A clustered plasticity model of long-term memory engrams

Nature Reviews Neuroscience

Volumn 7, Issue 7, 2006, Pages 575-583

  Govindarajan, Arvind ^a   Kelleher, Raymond J ^a,b   Tonegawa, Susumu ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; CLUSTER ANALYSIS; CONTROLLED STUDY; FACILITATION; LONG TERM DEPRESSION; LONG TERM MEMORY; LONG TERM POTENTIATION; MODEL; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; SYNAPTIC TRANSMISSION; TRANSCRIPTION REGULATION;

ANIMALS; CLUSTER ANALYSIS; HUMANS; MEMORY; NEURAL NETWORKS (COMPUTER); NEURONAL PLASTICITY;

EID: 33745597062     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn1937     Document Type: Review

References (108)

1. Malenka, R. C. & Bear, M. F. LTP and LTD: an embarrassment of riches. Neuron 44, 5-21 (2004).
2. Davis, H. P. & Squire, L. R. Protein synthesis and memory: a review. Psychol. Bull. 96, 518-559 (1984).
3. Krug, M., Lossner, B. & Ott, T. Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res. Bull. 13, 39-42 (1984).
4. Frey, U., Krug, M., Reymann, K. G. & Matthies, H. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res. 452, 57-65 (1988).
5. Frey, U. & Morris, R. G. Synaptic tagging and long-term potentiation. Nature 385, 533-536 (1997).
6. Huber, K. M., Kayser, M. S. & Bear, M. F. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288, 1254-1257 (2000).
7. Huber, K. M., Roder, J. C. & Bear, M. F. Chemical induction of mGluR5- and protein synthesis-dependent long-term depression in hippocampal area CA1. J. Neurophysiol. 86, 321-325 (2001).
8. Scharf, M. T. et al. Protein synthesis is required for the enhancement of long-term potentiation and long-term memory by spaced training. J. Neurophysiol. 87, 2770-2777 (2002).
9. Kelleher, R. J., Govindarajan, A. & Tonegawa, S. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44, 59-73 (2004).
10. Kelleher, R. J., Govindarajan, A., Jung, H. Y., Kang, H. & Tonegawa, S. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116, 467-479 (2004).
11. Manahan-Vaughan, D., Kulla, A. & Frey, J. U. Requirement of translation but not transcription for the maintenance of long-term depression in the CA1 region of freely moving rats. J. Neurosci. 20, 8572-8576 (2000).
12. Otani, S., Marshall, C. J., Tate, W. P., Coddard, G. V. & 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, 519-526 (1989).
13. Nguyen, P. V., Abel, T. & Kandel, E. R. Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265, 1104-1107 (1994).
14. Frey, U., Frey, S., Schollmeier, F. & Krug, M. Influence of actinomycin D, a RNA synthesis inhibitor, on long-term potentiation in rat hippocampal neurons in vivo and in vitro. J. Physiol. (London) 490, 703-711 (1996).
15. Kauderer, B. S. & Kandel, E. R. Capture of a protein synthesis-dependent component of long-term depression. Proc. Natl Acad. Sci. USA 97, 13342-13347 (2000).
16. Sajikumar, S. & Frey, J. U. Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD. Neurobiol. Learn. Mem. 82, 12-25 (2004).
17. Yuste, R. & Urban, R. Dendritic spines and linear networks. J. Physiol. (Paris) 98, 479-486 (2004).
18. Frey, J. U. Long-lasting hippocampal plasticity: cellular model for memory consolidation? Results Probl. Cell Differ. 34, 27-40 (2001).
19. Poirazi, P., Brannon, T. & Mel, B. W. Pyramidal neuron as two-layer neural network. Neuron 37, 989-999 (2003).
20. Poirazi, P., Brannon, T. & Mel, B. W. Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 37, 977-987 (2003).
21. Poirazi, P. & Mel, B. W. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 29, 779-796 (2001).
22. Klann, E. & Dever, T. E. Biochemical mechanisms for translational regulation in synaptic plasticity. Nature Rev. Neurosci. 5, 931-942 (2004).
23. Takei, N., Kawamura, M., Hara, K., Yonezawa, K. & Nawa, H. Brain-derived neurotrophic factor enhances neuronal translation by activating multiple initiation processes: comparison with the effects of insulin. J. Biol. Chem. 276, 42818-42825 (2001).
24. Takei, N. et al. Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J. Neurosci. 24, 9760-9769 (2004).
25. Banko, J. L., Hou, L. & Klann, E. NMDA receptor activation results in PKA- and ERK-dependent Mnk1 activation and increased eIF4E phosphorylation in hippocampal area CA1. J. Neurochem. 91, 462-470 (2004).
26. Banko, J. L. et al. The translation repressor 4E-BP2 is critical for eIF4F complex formation, synaptic plasticity, and memory in the hippocampus. J. Neurosci. 25, 9581-9590 (2005).
27. Banko, J. L., Hou, L., Poulin, F., Sonenberg, N. & Klann, E. Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 26, 2167-2173 (2006).
28. Tsokas, P. et al. Local protein synthesis mediates a rapid increase in dendritic elongation factor 1A after induction of late long-term potentiation. J. Neurosci. 25, 5833-5843 (2005).
29. Huang, F., Chotiner, J. K. & Steward, O. The mRNA for elongation factor 1α is localized in dendrites and translated in response to treatments that induce long-term depression. J. Neurosci. 25, 7199-7209 (2005).
30. English, J. D. & Sweatt, J. D. Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J. Biol. Chem. 271, 24329-24332 (1996).
31. English, J. D. & Sweatt, J. D. A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J. Biol. Chem. 272, 19103-19106 (1997).
32. Tang, S. J. et al. A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc. Natl Acad. Sci. USA 99, 467-472 (2002).
33. Hou, L. & Klann, E. Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 24, 6352-6361 (2004).
34. Callagher, S. M., Daly, C. A., Bear, M. F. & Huber, K. M. Extracellular signal-regulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1. J. Neurosci. 24, 4859-4864 (2004).
35. Gong, R., Park, C. S., Rezaei Abbassi, N. & Tang, S. J. Roles of glutamate receptors and the mTOR signaling pathway in activity-dependent dendritic protein synthesis in hippocampal neurons. J. Biol. Chem. 1 May 2006 [epub ahead of print].
36. Cammalleri, M. et al. Time-restricted role for dendritic activation of the mTOR-p70S6K pathway in the induction of late-phase long-term potentiation in the CA1. Proc. Natl Acad. Sci. USA 100, 14368-14373 (2003).
37. Steward, O. & Levy, W. B. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J. Neurosci. 2, 284-291 (1982).
38. Steward, O. & Fass, B. Polyribosomes associated with dendritic spines in the denervated dentate gyrus: evidence for local regulation of protein synthesis during reinnervation. Prog. Brain Res. 58, 131-136 (1983).
39. Rao, A. & Steward, O. Evidence that protein constituents of postsynaptic membrane specializations are locally synthesized: analysis of proteins synthesized within synaptosomes. J. Neurosci. 11, 2881-2895 (1991).
40. Torre, E. R. & Steward, O. Demonstration of local protein synthesis within dendrites using a new cell culture system that permits the isolation of living axons and dendrites from their cell bodies. J. Neurosci. 12, 762-772 (1992).
41. Torre, E. R. & Steward, O. Protein synthesis within dendrites: glycosylation of newly synthesized proteins in dendrites of hippocampal neurons in culture. J. Neurosci. 16, 5967-5978 (1996).
42. 2+/calmodulin-dependent protein kinase in developing rat brain. J. Neurosci. 10, 1788-1798 (1990).
43. Lowenstein, P. R. et al. Polarized distribution of the trans-Golgi network marker TGN38 during the in vitro development of neocortical neurons: effects of nocodazole and brefeldin A. Eur. J. Neurosci. 6, 1453-1465 (1994).
44. Tiedge, H. & Brosius, J. Translational machinery in dendrites of hippocampal neurons in culture. J. Neurosci. 16, 7171-7181 (1996).
45. Gardiol, A., Racca, C. & Triller, A. Dendritic and postsynaptic protein synthetic machinery. J. Neurosci. 19, 168-179 (1999).
46. Job, C. & Eberwine, J. Identification of sites for exponential translation in living dendrites. Proc. Natl Acad. Sci. USA 98, 13037-13042 (2001).
47. Steward, O. & Schuman, E. M. Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24, 299-325 (2001).
48. Kang, H. & Schuman, E. M. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273, 1402-1406 (1996).
49. Kacharmina, J. E., Job, C., Crino, P. & Eberwine, J. Stimulation of glutamate receptor protein synthesis and membrane insertion within isolated neuronal dendrites. Proc. Natl Acad. Sci. USA 97, 11545-11550 (2000).
50. Aakalu, G., Smith, W. B., Nguyen, N., Jiang, C. & Schuman, E. M. Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30, 489-502 (2001).
51. Martin, K. C. & Kosik, K. S. Synaptic tagging - who's it? Nature Rev. Neurosci. 3, 813-820 (2002).
52. Ju, W. et al. Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nature Neurosci. 7, 244-253 (2004).
53. Bradshaw, K. D., Emptage, N. J. & Bliss, T. V. A role for dendritic protein synthesis in hippocampal late LTP. Eur. J. Neurosci. 18, 3150-3152 (2003).
54. Vickers, C. A., Dickson, K. S. & Wyllie, D. J. Induction and maintenance of late-phase long-term potentiation in isolated dendrites of rat hippocampal CA1 pyramidal neurones. J. Physiol. (London) 568, 803-813 (2005).
55. Smith, W. B., Starck, S. R., Roberts, R. W. & Schuman, E. M. Dopaminergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons. Neuron 45, 765-779 (2005).
56. Augustine, G. J., Santamaria, F. & Tanaka, K. Local calcium signaling in neurons. Neuron 40, 331-346 (2003).
57. Sawano, A., Takayama, S., Matsuda, M. & Miyawaki, A. Lateral propagation of EGF signaling after local stimulation is dependent on receptor density. Dev. Cell 3, 245-257 (2002).
58. Dudek, S. M. & Fields, R. D. Mitogen-activated protein kinase/extracellular signal-regulated kinase activation in somatodendritic compartments: roles of action potentials, frequency, and mode of calcium entry. J. Neurosci. 21, RC122 (2001).
59. Dudek, S. M. & Fields, R. D. Somatic action potentials are sufficient for late-phase LTP-related cell signaling. Proc. Natl Acad. Sci. USA 99, 3962-3967 (2002).
60. Selcher, J. C. et al. A role for ERK MAP kinase in physiologic temporal integration in hippocampal area CA1. Learn. Mem. 10, 26-39 (2003).
61. Wu, G. Y., Deisseroth, K. & Tsien, R. W. Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nature Neurosci. 4, 151-158 (2001).
62. Wu, G. Y., Deisseroth, K. & Tsien, R. W. Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway. Proc. Natl Acad. Sci. USA 98, 2808-2813 (2001).
63. Rhodes, P. A. in Cerebral Cortex (eds Ulinski, P., Jones, E. G. & Peters, A.) 139-200 (Plenum, New York, 1999).
64. Golding, N. L., Staff, N. P. & Spruston, N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418, 326-331 (2002).
65. Gasparini, S., Migliore, M. & Magee, J. C. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J. Neurosci. 24, 11046-11056 (2004).
66. Sweatt, J. D. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr. Opin. Neurobiol. 14, 311-317 (2004).
67. Gelinas, J. N. & Nguyen, P. V. β-Adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J. Neurosci. 25, 3294-3303 (2005).
68. Huang, Y. Y. & Kandel, E. R. D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc. Natl Acad. Sci. USA 92, 2446-2450 (1995).
69. Mockett, B. G., Brooks, W. M., Tate, W. P. & Abraham, W. C. Dopamine D1/D5 receptor activation fails to initiate an activity-independent late-phase LTP in rat hippocampus. Brain Res. 1021, 92-100 (2004).
70. Frey, U., Matthies, H., Reymann, K. G. & Matthies, H. The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neurosci. Lett. 129, 111-114 (1991).
71. Frey, U., Schroeder, H. & Matthies, H. Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices. Brain Res. 522, 69-75 (1990).
72. Schultz, W. & Dickinson, A. Neuronal coding of prediction errors. Annu. Rev. Neurosci. 23, 473-500 (2000).
73. Otmakhova, N. A. & Lisman, J. E. D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J. Neurosci. 16, 7478-7486 (1996).
74. Swanson-Park, J. L. et al. A double dissociation within the hippocampus of dopamine D1/D5 receptor and β-adrenergic receptor contributions to the persistence of long-term potentiation. Neuroscience 92, 485-497 (1999).
75. Lee, K. S. Cooperativity among afferents for the induction of long-term potentiation in the CA1 region of the hippocampus. J. Neurosci. 3, 1369-1372 (1983).
76. Bennett, M. R. The concept of long term potentiation of transmission at synapses. Prog. Neurobiol. 60, 109-137 (2000).
77. Bear, M. F. A synaptic basis for memory storage in the cerebral cortex. Proc. Natl Acad. Sci. USA 93, 13453-13459 (1996).
78. Frey, U. & Morris, R. G. Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37, 545-552 (1998).
79. O'Carroll, C. M. & Morris, R. G. Heterosynaptic co-activation of glutamatergic and dopaminergic afferents is required to induce persistent long-term potentiation. Neuropharmacology 47, 324-332 (2004).
80. Fonseca, R., Nagerl, U. V., Morris, R. G. & Bonhoeffer, T. Competing for memory; hippocampal LTP under regimes of reduced protein synthesis. Neuron 44, 1011-1020 (2004).
81. Frey, U. & Morris, R. G. Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci. 21, 181-188 (1998).
82. Washbourne, P., Bennett, J. E. & McAllister, A. K. Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nature Neurosci. 5, 751-759 (2002).
83. Bannister, N. J. & Larkman, A. U. Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus: I. Branching patterns. J. Comp. Neurol. 360, 150-160 (1995).
84. Trommald, M., Jensen, V. & Andersen, P. Analysis of dendritic spines in rat CA1 pyramidal cells intracellularly filled with a fluorescent dye. J. Comp. Neurol. 353, 260-274 (1995).
85. Alarcon, J. M., Barco, A. & 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. J. Neurosci. 26, 256-264 (2006).
86. Martin, S. J. & Morris, R. G. New life in an old idea: the synaptic plasticity and memory hypothesis revisited. Hippocampus 12, 609-636 (2002).
87. Gasparini, S. & Magee, J. C. State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J. Neurosci. 26, 2088-2100 (2006).
88. Polsky, A., Mel, B. W. & Schiller, J. Computational subunits in thin dendrites of pyramidal cells. Nature Neurosci. 7, 621-627 (2004).
89. Losonczy, A. & Magee, J. C. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50, 291-307 (2006).
90. Mehta, M. R. Cooperative LTP can map memory sequences on dendritic branches. Trends Neurosci. 27, 69-72 (2004).
91. Wilson, M. A. & McNaughton, B. L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055-1058 (1993).
92. Nakazawa, K., McHugh, T. J., Wilson, M. A. & Tonegawa, S. NMDA receptors, place cells and hippocampal spatial memory. Nature Rev. Neurosci. 5, 361-372 (2004).
93. Otto, T., Eichenbaum, H., Wiener, S. I. & Wible, C. G. Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus 1, 181-192 (1991).
94. Stewart, M., Luo, Y. & Fox, S. E. Effects of atropine on hippocampal theta cells and complex-spike cells. Brain Res. 591, 122-128 (1992).
95. Jeffery, K. J., Donnett, J. G. & O'Keefe, J. Medial septal control of theta-correlated unit firing in the entorhinal cortex of awake rats. Neuroreport 6, 2166-2170 (1995).
96. Holscher, C. Synaptic plasticity and learning and memory: LTP and beyond. J. Neurosci. Res. 58, 62-75 (1999).
97. Petersen, C. C., Malenka, R. C., Nicoll, R. A. & Hopfield, J. J. All-or-none potentiation at CA3-CA1 synapses. Proc. Natl Acad. Sci. USA 95, 4732-4737 (1998).
98. O'Neill, J., Senior, T. & Csicsvari, J. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49, 143-155 (2006).
99. Foster, D. J. & Wilson, M. A. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680-683 (2006).
100. Guzowski, J. F., McNaughton, B. L., Barnes, C. A. & Worley, P. F. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal esembles. Nature Neurosci. 2, 1120-1124 (1999).
101. Tsien, R. Y. Imagining imaging's future. Nature Rev. Mol. Cell Biol. 4 (Suppl.), SS16-SS21 (2003).
102. Brecht, M. et al. Novel approaches to monitor and manipulate single neurons in vivo. J. Neurosci. 24, 9223-9227 (2004).
103. Mehta, A. D., Jung, J. C., Flusberg, B. A. & Schnitzer, M. J. Fiber optic in vivo imaging in the mammalian nervous system. Curr. Opin. Neurobiol. 14, 617-628 (2004).
104. Miyawaki, A. Innovations in the imaging of brain functions using fluorescent proteins. Neuron 48, 189-199 (2005).
105. Barco, A., Alarcon, J. M. & Kandel, E. R. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108, 689-703 (2002).
106. Woo, N. H. & Nguyen, P. V. 'Silent' metaplasticity of the late phase of long-term potentiation requires protein phosphatases. Learn. Mem. 9, 202-213 (2002).
107. Woo, N. H. & Nguyen, P. V. Protein synthesis is required for synaptic immunity to depotentiation. J. Neurosci. 23, 1125-1132 (2003).
108. Fiala, J. C. & Harris, K. M. in Dendrites (eds Stuart, G., Spruston, N. & Häusser, M.) 376 (Oxford Univ. Press, New York, 1999).