State-Dependent Mechanisms of LTP Expression Revealed by Optical Quantal Analysis

Neuron

Volumn 52, Issue 4, 2006, Pages 649-661

  Ward, Bonnie ^a   McGuinness, Lindsay ^a   Akerman, Colin J ^a   Fine, Alan ^b,c   Bliss, Tim V P ^b   Emptage, Nigel J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

MOLNEURO; SIGNALING

Indexed keywords

ANIMALS; ANIMALS, NEWBORN; CALCIUM SIGNALING; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FLUORESCENT DYES; GLUTAMIC ACID; HIPPOCAMPUS; LONG-TERM POTENTIATION; MAGNESIUM; MALE; MEMBRANE FUSION; NEURAL PATHWAYS; OPTICS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 33751007005     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.10.007     Document Type: Article

References (74)

1. Antonova I., Arancio O., Trillat A.C., Wang H.G., Zablow L., Udo H., Kandel E.R., and Hawkins R.D. Rapid increase in clusters of presynaptic proteins at onset of long-lasting potentiation. Science 294 (2001) 1547-1550
2. Arancio O., Lev-Ram V., Tsien R.Y., Kandel E.R., and Hawkins R.D. Nitric oxide acts as a retrograde messenger during long-term potentiation in cultured hippocampal neurons. J. Physiol. (Paris) 90 (1996) 321-322
3. Archer III B.T., Ozcelik T., Jahn R., Francke U., and Sudhof T.C. Structures and chromosomal localizations of two human genes encoding synaptobrevins 1 and 2. J. Biol. Chem. 265 (1990) 17267-17273
4. Baumert M., Maycox P.R., Navone F., De Camilli P., and Jahn R. Synaptobrevin: an integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain. EMBO J. 8 (1989) 379-384
5. Bliss T.V., and Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361 (1993) 31-39
6. Bolshakov V.Y., and Siegelbaum S.A. Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science 264 (1994) 1148-1152
7. Broutman G., and Baudry M. Involvement of the secretory pathway for AMPA receptors in NMDA-induced potentiation in hippocampus. J. Neurosci. 21 (2001) 27-34
8. Choi S., Klingauf J., and Tsien R.W. Postfusional regulation of cleft glutamate concentration during LTP at 'silent synapses'. Nat. Neurosci. 3 (2000) 330-336
9. Choi S., Klingauf J., and Tsien R.W. Fusion pore modulation as a presynaptic mechanism contributing to expression of long-term potentiation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 (2003) 695-705
10. Clements J.D., Lester R.A., Tong G., Jahr C.E., and Westbrook G.L. The time course of glutamate in the synaptic cleft. Science 258 (1992) 1498-1501
11. Collingridge G.L., Herron C.E., and Lester R.A. Synaptic activation of N-methyl-D-aspartate receptors in the Schaffer collateral-commissural pathway of rat hippocampus. J. Physiol. 399 (1988) 283-300
12. Contractor A., Rogers C., Maron C., Henkemeyer M., Swanson G.T., and Heinemann S.F. Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296 (2002) 1864-1869
13. Durand G.M., Kovalchuk Y., and Konnerth A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381 (1996) 71-75
14. Dodge F.A., and Rahamimoff R. Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193 (1967) 419-432
15. Elferink L.A., Trimble W.S., and Scheller R.H. Two vesicle-associated membrane protein genes are differentially expressed in the rat central nervous system. J. Biol. Chem. 264 (1989) 11061-11064
16. Emptage N., Bliss T.V., and Fine A. Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 22 (1999) 115-124
17. Emptage N.J., Reid C.A., Fine A., and Bliss T.V. Optical quantal analysis reveals a presynaptic component of LTP at hippocampal Schaffer-associational synapses. Neuron 38 (2003) 797-804
18. Gasparini S., Saviane C., Voronin L.L., and Cherubini E. Silent synapses in the developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release?. Proc. Natl. Acad. Sci. USA 97 (2000) 9741-9746
19. Hayashi Y., Shi S.H., Esteban J.A., Piccini A., Poncer J.C., and Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287 (2000) 2262-2267
20. Isaac J.T. Postsynaptic silent synapses: evidence and mechanisms. Neuropharmacology 45 (2003) 450-460
21. Isaac J.T., Nicoll R.A., and Malenka R.C. Evidence for silent synapses: implications for the expression of LTP. Neuron 15 (1995) 427-434
22. Isaac J.T., Nicoll R.A., and Malenka R.C. Silent glutamatergic synapses in the mammalian brain. Can. J. Physiol. Pharmacol. 77 (1999) 735-737
23. Kauer J.S. Olfactory processing: a time and place for everything. Curr. Biol. 8 (1998) R282-R283
24. Kovalchuk Y., Eilers J., Lisman J., and Konnerth A. NMDA receptor-mediated subthreshold Ca(2+) signals in spines of hippocampal neurons. J. Neurosci. 20 (2000) 1791-1799
25. Kullmann D.M., and Siegelbaum S.A. The site of expression of NMDA receptor-dependent LTP: new fuel for an old fire. Neuron 15 (1995) 997-1002
26. Kullmann D.M. Silent synapses: what are they telling us about long-term potentiation?. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 (2003) 727-733
27. Lee H.K., Barbarosie M., Kameyama K., Bear M.F., and Huganir R.L. Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405 (2000) 955-959
28. Lester R.A., Clements J.D., Westbrook G.L., and Jahr C.E. Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature 346 (1990) 565-567
29. Li Y.X., Zhang Y., Lester H.A., Schuman E.M., and Davidson N. Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons. J. Neurosci. 18 (1998) 10231-10240
30. Liao D., Hessler N.A., and Malinow R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375 (1995) 400-404
31. Liao D., Scannevin R.H., and Huganir R. Activation of silent synapses by rapid activity-dependent synaptic recruitment of AMPA receptors. J. Neurosci. 21 (2001) 6008-6017
32. Link E., Edelmann L., Chou J.H., Binz T., Yamasaki S., Eisel U., Baumert M., Sudhof T.C., Niemann H., and Jahn R. Tetanus toxin action: inhibition of neurotransmitter release linked to synaptobrevin proteolysis. Biochem. Biophys. Res. Commun. 189 (1992) 1017-1023
33. Lledo P.M., Zhang X., Sudhof T.C., Malenka R.C., and Nicoll R.A. Postsynaptic membrane fusion and long-term potentiation. Science 279 (1998) 399-403
34. Mainen Z.F., Malinow R., and Svoboda K. Synaptic calcium transients in single spines indicate that NMDA receptors are not saturated. Nature 399 (1999) 151-155
35. Malenka R.C. Synaptic plasticity and AMPA receptor trafficking. Ann. N Y Acad. Sci. 1003 (2003) 1-11
36. Malenka R.C., and Nicoll R.A. Long-term potentiation-a decade of progress?. Science 285 (1999) 1870-1874
37. Maletic-Savatic M., Koothan T., and Malinow R. Calcium-evoked dendritic exocytosis in cultured hippocampal neurons. Part II: mediation by calcium/calmodulin-dependent protein kinase II. J. Neurosci. 18 (1998) 6814-6821
38. Malgaroli A., Ting A.E., Wendland B., Bergamaschi A., Villa A., Tsien R.W., and Scheller R.H. Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science 268 (1995) 1624-1628
39. Malinow R. AMPA receptor trafficking and long-term potentiation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 (2003) 707-714
40. Malinow R., Otmakhov N., Blum K.I., and Lisman J. Visualizing hippocampal synaptic function by optical detection of Ca2+ entry through the N-methyl-D-aspartate channel. Proc. Natl. Acad. Sci. USA 91 (1994) 8170-8174
41. Mayer M.L., Westbrook G.L., and Guthrie P.B. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 309 (1984) 261-263
42. McLaughlin A., Grathwohl C., and McLaughlin S. The adsorption of divalent cations to phosphatidylcholine bilayer membranes. Biochim. Biophys. Acta 513 (1978) 338-357
43. Montgomery J.M., and Madison D.V. State-dependent heterogeneity in synaptic depression between pyramidal cell pairs. Neuron 33 (2002) 765-777
44. Montgomery J.M., Pavlidis P., and Madison D.V. Pair recordings reveal all-silent synaptic connections and the postsynaptic expression of long-term potentiation. Neuron 29 (2001) 691-701
45. Muller W., and Connor J.A. Dendritic spines as individual neuronal compartments for synaptic Ca2+ responses. Nature 354 (1991) 73-76
46. Muller D., and Lynch G. Long-term potentiation differentially affects two components of synaptic responses in hippocampus. Proc. Natl. Acad. Sci. USA 85 (1988) 9346-9350
47. Nicoll R.A. Expression mechanisms underlying long-term potentiation: a postsynaptic view. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 (2003) 721-726
48. Nishimune A., Isaac J.T., Molnar E., Noel J., Nash S.R., Tagaya M., Collingridge G.L., Nakanishi S., and Henley J.M. NSF binding to GluR2 regulates synaptic transmission. Neuron 21 (1998) 87-97
49. Nowak L., Bregestovski P., Ascher P., Herbet A., and Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307 (1984) 462-465
50. Oertner T.G., Sabatini B.L., Nimchinsky E.A., and Svoboda K. Facilitation at single synapses probed with optical quantal analysis. Nat. Neurosci. 5 (2002) 657-664
51. Passafaro M., Piech V., and Sheng M. Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat. Neurosci. 4 (2001) 917-926
52. Perkel D.J., and Nicoll R.A. Evidence for all-or-none regulation of neurotransmitter release: implications for long-term potentiation. J. Physiol. 471 (1993) 481-500
53. Portis A., Newton C., Pangborn W., and Papahadjopoulos D. Studies on the mechanism of membrane fusion: evidence for an intermembrane Ca2+-phospholipid complex, synergism with Mg2+, and inhibition by spectrin. Biochemistry 18 (1979) 780-790
54. Pothos E.N., Przedborski S., Davila V., Schmitz Y., and Sulzer D. D2-Like dopamine autoreceptor activation reduces quantal size in PC12 cells. J. Neurosci. 18 (1998) 5575-5585
55. Reid C.A., Fabian-Fine R., and Fine A. Postsynaptic calcium transients evoked by activation of individual hippocampal mossy fiber synapses. J. Neurosci. 21 (2001) 2206-2214
56. Reid C.A., Dixon D.B., Takahashi M., Bliss T.V., and Fine A. Optical quantal analysis indicates that long-term potentiation at single hippocampal mossy fiber synapses is expressed through increased release probability, recruitment of new release sites, and activation of silent synapses. J. Neurosci. 24 (2004) 3618-3626
57. Rumpel S., Hatt H., and Gottmann K. Silent synapses in the developing rat visual cortex: evidence for postsynaptic expression of synaptic plasticity. J. Neurosci. 18 (1998) 8863-8874
58. Schiavo G., Benfenati F., Poulain B., Rossetto O., Polverino de Laureto P., DasGupta B.R., and Montecucco C. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359 (1992) 832-835
59. Schoch S., Deak F., Konigstorfer A., Mozhayeva M., Sara Y., Sudhof T.C., and Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294 (2001) 1117-1122
60. Schuman E.M., and Madison D.V. Nitric oxide and synaptic function. Annu. Rev. Neurosci. 17 (1994) 153-183
61. Shi S.H., Hayashi Y., Petralia R.S., Zaman S.H., Wenthold R.J., Svoboda K., and Malinow R. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284 (1999) 1811-1816
62. Sollner T., Whiteheart S.W., Brunner M., Erdjument-Bromage H., Geromanos S., Tempst P., and Rothman J.E. SNAP receptors implicated in vesicle targeting and fusion. Nature 362 (1993) 318-324
63. Stoop R., and Poo M.M. Synaptic modulation by neurotrophic factors: differential and synergistic effects of brain-derived neurotrophic factor and ciliary neurotrophic factor. J. Neurosci. 16 (1996) 3256-3264
64. Stoppini L., Buchs P.A., and Muller D. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37 (1991) 173-182
65. Sudhof T.C. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375 (1995) 645-653
66. Torres R., Firestein B.L., Dong H., Staudinger J., Olson E.N., Huganir R.L., Bredt D.S., Gale N.W., and Yancopoulos G.D. PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 21 (1998) 1453-1463
67. Wang S., Prange O., and Murphy T.H. Amplification of calcium signals at dendritic spines provides a method for CNS quantal analysis. Can. J. Physiol. Pharmacol. 77 (1999) 651-659
68. Williams J.H., Errington M.L., Lynch M.A., and Bliss T.V. Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in the hippocampus. Nature 341 (1989) 739-742
69. Xiao M.Y., Wasling P., Hanse E., and Gustafsson B. Creation of AMPA-silent synapses in the neonatal hippocampus. Nat. Neurosci. 7 (2004) 236-243
70. Yamamoto N., Kurotani T., and Toyama K. Neural connections between the lateral geniculate nucleus and visual cortex in vitro. Science 245 (1989) 192-194
71. Yuste R., and Denk W. Dendritic spines as basic functional units of neuronal integration. Nature 375 (1995) 682-684
72. Yuste R., Majewska A., Cash S.S., and Denk W. Mechanisms of calcium influx into hippocampal spines: heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis. J. Neurosci. 19 (1999) 1976-1987
73. Zakharenko S.S., Zablow L., and Siegelbaum S.A. Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat. Neurosci. 4 (2001) 711-717
74. Zhuo M., Zhang W., Son H., Mansuy I., Sobel R.A., Seidman J., and Kandel E.R. A selective role of calcineurin aalpha in synaptic depotentiation in hippocampus. Proc. Natl. Acad. Sci. USA 96 (1999) 4650-4655