Maturation of EPSCs and intrinsic membrane properties enhances precision at a cerebellar synapse

Journal of Neuroscience

Volumn 23, Issue 14, 2003, Pages 6074-6085

  Cathala, Laurence ^a   Brickley, Stephen ^a   Cull Candy, Stuart ^a   Farrant, Mark ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

AMPA receptor; Cerebellum; EPSC; EPSP; Granule cell; Intrinsic membrane properties; NMDA receptor; Postnatal development

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CEREBELLUM; EXCITATORY POSTSYNAPTIC POTENTIAL; GRANULE CELL; MEMBRANE POTENTIAL; MOSSY FIBER; MOUSE; NERVE CONDUCTION; NONHUMAN; PATCH CLAMP; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SPIKE; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 0038825663     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-14-06074.2003     Document Type: Article

References (81)

1. Akazawa C, Shigemoto R, Bessho Y, Nakanishi S, Mizuno N (1994) Differential expression of five N-methyl-D-aspartate receptor subunit mRNAs in the cerebellum of developing and adult rats. J Comp Neurol 347:150-160.
2. Baude A, Molnar E, Latawiec D, McIlhinney RA, Somogyi P (1994) Synaptic and nonsynaptic localization of the GluR1 subunit of the AMPA-type excitatory amino acid receptor in the rat cerebellum. J Neurosci 14:2830-2843.
3. Bekkers JM, Stevens CF (1989) NMDA and non-NMDA receptors are colocalized at individual excitatory synapses in cultured rat hippocampus. Nature 341:230-233.
4. Brenowitz S, Trussell LO (2001) Maturation of synaptic transmission at end-bulb synapses of the cochlear nucleus. J Neurosci 21:9487-9498.
5. A receptors. J Physiol (Lond) 497:753-759.
6. Brickley SG, Revilla V, Cull-Candy SG, Wisden W, Farrant M (2001) Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409:88-92.
7. Carroll RC, Zukin RS (2002) NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci 25:571-577.
8. Carter AG, Regehr WG (2000) Prolonged synaptic currents and glutamate spillover at the parallel fiber to stellate cell synapse. J Neurosci 20:4423-4434.
9. Carter AG, Regehr WG (2002) Quantal events shape cerebellar interneuron firing. Nat Neurosci 5:1309-1318.
10. Cathala L, Misra C, Cull-Candy S (2000) Developmental profile of the changing properties of NMDA receptors at cerebellar mossy fiber-granule ceU synapses. J Neurosci 20:5899-5905.
11. Chen S, Diamond JS (2002) Synaptically released glutamate activates extrasynaptic NMDA receptors on cells in the ganglion cell layer of rat retina. J Neurosci 22:2165-2173.
12. Clark BA, Cull-Candy SG (2002) Activity-dependent recruitment of extrasynaptic NMDA receptor activation at an AMPA receptor-only synapse. J Neurosci 22:4428-4436.
13. Conti F, Weinberg RJ (1999) Shaping excitation at glutamatergic synapses. Trends Neurosci 22:451-458.
14. D'Angelo E, Rossi P, De Filippi G, Magistretti J, Taglietti V (1994) The relationship between synaptogenesis and expression of voltage-dependent currents in cerebellar granule cells in situ. J Physiol (Paris) 88:197-207.
15. 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 (Lond) 484:397-413.
16. D'Angelo E, Rossi P, Armano S, Taglietti V (1999) Evidence for NMDA and mGlu receptor-dependent long-term potentiation of mossy fiber-granule cell transmission in rat cerebellum. J Neurophysiol 81:277-287.
17. De Schutter E, Bjaalie JG (2001) Coding in the granular layer of the cerebellum. Prog Brain Res 130:279-296.
18. Diamond JS, Jahr CE (1995) Asynchronous release of synaptic vesicles determines the time course of the AMPA receptor-mediated EPSC. Neuron 15:1097-1107.
19. DiGregorio D, Nusser Z, Silver R (2002) Spillover of glutamate onto synaptic AMPA receptors enhances fast transmission at a cerebellar synapse. Neuron 35:521-533.
20. Edmonds B, Gibb AI, Colquhoun D (1995) Mechanisms of activation of glutamate receptors and the time course of excitatory synaptic currents. Annu Rev Physiol 57:495-519.
21. Farrant M, Feldmeyer D, Takahashi T, Cull-Candy SG (1994) NMDA-receptor channel diversity in the developing cerebellum. Nature 368:335-339.
22. Fricker D, Miles R (2000) EPSP amplification and the precision of spike timing in hippocampal neurons. Neuron 28:559-569.
23. Futai K, Okada M, Matsuyama K, Takahashi T (2001) High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J Neurosci 21:3342-3349.
24. Gabbiani F, Midtgaard J, Knopfel T (1994) Synaptic integration in a model of cerebellar granule cells. J Neurophysiol 72:999-1009.
25. Galarreta M, Hestrin S (2001) Spike transmission and synchrony detection in networks of GABAergic interneurons. Science 292:2295-2299.
26. Geiger JR, Lubke J, Roth A, Frotscher M, Jonas P (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18:1009-1023.
27. Gentet LJ, Stuart GJ, Clements JD (2000) Direct measurement of specific membrane capacitance in neurons. Biophys J 79:314-320.
28. Hamann M, Rossi DJ, Attwell D (2002) Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33:625-633.
29. Hamori J, Somogyi J (1983) Differentiation of cerebellar mossy fiber synapses in the rat: a quantitative electron microscope study. J Comp Neurol 220:365-377.
30. Harsch A, Robinson HP (2000) Postsynaptic variability of firing in rat cortical neurons: the roles of input synchronization and synaptic NMDA receptor conductance. J Neurosci 20:6181-6192.
31. Hashimoto K, Fukaya M, Qiao X, Sakimura K, Watanabe M, Kano M (1999) Impairment of AMPA receptor function in cerebellar granule cells of ataxic mutant mouse stargazer. J Neurosci 19:6027-6036.
32. Hausser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19:665-678.
33. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
34. Isaac JT, Nicoll RA, Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-434.
35. Jack JJ, Redman SJ (1971) The propagation of transient potentials in some linear cable structures. J Physiol (Lond) 215:283-320.
36. Jack JJB, Noble D, Tsien RW (1975) Electric current flow in excitable cells. Oxford: Clarendon.
37. Jonas P, Spruston N (1994) Mechanisms shaping glutamate-mediated excitatory postsynaptic currents in the CNS. Curr Opin Neurobiol 4:366-372.
38. Jones KA, Baughman RW (1991) Both NMDA and non-NMDA subtypes of glutamate receptors are concentrated at synapses on cerebral cortical neurons in culture. Neuron 7:593-603.
39. Kadotani H, Hirano T, Masugi M, Nakamura K, Nakao K, Katsuki M, Nakanishi S (1996) Motor discoordination results from combined gene disruption of the NMDA receptor NR2A and NR2C subunits, but not from single disruption of the NR2A or NR2C subunit. J Neurosci 16:7859-7867.
40. Kharazia VN, Phend KD, Rustioni A, Weinberg RJ (1996) EM colocalization of AMPA and NMDA receptor subunits at synapses in rat cerebral cortex. Neurosci Lett 210:37-40.
41. Kuba H, Koyano K, Ohmori H (2002) Development of membrane conductance improves coincidence detection in the nucleus laminaris of the chicken. J Physiol (Lond) 540:529-542.
42. 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.
43. London M, Schreibman A, Hausser M, Larkum ME, Segev I (2002) The information efficacy of a synapse. Nat Neurosci 5:332-340.
44. Losi G, Prybylowski K, Fu Z, Luo J, Wenthold RJ, Vicini S (2003) PSD-95 regulates NMDA receptors in developing cerebellar granule neurons of the rat. J Physiol (Lond) 548:21-29.
45. Maccaferri G, Dingledine R (2002) Control of feedforward dendritic inhibition by NMDA receptor-dependent spike timing in hippocampal interneurons. J Neurosci 22:5462-5472.
46. Maex R, Schutter ED (1998) Synchronization of Golgi and granule cell firing in a detailed network model of the cerebellar granule cell layer. J Neurophysiol 80:2521-2537.
47. Marr D (1969) A theory of cerebellar cortex. J Physiol (Lond) 202:437-470.
48. McCormick DA, Prince DA (1987) Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J Physiol (Lond) 393:743-762.
49. Millar JA, Barratt L, Southan AP, Page KM, Fyffe RE, Robertson B, Mathie A (2000) A functional role for the two-pore domain potassium channel TASK-1 in cerebellar granule neurons. Proc Natl Acad Sci USA 97:3614-3618.
50. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
51. Mosbacher J, Schoepfer R, Monyer H, Burnashev N, Seeburg PH, Ruppersberg JP (1994) A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266:1059-1062.
52. Palay SL, Chan-Palay V (1974) Cerebellar cortex: cytology and organization. Berlin: Springer.
53. Petralia RS, Esteban JA, Wang YX, Partridge JG, Zhao HM, Wenthold RJ, Malinow R (1999) Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci 2:31-36.
54. Petralia RS, Wang YX, Wenthold RJ (2002) NMDA receptors and PSD-95 are found in attachment plaques in cerebellar granular layer glomeruli. Eur J Neurosci 15:583-587.
55. Racca C, Stephenson FA, Streit P, Roberts JD, Somogyi P (2000) NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area. J Neurosci 20:2512-2522.
56. Rall W (1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J Neurophysiol 30:1138-1168.
57. Ramon y Cajal S (1995) Histology of the nervous system of man and vertebrates. New York: Oxford UP.
58. Reyes A (2001) Influence of dendritic conductances on the input-output properties of neurons. Annu Rev Neurosci 24:653-675.
59. Ripellino JA, Neve RL, Howe JR (1998) Expression and heteromeric interactions of non-N-methyl-D-aspartate glutamate receptor subunits in the developing and adult cerebellum. Neuroscience 82:485-497.
60. Robinson HP, Kawai N (1993) Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. J Neurosci Methods 49:157-165.
61. Rumbaugh G, Vicini S (1999) Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons. J Neurosci 19:10603-10610.
62. Schneidman E, Freedman B, Segev I (1998) Ion channel stochasticity maybe critical in determining the reliability and precision of spike timing. Neural Comput 10:1679-1703.
63. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284:1811-1816.
64. Silver RA, Traynelis SF, Cull-Candy SG (1992) Rapid-time-course miniature and evoked excitatory currents at cerebellar synapses in situ. Nature 355:163-166.
65. 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 (Lond) 494:231-250.
66. Singer JH, Talley EM, Bayliss DA, Berger AJ (1998) Development of glycinergic synaptic transmission to rat brain stem motoneurons. J Neurophysiol 80:2608-2620.
67. Smith TC, Wang LY, Howe JR (2000) Heterogeneous conductance levels of native AMPA receptors. J Neurosci 20:2073-2085.
68. Takahashi T, Feldmeyer D, Suzuki N, Onodera K, Cull-Candy SG, Sakimura K, Mishina M (1996) Functional correlation of NMDA receptor ε subunits expression with the properties of single-channel and synaptic currents in the developing cerebellum. J Neurosci 16:4376-4382.
69. Takahashi T, Svoboda K, Malinow R (2003) Experience strengthening transmission by driving AMPA receptors into synapses. Science 299:1585-1588.
70. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP (1999) Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2:618-624.
71. Taschenberger H, von Gersdorff H (2000) Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20:9162-9173.
72. Taschenberger H, Leao RM, Rowland KC, Spirou GA, von Gersdorff H (2002) Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 36:1127-1143.
73. Trussell LO (1997) Cellular mechanisms for preservation of timing in central auditory pathways. Curr Opin Neurobiol 7:487-492.
74. Tyrrell T, Willshaw D (1992) Cerebellar cortex: its simulation and the relevance of Marr's theory. Philos Trans R Soc Lond B Biol Sci 336:239-257.
75. Umemiya M, Senda M, Murphy TH (1999) Behaviour of NMDA and AMPA receptor-mediated miniature EPSCs at rat cortical neuron synapses identified by calcium imaging. J Physiol (Lond) 521:113-122.
76. van Kan PL, Gibson AR, Houk JC (1993) Movement-related inputs to intermediate cerebellum of the monkey. J Neurophysiol 69:74-94.
77. Wall MJ, Usowicz MM (1998) Development of the quantal properties of evoked and spontaneous synaptic currents at a brain synapse. Nat Neurosci 1:675-682.
78. Wall MJ, Robert A, Howe JR, Usowicz MM (2002) The speeding of EPSC kinetics during maturation of a central synapse. Eur J Neurosci 15:785-797.
79. Watanabe D, Inokawa H, Hashimoto K, Suzuki N, Kano M, Shigemoto R, Hirano T, Toyama K, Kaneko S, Yokoi M, Moriyoshi K, Suzuki M, Kobayashi K, Nagatsu T, Kreitman RJ, Pastan I, Nakanishi S (1998) Ablation of cerebellar Golgi cells disrupts synaptic integration involving GABA inhibition and NMDA receptor activation in motor coordination. Cell 95:17-27.
80. Wenthold RJ, Prybylowski K, Standley S, Sans N, Petralia RS (2003) Trafficking of NMDA receptors. Annu Rev Pharmacol Toxicol 43:335-358.
81. Yamada K, Fukaya M, Shimizu H, Sakimura K, Watanabe M (2001) NMDA receptor subunits GluRε1, GluRε3 and GluRζ1 are enriched at the mossy fibre-granule cell synapse in the adult mouse cerebellum. Eur J Neurosci 13:2025-2036.