Adaptation of granule cell to purkinje cell synapses to high-frequency transmission

Journal of Neuroscience

Volumn 32, Issue 9, 2012, Pages 3267-3280

  Valera, Antoine M ^a,b   Doussau, Frédéric ^a,b   Poulain, Bernard ^a,b   Barbour, Boris ^a,c,d   Isope, Philippe ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c ECOLE NORMALE SUPÉRIEURE   (France)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; GRANULE CELL; MALE; MATHEMATICAL MODEL; NERVE CELL STIMULATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PURKINJE CELL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; PURKINJE CELLS; RATS; RATS, WISTAR; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84857602574     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3175-11.2012     Document Type: Article

References (58)

1. Arenz A, Silver RA, Schaefer AT, Margrie TW (2008) The contribution of single synapses to sensory representation in vivo. Science 321:977-980
2. Atluri PP, Regehr WG (1996) Determinants of the time course of facilitation at the granule cell to Purkinje cell synapse. J Neurosci 16:5661-5671
3. Augustine GJ, Neher E (1992) Calcium requirements for secretion in bovine chromaffin cells. J Physiol 450:247-271
4. Barbour B (2001) An evaluation of synapse independence. J Neurosci 21:7969-7984
5. Barbour B, Isope P (2000) Combining loose cell-attached stimulation and recording. J Neurosci Methods 103:199-208
6. Bekkers JM, Clements JD (1999) Quantal amplitude and quantal variance of strontium-induced asynchronous EPSCs in rat dentate granule neurons. J Physiol 516:227-248
7. Bidoret C, Ayon A, Barbour B, Casado M (2009) Presynaptic NR2Acontaining NMDA receptors implement a high-pass filter synaptic plasticity rule. Proc Natl Acad Sci USA 106:14126-14131
8. Brown SP, Brenowitz SD, Regehr WG (2003) Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci 6:1048-1057
9. Brunel N, Hakim V, Isope P, Nadal JP, Barbour B (2004) Optimal information storage and the distribution of synaptic weights: perception versus Purkinje cell. Neuron 43:745-757
10. Chadderton P, Margrie TW, Häusser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428:856-860
11. Clements J (1991) Quantal synaptic transmission? Nature 353:396.
12. Clements JD (2003) Variance-mean analysis: a simple and reliable approach for investigating synaptic transmission and modulation. J Neurosci Methods 130:115-125
13. Clements JD, Silver RA (2000) Unveiling synaptic plasticity: a new graphical and analytical approach. Trends Neurosci 23:105-113
14. Coesmans M, Weber JT, De Zeeuw CI, Hansel C (2004) Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44:691-700
15. Crowley JJ, Carter AG, Regehr WG (2007) Fast vesicle replenishment and rapid recovery from desensitization at a single synaptic release site. J Neurosci 27:5448-5460
16. DiGregorio DA, Rothman JS, Nielsen TA, Silver RA (2007) Desensitization properties of AMPA receptors at the cerebellar mossy fiber granule cell synapse. J Neurosci 27:8344-8357
17. Dittman JS, Regehr WG (1998) Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18:6147-6162
18. Dittman JS, Kreitzer AC, Regehr WG (2000) Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20:1374-1385
19. Doussau F, Humeau Y, Benfenati F, Poulain B (2010) A novel form of presynaptic plasticity based on the fast reactivation of release sites switched off during low-frequency depression. J Neurosci 30:16679-16691
20. Dugué GP, Dumoulin A, Triller A, Dieudonné S (2005) Target-dependent use of co-released inhibitory transmitters at central synapses. J Neurosci 25:6490-6498
21. Efron B, Tibshirani R (1993) An introduction to the bootstrap. London: Chapman and Hall.
22. Ekerot CF, Jörntell H (2001) Parallel fibre receptive fields of Purkinje cells and interneurons are climbing fibre-specific. Eur J Neurosci 13:1303-1310
23. 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. J Neurosci 25:11655-11665
24. Hansel C, Linden DJ, D'Angelo E (2001) Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci 4:467-475
25. Humeau Y, Vitale N, Chasserot-Golaz S, Dupont JL, Du G, Frohman MA, Bader MF, Poulain B (2001) A role for phospholipase D1 in neurotransmitter release. Proc Natl Acad Sci USA 98:15300-15305
26. Humeau Y, Popoff MR, Kojima H, Doussau F, Poulain B (2002) Rac GTPase plays an essential role in exocytosis by controlling the fusion competence of release sites. J Neurosci 22:7968-7981
27. Humeau Y, Doussau F, Popoff MR, Benfenati F, Poulain B (2007) Fast changes in the functional status of release sites during short-term plasticity: involvement of a frequency-dependent bypass of Rac at Aplysia synapses. J Physiol 583:983-1004
28. Isope P, Barbour B (2002) Properties of unitary granule cell→Purkinje cell synapses in adult rat cerebellar slices. J Neurosci 22:9668-9678
29. Ito M (2006) Cerebellar circuitry as a neuronal machine. Prog Neurobiol 78:272-303
30. Jörntell H, Ekerot CF (2002) Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 34:797-806
31. Jörntell H, Ekerot CF (2006) Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. J Neurosci 26:11786-11797
32. Kim J, Alger BE (2001) Random response fluctuations lead to spurious paired-pulse facilitation. J Neurosci 21:9608-9618
33. Larkman A, Stratford K, Jack J (1991) Quantal analysis of excitatory synaptic action and depression in hippocampal slices. Nature 350:344-347
34. Lev-Ram V, Wong ST, Storm DR, Tsien RY (2002) A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP. Proc Natl Acad Sci USA 99:8389-8393
35. Markram H, Lübke J, Frotscher M, Roth A, Sakmann B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500:409-440
36. Matsukawa H, Wolf AM, Matsushita S, Joho RH, Knöpfel T (2003) Motor dysfunction and altered synaptic transmission at the parallel fiber-Purkinje cell synapse in mice lacking potassium channels Kv3.1 and Kv3.3. J Neurosci 23:7677-7684
37. Mintz IM, Sabatini BL, Regehr WG (1995) Calcium control of transmitter release at a cerebellar synapse. Neuron 15:675-688
38. Neher E (2006) A comparison between exocytic control mechanisms in adrenal chromaffin cells and a glutamatergic synapse. Pflugers Arch 453:261-268
39. Oleskevich S, Clements J, Walmsley B (2000) Release probability modulates short-term plasticity at a rat giant terminal. J Physiol 524:513-523
40. Perkel DJ, Hestrin S, Sah P, Nicoll RA (1990) Excitatory synaptic currents in Purkinje cells. Proc Biol Sci 241:116-121
41. Pyle JL, Kavalali ET, Piedras-Rentería ES, Tsien RW (2000) Rapid reuse of readily releasable pool vesicles at hippocampal synapses. Neuron 28:221-231
42. Rancz EA, Ishikawa T, Duguid I, Chadderton P, Mahon S, Häusser M (2007) High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons. Nature 450:1245-1248
43. Reid CA, Clements JD (1999) Postsynaptic expression of long-term potentiation in the rat dentate gyrus demonstrated by variance-mean analysis. J Physiol 518:121-130
44. Roth A, Häusser M (2001) Compartmental models of rat cerebellar Purkinje cells based on simultaneous somatic and dendritic patch-clamp recordings. J Physiol 535:445-472
45. Sakaba T, Neher E (2001) Quantitative relationship between transmitter release and calcium current at the calyx of held synapse. J Neurosci 21:462-476
46. Salin PA, Malenka RC, Nicoll RA (1996) CyclicAMPmediates a presynaptic form of LTP at cerebellar parallel fiber synapses. Neuron 16:797-803
47. Saviane C, Silver RA (2006) Fast vesicle reloading and a large pool sustain high bandwidth transmission at a central synapse. Nature 439:983-987
48. Saviane C, Silver RA (2007) Estimation of quantal parameters with multiple-probability fluctuation analysis. Methods Mol Biol 403:303-317
49. 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
50. Schneggenburger R, Sakaba T, Neher E (2002) Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25:206-212
51. 2+] in hypoxia and ischemia in rat brain in vivo. J Gen Physiol 95:837-866
52. Silver RA (2003) Estimation of nonuniform quantal parameters with multiple-probability fluctuation analysis: theory, application and limitations. J Neurosci Methods 130:127-141
53. 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 release sites. J Physiol 494:231-250
54. Silver RA, Momiyama A, Cull-Candy SG (1998) Locus of frequencydependent depression identified with multiple-probability fluctuation analysis at rat climbing fibre-Purkinje cell synapses. J Physiol 510: 881-902
55. Silver RA, Lubke J, Sakmann B, Feldmeyer D (2003) High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302:1981-1984
56. Sims RE, Hartell NA (2005) Differences in transmission properties and susceptibility to long-term depression reveal functional specialization of ascending axon and parallel fiber synapses to Purkinje cells. J Neurosci 25:3246-3257
57. Sims RE, Hartell NA (2006) Differential susceptibility to synaptic plasticity reveals a functional specialization of ascending axon and parallel fiber synapses to cerebellar Purkinje cells. J Neurosci 26:5153-5159
58. Xu-Friedman MA, Harris KM, Regehr WG (2001) Three-dimensional comparison of ultrastructural characteristics at depressing and facilitating synapses onto cerebellar Purkinje cells. J Neurosci 21:6666-6672.