Estimation of nonuniform quantal parameters with multiple-probability fluctuation analysis: Theory, application and limitations

Journal of Neuroscience Methods

Volumn 130, Issue 2, 2003, Pages 127-141

  Silver, R Angus ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Quantal analysis; Release site; Synapse; Transmitter release; Variance mean; Vesicle

Indexed keywords

ANALYTIC METHOD; ANALYTICAL ERROR; ARTICLE; EVOKED RESPONSE; INFORMATION PROCESSING; MULTIPLE PROBABILITY FLUCTUATION ANALYSIS; NERVE CONDUCTION; PARAMETER; PRIORITY JOURNAL; PROBABILITY; PROCESS MODEL; QUANTITATIVE ASSAY; RECORDING; STEADY STATE; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC POTENTIAL; THEORY;

EID: 0345550349     PISSN: 01650270     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2003.09.030     Document Type: Article

References (62)

1. Anderson C.R., Stevens C.F. Voltage clamp analysis of acetylcholine produced end-plate current fluctuations at frog neuromuscular junction. J. Physiol. 235:1973;655-691.
2. Barrett E.F., Stevens C.F. The kinetics of transmitter release at the frog neuromuscular junction. J. Physiol. (Lond.). 227:1972;691-708.
3. Bekkers J.M., Richerson G.B., Stevens C.F. Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. Proc. Natl. Acad. Sci. U.S.A. 87:1990;5359-5362.
4. Bennett M.R., Lavidis N.A. The effect of calcium ions on the secretion of quanta evoked by an impulse at nerve terminal release sites. J. Gen. Physiol. 74:1979;429-456.
5. Borst J.G., Lodder J.C., Kits K.S. Large amplitude variability of GABAergic IPSCs in melanotropes from Xenopus laevis: evidence that quantal size differs between synapses. J. Neurophysiol. 71:1994;639-655.
6. Brenowitz S., Trussell L.O. Minimizing synaptic depression by control of release probability. J. Neurosci. 21:2001;1857-1867.
7. Clamann H.P., Mathis J., Luscher H.R. Variance analysis of excitatory postsynaptic potentials in cat spinal motoneurons during posttetanic potentiation. J. Neurophysiol. 61:1989;403-416.
8. Clements J.D. Variance-mean analysis: a simple and reliable approach for investigating synaptic transmission and modulation. J. Neurosci. Methods. 130:2003;115-125.
9. Clements J.D., Silver R.A. Unveiling synaptic plasticity: a new graphical and analytical approach. Trends Neurosci. 23:2000;105-113.
10. del Castillo J., Katz B. Quantal components of the end-plate potential. J. Physiol. 124:1954;560-573.
11. Diamond J.S., Jahr C.E. Asynchronous release of synaptic vesicles determines the time course of the AMPA receptor-mediated EPSC. Neuron. 15:1995;1097-1107.
12. DiGregorio D.A., Nusser Z., Silver R.A. Spillover of glutamate onto synaptic AMPA receptors enhances fast transmission at a cerebellar synapse. Neuron. 35:2002;521-533.
13. Fatt P., Katz B. Spontaneous subthreshold activity at motor nerve endings. J. Physiol. 117:1952;109-128.
14. Feldmeyer D., Lubke J., Silver R.A., Sakmann B. Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J. Physiol. 538:2002;803-822.
15. Forti L., Bossi M., Bergamaschi A., Villa A., Malgaroli A. Loose-patch recordings of single quanta at individual hippocampal synapses. Nature. 388:1997;874-878.
16. Foster K.A., Kreitzer A.C., Regehr W.G. Interaction of postsynaptic receptor saturation with presynaptic mechanisms produces a reliable synapse. Neuron. 36:2002;1115-1126.
17. Frerking M., Wilson M. Effects of variance in mini amplitude on stimulus-evoked release: a comparison of two models. Biophys. J. 70:1996;2078-2091.
18. Harrison J., Jahr C.E. Receptor occupancy limits synaptic depression at climbing fiber synapses. J. Neurosci. 23:2003;377-383.
19. Hessler N.A., Shirke A.M., Malinow R. The probability of transmitter release at a mammalian central synapse. Nature. 366:1993;569-572.
20. Humeau Y., Popoff M.R., Kojima H., Doussau F., Poulain B. Rac GTPase plays an essential role in exocytosis by controlling the fusion competence of release sites. J. Neurosci. 22:2002;7968-7981.
21. Isaacson J.S., Walmsley B. Counting quanta: direct measurements of transmitter release at a central synapse. Neuron. 15:1995;875-884.
22. Jack J.J., Redman S.J., Wong K. The components of synaptic potentials evoked in cat spinal motoneurones by impulses in single group Ia afferents. J. Physiol. (Lond.). 321:1981;65-96.
23. Jack J.J., Kullmann D.M., Larkman A.U., Major G., Stratford K.J. Quantal analysis of excitatory synaptic mechanisms in the mammalian central nervous system. Cold Spring Harb. Symp. Quant. Biol. 55:1990;57-67.
24. Katz B. The release of neural transmitter substances. Liverpool: Liverpool University Press; 1969.
25. Katz B., Miledi R. Membrane noise produced by acetylcholine. Nature. 226:1970;962-963.
26. Kenney JF, Keeping ES. Mathematics of statistics II, 2nd ed. Princeton, NJ: Van Nostrand; 1965.
27. Kullmann D.M., Asztely F. Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends Neurosci. 21:1998;8-14.
28. Kuno M. Quantal components of excitatory synaptic potentials in spinal motoneurons. J. Physiol. 175:1964;81-99.
29. Leinders T., van Kleef R.G., Vijverberg H.P. Divalent cations activate small- (SK) and large-conductance (BK) channels in mouse neuroblastoma cells: selective activation of SK channels by cadmium. Pflugers Arch. 422:1992;217-222.
30. Liu G., Choi S., Tsien R.W. Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices. Neuron. 22:1999;395-409.
31. Magleby K.L. Facilitation, augmentation, and potentiation of transmitter release. Prog. Brain Res. 49:1979;175-182.
32. Meyer A.C., Neher E., Schneggenburger R. Estimation of quantal size and number of functional active zones at the Calyx of Held synapse by nonstationary EPSC variance analysis. J. Neurosci. 21:2001;7889-7900.
33. Miyamoto M.D. Binomial analysis of quantal transmitter release at glycerol treated frog neuromuscular junctions. J. Physiol. 250:1975;121-142.
34. Mood AM, Graybill FA, Boes DC. Introduction to the theory of statistics. 3rd ed. New York: McGraw-Hill; 1974.
35. Murthy V.N., Sejnowski T.J., Stevens C.F. Heterogeneous release properties of visualized individual hippocampal synapses. Neuron. 18:1997;599-612.
36. Neher E., Sakaba T. Estimating transmitter release rates from postsynaptic current fluctuations. J. Neurosci. 21:2001;9638-9654.
37. Oertner T.G., Sabatini B.L., Nimchinsky E.A., Svoboda K. Facilitation at single synapses probed with optical quantal analysis. Nat. Neurosci. 5:2002;657-664.
38. Oleskevich S., Clements J., Walmsley B. Release probability modulates short-term plasticity at a rat giant terminal. J. Physiol. 524(Part 2):2000;513-523.
39. Quastel D.M. The binomial model in fluctuation analysis of quantal neurotransmitter release. Biophys. J. 72:1997;728-753.
40. Redman S. Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol. Rev. 70:1990;165-198.
41. Reid C.A., Clements J.D. Postsynaptic expression of long-term potentiation in the rat dentate gyrus demonstrated by variance-mean analysis. J. Physiol. 518:1999;121-130.
42. Rose C, Smith MD. Mathematical statistics with mathematics. New York: Springer-Verlag; 2002.
43. Rosenmund C., Clements J.D., Westbrook G.L. Nonuniform probability of glutamate release at a hippocampal synapse. Science. 262:1993;754-757.
44. Rossi D.J., Hamann M. Spillover-mediated transmission at inhibitory synapses promoted by high affinity alpha6 subunit GABA(A) receptors and glomerular geometry [published erratum appears in Neuron 1998 Jul;21(1):527]. Neuron. 20:1998;783-795.
45. Ryan T.A., Reuter H. Measurements of vesicle recycling in central neurons. News Physiol. Sci. 16:2001;10-14.
46. Sahara Y., Takahashi T. Quantal components of the excitatory postsynaptic currents at a rat central auditory synapse. J. Physiol. 536:2001;189-197.
47. Sankaranarayanan S., De Angelis D., Rothman J.E., Ryan T.A. The use of pHluorins for optical measurements of presynaptic activity. Biophys. J. 79:2000;2199-2208.
48. Scheuss V., Neher E. Estimating synaptic parameters from mean, variance, and covariance in trains of synaptic responses. Biophys. J. 81:2001;1970-1989.
49. Scheuss V., Schneggenburger R., Neher E. Separation of presynaptic and postsynaptic contributions to depression by covariance analysis of successive EPSCs at the Calyx of Held synapse. J. Neurosci. 22:2002;728-739.
50. Segal J.R., Ceccarelli B., Fesce R., Hurlbut W.P. Miniature endplate potential frequency and amplitude determined by an extension of Campbell's theorem. Biophys. J. 47:1985;183-202.
51. Sigworth F.J. The variance of sodium current fluctuations at the node of Ranvier. J. Physiol. 307:1980;97-129.
52. Silver RA. Neurotransmission at synapses with single and multiple release sites. In: Faber DS, Korn H, Redman S, Thompson SM, Altman JS, editors. Central synapses: quantal mechanisms and plasticity. Strasbourg: Human Frontier Science Program; 1998. p. 130-9.
53. Silver R.A., Traynelis S.F., Cull-Candy S.G. Rapid-time-course miniature and evoked excitatory currents at cerebellar synapses in situ. Nature. 355:1992;163-166.
54. Silver R.A., Cull-Candy S.G., Takahashi T. NonNMDA glutamate receptor occupancy and open probability at a rat cerebellar synapse with single and multiple release sites. J. Physiol. (Lond.). 494:1996;231-250.
55. Silver R.A., Momiyama A., Cull-Candy S.G. Locus of frequency-dependent depression identified with multiple-probability fluctuation analysis at rat climbing fibre-Purkinje cell synapses. J. Physiol. (Lond.). 510:1998;881-902.
56. Stricker C., Field A.C., Redman S.J. Statistical analysis of amplitude fluctuations in EPSCs evoked in rat CA1 pyramidal neurones in vitro. J. Physiol. 490:1996;419-441.
57. Wadiche J.I., Jahr C.E. Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron. 32:2001;301-313.
58. Walmsley B. Interpretation of 'quantal' peaks in distributions of evoked synaptic transmission at central synapses. Proc. R. Soc. Lond. B Biol. Sci. 261:1995;245-250.
59. Walmsley B., Edwards F.R., Tracey D.J. Nonuniform release probabilities underlie quantal synaptic transmission at a mammalian excitatory central synapse. J. Neurophysiol. 60:1988;889-908.
60. Wang S., Prange O., Murphy T.H. Amplification of calcium signals at dendritic spines provides a method for CNS quantal analysis. Can. J. Physiol. Pharmacol. 77:1999;651-659.
61. Yuste R., Majewska A., Cash S.S., Denk W. Mechanisms of calcium influx into hippocampal spines: heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis. J. Neurosci. 19:1999;1976-1987.
62. Zucker R.S., Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64:2002;355-405.