Synapse-specific stabilization of plasticity processes: The synaptic tagging and capture hypothesis revisited 10 years later

Neuroscience and Biobehavioral Reviews

Volumn 32, Issue 4, 2008, Pages 831-851

  Barco, Angel ^a   Lopez de Armentia, Mikel ^a   Alarcon, Juan M ^b  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

Associative learning; LTP; Metaplasticity; Neuronal computation; Synaptic capture; Synaptic plasticity; Synaptic tagging

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; IONOTROPIC RECEPTOR; NEUROTROPHIN; PROTEIN KINASE; PROTEIN KINASE (CALCIUM,CALMODULIN);

ASSOCIATIVE MEMORY; BRAIN REGION; CELLULAR DISTRIBUTION; ELECTROPHYSIOLOGY; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; LONG TERM POTENTIATION; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; SENSITIZATION; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; SYNAPTIC MEMBRANE;

ANIMALS; COMPUTER SIMULATION; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; PROTEIN KINASES; SYNAPSES;

EID: 40149084151     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2008.01.002     Document Type: Review

References (150)

1. Aakalu G., Smith W.B., Nguyen N., Jiang C., and Schuman E.M. Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30 (2001) 489-502
2. Abraham W.C., and Williams J.M. LTP maintenance and its protein synthesis-dependence. Neurobiology of Learning and Memory (2007)
3. Abraham W.C., Logan B., Greenwood J.M., and Dragunow M. Induction and experience-dependent consolidation of stable long-term potentiation lasting months in the hippocampus. Journal of Neuroscience 22 (2002) 9626-9634
4. Adams J.P., Anderson A.E., Varga A.W., Dineley K.T., Cook R.G., Pfaffinger P.J., and Sweatt J.D. The A-type potassium channel Kv4.2 is a substrate for the mitogen-activated protein kinase ERK. Journal of Neurochemistry 75 (2000) 2277-2287
5. Ahmed T., Frey J.U., and Korz V. Long-term effects of brief acute stress on cellular signaling and hippocampal LTP. Journal of Neuroscience 26 (2006) 3951-3958
6. Alarcon J.M., Hodgman R., Theis M., Huang Y.S., Kandel E.R., and Richter J.D. Selective modulation of some forms of schaffer collateral-CA1 synaptic plasticity in mice with a disruption of the CPEB-1 gene. Learn Memory 11 (2004) 318-327
7. Alarcon J.M., Barco A., and Kandel E.R. Capture of the late phase of long-term potentiation within and across the apical and basilar dendritic compartments of CA1 pyramidal neurons: synaptic tagging is compartment restricted. Journal of Neuroscience 26 (2006) 256-264
8. Albensi B.C., and Mattson M.P. Evidence for the involvement of TNF and NF-kappaB in hippocampal synaptic plasticity. Synapse 35 (2000) 151-159
9. Amaral D.G., and Witter M.P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31 (1989) 571-591
10. Anderson A.E., Adams J.P., Qian Y., Cook R.G., Pfaffinger P.J., and Sweatt J.D. Kv4.2 phosphorylation by cyclic AMP-dependent protein kinase. Journal of Biological Chemistry 275 (2000) 5337-5346
11. Balschun D., Wolfer D.P., Gass P., Mantamadiotis T., Welzl H., Schutz G., Frey J.U., and Lipp H.P. Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory?. Journal of Neuroscience 23 (2003) 6304-6314
12. Banko J.L., Poulin F., Hou L., DeMaria C.T., Sonenberg N., and Klann E. The translation repressor 4E-BP2 is critical for eIF4F complex formation, synaptic plasticity, and memory in the hippocampus. Journal of Neuroscience 25 (2005) 9581-9590
13. Banko J.L., Hou L., Poulin F., Sonenberg N., and Klann E. Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. Journal of Neuroscience 26 (2006) 2167-2173
14. Barco A., and Kandel E.R. Role of CREB and CBP in brain function. In: Thiel G. (Ed). Transcription Factors in the Nervous System: Development, Brain Function and Disease (2005), Wiley-VCH publishers
15. Barco A., Alarcon J.M., and Kandel E.R. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108 (2002) 689-703
16. Barco A., Patterson S., Alarcon J.M., Gromova P., Mata-Roig M., Morozov A., and Kandel E.R. Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture. Neuron 48 (2005) 123-137
17. Barco A., Jancic D., and Kandel E.R. CREB-dependent transcription and synaptic plasticity. In: Dudek S. (Ed). Regulation of Transcription by Neuronal Activity: To the Nucleus and Back (2007), Springer Science Publishers
18. Barondes S.H., and Jarvik M.E. The influence of actinomycin-D on brain Rna synthesis and on memory. Journal of Neurochemistry 11 (1964) 187-195
19. Berke J.D., and Hyman S.E. Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25 (2000) 515-532
20. Carroll R.C., and Malenka R.C. Delivering the goods to synapses. Nature Neuroscience 3 (2000) 1064-1066
21. Casadio A., Martin K.C., Giustetto M., Zhu H., Chen M., Bartsch D., Bailey C.H., and Kandel E.R. A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99 (1999) 221-237
22. Cohen A.S., Coussens C.M., Raymond C.R., and Abraham W.C. Long-lasting increase in cellular excitability associated with the priming of LTP induction in rat hippocampus. Journal of Neurophysiology 82 (1999) 3139-3148
23. Colicos M.A., Collins B.E., Sailor M.J., and Goda Y. Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107 (2001) 605-616
24. Costa-Mattioli M., Gobert D., Harding H., Herdy B., Azzi M., Bruno M., Bidinosti M., Ben Mamou C., Marcinkiewicz E., Yoshida M., Imataka H., Cuello A.C., Seidah N., Sossin W., Lacaille J.C., Ron D., Nader K., and Sonenberg N. Translational control of hippocampal synaptic plasticity and memory by the eIF2alpha kinase GCN2. Nature 436 (2005) 1166-1173
25. Costa-Mattioli M., Gobert D., Stern E., Gamache K., Colina R., Cuello C., Sossin W., Kaufman R., Pelletier J., Rosenblum K., Krnjevic K., Lacaille J.C., Nader K., and Sonenberg N. eIF2alpha phosphorylation bidirectionally regulates the switch from short- to long-term synaptic plasticity and memory. Cell 129 (2007) 195-206
26. Cracco J.B., Serrano P., Moskowitz S.I., Bergold P.J., and Sacktor T.C. Protein synthesis-dependent LTP in isolated dendrites of CA1 pyramidal cells. Hippocampus 15 (2005) 551-556
27. Deng P., Zhang Y., and Xu Z.C. Involvement of I(h) in dopamine modulation of tonic firing in striatal cholinergic interneurons. Journal of Neuroscience 27 (2007) 3148-3156
28. Deuchars J., and Thomson A.M. CA1 pyramid-pyramid connections in rat hippocampus in vitro: dual intracellular recordings with biocytin filling. Neuroscience 74 (1996) 1009-1018
29. Dolleman-Van Der Weel M.J., and Witter M.P. Projections from the nucleus reuniens thalami to the entorhinal cortex, hippocampal field CA1, and the subiculum in the rat arise from different populations of neurons. Journal of Comparative Neurology 364 (1996) 637-650
30. Dong Y., Green T., Saal D., Marie H., Neve R., Nestler E.J., and Malenka R.C. CREB modulates excitability of nucleus accumbens neurons. Nature Neuroscience 9 (2006) 475-477
31. Dudek S.M., and Fields R.D. Somatic action potentials are sufficient for late-phase LTP-related cell signaling. Proceedings of the National Academy of Sciences USA 99 (2002) 3962-3967
32. Flexner J.B., Flexner L.B., Stellar E., De La Haba G., and Roberts R.B. Inhibition of protein synthesis in brain and learning and memory following puromycin. Journal of Neurochemistry 9 (1962) 595-605
33. Flexner L.B., Flexner J.B., and Stellar E. Memory and cerebral protein synthesis in mice as affected by graded amounts of puromycin. Experimental Neurology 13 (1965) 264-272
34. Fonseca R., Nagerl U.V., Morris R.G., and Bonhoeffer T. Competing for memory: hippocampal LTP under regimes of reduced protein synthesis. Neuron 44 (2004) 1011-1020
35. Fonseca R., Vabulas R.M., Hartl F.U., Bonhoeffer T., and Nagerl U.V. A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron 52 (2006) 239-245
36. Frey U., and Morris R.G. Synaptic tagging and long-term potentiation. Nature 385 (1997) 533-536
37. Frey U., and Morris R.G. Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation [see comments]. Trends in Neurosciences 21 (1998) 181-188
38. Frey U., and Morris R.G. Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37 (1998) 545-552
39. Frey U., Krug M., Reymann K.G., and Matthies H. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Research 452 (1988) 57-65
40. Frey U., Schroeder H., and Matthies H. Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices. Brain Research 522 (1990) 69-75
41. Frey U., Matthies H., and Reymann K.G. The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neuroscience Letters 129 (1991) 111-114
42. Frey U., Frey S., Schollmeier F., and Krug M. Influence of actinomycin D, a RNA synthesis inhibitor, on long-term potentiation in rat hippocampal neurons in vivo and in vitro. Journal of Physiology 490 Part 3 (1996) 703-711
43. Frick A., Magee J., and Johnston D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nature Neuroscience 7 (2004) 126-135
44. Fuenzalida M., Fernandez de Sevilla D., and Buno W. Changes of the EPSP waveform regulate the temporal window for spike-timing-dependent plasticity. Journal of Neuroscience 27 (2007) 11,940-11,948
45. Gelinas J.N., and Nguyen P.V. Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. Journal of Neuroscience 25 (2005) 3294-3303
46. Giustetto M., Hegde A.N., Si K., Casadio A., Inokuchi K., Pei W., Kandel E.R., and Schwartz J.H. Axonal transport of eukaryotic translation elongation factor 1alpha mRNA couples transcription in the nucleus to long-term facilitation at the synapse. Proceedings of the National Academy of Sciences USA 100 (2003) 13,680-13,685
47. Govindarajan A., Kelleher R.J., and Tonegawa S. A clustered plasticity model of long-term memory engrams. Nature Reviews Neuroscience 7 (2006) 575-583
48. Guan Z., Giustetto M., Lomvardas S., Kim J.H., Miniaci M.C., Schwartz J.H., Thanos D., and Kandel E.R. Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111 (2002) 483-493
49. Han M.H., Bolanos C.A., Green T.A., Olson V.G., Neve R.L., Liu R.J., Aghajanian G.K., and Nestler E.J. Role of cAMP response element-binding protein in the rat locus ceruleus: regulation of neuronal activity and opiate withdrawal behaviors. Journal of Neuroscience 26 (2006) 4624-4629
50. Hassan H., Frey S., and Frey J.U. Search for a two-input model for future investigations of 'synaptic tagging' in freely moving animals in vivo. Journal of Neuroscience Methods 152 (2006) 220-228
51. Haug T., and Storm J.F. Protein kinase A mediates the modulation of the slow Ca(2+)-dependent K(+) current, I(sAHP), by the neuropeptides CRF, VIP, and CGRP in hippocampal pyramidal neurons. Journal of Neurophysiology 83 (2000) 2071-2079
52. Hay N., and Sonenberg N. Upstream and downstream of mTOR. Genes & Development 18 (2004) 1926-1945
53. Hegde A.N., Inokuchi K., Pei W., Casadio A., Ghirardi M., Chain D.G., Martin K.C., Kandel E.R., and Schwartz J.H. Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89 (1997) 115-126
54. Horton A.C., Racz B., Monson E.E., Lin A.L., Weinberg R.J., and Ehlers M.D. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48 (2005) 757-771
55. Hu H., Real E., Takamiya K., Kang M.G., Ledoux J., Huganir R.L., and Malinow R. Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell 131 (2007) 160-173
56. Huang F., Chotiner J.K., and Steward O. The mRNA for elongation factor 1alpha is localized in dendrites and translated in response to treatments that induce long-term depression. Journal of Neuroscience 25 (2005) 7199-7209
57. Huang T., McDonough C.B., and Abel T. Compartmentalized PKA signaling events are required for synaptic tagging and capture during hippocampal late-phase long-term potentiation. European Journal of Cell Biology 85 (2006) 635-642
58. Huang Y.S., Jung M.Y., Sarkissian M., and Richter J.D. N-methyl-d-aspartate receptor signaling results in Aurora kinase-catalyzed CPEB phosphorylation and alpha CaMKII mRNA polyadenylation at synapses. Embo Journal 21 (2002) 2139-2148
59. Huang Y.S., Carson J.H., Barbarese E., and Richter J.D. Facilitation of dendritic mRNA transport by CPEB. Genes & Development 17 (2003) 638-653
60. Huang Y.Y., and Kandel E.R. Theta frequency stimulation induces a local form of late phase LTP in the CA1 region of the hippocampus. Learn Memory 12 (2005) 587-593
61. Ishizuka N., Weber J., and Amaral D.G. Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. Journal of Comparative Neurology 295 (1990) 580-623
62. Izquierdo I., and Cammarota M. Neuroscience. Zif and the survival of memory. Science 304 (2004) 829-830
63. Jarsky T., Roxin A., Kath W.L., and Spruston N. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nature Neuroscience 8 (2005) 1667-1676
64. Johnston D., Christie B.R., Frick A., Gray R., Hoffman D.A., Schexnayder L.K., Watanabe S., and Yuan L.L. Active dendrites, potassium channels and synaptic plasticity. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 358 (2003) 667-674
65. Kanai Y., Dohmae N., and Hirokawa N. Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43 (2004) 513-525
66. Kandel E.R. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294 (2001) 1030-1038
67. Kauderer B.S., and Kandel E.R. Capture of a protein synthesis-dependent component of long-term depression. Proceedings of the National Academy of Sciences USA 97 (2000) 13,342-13,347
68. Keleman K., Kruttner S., Alenius M., and Dickson B.J. Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nature Neuroscience 10 (2007) 1587-1593
69. Kelleher III R.J., Govindarajan A., Jung H.Y., Kang H., and Tonegawa S. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116 (2004) 467-479
70. Kelleher III R.J., Govindarajan A., and Tonegawa S. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44 (2004) 59-73
71. Kiebler M.A., and Bassell G.J. Neuronal RNA granules: movers and makers. Neuron 51 (2006) 685-690
72. Klann E., and Dever T.E. Biochemical mechanisms for translational regulation in synaptic plasticity. Nature Reviews Neuroscience 5 (2004) 931-942
73. Klann E., and Sweatt J.D. Altered protein synthesis is a trigger for long-term memory formation. Neurobiology of Learning and Memory (2007)
74. Korz V., and Frey J.U. Hormonal and monoamine signaling during reinforcement of hippocampal long-term potentiation and memory retrieval. Learn Memory 14 (2007) 160-166
75. Kotz K.J., and McNiven M.A. Intracellular calcium and cAMP regulate directional pigment movements in teleost erythrophores. Journal of Cell Biology 124 (1994) 463-474
76. Lang C., Barco A., Zablow L., Kandel E.R., Siegelbaum S.A., and Zakharenko S.S. Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. Proceedings of the National Academy of Sciences USA 101 (2004) 16,665-16,670
77. Levenson J.M., O'Riordan K.J., Brown K.D., Trinh M.A., Molfese D.L., and Sweatt J.D. Regulation of histone acetylation during memory formation in the hippocampus. Journal of Biological Chemistry 279 (2004) 40,545-40,559
78. Ling D.S., Benardo L.S., Serrano P.A., Blace N., Kelly M.T., Crary J.F., and Sacktor T.C. Protein kinase Mzeta is necessary and sufficient for LTP maintenance. Nature Neuroscience 5 (2002) 295-296
79. Ling D.S., Benardo L.S., and Sacktor T.C. Protein kinase Mzeta enhances excitatory synaptic transmission by increasing the number of active postsynaptic AMPA receptors. Hippocampus 16 (2006) 443-452
80. Lonze B.E., and Ginty D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35 (2002) 605-623
81. Lopez de Armentia M., Jancic D., Olivares R., Alarcon J.M., Kandel E.R., and Barco A. cAMP response element-binding protein-mediated gene expression increases the intrinsic excitability of CA1 pyramidal neurons. Journal of Neuroscience 27 50 (2007) 13909-13918
82. Lu Y., Christian K., and Lu B. BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory?. Neurobiology of Learning and Memory (2007)
83. Luo L. Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annual Review of Cell and Developmental Biology 18 (2002) 601-635
84. Magee J.C. Dendritic integration of excitatory synaptic input. Nature Reviews Neuroscience 1 (2000) 181-190
85. Magee J.C., and Johnston D. Plasticity of dendritic function. Current Opinion in Neurobiology 15 (2005) 334-342
86. Malinow R., and Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annual Review of Neuroscience 25 (2002) 103-126
87. Malinow R., Mainen Z.F., and Hayashi Y. LTP mechanisms: from silence to four-lane traffic. Current Opinion in Neurobiology 10 (2000) 352-357
88. Marie H., Morishita W., Yu X., Calakos N., and Malenka R.C. Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45 (2005) 741-752
89. Martin K.C., and Kosik K.S. Synaptic tagging-who's it?. Nature Reviews Neuroscience 3 (2002) 813-820
90. Martin K.C., Casadio A., Zhu H.E.Y., Rose J.C., Chen M., Bailey C.H., and Kandel E.R. Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91 (1997) 927-938
91. Martin K.C., Barad M., and Kandel E.R. Local protein synthesis and its role in synapse-specific plasticity. Current Opinion in Neurobiology 10 (2000) 587-592
92. Martin S.J., Grimwood P.D., and Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annual Review of Neuroscience 23 (2000) 649-711
93. Moncada D., and Viola H. Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. Journal of Neuroscience 27 (2007) 7476-7481
94. Montarolo P.G., Goelet P., Castellucci V.F., Morgan J., Kandel E.R., and Schacher S. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234 (1986) 1249-1254
95. Morris R.G. Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. European Journal of Neuroscience 23 (2006) 2829-2846
96. Navakkode S., Sajikumar S., and Frey J.U. The type IV-specific phosphodiesterase inhibitor rolipram and its effect on hippocampal long-term potentiation and synaptic tagging. Journal of Neuroscience 24 (2004) 7740-7744
97. Navakkode S., Sajikumar S., and Frey J.U. Mitogen-activated protein kinase-mediated reinforcement of hippocampal early long-term depression by the type IV-specific phosphodiesterase inhibitor rolipram and its effect on synaptic tagging. Journal of Neuroscience 25 (2005) 10,664-10,670
98. Navakkode S., Sajikumar S., and Frey J.U. Synergistic requirements for the induction of dopaminergic D1/D5-receptor-mediated LTP in hippocampal slices of rat CA1 in vitro. Neuropharmacology 52 (2007) 1547-1554
99. Nguyen P.V., and Kandel E.R. A macromolecular synthesis-dependent late phase of long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. Journal of Neuroscience 16 (1996) 3189-3198
100. Nguyen P.V., Abel T., and Kandel E.R. Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265 (1994) 1104-1107
101. Nicholson D.A., Trana R., Katz Y., Kath W.L., Spruston N., and Geinisman Y. Distance-dependent differences in synapse number and AMPA receptor expression in hippocampal CA1 pyramidal neurons. Neuron 50 (2006) 431-442
102. Nie T., McDonough C.B., Huang T., Nguyen P.V., and Abel T. Genetic disruption of protein kinase A anchoring reveals a role for compartmentalized kinase signaling in theta-burst long-term potentiation and spatial memory. Journal of Neuroscience 27 (2007) 10,278-10,288
103. O'Carroll C.M., and Morris R.G. Heterosynaptic co-activation of glutamatergic and dopaminergic afferents is required to induce persistent long-term potentiation. Neuropharmacology 47 (2004) 324-332
104. Ostroff L.E., Fiala J.C., Allwardt B., and Harris K.M. Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35 (2002) 535-545
105. Otani S., Marshall C.J., Tate W.P., Goddard G.V., and Abraham W.C. Maintenance of long-term potentiation in rat dentate gyrus requires protein synthesis but not messenger RNA synthesis immediately post-tetanization. Neuroscience 28 (1989) 519-526
106. Ouyang Y., Kantor D., Harris K.M., Schuman E.M., and Kennedy M.B. Visualization of the distribution of autophosphorylated calcium/calmodulin-dependent protein kinase II after tetanic stimulation in the CA1 area of the hippocampus. Journal of Neuroscience 17 (1997) 5416-5427
107. Ouyang Y., Rosenstein A., Kreiman G., Schuman E.M., and Kennedy M.B. Tetanic stimulation leads to increased accumulation of Ca(2+)/calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. Journal of Neuroscience 19 (1999) 7823-7833
108. Pastalkova E., Serrano P., Pinkhasova D., Wallace E., Fenton A.A., and Sacktor T.C. Storage of spatial information by the maintenance mechanism of LTP. Science 313 (2006) 1141-1144
109. Pedarzani P., and Storm J.F. PKA mediates the effects of monoamine transmitters on the K+ current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron 11 (1993) 1023-1035
110. Pedarzani P., and Storm J.F. Dopamine modulates the slow Ca(2+)-activated K+ current IAHP via cyclic AMP-dependent protein kinase in hippocampal neurons. Journal of Neurophysiology 74 (1995) 2749-2753
111. Pikkarainen M., Ronkko S., Savander V., Insausti R., and Pitkanen A. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. Journal of Comparative Neurology 403 (1999) 229-260
112. Plant K., Pelkey K.A., Bortolotto Z.A., Morita D., Terashima A., McBain C.J., Collingridge G.L., and Isaac J.T. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nature Neuroscience 9 (2006) 602-604
113. Purcell A.L., Sharma S.K., Bagnall M.W., Sutton M.A., and Carew T.J. Activation of a tyrosine kinase-MAPK cascade enhances the induction of long-term synaptic facilitation and long-term memory in Aplysia. Neuron 37 (2003) 473-484
114. Ramanan N., Shen Y., Sarsfield S., Lemberger T., Schutz G., Linden D.J., and Ginty D.D. SRF mediates activity-induced gene expression and synaptic plasticity but not neuronal viability. Nature Neuroscience 8 (2005) 759-767
115. Raymond C.R., and Redman S.J. Different calcium sources are narrowly tuned to the induction of different forms of LTP. Journal of Neurophysiology 88 (2002) 249-255
116. Raymond C.R., and Redman S.J. Spatial segregation of neuronal calcium signals encodes different forms of LTP in rat hippocampus. Journal of Physiology 570 (2006) 97-111
117. Reymann K.G., and Frey J.U. The late maintenance of hippocampal LTP: requirements, phases, 'synaptic tagging', 'late-associativity' and implications. Neuropharmacology 52 (2007) 24-40
118. Richter J.D. Think globally, translate locally: what mitotic spindles and neuronal synapses have in common. Proceedings of the National Academy of Sciences USA 98 (2001) 7069-7071
119. Rodionov V., Yi J., Kashina A., Oladipo A., and Gross S.P. Switching between microtubule- and actin-based transport systems in melanophores is controlled by cAMP levels. Current Biology 13 (2003) 1837-1847
120. Rolls E.T., and Kesner R.P. A computational theory of hippocampal function, and empirical tests of the theory. Progress in Neurobiology 79 (2006) 1-48
121. Routtenberg A. Tagging the Hebb synapse. Trends in Neuroscience 22 (1999) 255-256
122. Sah P., and Bekkers J.M. Apical dendritic location of slow afterhyperpolarization current in hippocampal pyramidal neurons: implications for the integration of long-term potentiation. Journal of Neuroscience 16 (1996) 4537-4542
123. Sajikumar S., and Frey J.U. Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD. Neurobiology of Learning and Memory 82 (2004) 12-25
124. Sajikumar S., and Frey J.U. Resetting of 'synaptic tags' is time- and activity-dependent in rat hippocampal CA1 in vitro. Neuroscience 129 (2004) 503-507
125. Sajikumar S., Navakkode S., Sacktor T.C., and Frey J.U. Synaptic tagging and cross-tagging: the role of protein kinase Mzeta in maintaining long-term potentiation but not long-term depression. Journal of Neuroscience 25 (2005) 5750-5756
126. Sajikumar S., Navakkode S., and Frey J.U. Identification of compartment- and process-specific molecules required for "synaptic tagging" during long-term potentiation and long-term depression in hippocampal CA1. Journal of Neuroscience 27 (2007) 5068-5080
127. Sajikumar S., Navakkode S., Korz V., and Frey J.U. Cognitive and emotional information processing: protein synthesis versus gene expression. Journal of Physiology (2007)
128. Sanchez C., Diaz-Nido J., and Avila J. Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Progress in Neurobiology 61 (2000) 133-168
129. Seidenbecher T., Balschun D., and Reymann K.G. Drinking after water deprivation prolongs "unsaturated" LTP in the dentate gyrus of rats. Physiology & Behavior 57 (1995) 1001-1004
130. Seidenbecher T., Reymann K.G., and Balschun D. A post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli. Proceedings of the National Academy of Sciences USA 94 (1997) 1494-1499
131. Shakiryanova D., Tully A., and Levitan E.S. Activity-dependent synaptic capture of transiting peptidergic vesicles. Nature Neuroscience 9 (2006) 896-900
132. Si K., Giustetto M., Etkin A., Hsu R., Janisiewicz A.M., Miniaci M.C., Kim J.H., Zhu H., and Kandel E.R. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in aplysia. Cell 115 (2003) 893-904
133. Si K., Lindquist S., and Kandel E.R. A neuronal isoform of the aplysia CPEB has prion-like properties. Cell 115 (2003) 879-891
134. Smolen P., Baxter D.A., and Byrne J.H. A model of the roles of essential kinases in the induction and expression of late long-term potentiation. Biophysical Journal 90 (2006) 2760-2775
135. Song H., Smolen P., Av-Ron E., Baxter D.A., and Byrne J.H. Bifurcation and singularity analysis of a molecular network for the induction of long-term memory. Biophysical Journal 90 (2006) 2309-2325
136. Steward O., and Halpain S. Lamina-specific synaptic activation causes domain-specific alterations in dendritic immunostaining for MAP2 and CAM kinase II. Journal of Neuroscience 19 (1999) 7834-7845
137. Steward O., Wallace C.S., Lyford G.L., and Worley P.F. Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21 (1998) 741-751
138. Straube T., Korz V., Balschun D., and Frey J.U. Requirement of beta-adrenergic receptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus. Journal of Physiology 552 (2003) 953-960
139. Straube T., Korz V., and Frey J.U. Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus. Neuroscience Letters 344 (2003) 5-8
140. Sutton M.A., and Schuman E.M. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127 (2006) 49-58
141. Theis M., Si K., and Kandel E.R. Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus. Proceedings of the National Academy of Sciences USA 100 (2003) 9602-9607
142. Tischmeyer W., and Grimm R. Activation of immediate early genes and memory formation. Cellular and Molecular Life Sciences 55 (1999) 564-574
143. Tzingounis A.V., and Nicoll R.A. Arc/Arg3.1: linking gene expression to synaptic plasticity and memory. Neuron 52 (2006) 403-407
144. Vickers C.A., Dickson K.S., and Wyllie D.J. Induction and maintenance of late-phase long-term potentiation in isolated dendrites of rat hippocampal CA1 pyramidal neurones. Journal of Physiology 568 (2005) 803-813
145. Wells D.G., Dong X., Quinlan E.M., Huang Y.S., Bear M.F., Richter J.D., and Fallon J.R. A role for the cytoplasmic polyadenylation element in NMDA receptor-regulated mRNA translation in neurons. Journal of Neuroscience 21 (2001) 9541-9548
146. Wu L., Wells D., Tay J., Mendis D., Abbott M.A., Barnitt A., Quinlan E., Heynen A., Fallon J.R., and Richter J.D. CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of alpha-CaMKII mRNA at synapses. Neuron 21 (1998) 1129-1139
147. Xu L., Anwyl R., and Rowan M.J. Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 394 (1998) 891-894
148. Young J.Z., and Nguyen P.V. Homosynaptic and heterosynaptic inhibition of synaptic tagging and capture of long-term potentiation by previous synaptic activity. Journal of Neuroscience 25 (2005) 7221-7231
149. Young J.Z., Isiegas C., Abel T., and Nguyen P.V. Metaplasticity of the late-phase of long-term potentiation: a critical role for protein kinase A in synaptic tagging. European Journal of Neuroscience 23 (2006) 1784-1794
150. Zhang W., and Linden D.J. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nature Reviews Neuroscience 4 (2003) 885-900