Recruitment of new sites of synaptic transmission during the cAMP- dependent late phase of LTP at CA3-CA1 synapses in the hippocampus

Neuron

Volumn 19, Issue 3, 1997, Pages 635-651

  Bolshakov, Vadim Y ^a   Golan, Hava ^a   Kandel, Eric R ^a   Siegelbaum, Steven A ^a  

^a Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOMYCIN; CALCIUM ION; CYCLIC AMP; NEUROTRANSMITTER; PROTEIN;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; LONG TERM POTENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; REFLEX RECRUITMENT; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 0030961082     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80377-3     Document Type: Article

References (66)

1. Abel, T., Nguyen, P.V., Barad, M., Deuel, T.A., Kandel, E.R., Bourtchouladze, R. (1997). Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88, 615-626.
2. Barnes, C.A. (1995). Involvement of LTP in memory: are we "searching under the street light"? Neuron 15, 751-754.
3. Bekkers, J.M., and Stevens, C.F. (1990). Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 346, 724-729.
4. Bekkers, J.M., Richerson, G.B., and Stevens, C.F. (1990). Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. Proc. Natl. Acad. Sci. USA 87, 5359-5362.
5. Blanton, M.G., Lo Turco, J.J., and Kriegstein, A.R. (1989). Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J. Neurosci. Meth. 30, 203-210.
6. Bliss, T.V.P., and Collingridge, G.L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
7. Blitzer, R.D., Wong, T., Nouranifar, R., Iyengar, R., and Landau, E.M. (1995). Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 15, 1403-1414.
8. Bolshakov, V.Y., and Siegelbaum, S.A. (1994). Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science 264, 1148-1152.
9. Bolshakov, V.Y., and Siegelbaum, S.A. (1995). Regulation of hippocampal transmitter release during development and long-term potentiation. Science 269, 1730-1734.
10. del Castillo, J., and Katz, B. (1954). Quantal components of the endplate potential. J. Physiol. 124, 560-573.
11. Dityatev, A.E., Kozhanov, V.M., Gapanovich, S.O., and Clamann, H.P. (1994). Quantal analysis based on spectral methods. Pflügers Arch. 429, 22-26.
12. Edwards, F. (1991). LTP is a long term problem. Nature 350, 271-272.
13. Edwards, F. (1995). LTP - a structural model to explain the inconsistencies. Trends Neurosci. 18, 250-255.
14. Fatt, P., and Katz, B. (1952). Spontaneous subthreshold activity at motor nerve endings. J. Physiol. 117, 109-128.
15. Foster, T.C., and McNaughton, B.L. (1991). Long-term enhancement of CA1 synaptic transmission is due to increased quantal size, not quantal content. Hippocampus 1, 79-91.
16. Frey, U., Krug, M., Reymann, K.G., and Matties, H. (1988). Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res. 452, 57-65.
17. Frey, U., Huang, Y.-Y., and Kandel, E.R. (1993). Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260, 1661-1664.
18. Geinisman, Y., de Toledo-Morrell, L., Morrell, F., Heller, R.E., Rossi, M., and Parshall, R.F. (1993). Structural synaptic correlate of long-term potentiation: formation of axospinous synapses with multiple, completely partitioned transmission. Hippocampus 3, 435-445.
19. Goda, Y., and Stevens, C.F. (1994). Two components of transmitter release at a central synapse. Proc. Natl. Acad. Sci. USA 91, 12942-12946.
20. Huang, Y.Y., and Kandel, E.R. (1994). Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn. Mem. 1, 74-82.
21. Huang, Y.Y., Nguyen, P.V., Abel, T., and Kandel, E.R. (1996a). Long lasting forms of synaptic potentiation in the mammalian hippocampus. Learn. Mem. 3, 74-85.
22. Huang, Y.Y., Bach, M.E., Lipp, H.P., Zhuo, M., Wolfer, D.P., Hawkins, R.D., Schoonjans, L., Kandel, E.R., Godfraind, J.M., Mulligan, R., Collen, D., and Carmeliet, P. (1996b). Mice lacking the gene encoding tissue-type plasminogen activator show a selective interference with late-phase long-term potentiation in both Schaffer collateral and mossy fiber pathways. Proc. Natl. Acad. Sci. USA 93, 8699-8704.
23. Impey, S., Mark, M., Villacres, E.G., Poser, S., Chavkin, C., and Storm, D.R. (1996). Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 16, 973-982.
24. Isaac, J.T.R., Nicoll, R.A., and Malenka, R.C. (1995). Evidence for silent synapses: implications for the expression of LTP. Neuron 15, 427-434.
25. Isaac, J.T., Hjelmstad, G.O., Nicoll, R.A., and Malenka, R.C. (1996). Long-term potentiation at single fiber inputs to hippocampal CA1 pyramidal cells. Proc. Natl. Acad. Sci. USA 93, 8710-8715.
26. Jack, J.J.B., Larkman, A.U., Major, G., and Stratford, K.J. (1994). Quantal analysis of the synaptic excitation of CA1 hippocampal pyramidal cells. In Molecular and Cellular Mechanisms of Neurotransmitter Release, L. Stjarne, P. Greengard, S. Grillner, T. Hokfelt, and D. Ottoson, eds. (New York: Raven Press, Ltd.), pp. 275-299.
27. Jonas, P., Major, G., and Sakmann, B. (1993). Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J. Physiol. 472, 615-663.
28. Korn, H., Bausela, F., Charpier, S., and Faber, D.S. (1993). Synaptic noise and multiquantal release at dendritic synapses. J. Neurophysiol. 70, 1249-1254.
29. Korn, H., Sur, C., Charpier, S., Legendre, P., and Faber, D.S. (1994). The one-vesicle hypothesis and multivesicular release. In Molecular and Cellular Mechanisms of Neurotransmitter Release, L. Stjarne, P. Greengard, S. Grillner, T. Hokfelt, and D. Ottoson, eds. (New York: Raven Press, Ltd.), pp. 301-322.
30. Kraszewski, K., and Grantyn, R. (1992). Unitary, quantal and miniature GABA-activated synaptic chloride currents in cultured neurons from the rat superior colliculus. Neuroscience 47, 555-570.
31. Kullman, D.M. (1994). Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: implications for long-term potentiation. Neuron 12, 1111-1120.
32. Kullmann, D.M., and Nicoll, R.A. (1992). Long-term potentiation is associated with increases in quantal content and quantal amplitude. Nature 357, 240-244.
33. Kullmann, D.M., and Siegelbaum, S.A. (1995). The site of expression of NMDA receptor-dependent LTP: new fuel for an old fire. Neuron 15, 997-1002.
34. Larkman, A.U., and Jack, J.J.B. (1995). Synaptic plasticity: hippocampal LTP. Curr. Opin. Neurobiol. 5, 324-334.
35. Larkman, A., Hannay, T., Stratford, K., and Jack, J. (1992). Presynaptic release probability influences the locus of long-term potentiation. Nature 360, 70-73.
36. Liao, D., Jones, A., and Malinow, R. (1992). Direct measurement of quantal changes underlying long-term potentiation in CA1 hippocampus. Neuron 9, 1089-1097.
37. Liao, D., Hessler, N.A., and Malinow, R. (1995). Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400-404.
38. Liley, A.W. (1957). Spontaneous release of transmitter substance in multiquantal units. J. Physiol. 136, 595-605.
39. Liu, G., and Tsien, R.W. (1995). Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 375, 404-408.
40. Malgaroli, A., and Tsien, R.W. (1992). Glutamate-induced long-term potentiation of the frequency of miniature synaptic currents in cultured hippocampal neurons. Nature 357, 134-139.
41. Malinow, R. (1991). Transmission between pairs of hippocampal slice neurons: quantal levels, oscillations, and LTP. Science 252, 722-724.
42. Malinow, R., and Tsien, R.W. (1990). Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346, 177-180.
43. Manabe, T., Renner, P., and Nicoll, R.A. (1992). Postsynaptic contribution to long-term potentiation revealed by the analysis of miniature synaptic currents. Nature 355, 50-55.
44. Matthies, H., and Reymann, K.G. (1993). Protein kinase A inhibitors prevent the maintenance of hippocampal long-term potentiation. Neuroreport 4, 712-714.
45. Mayford, M., Abel, T., and Kandel, E.R. (1995). Transgenic approaches to cognition. Curr. Opin. Neurobiol. 5, 141-148.
46. Melamed, N., Helm, P.J., and Rahamimoff, R. (1993). Confocal microscopy reveals coordinated calcium fluctuations and oscillations in synaptic boutons. J. Neurosci. 13, 632-649.
47. Miledi, R. (1966). Strontium as a substitute for calcium in the process of transmitter release at the neuromuscular junction. Nature 212, 1233-1235.
48. Nguyen, P.V., Abel, T., and Kandel, E.R. (1994). Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265, 1104-1107.
49. Nicoll, R.A., and Malenka, R.C. (1995). Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377, 115-118.
50. Oliet, S.H.R., Malenka, R.C., and Nicoll, R.A. (1996). Bidirectional control of quantal size by synaptic activity in the hippocampus. Science 271, 1294-1297.
51. Pockett, S., Slack, J.R., and Peacock, S. (1993). Cyclic AMP and long-term potentiation in the CA1 region of rat hippocampus. Neuroscience 52, 229-236.
52. Qi, M., Zhuo, M., Skålhegg, B.S., Brandon, E.P., Kandel, E.R., McKnight, G.S., and Idzerda, R.L. (1996). Impaired hippocampal plasticity in mice lacking the Cβ1 catalytic subunit of cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 93, 1571-1576.
53. Raastad, M., Storm, J.F., and Andersen, P. (1992). Putative single quantum and single fibre excitatory postsynaptic currents show similar amplitude range and variability in rat hippocampal slices. Eur. J. Neurosci. 4, 113-117.
54. Redman, S.J. (1990). Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol. Rev. 70, 165-198.
55. Silver, R.A., Cull-Candy, S.G., and 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.
56. Stevens, C.F., and Wang, Y. (1994). Changes in reliability of synaptic function as a mechanism for plasticity. Nature 377, 704-707.
57. Stevens, C.F., and Wang, Y. (1995). Facilitation and depression at single central synapses. Neuron 14, 795-802.
58. Stricker, C., and Redman, S.J. (1994). Statistical models of synaptic transmission valuated using the expectation-maximization algorithm. Biophys. J. 67, 656-670.
59. Stricker, C., Redman, S., and Daley, D. (1994). Statistical analysis of synaptic transmission: model discrimination and confidence limits. Biophys. J. 67, 532-547.
60. Stricker, C., Field, A.C., and Redman, S.J. (1996). Changes in quantal parameters of PSCs in rat CA1 neurones in vitro after the induction of long-term potentiation. J. Physiol. 490, 443-454.
61. Tang, C.-M., Margulis, M., Shi, Q.-Y., and Fielding, A. (1994). Saturation of postsynaptic glutamate receptors after quantal release of transmitter. Neuron 13, 1385-1393.
62. Thomas, M.J., Moody, T.D., Makhinson, M., and O'Dell, T.J. (1996). Activity dependent β-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 17, 475-482.
63. Tong, G., and Jahr, C.E. (1994). Multivesicular release from excitatory synapses of cultured hippocampal neurons. Neuron 12, 51-59.
64. Ulrich, D., and Luscher, H.R. (1993). Miniature excitatory synaptic currents corrected for dendritic cable properties reveal quantal size and variance. J. Neurophysiol. 69, 1769-1773.
65. Van Haastert, P.J., Van Driel, R., Jastorff, B., Baraniak, J., Stec, W.J., and De Wit, R.J. (1984). Competitive cAMP antagonists for cAMP-receptor proteins. J. Biol. Chem. 259, 10020-10024.
66. Zucker, R.S. (1988). Short-term synaptic plasticity. Annu. Rev. Neurosci. 12, 13-31.