Single calcium channel domain gating of synaptic vesicle fusion at fast synapses; analysis by graphic modeling

References

• Dodge FA Jr, Rahamimoff R. Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J Physiol (Lond.) 1967; 193:419-32; PMID:6065887; http://dx.doi.org/10.1113/jphysiol.1967.sp008367
   PubMedGoogle Scholar
• Stanley EF. Decline in calcium cooperativity as the basis of facilitation at the squid giant synapse. J Neurosci 1986; 6:782-9; PMID:2870141
   PubMed Web of Science ®Google Scholar
• Bollmann JH, Sakmann B, Borst JG. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 2000; 289:953-7; PMID:10937999; http://dx.doi.org/10.1126/science.289.5481.953
   PubMed Web of Science ®Google Scholar
• Bollmann JH, Sakmann B. Control of synaptic strength and timing by the release-site Ca2+ signal. Nat Neurosci 2005; 8, 426-34; PMID:15750590
   PubMed Web of Science ®Google Scholar
• Simon SM, Llinas RR. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys J 1985; 48:485-98; PMID:2412607; http://dx.doi.org/10.1016/S0006-3495(85)83804-2
   PubMed Web of Science ®Google Scholar
• Zucker RS, Fogelson AL. Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. Proc Natl Acad Sci U S A 1986; 83:3032-6; PMID:2422666; http://dx.doi.org/10.1073/pnas.83.9.3032
   PubMed Web of Science ®Google Scholar
• Schneggenburger R, Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature(Lond.) 2000; 406:889-93; http://dx.doi.org/10.1038/35022702
   PubMed Web of Science ®Google Scholar
• Branco T, Staras K. The probability of neurotransmitter release: variability and feedback control at single synapses. Nat Rev Neurosci 2009; 10:373-83; PMID:19377502; http://dx.doi.org/10.1038/nrn2634
   PubMed Web of Science ®Google Scholar
• Llinas RR, Steinberg IZ, Walton K. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys J 1981; 33:323-51; PMID:6261850; http://dx.doi.org/10.1016/S0006-3495(81)84899-0
   PubMed Web of Science ®Google Scholar
• Chad JE, Eckert R. Calcium domains associated with individual channels can account for anomalous voltage relations of Ca-dependent responses. Biophys J 1984; 45:993-99; PMID:6329349; http://dx.doi.org/10.1016/S0006-3495(84)84244-7
   PubMed Web of Science ®Google Scholar
• Augustine GJ, Charlton MP. Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse. J Physiol (Lond.) 1986; 381:619-40; PMID:2442355; http://dx.doi.org/10.1113/jphysiol.1986.sp016347
   PubMedGoogle Scholar
• Fogelson AL, Zucker RS. Presynaptic calcium diffusion from various arrays of single channels. Biophys J 1985; 48:1003-7; PMID:2418887; http://dx.doi.org/10.1016/S0006-3495(85)83863-7
   PubMed Web of Science ®Google Scholar
• Yoshikami D, Bagaboldo Z, Olivera BM. The inhibitory effects of omega-conotoxins on Ca channel and synapses. Ann N Y Acad Sci 1989; 560:230-48; PMID:2545135; http://dx.doi.org/10.1111/j.1749-6632.1989.tb24100.x
   PubMed Web of Science ®Google Scholar
• Augustine GJ. Regulation of transmitter release at the squid giant synapse by presynaptic delayed rectifier potassium current. J Physiol (Lond.) 1990; 431:343-64; PMID:1983120; http://dx.doi.org/10.1113/jphysiol.1990.sp018333
   PubMedGoogle Scholar
• Adler EM, Augustine GJ, Duffy SN, Charlton MP. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J Neurosci 1991; 11, 1496-507; PMID:1675264
   PubMed Web of Science ®Google Scholar
• Augustine GJ, Adler EM, Charlton MP. The calcium signal for transmitter secretion from presynaptic nerve terminals. Ann NY Acad Sci 1991; 635:365-81; http://dx.doi.org/10.1111/j.1749-6632.1991.tb36505.x
   PubMed Web of Science ®Google Scholar
• Stanley EF. Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron 1993; 11:1007-11; PMID:8274272; http://dx.doi.org/10.1016/0896-6273(93)90214-C
   PubMed Web of Science ®Google Scholar
• Matveev V, Bertram R, Sherman A. Calcium cooperativity of exocytosis as a measure of Ca(2)+ channel domain overlap. Brain Res 2011; 1398:126-38; PMID:21621748
   PubMed Web of Science ®Google Scholar
• Bertram R, Smith GD, Sherman A. Modeling study of the effects of overlapping Ca2+ microdomains on neurotransmitter release. Biophys J 1999; 76:735-50; PMID:9929478; http://dx.doi.org/10.1016/S0006-3495(99)77240-1
   PubMed Web of Science ®Google Scholar
• Mulligan SJ, Davison I, Delaney KR. Mitral cell presynaptic Ca(2+) influx and synaptic transmission in frog amygdala. Neuroscience 2001; 104:137-51; PMID:11311538; http://dx.doi.org/10.1016/S0306-4522(01)00057-4
   PubMed Web of Science ®Google Scholar
• Wachman ES, Poage RE, Stiles JR, Farkas DL, Meriney SD. Spatial distribution of calcium entry evoked by single action potentials within the presynaptic active zone. J Neurosci 2004; 24:2877-85; PMID:15044526; http://dx.doi.org/10.1523/JNEUROSCI.1660-03.2004
   PubMed Web of Science ®Google Scholar
• Gentile L, Stanley EF. A unified model of presynaptic release site gating by calcium channel domains. Eur J Neurosci 2005; 21:278-82; PMID:15654866; http://dx.doi.org/10.1111/j.1460-9568.2004.03841.x
   PubMed Web of Science ®Google Scholar
• Brandt A, Khimich D, Moser T. Few CaV1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 2005; 25:11577-85; PMID:16354915; http://dx.doi.org/10.1523/JNEUROSCI.3411-05.2005
   PubMed Web of Science ®Google Scholar
• Shahrezaei V, Cao A, Delaney KR. Ca2+ from one or two channels controls fusion of a single vesicle at the frog neuromuscular junction. J Neurosci 2006; 26:13240-9; PMID:17182774; http://dx.doi.org/10.1523/JNEUROSCI.1418-06.2006
   PubMed Web of Science ®Google Scholar
• Eggermann E, Bucurenciu I, Goswami SP, Jonas P. Nanodomain coupling between Ca(2) channels and sensors of exocytosis at fast mammalian synapses. Nat Rev Neurosci 2011; 13:7-21; PMID:22183436; http://dx.doi.org/10.1038/nrn3125
   PubMed Web of Science ®Google Scholar
• Bucurenciu I, Kulik A, Schwaller B, Frotscher M, Jonas P. Nanodomain coupling between Ca2+ channels and Ca2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 2008; 57:536-45; PMID:18304483; http://dx.doi.org/10.1016/j.neuron.2007.12.026
   PubMed Web of Science ®Google Scholar
• Scimemi A, Diamond JS. The number and organization of Ca2+ channels in the active zone shapes neurotransmitter release from Schaffer collateral synapses. J Neurosci 2012; 32:18157-76; PMID:23238730; http://dx.doi.org/10.1523/JNEUROSCI.3827-12.2012
   PubMed Web of Science ®Google Scholar
• Kim MH, Li GL, Von Gersdorff H. Single Ca2+ channels and exocytosis at sensory synapses. J Physiol 2013; 591:3167-78; PMID:23459757; http://dx.doi.org/10.1113/jphysiol.2012.249482
   PubMed Web of Science ®Google Scholar
• Tarr TB, Dittrich M, Meriney SD. Are unreliable release mechanisms conserved from NMJ to CNS? Trends Neurosci 2013; 36:14-22; PMID:23102681; http://dx.doi.org/10.1016/j.tins.2012.09.009
   PubMed Web of Science ®Google Scholar
• Weber AM, Wong FK, Tufford AR, Schlichter LC, Matveev V, Stanley EF. N-type Ca2+ channels carry the largest current: implications for nanodomains and transmitter release. Nat Neurosci 2010; 13, 1348-50; PMID:20953196; http://dx.doi.org/10.1038/nn.2657
   PubMed Web of Science ®Google Scholar
• Naraghi M, Neher E. Linearized buffered Ca2+ diffusion in microdomains and its implications for calculation of [Ca2+] at the month of a calcium channel. J Neurosci 1997; 17:6961-73; PMID:9278532
   PubMed Web of Science ®Google Scholar
• Matveev V, Bertram R, Sherman A. Ca2+ current versus Ca2+ channel cooperativity of exocytosis. J Neurosci 2009; 29:12196-209; PMID:19793978; http://dx.doi.org/10.1523/JNEUROSCI.0263-09.2009
   PubMed Web of Science ®Google Scholar
• Robitaille R, Adler EM, Charlton MP. Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses. Neuron 1990; 5:773-9; PMID:1980068; http://dx.doi.org/10.1016/0896-6273(90)90336-E
   PubMed Web of Science ®Google Scholar
• Heuser JE, Reese TS, Landis DMD. Functional changes in frog neuromuscular junctions studied with freeze fracture. J Neurocytol 1974; 3, 109-31; PMID:4596345; http://dx.doi.org/10.1007/BF01111936
   PubMedGoogle Scholar
• Pumplin DW, Reese TS, Llinas RR. Are the presynaptic membrane particles the calcium channels? Proc Natl Acad Sci U S A 1981; 78:7210-3; PMID:6273920; http://dx.doi.org/10.1073/pnas.78.11.7210
   PubMed Web of Science ®Google Scholar
• Venzin M, Sandri C, Akert K, Wyss UR. Membrane associated particles of the presynaptic active zone in rat spinal cord. A morphometric analysis. Bain Res 1977; 130:393-404.
   PubMed Web of Science ®Google Scholar
• Luo F, Dittrich M, Stiles JR, Meriney SD. Single-pixel optical fluctuation analysis of calcium channel function in active zones of motor nerve terminals. J Neurosci 2011; 31:11268-81; PMID:21813687; http://dx.doi.org/10.1523/JNEUROSCI.1394-11.2011
   PubMed Web of Science ®Google Scholar
• Luo F, Dittrich M, Cho S, Stiles JR, Meriney SD. Transmitter release is evoked with low probability predominately by calcium flux through single channel openings at the frog neuromuscular junction. J Neurophysiol 2015; 113(7):2480-9.
   PubMed Web of Science ®Google Scholar
• Stanley EF. The calcium channel and the organization of the presynaptic transmitter release face. TINS 1997; 20:404-9; PMID:9292969
   PubMed Web of Science ®Google Scholar
• Fedchyshyn MJ, Wang LY. Developmental transformation of the release modality at the calyx of held synapse. J Neurosci 2005; 25, 4131-40; PMID:15843616; http://dx.doi.org/10.1523/JNEUROSCI.0350-05.2005
   PubMed Web of Science ®Google Scholar
• Wang LY, Neher E, Taschenberger H. Synaptic vesicles in mature calyx of Held synapses sense higher nanodomain calcium concentrations during action potential-evoked glutamate release. J Neurosci 2008; 28:14450-8; PMID:19118179; http://dx.doi.org/10.1523/JNEUROSCI.4245-08.2008
   PubMed Web of Science ®Google Scholar
• Kochubey O, Han Y, Schneggenburger R. Developmental regulation of the intracellular Ca2+ sensitivity of vesicle fusion and Ca2+-secretion coupling at the rat calyx of Held. J Physiol 2009; 587:3009-23; PMID:19403608; http://dx.doi.org/10.1113/jphysiol.2009.172387
   PubMed Web of Science ®Google Scholar
• Yamashita T, Eguchi K, Saitoh N, von GH, Takahashi T. Developmental shift to a mechanism of synaptic vesicle endocytosis requiring nanodomain Ca2+. Nat Neurosci 2010; 13, 838-44; PMID:20562869; http://dx.doi.org/10.1038/nn.2576
   PubMed Web of Science ®Google Scholar
• Schneggenburger R, Han Y, Kochubey O. Ca(2+) channels and transmitter release at the active zone. Cell Calcium 2012; 52:199-207; PMID:22682961; http://dx.doi.org/10.1016/j.ceca.2012.04.011
   PubMed Web of Science ®Google Scholar
• Erazo-Fischer E, Striessnig J, Taschenberger H. The role of physiological afferent nerve activity during in vivo maturation of the calyx of Held synapse. J Neurosci 2007; 27, 1725-37; PMID:17301180; http://dx.doi.org/10.1523/JNEUROSCI.4116-06.2007
   PubMed Web of Science ®Google Scholar
• Yang YM, Wang LY. Amplitude and kinetics of action potential-evoked Ca2+ current and its efficacy in triggering transmitter release at the developing calyx of held synapse. J Neurosci 2006; 26, 5698-708; PMID:16723526; http://dx.doi.org/10.1523/JNEUROSCI.4889-05.2006
   PubMed Web of Science ®Google Scholar
• Iwasaki S, Takahashi T. Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem. J Physiol 2001; 534:861-71; PMID:11483715; http://dx.doi.org/10.1111/j.1469-7793.2001.00861.x
   PubMed Web of Science ®Google Scholar
• Jewett DL, Romano MN. Neonatal development of auditory system potentials averaged from the scalp of rat and cat. Brain Res 1972; 36:101-15; PMID:5008374; http://dx.doi.org/10.1016/0006-8993(72)90769-X
   PubMed Web of Science ®Google Scholar
• Borst JG, Sakmann B. Calcium influx and transmitter release in a fast CNS synapse. Nature(Lond.) 1996; 383:431-5; http://dx.doi.org/10.1038/383431a0
   PubMed Web of Science ®Google Scholar
• Fedchyshyn MJ, Wang LY. Activity-dependent changes in temporal components of neurotransmission at the juvenile mouse calyx of Held synapse. J Physiol 2007; 581:581-602; PMID:17347264; http://dx.doi.org/10.1113/jphysiol.2007.129833
   PubMed Web of Science ®Google Scholar
• Indriati DW, Kamasawa N, Matsui K, Meredith AL, Watanabe M, Shigemoto R. 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. J Neurosci 2013; 33:3668-78; PMID:23426693; http://dx.doi.org/10.1523/JNEUROSCI.2921-12.2013
   PubMed Web of Science ®Google Scholar
• Nakamura Y, Harada H, Kamasawa N, Matsui K, Rothman JS, Shigemoto R, Silver RA, DiGregorio DA, Takahashi T. Nanoscale distribution of presynaptic Ca(2+) channels and its impact on vesicular release during development. Neuron 2015; 85:145-58; PMID:25533484; http://dx.doi.org/10.1016/j.neuron.2014.11.019
   PubMed Web of Science ®Google Scholar
• Stanley EF. Presynaptic calcium channels and the transmitter release mechanism. Ann N Y Acad Sci 1993; 681:368-72; PMID:8102841; http://dx.doi.org/10.1111/j.1749-6632.1993.tb22915.x
   PubMed Web of Science ®Google Scholar
• Sheng J, He L, Zheng H, Xue L, Luo F, Shin W, Sun T, Kuner T, Yue DT, Wu LG. Calcium-channel number critically influences synaptic strength and plasticity at the active zone. Nat Neurosci 2012; 15, 998-1006; PMID:22683682; http://dx.doi.org/10.1038/nn.3129
   PubMed Web of Science ®Google Scholar
• Thomson AM. Facilitation, augmentation and potentiation at central synapses. Trends Neurosci 2000; 23:305-12; PMID:10856940; http://dx.doi.org/10.1016/S0166-2236(00)01580-0
   PubMed Web of Science ®Google Scholar
• Gonzalez JC, Lignani G, Maroto M, Baldelli P, Hernandez-Guijo JM. Presynaptic muscarinic receptors reduce synaptic depression and facilitate its recovery at hippocampal GABAergic synapses. Cereb Cortex 2014; 24:1818-31; http://dx.doi.org/10.1093/cercor/bht032
   PubMed Web of Science ®Google Scholar
• Wang LY, Fedchyshyn MJ, Yang YM. Action potential evoked transmitter release in central synapses: insights from the developing calyx of Held. Mol Brain 2009; 2:36; PMID:19939269; http://dx.doi.org/10.1186/1756-6606-2-36
   PubMed Web of Science ®Google Scholar
• Shahrezaei V, Delaney KR. Consequences of Molecular-Level Ca2+ Channel and Synaptic Vesicle Colocalization for the Ca2+ Microdomain and Neurotransmitter Exocytosis: A Monte Carlo Study. Biophys J 2004; 87:2352-64; PMID:15454435; http://dx.doi.org/10.1529/biophysj.104.043380
   PubMed Web of Science ®Google Scholar
• Meinrenken CJ, Borst JG, Sakmann B. Local routes revisited: the space and time dependence of the Ca2+ signal for phasic transmitter release at the rat calyx of Held. J Physiol 2003; 547:665-89; PMID:12562955
   PubMed Web of Science ®Google Scholar
• Stanley EF. The calcium channel and the organization of the presynaptic transmitter release face. Trends Neurosci 1997; 20:404-9; PMID:9292969; http://dx.doi.org/10.1016/S0166-2236(97)01091-6
   PubMed Web of Science ®Google Scholar
• Koike-Tani M, Kanda T, Saitoh N, Yamashita T, Takahashi T. Involvement of AMPA receptor desensitization in short-term synaptic depression at the calyx of Held in developing rats. J Physiol 2008; 586:2263-75; http://dx.doi.org/10.1113/jphysiol.2007.142547
   PubMed Web of Science ®Google Scholar
• Iwasaki S, Takahashi T. Developmental changes in calcium channel types mediating synaptic transmission in rat auditory brainstem. J Physiol (Lond) 1998; 509:419-23; PMID:9575291; http://dx.doi.org/10.1111/j.1469-7793.1998.419bn.x
   PubMedGoogle Scholar
• Matveev V. Calcium-Dependent Exocytosis, Biophysical Models of in Encyclopedia of Computational Neuroscience (eds. Jaeger D, Jung R) 1-17 (Springer New York, 2014).
   Google Scholar
• Bennett MR, Farnell L, Gibson WG. The probability of quantal secretion within an array of calcium channels of an active zone. Biophys J 2000; 78:2222-40; PMID:10777722; http://dx.doi.org/10.1016/S0006-3495(00)76770-1
   PubMed Web of Science ®Google Scholar
• Bertram R, Sherman AD, Stanley EF. The single domain/bound calcium hypothesis of transmitter release and facilitation. J Neurophysiol 1996; 75:1919-31; PMID:8734591
   PubMed Web of Science ®Google Scholar
• Shahrezaei V, Delaney KR. Brevity of the Ca2+ microdomain and active zone geometry prevent Ca2+-sensor saturation for neurotransmitter release. J Neurophysiol 2005; 94:1912-9; PMID:15888526; http://dx.doi.org/10.1152/jn.00256.2005
   PubMed Web of Science ®Google Scholar
• Meinrenken CJ, Borst JG, Sakmann B. Calcium secretion coupling at calyx of held governed by nonuniform channel-vesicle topography. J Neurosci 2002; 22:1648-67; PMID:11880495
   PubMed Web of Science ®Google Scholar
• Vyleta NP, Jonas P. Loose coupling between Ca2+ channels and release sensors at a plastic hippocampal synapse. Science 2014; 343:665-70; PMID:24503854; http://dx.doi.org/10.1126/science.1244811
   PubMed Web of Science ®Google Scholar
• Soldo BL, Giovannucci DR, Stuenkel EL, Moises HC. Ca(2+) and frequency dependence of exocytosis in isolated somata of magnocellular supraoptic neurones of the rat hypothalamus. J Physiol 2004; 555:699-711; PMID:14645448; http://dx.doi.org/10.1113/jphysiol.2003.051136
   PubMed Web of Science ®Google Scholar
• Baur D, Bornschein G, Althof D, Watanabe M, Kulik A, Eilers J, Schmidt H. Developmental tightening of cerebellar cortical synaptic influx-release coupling. J Neurosci 2015; 35:1858-71; PMID:25653347; http://dx.doi.org/10.1523/JNEUROSCI.2900-14.2015
   PubMed Web of Science ®Google Scholar
• Okawa H, Hoon M, Yoshimatsu T, Della SL, Wong RO. Illuminating the multifaceted roles of neurotransmission in shaping neuronal circuitry. Neuron 2014; 83:1303-18; PMID:25233313; http://dx.doi.org/10.1016/j.neuron.2014.08.029
   PubMed Web of Science ®Google Scholar
• Pangrsic T, Gabrielaitis M, Michanski S, Schwaller B, Wolf F, Strenzke N, Moser T. EF-hand protein Ca2+ buffers regulate Ca2+ influx and exocytosis in sensory hair cells. Proc Natl Acad Sci U S A 2015; 112, E1028-37; PMID:25691754; http://dx.doi.org/10.1073/pnas.1416424112
   PubMed Web of Science ®Google Scholar
• Schmidt H, Brachtendorf S, Arendt O, Hallermann S, Ishiyama S, Bornschein G, Gall D, Schiffmann SN, Heckmann M, Eilers J. Nanodomain coupling at an excitatory cortical synapse. Curr Biol 2013; 23:244-9; PMID:23273895; http://dx.doi.org/10.1016/j.cub.2012.12.007
   PubMed Web of Science ®Google Scholar
• Bucurenciu I, Bischofberger J, Jonas P. A small number of open Ca(2+) channels trigger transmitter release at a central GABAergic synapse. Nat Neurosci 2010; 13, 19-21; PMID:20010820; http://dx.doi.org/10.1038/nn.2461
   PubMed Web of Science ®Google Scholar
• Keller D, Babai N, Kochubey O, Han Y, Markram H, Schürmann F, Schneggenburger R. An Exclusion Zone for Ca2+ Channels around Docked Vesicles Explains Release Control by Multiple Channels at a CNS Synapse. PLoS Comput Biol 2015; 11:e1004253; PMID:25951120; http://dx.doi.org/10.1371/journal.pcbi.1004253
   PubMed Web of Science ®Google Scholar
• Harlow ML, Szule JA, Xu J, Jung JH, Marshall RM, McMahan UJ. Alignment of synaptic vesicle macromolecules with the macromolecules in active zone material that direct vesicle docking. PLoS ONE 2013; 8:e69410; PMID:23894473; http://dx.doi.org/10.1371/journal.pone.0069410
   PubMed Web of Science ®Google Scholar
• Nagwaney S, Harlow ML, Jung JH, Szule JA, Ress D, Xu J, Marshall RM, McMahan UJ. Macromolecular connections of active zone material to docked synaptic vesicles and presynaptic membrane at neuromuscular junctions of mouse. J Comp Neurol 2009; 513:457-68; PMID:19226520; http://dx.doi.org/10.1002/cne.21975
   PubMed Web of Science ®Google Scholar
• Harlow M, Ress D, Koster A, Marshall RM, Schwarz M, McMahan UJ. Dissection of active zones at the neuromuscular junction by EM tomography. J Physiol Paris 1998; 92:75-8; PMID:9782447; http://dx.doi.org/10.1016/S0928-4257(98)80141-1
   PubMed Web of Science ®Google Scholar
• Mochida S, Westenbroek RE, Yokoyama CT, Zhong H, Myers SJ, Scheuer T, Itoh K, Catterall WA. Requirement for the synaptic protein interaction site for reconstitution of synaptic transmission by P/Q-type calcium channels. Proc Natl Acad Sci U S A 2003; 100:2819-24; PMID:12601156; http://dx.doi.org/10.1073/pnas.262787699
   PubMed Web of Science ®Google Scholar
• Wong FK, Li Q, Stanley EF. Synaptic vesicle capture by CaV2.2 calcium channels. Front Cell Neurosci 2013; 7:101; PMID:23874268
   PubMed Web of Science ®Google Scholar
• Catterall WA. Interactions of presynaptic Ca2+ channels and snare proteins in neurotransmitter release. Ann N Y Acad Sci 1999; 868:144-59; PMID:10414292; http://dx.doi.org/10.1111/j.1749-6632.1999.tb11284.x
   PubMed Web of Science ®Google Scholar
• Sheng ZH, Westenbroek RE, Catterall WA. Physical link and functional coupling of presynaptic calcium channels and the synaptic vesicle docking/fusion machinery. J Bioenerg Biomembr 1998; 30, 335-45; PMID:9758330; http://dx.doi.org/10.1023/A:1021985521748
   PubMed Web of Science ®Google Scholar
• Llinas RR, Sugimori M, Simon SM. Transmission by presynaptic spike-like depolarization in the squid giant synapse. Proc Natl Acad Sci U S A 1982; 79:2415-9; PMID:6954549; http://dx.doi.org/10.1073/pnas.79.7.2415
   PubMed Web of Science ®Google Scholar
• Luvisetto S, Fellin T, Spagnolo M, Hivert B, Brust PF, Harpold MM, Stauderman KA, Williams ME, Pietrobon D. Modal gating of human CaV2.1 (P/Q-type) calcium channels: I. The slow and the fast gating modes and their modulation by β subunits. J Gen Physiol 2004; 124:445-61; PMID:15504896; http://dx.doi.org/10.1085/jgp.200409034
   PubMed Web of Science ®Google Scholar
• Stanley EF. PresyNaptic calcium channels: why is P selected before N? Biophys J 2015; 108:451-2; PMID:25650909; http://dx.doi.org/10.1016/j.bpj.2014.12.021
   PubMed Web of Science ®Google Scholar
• Ravin R, Parnas H, Spira ME, Volfovsky N, Parnas I. Simultaneous measurement of evoked release and [Ca2+]i in a crayfish release bouton reveals high affinity of release to Ca2+. J Neurophysiol 1999; 81:634-42; PMID:10036266
   PubMed Web of Science ®Google Scholar
• Parnas H, Segel LA. A theoretical explanation for some effects of calcium on the facilitation of neurotransmitter release. J Theor Biol 1980; 84:3-29; PMID:6106090; http://dx.doi.org/10.1016/S0022-5193(80)81035-6
   PubMed Web of Science ®Google Scholar
• Haydon PG, Henderson E, Stanley EF. Localization of individual calcium channels at the release face of a presynaptic nerve terminal. Neuron 1994; 13:1275-80; PMID:7993621; http://dx.doi.org/10.1016/0896-6273(94)90414-6
   PubMed Web of Science ®Google Scholar
• Stanley EF, Reese TS, Wang GZ. Molecular scaffold reorganization at the transmitter release site with vesicle exocytosis or botulinum toxin C1. Eur J Neurosci 2003; 18:2403-7; PMID:14622203; http://dx.doi.org/10.1046/j.1460-9568.2003.02948.x
   PubMed Web of Science ®Google Scholar