Molecular mechanisms of synaptic plasticity underlying long-term memory formation

Neural Plasticity and Memory: From Genes to Brain Imaging

Volumn , Issue , 2007, Pages 47-66

  Ramirez Amaya, Victor ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

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EID: 85047244899     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (122)

1. Hebb, D.O. The Organization of Behavior. John Wiley & Sons, New York, 1949.
2. Dudai, Y. Molecular bases of long term memories: a question of persistence. Curr. Opin. Neurobiol., 12, 211, 2002.
3. Lamprecht, R. and LeDoux, J. Structural plasticity and memory. Nat. Rev. Neurosci., 5, 45, 2004.
4. Fischer, M., Kaech, S., Wagner, UY., Brinkhaus, H., and Matus, A.M. Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat. Neurosci., 3, 887, 2000
5. Washbourne, P., Bennett, J.E., and McAllister, A.K. Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat. Neurosci., 5, 751, 2002.
6. Chang, S. and DeCamilli, P. Glutamate regulates actin-based motility in axonal filopodia. Nat. Neurosci., 4, 787, 2001.
7. Desmond, N.L. and Levy, W.B. Synaptic correlates of associative potentiation and depression: an ultrastructural study in the hippocampus. Brain Res., 265, 21, 1983.
8. Escobar, M.L., Barea-Rodriguez, E.J., Derrick, B.E., Reyes. J.A. and Martinez, Jr. J.L. Opioid receptor modulation of mossy fiber synaptogenesis: independence from long term potentiation. Brain Res., 751, 330, 1997.
9. Toni, N., Buchs, P.A., Nikonenko, I., Bron, C.R., and Muller, D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature, 402, 421, 1999.
10. Ramirez-Amaya, V., Escobar, M.L., Chao, V., and Bermudez-Rattoni, F. Synaptogenesis of mossy fibers induced by spatial water maze overtraining. Hippocampus, 9, 631, 1999.
11. Ramirez-Amaya. V., Balderas, I., Sandoval, J., Escobar, M.L. and Bermudez-Rattoni, F. Spatial long-term memory is related to mossy fiber synaptogenesis. J. Neurosci., 21, 7340, 2001.
12. Leuner, B., Falduto, J., and Shors, T.J. Associative memory formation increases the observation of dendritic spines in the hippocampus. J. Neurosci., 23, 659, 2003.
13. Lüscher, C. et al. Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron, 24, 649, 1999.
14. Shi, S.H. et al. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science, 284, 1811, 1999.
15. Lan, J.Y. et al. Activation of metabotropic glutamate receptor 1 accelerates NMDA receptor trafficking. J. Neurosci., 21, 6058, 2001.
16. Crump, F.T., Dillman, K.S., and Craig, A.M. cAMP-dependent protein kinase mediates activity regulated synaptic targeting of NMDA receptors. J. Neurosci., 21, 5079, 2001.
17. Perez-Otano, I. and Ehlers, M.D. Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci., 28, 229, 2005.
18. Wierenga, C.J., Ibata, K., and Turrigiano, G.G. Postsynaptic expression of homeostatic plasticity at neocortical synapses. J. Neurosci., 16, 2895, 2005.
19. Andrasfalvy, B.K. and Magee, J.C. Distance-dependent increase in AMPA receptor number in the dendrites of adult hippocampal CA1 pyramidal neurons. J. Neurosci., 21, 9151, 2001.
20. Turrigiano, G.G., Leslie, K.R., Desai, N.S., Rutherford, L.C., and Nelson, S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature, 391, 892, 1998.
21. Abbott, L.F. and Nelson, S.B. Synaptic plasticity: taming the beast. Nat. Neurosci., 3 (Suppl.), 1178, 2000.
22. London, L. and Segev, I. Synaptic scaling in vitro and in vivo. Nat. Neurosci., 4, 853, 2001.
23. Izquierdo, I., Medina, J.H., Vianna, M.R., Isquierdo, L.A., and Barros, D.M. Separate mechanisms for short- and long-term memory. Behav. Brain Res., 103, 1, 1999.
24. Ferreira, G., Gutierrez, R., DeLaCruz, V., and Bermudez-Rattoni, F. Differential involvement of cortical muscarinic and NMDA receptors in short- and long-term taste aversion memory. Eur. J. Neurosci., 16, 1139, 2002.
25. Woolf, N.J. A structural basis for memory storage in mammals. Progr. Neurobiol., 55, 59, 1998.
26. Rosenblum, K. Futter, M., Jones, M., Hulme, E.C., and Bliss, T.V. ERKI/II regulation by the muscarinic acetylcholine receptors in neurons. J. Neurosci., 20, 977, 2000.
27. Woolf, N.J. Critical role of cholinergic basal forebrain neurons in morphological change and memory encoding: a hypothesis. Neurobiol. Learn. Mem., 66, 258, 1996.
28. Woodin, M.A., Munno, D.W., and Syed, N.I. Trophic factor-induced excitatory synaptogenesis involves post-synaptic modulation of nicotinic acetylcholine receptors. J. Neurosci., 22, 505, 2002.
29. Hohmann, C.F. A morphogenetic role for acetylcholine in mouse cerebral neocortex. Neurosci. Biobehav. Rev., 27, 351, 2003.
30. Ismail, N., Robinson, G.E., and Fahrbach, S.E. Stimulation of muscarinic receptors mimics experience-dependent plasticity in the honey bee brain. Proc. Natl. Acad. Sci. USA, 103, 207, 2006.
31. Imai, H., Mutsumi-Matsukawa, M., and Okado, N. Lamina-selective changes in the density of synapses following perturbation of monoamines and acetylcholine in the rat medial prefrontal cortex. Brain Res., 1012, 138, 2004.
32. Oertner, T.G. and Matus, A. Calcium regulation of actin dynamics in dendritic spines. Cell Calcium, 37, 477, 2005.
33. Lisman, J.E. and McIntyre, C.C. Synaptic plasticity: a molecular memory switch. Curr. Biol., 11, R788, 2001.
34. DeKoninck, P. and Schulman, H. Sensitivity of CaM kinase II to the frequency of Ca2C oscillations. Science, 279, 227, 1998.
35. Cammarota, M. et al. Participation of CaMKII in neuronal plasticity and memory formation. Cell. Mol. Neurobiol., 22, 259, 2002.
36. Lisman, J., Schulman, H., and Cline, H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci., 3, 175, 2002.
37. Mayford, M. et al. Control of memory formation through regulated expression of a CaMKII transgene. Science, 174, 1678, 1996.
38. Steward, O. and Halpain, S. Lamina-specific synaptic activation causes domainspecific alterations in dendritic immunostaining for MAP2 and CAM kinase II. J. Neurosci., 19, 7834, 1999.
39. Steward, O. and Worley, P. Localization of mRNAs at synaptic sites on dendrites. Results Probl. Cell. Differ., 34, 1, 2001.
40. Steward, O. and Schuman, E.M. Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci., 24, 299, 2001.
41. Greenough, W.T. et al. Synaptic regulation of protein synthesis and the fragile X protein. Proc. Natl. Acad. Sci. USA, 98, 7101, 2001.
42. Scheetz, A.J., Nairn, A.C., and Constantine-Paton, M. MDA receptor-mediated control of protein synthesis at developing synapses. Nat. Neurosci., 3, 211, 2000.
43. 2+/calmodulin-dependent protein kinase II from the postsynaptic density in the rat forebrain. J. Biochem. (Tokyo), 119, 268, 1996.
44. Yoshimura, Y., Aoi, C., and Yamauchi, T. Investigation of protein substrates of Ca2C/calmodulin-dependent protein kinase II translocated to the postsynaptic density. Brain Res. Mol. Brain Res., 81, 118, 2000.
45. Strack, S., Robison, A., Bass, M., and Colbran, R. Association of calcium/calmodulindependent kinase II with developmentally regulated splice variants of the postsynaptic density protein densin-180. J. Biol. Chem., 275, 25061, 2000.
46. Walikonis, R., Oguni, A., Khorosheva, E., Jeng, C., Asuncion, F. and Kennedy, M. Densin-180 forms a ternary complex with the (alpha)-subunit of Ca2+/calmodulindependent protein kinase II and (alpha)-actinin. J. Neurosci., 21,423, 2001.
47. Allison, D., Chervin, A., Gelfand, V., and Craig, A. Post-synaptic scaffolds of excitatory and inhibitory synapses in hippocampal neurons: maintenance of core components independent of actin filaments and microtubules. J. Neurosci., 20, 4545, 2000.
48. Gardoni, F. et al. Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities. J. Neurochem., 71, 1733, 1998.
49. Bayer, K.U., DeKoninck, P., Leonard, A.S., Hell, J.W., and Schulman, H. Interaction with the NMDA receptor locks CaMKII in active conformation. Nature, 411, 801, 2001.
50. 2+/calmodulin kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc. Natl. Acad. Sci. USA, 96, 3269, 1999.
51. Lisman, J.E. and Zhabotinsky, A.M. Model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron, 31, 191, 2001.
52. Hayachi Y. et al. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science, 287, 2262, 2000.
53. Bayer, K.U. et al. Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B. J. Neurosci., 26, 1164, 2006.
54. Ouyang, Y., Rosenstein, A., Kreiman, G., Schuman, E., and Kennedy, M. Tetanic stimulation leads to increased accumulation of Ca2C/calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. J. Neurosci., 19, 7823, 1999.
55. Fukunaga, K., Stoppini, L., Miyamoto, E., and Muller, D. Long-term potentiation is associated with increased activity of Ca2C/calmodulin-dependent protein kinase II. J. Biol. Chem., 268, 7863, 1993.
56. Fukunaga, K., Muller, D., and Miyamoto, E. Increased phosphorylation of Ca2C/calmodulin-dependent protein kinase II and its endogenous substrates in the induction of long term potentiation. J. Biol. Chem., 270, 6119, 1995.
57. 2+/CaM induces synaptic potentiation requiring CaMKII and PKC activity. Neuron, 15, 443, 1995.
58. Shi, S. et al. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science, 284, 1811, 1999.
59. Miller, S. et al. Disruption of dendritic translation of CaMKII-alpha impairs stabilization of synaptic plasticity and memory consolidation. Neuron, 36, 507, 2002.
60. Engert, F. and Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature, 399, 66, 1999.
61. Jourdain, P., Fukunaga, K., and Muller, D. Calcium/calmodulin-dependent protein kinase II contributes to activity-dependent filopodia growth and spine formation. J. Neurosci., 23, 10645, 2003.
62. Fink, C.C. et al. Selective regulation of neurite extension and synapse formation by the beta but not the alpha isoform of CaMKII. Neuron, 39, 283, 2003.
63. 2+/calmodulin-dependent protein kinase IImediated actin reorganization. J. Neurosci., 26, 1813, 2006.
64. Andersen, R., Li, Y., Resseguie, M., and Brenman, J.E. Calcium/calmodulin-dependent protein kinase II alters structural plasticity and cytoskeletal dynamics in Drosophila. J. Neurosci., 25, 8878, 2005.
65. Griffith, L. et al. Inhibition of calcium/calmodulin-dependent protein kinase in Drosophila disrupts behavioral plasticity. Neuron, 10, 501, 1993.
66. Tan, S. and Liang, K. Spatial learning alters hippocampal calcium/calmodulin-dependent protein kinase II activity in rats. Brain Res., 711, 234, 1996.
67. Frankland, P., O’Brien, C., Ohno, M., Kirkwood, A., and Silva, A. Alpha CaMKIIdependent plasticity in the cortex is required for permanent memory. Nature, 411, 309, 2001.
68. Lanahan, A. and Worley, P. Immediate early genes and synaptic function. Neurobiol. Learn. Mem., 70, 37, 1998.
69. Abraham, W.C., Dragunow, M., and Tate, W.P. Role of immediate early genes in the stabilization of long-term potentiation. Mol. Neurobiol., 5, 297, 1991.
70. Worley, P.F. et al. Thresholds for synaptic activation of transcription factors in hippocampus: correlation with long-term enhancement. J. Neurosci., 13, 4776, 1993.
71. Dragunow, M., Yamada, N., Bilkey, D.K., and Lawlor, P. Induction of immediate early gene proteins in dentate granule cells and somatostatin interneurons after hippocampal seizures. Brain Res. Mol. Brain Res., 13, 119, 1992.
72. Epsztein, J., Represa, A., Jorquera, I., Ben-Ari, Y., and Crepel, V. Recurrent mossy fibers establish aberrant kainate receptor-operated synapses on granule cells from epileptic rats. J. Neurosci., 25, 8229, 2005.
73. Kleim, J.A., Lussnig, E., Schwarz, E.R., Comery, T.A., and Greenough, W.T. Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J. Neurosci., 16, 4529, 1996.
74. Watanabe, Y. et al. Null mutation of c-fos impairs structural and functional plasticities in the kindling model of epilepsy. J. Neurosci., 16, 3827, 1996.
75. Dong, M., Wu, Y., Fan, Y., Xu, M., and Zhang, J. c-fos modulates brain-derived neurotrophic factor mRNA expression in mouse hippocampal CA3 and dentate gyrus neurons. Neurosci. Lett., 400, 177, 2006; epub, March 13, 2006.
76. Lyford, G.L. et al. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron, 14, 433, 1995.
77. Link, W. et al. Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc. Natl. Acad. Sci. USA, 92, 5734, 1995.
78. Guzowski, J.F., McNaughton, B.L., Barnes, C.A., and Worley, P.F. Environmentspecific expression of the immediate early gene Arc in hippocampal neuronal ensembles. Nat. Neurosci., 2, 1120, 1999.
79. O’Keefe, J. Place units in the hippocampus of the freely moving rat. Exp. Neurol., 51, 78, 1976.
80. O’Keefe, J. and Nadel, L. The Hippocampus as a Cognitive Map. Clarendon Press, Oxford, 1978.
81. Leitner, S., Voigt, C., Metzdorf, R., and Catchpole, C.K. Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J. Neurobiol., 64, 275, 2005.
82. Ons, S., Marti, O., and Armario, A. Stress-induced activation of the immediate early gene Arc (activity-regulated cytoskeleton-associated protein) is restricted to telencephalic areas in the rat brain: relationship to c-fos mRNA. J. Neurochem., 89, 1111, 2004.
83. Ostrander, M.M. et al. Environmental context and drug history modulate amphetamine-induced c-fos mRNA expression in the basal ganglia, central extended amygdala, and associated limbic forebrain. Neuroscience, 120, 551, 2003.
84. Kelly, M.P. and Deadwyler, S.A. Experience-dependent regulation of the immediate early gene arc differs across brain regions. J. Neurosci., 23, 6443, 2003.
85. Wallace, C.S., Lyford, G.L., Worley, P.F., and Steward, O. Differential intracellular sorting of immediate early gene mRNAs depends on signals in the mRNA sequence. J. Neurosci., 18, 26, 1998.
86. 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 post-synaptic sites on dendrites. Neuron, 21, 741, 1998.
87. Steward, O. and Worley, P.F. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron, 30, 227, 2001.
88. Guzowski, J.F. et al. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long term memory. J. Neurosci., 20, 3993, 2000.
89. Braham, C.R. and Messaoudi, E. BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Progr. Neurobiol., 76, 99, 2005.
90. Plath, N., Ohana, O., Dammermann, B., Errington, M.L., Schmitz, D., Gross, C., Mao, X., Engelsberg, A., Mahlke, C., Welzl, H., Kobalz, U., Stawrakakis, A., Fernandez, E., Waltereit, R., Bick-Sander, A., Therstappen, E., Cooke, S.F., Blanquet, V., Wurst, W., Salmen, B., Bosl, MR., Lipp, H.P., Grant, S.G., Bliss, T.V., Wolfer, D.P. and Kuhl, D. Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron., 52, 437, 2006.
91. Vazdarjanova, A. and Guzowski, J.F. Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J. Neurosci., 24, 6489, 2004.
92. Burke, S.N. et al. Differential encoding of behavior and spatial context in deep and superficial layers of the neocortex. Neuron, 45, 667, 2005.
93. Petrovich, G.D., Holland, P.C., and Gallagher, M. Amygdalar and prefrontal pathways to the lateral hypothalamus are activated by a learned cue that stimulates eating. J. Neurosci., 25, 8295, 2005.
94. Vazdarjanova, A., McNaughton, B.L., Barnes, C.A., Worley, P.F., and Guzowski, J.F. Experience-dependent coincident expression of the effector immediate early genes arc and Homer-1a in hippocampal and neocortical neuronal networks. J. Neurosci., 22, 10067, 2002.
95. Leutgeb, S., Leutgeb, J.K., Treves, A., Moser, M.B., and Moser, E.I. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science, 305, 1295, 2004; epub, July 22, 2004.
96. McNaughton, B.L. et al. Cortical representation of motion during unrestrained spatial navigation in the rat. Cerebr. Cortex, 4, 27, 1994.
97. McNaughton, B.L. et al. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J. Exp. Biol., 199, 173, 1996.
98. Sakurai, Y. How do cell assemblies encode information in the brain? Neurosci. Biobehav. Rev., 23, 785, 1999.
99. Dong, E. et al. A reelin-integrin receptor interaction regulates Arc mRNA translation in synaptoneurosomes. Proc. Natl. Acad. Sci. USA, 100, 5479, 2003.
100. Ramirez-Amaya V. et al. Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network specific reactivation. J. Neurosci., 25, 1761, 2005.
101. Wang, K.H. et al. In vivo two-photon imaging reveals a role of arc in enhancing orientation specificity in visual cortex. Cell, 126, 389, 2006.
102. Rosi, S. et al. Neuroinflammation alters the hippocampal pattern of behaviorally induced Arc expression. J. Neurosci., 25, 723, 2005.
103. Chawla, M.K. et al. Sparse environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus, 15, 579, 2005.
104. Chowdhury, S., Shepherd, J.D., Okuno, H., Lyford, G., Petralia, R.S., Plath, N., Kuhl.D., Huganir, R.L. and Worley, P.F. Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron., 52,445, 2006.
105. Shepherd, J.D., Rumbaugh, G., Wu, J., Chowdhury, S., Plath, N., Kuhl, D., Huganir, R.L. and Worley, P.F. Arc/Arg3.1 Mediates Homeostatic Synaptic Scaling of AMPA Receptors. Neuron., 52,475, 2006.
106. Rial-Verde, E.M., Lee-Osbourne, J., Worley, P.F., Malinow, R. and Cline, H.T. Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptormediated synaptic transmission. Neuron., 52,461, 2006.
107. Vazdarjanova, A. et al. Spatial exploration induces ARC, a plasticity-related immediate early gene, only in calcium/calmodulin-dependent protein kinase II positive principal excitatory and inhibitory neurons of the rat forebrain. J. Comp. Neurol., 498, 317, 2006.
108. Okuno, H., Chowdhury, S., Worley, P. and Bito, H. Interaction between Arc and CaM Kinase II in dendrites monitored by fluorescence resonance energy transfer. Soc. Neurosci. Abstracts, 164,16, 2004.
109. Donai, H. et al. Interaction of Arc with CaM kinase II and stimulation of neurite extension by Arc in neuroblastoma cells expressing CaM kinase II. Neurosci. Res., 47, 399, 2003.
110. McAllister, A.K. Neurotrophins and cortical development. Results Probl. Cell Differ., 39, 89, 2002.
111. Frade, J.M., Bovolenta, P., and Rodriguez-Tebar, A. Neurotrophins and other growth factors in the generation of retinal neurons. Microsc. Res. Tech., 45, 243, 1999.
112. Horch, H.W. Local effects of BDNF on dendritic growth. Rev. Neurosci., 15,117, 2004.
113. McAllister, A.K., Lo, D.C., and Katz, L.C. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron, 15, 791, 1995.
114. Slack, S.E., Pezet, S., McMahon, S.B., Thompson, S.W., and Malcangio, M. Brainderived neurotrophic factor induces NMDA receptor subunit I phosphorylation via ERK and PKC in the rat spinal cord. Eur. J. Neurosci., 20, 1769, 2004.
115. Thomas, K. and Davies, A. Neurotrophins: a ticket to ride for BDNF. Curr. Biol., 15, R262, 2005.
116. Mizuno, M., Yamada, K., Olariu, A., Nawa, H., and Nabeshima, T. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J. Neurosci., 20, 7116, 2000.
117. Kesslak, J.P. et al. Learning up-regulates brain-derived neurotrophic factor messenger ribonucleic acid: a mechanism to facilitate encoding and circuit maintenance? Behav. Neurosci., 112, 1012, 1998.
118. Gomez-Pinilla, F., So, V., and Kesslak, J.P. Spatial learning induces neurotrophin receptor and synapsin I in the hippocampus. Brain Res., 904, 13, 2001.
119. Mu, J.S., Li, W.P., Yao, Z.B., and Zhou, X.F. Deprivation of endogenous brain-derived neurotrophic factor results in impairment of spatial learning and memory in adult rats. Brain Res., 835, 269, 1999.
120. Yin, Y., Edelman, G.M., and Vanderklish, P.W. The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes. Proc. Natl. Acad. Sci. USA, 99, 2368, 2002; epub, February 12, 2002.
121. Braham, C.R. and Messaoudi, E. BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Progr. Neurobiol., 76, 125, 2005.
122. Aakalu, G., Smith, W.B., Nguyen, N., Jiang, C., and Schuman, E.M. Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron, 30, 489, 2001.