Augmentation controls the fast rebound from depression at excitatory hippocampal synapses

Journal of Neurophysiology

Volumn 99, Issue 4, 2008, Pages 1770-1786

  Garcia Perez, Elizabeth ^a   Wesseling, John F ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUGMENTATION INDEX; CELL ISOLATION; CONTROLLED STUDY; DEPRESSION; HIPPOCAMPUS; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SYNAPSE;

ANIMALS; AXONAL TRANSPORT; AXONS; BODY TEMPERATURE; CALCIUM; CELLS, CULTURED; ELECTROPHYSIOLOGY; FLUORESCENT DYES; HIPPOCAMPUS; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; RATS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 42249088611     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01348.2007     Document Type: Article

References (71)

1. Abbott LF, Nelson SB. Synaptic plasticity: taming the beast. Nat Neurosci 3, Suppl: 1178-1183, 2000.
2. Abbott LF, Varela JA, Sen K, Nelson SB. Synaptic depression and cortical gain control. Science 275: 220-224, 1997.
3. Allen C, Stevens CF. An evaluation of causes for unreliability of synaptic transmission. Proc Natl Acad Sci USA 91: 10380-10383, 1994.
4. Augustine GJ, Charlton MP. Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse. J Physiol 381: 619-640, 1986.
5. Basu J, Betz A, Brose N, Rosenmund C. Munc13-1 C1 domain activation lowers the energy barrier for synaptic vesicle fusion. J Neurosci 27: 1200-1210, 2007.
6. Bekkers JM, Stevens CF. Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci USA 88: 7834-7838, 1991.
7. Brager DH, Cai X, Thompson SM. Activity-dependent activation of presynaptic protein kinase C mediates post-tetanic potentiation. Nat Neurosci 6: 551-552, 2003.
8. Chance FS, Nelson SB, Abbott LF. Synaptic depression and the temporal response characteristics of V1 cells. J Neurosci 18: 4785-4799, 1998.
9. Chung S, Li X, Nelson SB. Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34: 437-446, 2002.
10. Cook DL, Schwindt PC, Grande LA, Spain WJ. Synaptic depression in the localization of sound. Nature 421: 66-70, 2003.
11. Delaney KR, Tank DW. A quantitative measurement of the dependence of short-term synaptic enhancement on presynaptic residual calcium. J Neurosci 14: 5885-5902, 1994.
12. Dittman JS, Regehr WG. Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18: 6147-6162, 1998.
13. Dobrunz LE, Stevens CF. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008, 1997.
14. Dodge FA Jr, Rahamimoff R. Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J Physiol 193: 419-432, 1967.
15. Felmy F, Neher E, Schneggenburger R. Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation. Neuron 37: 801-811, 2003.
16. Feng TP. Studies on the neuromuscular junction XXVI, the changes of the end-plate potential during and after prolonged stimulation. Chin J Physiol 16: 341-372, 1941.
17. Fernandez-Chacon R, Konigstorfer A, Gerber SH, Garcia J, Matos MF, Stevens CF, Brose N, Rizo J, Rosenmund C, Sudhof TC. Synaptotagmin I functions as a calcium regulator of release probability. Nature 410: 41-49, 2001.
18. Fisher SA, Fischer TM, Carew TJ. Multiple overlapping processes underlying short-term synaptic enhancement. Trends Neurosci 20: 170-177, 1997.
19. Frakenhaeuser B, Hodgkin AL. The action of calcium on the electrical properties of squid axons. J Physiol 137: 218-244, 1957.
20. Fuhrmann G, Segev I, Markram H, Tsodyks M. Coding of temporal information by activity-dependent synapses. J Neurophysiol 87: 140-148, 2002.
21. Hagler DJ Jr, Goda Y. Properties of synchronous and asynchronous release during pulse train depression in cultured hippocampal neurons. J Neurophysiol 85: 2324-2334, 2001.
22. Hanse E, Gustafsson B. Vesicle release probability and pre-primed pool at glutamatergic synapses in area CA1 of the rat neonatal hippocampus. J Physiol 531: 481-493, 2001.
23. Hanse E, Gustafsson B. Release dependence to a paired stimulus at a synaptic release site with a small variable pool of immediately releasable vesicles. J Neurosci 22: 4381-4387, 2002.
24. Haugland RP. Handbook of Fluorescent Probes and Research Chemicals. Eugene, OR: Molecular Probes, 1992.
25. Hermann J, Pecka M, von Gersdorff H, Grothe B, Klug A. Synaptic transmission at the calyx of Held under in vivo like activity levels. J Neurophysiol 98: 807-820, 2007.
26. Hubbard JI. Repetitive stimulation at the mammalian neuromuscular junction, and the mobilization of transmitter. J Physiol 169: 641-662, 1963.
27. Kalkstein JM, Magleby KL. Augmentation increases vesicular release probability in the presence of masking depression at the frog neuromuscular junction. J Neurosci 24: 11391-11403, 2004.
28. 2+ and short-term synaptic plasticity. Nature 371: 603-606, 1994.
29. Klyachko VA, Stevens CF. Temperature-dependent shift of balance among the components of short-term plasticity in hippocampal synapses. J Neurosci 26: 6945-6957, 2006.
30. Korn H, Faber DS. Regulation and significance of probabilistic release mechanism at central synapses. In: Synaptic Function, edited by Edelman GM, Gall WE, Cowan WM. New York: Wiley, 1987, p. 57-108.
31. Korogod N, Lou X, Schneggenburger R. Posttetanic potentiation critically depends on an enhanced Ca (2+) sensitivity of vesicle fusion mediated by presynaptic PKC. Proc Natl Acad Sci USA 104: 15923-15928, 2007.
32. Liley AW, North KA. An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction. J Neurophysiol 16: 509-527, 1953.
33. Magleby KL, Zengel JE. Augmentation: a process that acts to increase transmitter release at the frog neuromuscular junction. J Physiol 257: 449-470, 1976a.
34. Magleby KL, Zengel JE. Long term changes in augmentation, potentiation, and depression of transmitter release as a function of repeated synaptic activity at the frog neuromuscular junction. J Physiol 257: 471-494, 1976b.
35. Manabe T, Wyllie DJ, Perkel DJ, Nicoll RA. 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, 1993.
36. Markram H, Tsodyks M. Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature 382: 807-810, 1996.
37. Markram H, Wang Y, Tsodyks M. Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95: 5323-5328, 1998.
38. McNaughton BL. Long-term synaptic enhancement and short-term potentiation in rat fascia dentata act through different mechanisms. J Physiol 324: 249-262, 1982.
39. Millar AG, Zucker RS, Ellis-Davies GC, Charlton MP, Atwood HL. Calcium sensitivity of neurotransmitter release differs at phasic and tonic synapses. J Neurosci 25: 3113-3125, 2005.
40. Moulder KL, Mennerick S. Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons. J Neurosci 25: 3842-3850, 2005.
41. Nadim F, Manor Y, Kopell N, Marder E. Synaptic depression creates a switch that controls the frequency of an oscillatory circuit. Proc Natl Acad Sci USA 96: 8206-8211, 1999.
42. Natschlager T, Maass W, Zador A. Efficient temporal processing with biologically realistic dynamic synapses. Network 12: 75-87, 2001.
43. Neher E, Zucker RS. Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron 10: 21-30, 1993.
44. O'Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34: 171-175, 1971.
45. Otsu Y, Shahrezaei V, Li B, Raymond LA, Delaney KR, Murphy TH. Competition between phasic and asynchronous release for recovered synaptic vesicles at developing hippocampal autaptic synapses. J Neurosci 24: 420-433, 2004.
46. Raastad M, Storm JF, Andersen P. Putative single quantum and single fiber excitatory postsynaptic currents show similar amplitude range and variability in rat hippocampal slices. Eur J Neurosci 4: 113-117, 1992.
47. Ranck JB Jr. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol 41: 462-531, 1973.
48. Rosenmund C, Sigler A, Augustin I, Reim K, Brose N, Rhee JS. Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33: 411-424, 2002.
49. Rosenmund C, Stevens CF. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207, 1996.
50. Sabatini BL, Regehr WG. Optical measurement of presynaptic calcium currents. Biophys J 74: 1549-1563, 1998.
51. Sakaba T, Neher E. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32: 1119-1131, 2001a.
52. Sakaba T, Neher E. Quantitative relationship between transmitter release and calcium current at the calyx of held synapse. J Neurosci 21: 462-476, 2001b.
53. Schluter OM, Basu J, Sudhof TC, Rosenmund C. Rab3 superprimes synaptic vesicles for release: implications for short-term synaptic plasticity. J Neurosci 26: 1239-1246, 2006.
54. Silberberg G, Wu C, Markram H. Synaptic dynamics control the timing of neuronal excitation in the activated neocortical microcircuit. J Physiol 556: 19-27, 2004.
55. Stevens CF, Tsujimoto T. Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc Natl Acad Sci USA 92: 846-849, 1995.
56. Stevens CF, Wesseling JF. Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron 21: 415-424, 1998.
57. Stevens CF, Wesseling JF. Augmentation is a potentiation of the exocytotic process. Neuron 22: 139-146, 1999a.
58. Stevens CF, Wesseling JF. Identification of a novel process limiting the rate of synaptic vesicle cycling at hippocampal synapses. Neuron 24: 1017-1028, 1999b.
59. Stevens CF, Williams JH. Discharge of the readily releasable pool with action potentials at hippocampal synapses. J Neurophysiol 98: 3221-3229, 2007.
60. Toonen RF, Wierda K, Sons MS, de Wit H, Cornelisse LN, Brussaard A, Plomp JJ, Verhage M. Munc18-1 expression levels control synapse recovery by regulating readily releasable pool size. Proc Natl Acad Sci USA 103: 18332-18337, Epub 12006 Nov 18316, 2006.
61. Tsodyks MV, Markram H. The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci USA 94: 719-723, 1997.
62. Wadel K, Neher E, Sakaba T. The Coupling between synaptic vesicles and Ca(2+) channels determines fast neurotransmitter release. Neuron 53: 563-575, 2007.
63. Wang LY, Kaczmarek LK. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394: 384-388, 1998.
64. Wesseling JF, Lo DC. Limit on the role of activity in controlling the release-ready supply of synaptic vesicles. J Neurosci 22: 9708-9720, 2002.
65. Wierda KD, Toonen RF, de Wit H, Brussaard AB, Verhage M. Interdependence of PKC-dependent and PKC-independent pathways for presynaptic plasticity. Neuron 54: 275-290, 2007.
66. Wu LG, Borst JG. The reduced release probability of releasable vesicles during recovery from short-term synaptic depression. Neuron 23: 821-832, 1999.
67. Wu LG, Saggau P. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J Neurosci 14: 645-654, 1994.
68. Zengel JE, Magleby KL. Augmentation and facilitation of transmitter release. A quantitative description at the frog neuromuscular junction. J Gen Physiol 80: 583-611, 1982.
69. Zucker RS. Changes in the statistics of transmitter release during facilitation. J Physiol 229: 787-810, 1973.
70. Zucker RS. NCS-1 stirs somnolent synapses. Nat Neurosci 6: 1006-1008, 2003.
71. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405, 2002.