Increased neurotransmitter release during long-term potentiation at mossy fibre-granule cell synapses in rat cerebellum

Journal of Physiology

Volumn 557, Issue 3, 2004, Pages 843-861

  Sola, Elisabetta ^a,c   Prestori, Francesca ^a   Rossi, Paola ^a   Taglietti, Vanni ^a   D'Angelo, Egidio ^a,b  

^a UNIVERSITY OF PAVIA   (Italy)

^b UNIVERSITY OF PARMA   (Italy)

^c SISSA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CALCIUM ION; CHLORIDE; MAGNESIUM ION; N METHYL DEXTRO ASPARTIC ACID; NEUROTRANSMITTER; AMPA RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL TISSUE; ARTICLE; BINOMIAL DISTRIBUTION; BRAIN SLICE; CELL MEMBRANE DEPOLARIZATION; CEREBELLUM; CONCENTRATION RESPONSE; CONSTANTS AND COEFFICIENTS; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; EXTRACELLULAR FLUID; GRANULE CELL; LONG TERM POTENTIATION; MEMBRANE CURRENT; MOSSY FIBER; NERVE CELL STIMULATION; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROBABILITY; RAT; SYNAPSE; THETA RHYTHM; AMINO ACID TRANSPORT; AMPLITUDE MODULATION; ANIMAL CELL; CEREBELLAR MOSSY FIBER; EVOKED POSTSYNAPTIC CURRENT; EXTRACELLULAR SPACE; FREQUENCY MODULATION; MEMBRANE DEPOLARIZATION; MINIATURE SYNAPTIC CURRENT; NERVE CELL EXCITABILITY; NERVE STIMULATION; PATCH CLAMP TECHNIQUE; SYNAPTIC POTENTIAL;

ALGORITHMS; ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CEREBELLUM; CYTOPLASMIC GRANULES; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; MEMBRANE POTENTIALS; N-METHYLASPARTATE; NERVE FIBERS; NEURONS; NEUROTRANSMITTER AGENTS; PATCH-CLAMP TECHNIQUES; RATS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 3242660931     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2003.060285     Document Type: Article

References (49)

1. Arancio O, Kiebler M, Lee CJ, Lev-Ram V, Tsien RY, Kandel ER et al. (1996). Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87, 1025-1035.
2. Armano S, Rossi P, Taglietti V & D'Angelo E (2000). Long-term potentiation of intrinsic excitability at the mossy fibre - granule cell synapse of rat cerebellum. J Neurosci 20, 5208-5216.
3. Auger C & Marty A (2000). Quantal currents at single-site central synapses. J Physiol 526, 3-11.
4. Bekkers JM & Stevens CF (1990). Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 346, 724-729.
5. Benke TA, Luthi A, Isaac JTR & Collingridge GL (1998). Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393, 793-797.
6. Bliss TVP & Collingridge GL (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
7. Carey MR & Lisberger SG (2002). Embarassed, but not depressed: eye opening lessons for cerebellar learning. Neuron 35, 223-226.
8. Cathala L, Brickley S, Cull-Candy S & Farrant M (2003). Maturation of EPSCs and intrinsic membrane properties enhances precision at a cerebellar synapse. J Neurosci 23, 6074-6085.
9. Clements JD (2003). Variance-mean analysis: a simple and reliable approach for investigating synaptic transmission and modulation. J Neurosci Meth 130, 115-125.
10. Clements JD & Silver RA (2000). Unveiling synaptic plasticity: a new graphical and analytical approach. Trends Neurosci 23, 105-113.
11. D'Angelo E, De Filippi G, Rossi P & Taglietti V (1995). Synaptic excitation of individual rat cerebellar granule cells in situ: evidence for the role of NMDA receptors. J Physiol 484, 397-413.
12. D'Angelo E, Rossi P, Armano S & Taglietti V (1999). Evidence for NMDA and mGlu receptor-dependent long-term potentiation of mossy fibre - granule cell transmission in rat cerebellum. J Neurophysiol 81, 277-287.
13. D'Angelo E, Rossi P & Taglietti V (1993). Different proportions of N-methyl-D-aspartate and non-N-methyl-D-aspartate receptor currents at the mossy fibre-granule cell synapse of developing rat cerebellum. Neuroscience 53, 121-130.
14. DiGregorio DA, Nusser Z & Silver RA (2002). Spillover of glutamate onto synaptic AMPA receptors enhances fast transmission at a cerebellar synapse. Neuron 35, 521-533.
15. Dodge FA Jr & Rahamimoff R (1967). Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J Physiol 193, 419-432.
16. Eccles JC, Ito M & Szentagothai J (1967). The Cerebellum as a Neuronal Machine. Springer Verlag, Berlin.
17. Edwards FA (1995). Anatomy and electrophysiology of fast central synapses lead to a structural model for long-term potentiation. Physiol Rev 75, 759-787.
18. Gasparini S, Saviane C, Voronin LL & Cherubini E (2000). Silent synapses in the developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release? Proc Natl Acad Sci U S A 97, 9741-9746.
19. Hansel C, Linden DJ & D'Angelo E (2001). Beyond parallel fibre LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nature Neurosci 4, 467-475.
20. Hawkins RD, Kandel ER & Siegelbaum SA (1993). Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annu Rev Neurosci 16, 625-665.
21. Hayashi Y, Shi S-H, Esteban JA, Piccini A, Poncer J-C & Malinow R (2000). Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262-2267.
22. Isaac JTR, Hjelmstad GO, Nicoll RA & Malenka RC (1996). Long-term potentiation at single fiber inputs to hippocampal CA1 pyramidal cells. Proc Natl Acad Sci U S A 93, 8710-8715.
23. Jakab J & Hamori J (1988). Quantitative morphology and synaptology of cerebellar glomeruli in the rat. Anat Embriol 179, 81-88.
24. Katz B & Miledi R (1968). The role of calcium in neuromuscular facilitation. J Physiol 195, 481-492.
25. Kullmann DM, Erdemli G & Asztely F (1996). LTP of AMPA and NMDA receptor-mediated signals: evidence for presynaptic expression and extrasynaptic glutamate spillover. Neuron 17, 461-474.
26. Kullmann DM & Nicoll RA (1992). Long-term potentiation is associated with increases in quantal content and quantal amplitude. Nature 357, 240-244.
27. Larkman A, Hannay T, Stratford K & Jack J (1992). Presynaptic release probability influences the locus of long-term potentiation. Nature 360, 70-73.
28. Liao D, Hessler NA & Malinow R (1995). Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400-404.
29. Losi G, Prybylowski K, Fu Z, Luo JH & Vicini S (2002). Silent synapses in developing cerebellar granule neurons. J Neurophysiol 87, 1263-1270.
30. Lupica CR, Proctor WR & Dunwiddie TV (1992). Presynaptic inhibition of excitatory synaptic transmission by adenosine in rat hippocampus: analysis of unitary EPSP variance measured by whole-cell recordings. J Neurosci 12, 3753-3764.
31. Maffei A, Prestori F, Rossi P, Taglietti V & D'Angelo E (2002). Presynaptic current changes at the mossy fiber-granule cell synapse of cerebellum during LTP. J Neurophysiol 88, 627-638.
32. Maffei A, Prestori F, Shibuki K, Rossi P, Taglietti V & D'Angelo E (2003). NO enhances presynaptic currents during cerebellar mossy fiber-granule cell LTP. J Neurophysiol 90, 2478-2483.
33. Malenka RC & Nicoll RA (1999). Long-term potentiation - A decade of progress? Science 285, 1870-1874.
34. Malgaroli A, Ting AE, Wendland B, Bergamaschi A, Villa A, Tsien RW et al. (1995). Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science 268, 1624-1628.
35. Malinow R (1991). Is maintenance of LTP presynaptic? Nature 350, 282.
36. Malinow R & Tsien RW (1990). Presynaptic enhancement shown by whole-cell recording of long-term potentiation in hippocampal slices. Nature 346, 177-180.
37. Manabe T, Renner P & Nicoll RA (1992). Postsynaptic contribution to long-term potentiation revealed by the analysis of miniature synaptic currents. Nature 355, 50-55.
38. Manabe T, Wyllie DJ, Perkel DJ & Nicoll RA (1993). Modulation of synaptic transmission and long-term potentiation: effects on paired-pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neurophysiol 70, 1451-1459.
39. McLachlan EM (1978). The statistics of transmitter release at chemical synapses. In International Rev Physiol Neurophysiol III, vol. 17, ed. Porter R. University Park Press, Baltimore.
40. Monti B, Marri L & Contestabile A (2002). NMDA receptor-dependent CREB activation in survival of cerebellar granule cells during in vivo and in vitro development. Eur J Neurosci 16, 1490-1498.
41. Rossi P, Sola E, Taglietti V, Borchardt T, Steigerwald F, Utvik K et al. (2002). NMDA receptor 2 (NR2) C-terminal control of NR open probability regulates synaptic transmission and plasticity at a cerebellar synapse. J Neurosci 22, 9687-9697.
42. Sakmann B (1998). Unitary EPSPs in pairs of anatomically reconstructed cortical pyramidal neurons. In Central Synapses: Quantal Mechanisms and Plasticity, ed. Faber DS, Korn H, Redman SJ, Thomson SM & Altman JS, pp. 64-73. HFSP, Strasbourg.
43. Schulz PE, Cook EP & Johnston D (1994). Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation. J Neurosci 14, 5325-5337.
44. Schweighofer N, Doya K & Lay F (2001). Unsupervised learning of granule cell sparse codes enhances cerebellar adaptive control. Neuroscience 103, 35-50.
45. Silver RA (2003). Estimation of nonuniform quantal parameters with multiple-probability fluctuation analysis: theory, application and limitations. J Neurosci Meth 130, 127-141.
46. Silver RA, Cull-Candy SG & Takahashi T (1996). Non-NMDA glutamate receptor occupancy and open probability at a rat cerebellar synapse with single and multiple releases sites. J Physiol 494, 231-250.
47. Von Kitzing E, Jonas P & Sakmann B (1994). Quantal analysis of excitatory postsynaptic currents at the hippocampal mossy fiber - CA3 pyramidal cell synapse. In Molecular and Cellular Mechanisms of Neurotransmitter Release, ed. Stjärne L, Greengard P, Grillner S, Öchfelt T & Ottoson D, pp. 235-260. Raven Press Ltd, New York.
48. Wernig A (1975). Estimates of statistical release parameters from crayfish and frog neuromuscular junctions. J Physiol 244, 207-221.
49. Xu-Friedman MA & Regehr WG (2003). Ultrastructural contributions to desensitization at cerebellar mossy fiber to granule cell synapses. J Neurosci 23, 2182-2192.