Nature 375 488 493 10.1038/375488a0 7777057 · DOI · Paper page
  60. Rozov A Burnashev N Sakmann B Neher E 2001 Transmitter release modulation by intracellular Ca 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics The Journal of Physiology 531 807 826 10.1111/j.1469-7793.2001.0807h.x 11251060 PMC2278500 · DOI
  61. Rudolph S Overstreet-Wadiche L Wadiche JI 2011 Desynchronization of multivesicular release enhances purkinje cell output Neuron 70 991 1004 10.1016/j.neuron.2011.03.029 21658590 PMC3148031 · DOI
  62. Rudolph S Tsai MC von Gersdorff H Wadiche JI 2015 The ubiquitous nature of multivesicular release Trends in Neurosciences 38 428 438 10.1016/j.tins.2015.05.008 26100141 PMC4495900 · DOI
  63. Ryan TA Reuter H Smith SJ 1997 Optical detection of a quantal presynaptic membrane turnover Nature 388 478 482 10.1038/41335 9242407 · DOI
  64. Sakaba T Neher E 2001 Preferential potentiation of fast-releasing synaptic vesicles by cAMP at the Calyx of held PNAS 98 331 336 10.1073/pnas.98.1.331 11134533 PMC14590 · DOI
  65. Salin PA Malenka RC Nicoll RA 1996 Cyclic AMP mediates a presynaptic form of LTP at cerebellar parallel fiber synapses Neuron 16 797 803 10.1016/S0896-6273(00)80099-9 8607997 · DOI
  66. Schikorski T Stevens CF 1997 Quantitative ultrastructural analysis of hippocampal excitatory synapses The Journal of Neuroscience 17 5858 5867 10.1523/JNEUROSCI.17-15-05858.1997 9221783 PMC6573206 · DOI · Paper page
  67. Schikorski T Stevens CF 2001 Morphological correlates of functionally defined synaptic vesicle populations Nature Neuroscience 4 391 395 10.1038/86042 11276229 · DOI · Paper page
  68. Schneggenburger R Meyer AC Neher E 1999 Released fraction and total size of a pool of immediately available transmitter quanta at a Calyx synapse Neuron 23 399 409 10.1016/S0896-6273(00)80789-8 10399944 · DOI
  69. Silver RA Momiyama A Cull-Candy SG 1998 Locus of frequency-dependent depression identified with multiple-probability fluctuation analysis at rat climbing fibre-Purkinje cell synapses The Journal of Physiology 510 881 902 10.1111/j.1469-7793.1998.881bj.x 9660900 PMC2231069 · DOI
  70. Silver RA 2003 High-Probability uniquantal transmission at excitatory synapses in barrel cortex Science 302 1981 1984 10.1126/science.1087160 14671309 · DOI
  71. Singer JH Lassová L Vardi N Diamond JS 2004 Coordinated multivesicular release at a mammalian ribbon synapse Nature Neuroscience 7 826 833 10.1038/nn1280 15235608 · DOI
  72. Song SH Augustine GJ 2015 Synapsin isoforms and synaptic vesicle trafficking Molecules and Cells 38 936 940 10.14348/molcells.2015.0233 26627875 PMC4673407 · DOI
  73. Song SH Augustine GJ 2016 Synapsin isoforms regulating GABA release from hippocampal interneurons The Journal of Neuroscience 36 6742 6757 10.1523/JNEUROSCI.0011-16.2016 27335405 PMC6601744 · DOI
  74. Steinberg SF Brunton LL 2001 Compartmentation of G protein-coupled signaling pathways in cardiac myocytes Annual Review of Pharmacology and Toxicology 41 751 773 10.1146/annurev.pharmtox.41.1.751 11264475 · DOI
  75. Stevens CF Wang Y 1995 Facilitation and depression at single central synapses Neuron 14 795 802 10.1016/0896-6273(95)90223-6 7718241 · DOI
  76. Sudhof TC 2004 The synaptic vesicle cycle Annual Review of Neuroscience 27 509 547 10.1146/annurev.neuro.26.041002.131412 15217342 · DOI · Paper page
  77. Sun J Bronk P Liu X Han W Sudhof TC 2006 Synapsins regulate use-dependent synaptic plasticity in the Calyx of held by a Ca2+/calmodulin-dependent pathway PNAS 103 2880 2885 10.1073/pnas.0511300103 16481620 PMC1413856 · DOI
  78. Taschenberger H Leão RM Rowland KC Spirou GA von Gersdorff H 2002 Optimizing synaptic architecture and efficiency for high-frequency transmission Neuron 36 1127 1143 10.1016/S0896-6273(02)01137-6 12495627 · DOI
  79. Thanawala MS Regehr WG 2013 Presynaptic calcium influx controls neurotransmitter release in part by regulating the effective size of the readily releasable pool Journal of Neuroscience 33 4625 4633 10.1523/JNEUROSCI.4031-12.2013 23486937 PMC3711668 · DOI
  80. Tong G Jahr CE 1994 Multivesicular release from excitatory synapses of cultured hippocampal neurons Neuron 12 51 59 10.1016/0896-6273(94)90151-1 7507341 · DOI
  81. Vasileva M Horstmann H Geumann C Gitler D Kuner T 2012 Synapsin-dependent reserve pool of synaptic vesicles supports replenishment of the readily releasable pool under intense synaptic transmission European Journal of Neuroscience 36 3005 3020 10.1111/j.1460-9568.2012.08225.x 22805168 · DOI
  82. 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 10.1016/S0896-6273(00)80148-8 8663998 · DOI
  83. Vyleta NP Smith SM 2011 Spontaneous glutamate release is independent of calcium influx and tonically activated by the calcium-sensing receptor Journal of Neuroscience 31 4593 4606 10.1523/JNEUROSCI.6398-10.2011 21430159 PMC3097128 · DOI
  84. Wadiche JI Jahr CE 2001 Multivesicular release at climbing fiber-Purkinje cell synapses Neuron 32 301 313 10.1016/S0896-6273(01)00488-3 11683999 · DOI
  85. Wilhelm BG Mandad S Truckenbrodt S Kröhnert K Schäfer C Rammner B Koo SJ Claßen GA Krauss M Haucke V Urlaub H Rizzoli SO 2014 Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins Science 344 1023 1028 10.1126/science.1252884 24876496 · DOI · Paper page
  86. Wong ST Athos J Figueroa XA Pineda VV Schaefer ML Chavkin CC Muglia LJ Storm DR 1999 Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP Neuron 23 787 798 10.1016/S0896-6273(01)80036-2 10482244 · DOI · Paper page
  87. Wong AY Graham BP Billups B Forsythe ID 2003 Distinguishing between presynaptic and postsynaptic mechanisms of short-term depression during action potential trains The Journal of Neuroscience 23 4868 4877 10.1523/JNEUROSCI.23-12-04868.2003 12832509 PMC6741172 · DOI
  88. Xu-Friedman MA Harris KM Regehr WG 2001 Three-dimensional comparison of ultrastructural characteristics at depressing and facilitating synapses onto cerebellar purkinje cells The Journal of Neuroscience 21 6666 6672 10.1523/JNEUROSCI.21-17-06666.2001 11517256 PMC6763067 · DOI
  89. Zenisek D Steyer JA Almers W 2000 Transport, capture and exocytosis of single synaptic vesicles at active zones Nature 406 849 854 10.1038/35022500 10972279 · DOI
  90. Zucker RS Regehr WG 2002 Short-term synaptic plasticity Annual Review of Physiology 64 355 405 10.1146/annurev.physiol.64.092501.114547 11826273 · DOI · Paper page

Cited by

Sorted by citations

Authors
Vaden, J. H., Banumurthy, G., Gusarevich, E. S., Overstreet-Wadiche, L., & Wadiche, J. I.
Affiliations
  • University of Alabama at Birmingham (US)
  • Northern (Arctic) Federal University (RU)
  • Department of Neurobiology, University of Alabama at Birmingham, Birmingham, United States
Corresponding author
Wadiche, Jacques I
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2019-07-31
Volume
8
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.47434
PMC
PMC6716946
OpenAlex
W2965372978
Cited by
61
References
4
Citations by year
2026: 3 · 2025: 6 · 2024: 17 · 2023: 5 · 2022: 9 · 2021: 10 · 2020: 8 · 2019: 3
FWCI
3.58
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Institute of Neurological Disorders and Stroke (NS065920, NS064025, NS105438)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Keywords
multivesicular release, readily releasable pool, synaptic vesicle release, release probability, protein kinase A, synapsin, neurotransmitter release, calcium-dependent release
MeSH terms
Animals, Calcium, Models, Biological, Synaptic Transmission, Synaptic Vesicles, Synapsins, Cyclic AMP-Dependent Protein Kinases, Calcium Signaling, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review