Desynchronization of Multivesicular Release Enhances Purkinje Cell Output

Neuron

Volumn 70, Issue 5, 2011, Pages 991-1004

  Rudolph, Stephanie ^a,b   Overstreet Wadiche, Linda ^b   Wadiche, Jacques I ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; KINETICS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SPIKE; SYNAPSE; SYNAPSE VESICLE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; ASPARTIC ACID; BIOPHYSICAL PHENOMENA; CALCIUM; CEREBELLUM; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; KYNURENIC ACID; LINEAR MODELS; MICE; NERVE FIBERS; NERVE NET; PATCH-CLAMP TECHNIQUES; PURKINJE CELLS; QUINOXALINES; STRONTIUM; SYNAPSES; TIME FACTORS;

EID: 79958023044     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.03.029     Document Type: Article

References (65)

1. Aizenman C.D., Manis P.B., Linden D.J. Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse. Neuron 1998, 21:827-835.
2. Armstrong D.M., Rawson J.A. Activity patterns of cerebellar cortical neurones and climbing fibre afferents in the awake cat. J. Physiol. 1979, 289:425-448.
3. Atluri P.P., Regehr W.G. Delayed release of neurotransmitter from cerebellar granule cells. J. Neurosci. 1998, 18:8214-8227.
4. Auger C., Kondo S., Marty A. Multivesicular release at single functional synaptic sites in cerebellar stellate and basket cells. J. Neurosci. 1998, 18:4532-4547.
5. Barrett E.F., Stevens C.F. The kinetics of transmitter release at the frog neuromuscular junction. J. Physiol. 1972, 227:691-708.
6. Biró A.A., Holderith N.B., Nusser Z. Release probability-dependent scaling of the postsynaptic responses at single hippocampal GABAergic synapses. J. Neurosci. 2006, 26:12487-12496.
7. Borst J.G. The low synaptic release probability in vivo. Trends Neurosci. 2010, 33:259-266.
8. Borst J.G., Sakmann B. Depletion of calcium in the synaptic cleft of a calyx-type synapse in the rat brainstem. J. Physiol. 1999, 521:123-133.
9. Boudkkazi S., Carlier E., Ankri N., Caillard O., Giraud P., Fronzaroli-Molinieres L., Debanne D. Release-dependent variations in synaptic latency: a putative code for short- and long-term synaptic dynamics. Neuron 2007, 56:1048-1060.
10. Campbell N.C., Hesslow G. The secondary spikes of climbing fibre responses recorded from Purkinje cell axons in cat cerebellum. J. Physiol. 1986, 377:225-235.
11. Choi S., Klingauf J., Tsien R.W. Postfusional regulation of cleft glutamate concentration during LTP at 'silent synapses'. Nat. Neurosci. 2000, 3:330-336.
12. Christie J.M., Jahr C.E. Multivesicular release at Schaffer collateral-CA1 hippocampal synapses. J. Neurosci. 2006, 26:210-216.
13. Clark B.A., Monsivais P., Branco T., London M., Häusser M. The site of action potential initiation in cerebellar Purkinje neurons. Nat. Neurosci. 2005, 8:137-139.
14. Crowley J.J., Fioravante D., Regehr W.G. Dynamics of fast and slow inhibition from cerebellar golgi cells allow flexible control of synaptic integration. Neuron 2009, 63:843-853.
15. Davie J.T., Clark B.A., Häusser M. The origin of the complex spike in cerebellar Purkinje cells. J. Neurosci. 2008, 28:7599-7609.
16. Diamond J.S., Jahr C.E. Asynchronous release of synaptic vesicles determines the time course of the AMPA receptor-mediated EPSC. Neuron 1995, 15:1097-1107.
17. DiGregorio D.A., Nusser Z., Silver R.A. Spillover of glutamate onto synaptic AMPA receptors enhances fast transmission at a cerebellar synapse. Neuron 2002, 35:521-533.
18. Dittman J.S., Regehr W.G. Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J. Neurosci. 1998, 18:6147-6162.
19. Eccles J.C., Llinás R., Sasaki K. The excitatory synaptic action of climbing fibres on the purinje cells of the cerebellum. J. Physiol. 1966, 182:268-296.
20. Fedchyshyn M.J., Wang L.Y. Activity-dependent changes in temporal components of neurotransmission at the juvenile mouse calyx of Held synapse. J. Physiol. 2007, 581:581-602.
21. Foster K.A., Regehr W.G. Variance-mean analysis in the presence of a rapid antagonist indicates vesicle depletion underlies depression at the climbing fiber synapse. Neuron 2004, 43:119-131.
22. Foster K.A., Kreitzer A.C., Regehr W.G. Interaction of postsynaptic receptor saturation with presynaptic mechanisms produces a reliable synapse. Neuron 2002, 36:1115-1126.
23. Geiger J.R., Jonas P. Dynamic control of presynaptic Ca(2+) inflow by fast-inactivating K(+) channels in hippocampal mossy fiber boutons. Neuron 2000, 28:927-939.
24. Goda Y., Stevens C.F. Two components of transmitter release at a central synapse. Proc. Natl. Acad. Sci. USA 1994, 91:12942-12946.
25. Hansel C., Linden D.J. Long-term depression of the cerebellar climbing fiber-Purkinje neuron synapse. Neuron 2000, 26:473-482.
26. Harrison J., Jahr C.E. Receptor occupancy limits synaptic depression at climbing fiber synapses. J. Neurosci. 2003, 23:377-383.
27. Hashimoto K., Kano M. Presynaptic origin of paired-pulse depression at climbing fibre-Purkinje cell synapses in the rat cerebellum. J. Physiol. 1998, 506:391-405.
28. He L., Xue L., Xu J., McNeil B.D., Bai L., Melicoff E., Adachi R., Wu L.G. Compound vesicle fusion increases quantal size and potentiates synaptic transmission. Nature 2009, 459:93-97.
29. Hefft S., Jonas P. Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat. Neurosci. 2005, 8:1319-1328.
30. Hestrin S., Nicoll R.A., Perkel D.J., Sah P. Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J. Physiol. 1990, 422:203-225.
31. Iremonger K.J., Bains J.S. Integration of asynchronously released quanta prolongs the postsynaptic spike window. J. Neurosci. 2007, 27:6684-6691.
32. Isaacson J.S., Walmsley B. Counting quanta: direct measurements of transmitter release at a central synapse. Neuron 1995, 15:875-884.
33. Katz B., Miledi R. The effect of temperature on the synaptic delay at the neuromuscular junction. J. Physiol. 1965, 181:656-670.
34. Katz B., Miledi R. The measurement of synaptic delay, and the time course of acetylcholine release at the neuromuscular junction. Proc. R. Soc. Lond. B Biol. Sci. 1965, 161:483-495.
35. Khaliq Z.M., Raman I.M. Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons. J. Neurosci. 2005, 25:454-463.
36. Llinás R., Mühlethaler M. Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation. J. Physiol. 1988, 404:241-258.
37. Lu T., Trussell L.O. Inhibitory transmission mediated by asynchronous transmitter release. Neuron 2000, 26:683-694.
38. Maruta J., Hensbroek R.A., Simpson J.I. Intraburst and interburst signaling by climbing fibers. J. Neurosci. 2007, 27:11263-11270.
39. Matthews G., Sterling P. Evidence that vesicles undergo compound fusion on the synaptic ribbon. J. Neurosci. 2008, 28:5403-5411.
40. McKay B.E., Molineux M.L., Mehaffey W.H., Turner R.W. Kv1 K+ channels control Purkinje cell output to facilitate postsynaptic rebound discharge in deep cerebellar neurons. J. Neurosci. 2005, 25:1481-1492.
41. Monsivais P., Clark B.A., Roth A., Häusser M. Determinants of action potential propagation in cerebellar Purkinje cell axons. J. Neurosci. 2005, 25:464-472.
42. Oertner T.G., Sabatini B.L., Nimchinsky E.A., Svoboda K. Facilitation at single synapses probed with optical quantal analysis. Nat. Neurosci. 2002, 5:657-664.
43. Piochon C., Irinopoulou T., Brusciano D., Bailly Y., Mariani J., Levenes C. NMDA receptor contribution to the climbing fiber response in the adult mouse Purkinje cell. J. Neurosci. 2007, 27:10797-10809.
44. Prange O., Murphy T.H. Analysis of multiquantal transmitter release from single cultured cortical neuron terminals. J. Neurophysiol. 1999, 81:1810-1817.
45. Raman I.M., Bean B.P. Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J. Neurosci. 1997, 17:4517-4526.
46. Sato Y., Miura A., Fushiki H., Kawasaki T. Short-term modulation of cerebellar Purkinje cell activity after spontaneous climbing fiber input. J. Neurophysiol. 1992, 68:2051-2062.
47. Scheuss V., Taschenberger H., Neher E. Kinetics of both synchronous and asynchronous quantal release during trains of action potential-evoked EPSCs at the rat calyx of Held. J. Physiol. 2007, 585:361-381.
48. Schmolesky M.T., Weber J.T., De Zeeuw C.I., Hansel C. The making of a complex spike: ionic composition and plasticity. Ann. N Y Acad. Sci. 2002, 978:359-390.
49. Schneggenburger R., Meyer A.C., Neher E. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 1999, 23:399-409.
50. Singer J.H., Lassová L., Vardi N., Diamond J.S. Coordinated multivesicular release at a mammalian ribbon synapse. Nat. Neurosci. 2004, 7:826-833.
51. Sun J., Pang Z.P., Qin D., Fahim A.T., Adachi R., Südhof T.C. A dual-Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 2007, 450:676-682.
52. Swensen A.M., Bean B.P. Ionic mechanisms of burst firing in dissociated Purkinje neurons. J. Neurosci. 2003, 23:9650-9663.
53. Takahashi T., Forsythe I.D., Tsujimoto T., Barnes-Davies M., Onodera K. Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science 1996, 274:594-597.
54. Telgkamp P., Raman I.M. Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J. Neurosci. 2002, 22:8447-8457.
55. Tong G., Jahr C.E. Multivesicular release from excitatory synapses of cultured hippocampal neurons. Neuron 1994, 12:51-59.
56. Tzingounis A.V., Wadiche J.I. Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat. Rev. Neurosci. 2007, 8:935-947.
57. Vyshedskiy A., Allana T., Lin J.W. Analysis of presynaptic Ca2+ influx and transmitter release kinetics during facilitation at the inhibitor of the crayfish neuromuscular junction. J. Neurosci. 2000, 20:6326-6332.
58. Wadiche J.I., Jahr C.E. Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 2001, 32:301-313.
59. Waldeck R.F., Pereda A., Faber D.S. Properties and plasticity of paired-pulse depression at a central synapse. J. Neurosci. 2000, 20:5312-5320.
60. Weber J.T., De Zeeuw C.I., Linden D.J., Hansel C. Long-term depression of climbing fiber-evoked calcium transients in Purkinje cell dendrites. Proc. Natl. Acad. Sci. USA 2003, 100:2878-2883.
61. Xu J., He L., Wu L.G. Role of Ca(2+) channels in short-term synaptic plasticity. Curr. Opin. Neurobiol. 2007, 17:352-359.
62. Xu-Friedman M.A., Regehr W.G. Probing fundamental aspects of synaptic transmission with strontium. J. Neurosci. 2000, 20:4414-4422.
63. Xu-Friedman M.A., Regehr W.G. Ultrastructural contributions to desensitization at cerebellar mossy fiber to granule cell synapses. J. Neurosci. 2003, 23:2182-2192.
64. Zagha E., Lang E.J., Rudy B. Kv3.3 channels at the Purkinje cell soma are necessary for generation of the classical complex spike waveform. J. Neurosci. 2008, 28:1291-1300.
65. Zucker R.S., Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 2002, 64:355-405.