Molecular mechanisms of memory storage in Aplysia

Biological Bulletin

Volumn 210, Issue 3, 2006, Pages 174-191

  Hawkins, Robert D ^a,b   Kandel, Eric R ^a,b,c,d   Bailey, Craig H ^a,b,d  

^a College of Physicians and Surgeons of Columbia University ^*  (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d Kavli Institute for Brain Science   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; MEMORY; SNAIL;

APLYSIA; APLYSIA CALIFORNICA; INVERTEBRATA;

EID: 33745700968     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.2307/4134556     Document Type: Review

References (159)

1. Aakalu, G., W. B. Smith, N. Nguyen, C. Jiang, and E. M. Schuman. 2001. Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30: 489-502.
2. Abel, T., K. C. Martin, D. Bartsch, and E. R. Kandel. 1998. Memory suppressor genes: inhibitory constraints on the storage of long-term memory. Science 279: 338-341.
3. Abrams, T. W., Y. Yovell, C. U. Onyike, J. E. Cohen, and H. E. Jarrard. 1998. Analysis of sequence-dependent interactions between calcium and transmitter stimuli in activating adenylyl cyclase in Aplysia: possible contributions to CS-US sequence requirement during conditioning. Learn. Mem. 4: 496-509.
4. Albensi, B. C., and M. P. Mattson. 2000. Evidence for the involvement of TNF and NF-kappaB in hippocampal synaptic plasticity. Synapse 35: 151-159.
5. Alberini, C. M., M. Ghirardi, R. Metz, and E. R. Kandel. 1994. C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76: 1099-1114.
6. Antonov, I., E. R. Kandel, and R. D. Hawkins. 1999. The contribution of facilitation of monosynaptic PSPs to dishabituation and sensitization of the Aplysia siphon withdrawal reflex. J Neurosci. 19: 10438-10450.
7. Antonov, I., I. Antonova, E. R. Kandel, and R. D. Hawkins. 2001. The contribution of activity-dependent synaptic plasticity to classical conditioning in Aplysia. J. Neurosci. 21: 6413-6422.
8. Antonov, I., I. Antonova, E. R. Kandel, and R. D. Hawkins. 2003. Activity-dependent presynaptic facilitation and Hebbian LTP are both required and interact during classical conditioning in Aplysia. Neuron 37: 135-147.
9. Antonov, I., E. R. Kandel, and R. D. Hawkins. 2004. Tests of pre- and postsynaptic mechanisms contributing to simple forms of learning in Aplysia. Soc. Neurosci. Abstr. 778.17 [Online].
10. Antonov, I., E. R. Kandel, and R. D. Hawkins. 2005. Roles of PKA, PKC, and CamKII in dishabituation and sensitization of the Aplysia siphon-withdrawal reflex. Soc. Neurosci. Abstr. 540.6 [Online].
11. 2+, and CamKII in sensitization of the Aplysia siphon-withdrawal reflex. Soc. Neurosci. Abstr. Forthcoming [Online].
12. Antonova, I., O. Arancio, A.-C. Trillat, H.-G. Wang, L. Zablow, H. Udo, E. R. Kandel, and R. D. Hawkins. 2001. Rapid increase in clusters of presynaptic proteins at onset of long-lasting potentiation. Science 294: 1547-1550.
13. Arancio, O., E. R. Kandel, and R. D. Hawkins. 1995. Activity-dependent long-term enhancement of transmitter release by presynaptic 3′, 5′-cyclic cGMP in cultured hippocampal neurons. Nature 376: 74-80.
14. Arancio, O., M. Kiebler, C. J. Lee, V. Lev-Ram, R. Y. Tsien, E. R. Kandel, and R. D. Hawkins. 1996. Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87: 1025-1035.
15. Arancio, O., I. Antonova, S. Gambaryan, S. M. Lohmann, J. S. Wood, D. S. Lawrence, and R. D. Hawkins. 2001. Presynaptic role of cGMP-dependent protein kinase during long-lasting potentiation. J. Neurosci. 21: 143-149.
16. Bacskai, B. J., B. Hochner, M. Mahaut-Smith, S. R. Adams, B. K. Kaang, E. R. Kandel, and R. Y. Tsien. 1993. Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science 260: 222-226.
17. Bailey, C. H., and M. Chen. 1983. Morphological basis of long-term habituation and sensitization in Aplysia. Science 220: 91-93.
18. Bailey, C. H., and M. Chen. 1988a. Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons. Proc. Natl. Acad. Sci. USA 85: 2373-2377.
19. Bailey, C. H., and M. Chen. 1988b. Long-term sensitization in Aplysia increases the number of presynaptic contacts onto the identified gill motor neuron L7. Proc. Natl. Acad. Sci. USA 85: 9356-9359.
20. Bailey, C. H., and M. Chen. 1989. Structural plasticity at identified synapses during long-term memory in Aplysia. J. Neurobiol. 20: 356-372.
21. Bailey, C. H., and E. R. Kandel. 1993. Structural changes accompanying memory storage. Annu. Rev. Physiol. 55: 397-426.
22. Bailey, C. H., V. F. Castellucci, J. Koester, and E. R. Kandel. 1979. Cellular studies of peripheral neurons in siphon skin of Aplysia californica. J. Neurophysiol. 42: 530-557.
23. Bailey, C. H., M. Chen, F. Keller, and E. R. Kandel. 1992a. Serotonin-mediated endocytosis of apCAM: an early step of learning-related synaptic growth in Aplysia. Science 256: 645-649.
24. Bailey, C. H., P. Montarolo, M. Chen, E. R. Kandel, and S. Schacher. 1992b. Inhibitors of protein and RNA synthesis block structural changes that accompany long-term heterosynaptic plasticity in Aplysia. Neuron 9: 749-758.
25. Bailey, C. H., B. K. Kaang, M. Chen, K. C. Martin, C. S. Lim, A. Casadio, and E. R. Kandel. 1997. Mutation in the phosphorylation sites of MAP kinase blocks learning-related internalization of apCAM in Aplysia sensory neurons. Neuron 18: 913-924.
26. Bailey, C. H., E. R. Kandel, and K. Si. 2004. The persistence of long-term memory: a molecular approach to self-sustaining changes in learning-induced synaptic growth. Neuron 44: 49-57.
27. Bao, J.-X., E. R. Kandel, and R. D. Hawkins. 1997. Involvement of pre- and postsynaptic mechanisms in posttetanic potentiation at Aplysia synapses. Science 275: 969-973.
28. Bao, J.-X., E. R. Kandel, and R. D. Hawkins. 1998. Involvement of presynaptic and postsynaptic mechanisms in a cellular analog of classical conditioning at Aplysia sensory-motor neuron synapses in isolated cell culture. J. Neurosci. 18: 458-466.
29. Barco, A., J. M. Alarcon, and E. R. Kandel. 2002. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108: 689-703.
30. Barco, A., C. Pittenger, and E. R. Kandel. 2003. CREB, memory enhancement and the treatment of memory disorders: promises, pitfalls and prospects. Expert Opin. Ther. Targets 7: 101-114.
31. Bartsch, D., A. Casadio, K. A. Karl, P. Serodio, and E. R. Kandel. 1998. CREB1 encodes a nuclear activator, a repressor, and a cytoplasmic modulator that form a regulatory unit critical for long-term facilitation. Cell 95: 211-223.
32. Bartsch, D., M. Ghirardi, A. Casadio, M. Giustetto, K. A. Karl, H. Zhu, and E. R. Kandel. 2000. Enhancement of memory-related long-term facilitation by ApAF, a novel transcription factor that acts downstream from both CREB1 and CREB2. Cell 103: 595-608.
33. Bartsch, D., M. Ghirardi, P. A. Skehel, K. A. Karl, S. P. Herder, M. Chen, C. H. Bailey, and E. R. Kandel. 1995. Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change. Cell 83: 979-992.
34. Bozdagi, O., W. Shan, H. Tanaka, D. L. Benson, and G. W. Huntley. 2000. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28: 245-259.
35. Brunelli, M., V. Castellucci, and E. R. Kandel. 1976. Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. Science 194: 1178-1181.
36. Byers, D., R. L. Davis, and J. A. Kiger, Jr. 1981. Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature 289: 79-81.
37. Byrne, J. 1987. Cellular analysis of associative learning. Physiol. Rev. 6: 329-439.
38. Byrne, J. H., and E. R. Kandel. 1996. Presynaptic facilitation revisited: state and time dependence. J. Neurosci. 16: 425-435.
39. Byrne, J. H., V. Castellucci, and E. R. Kandel. 1974. Receptive fields and response properties of mechanoreceptor neurons innervating skin and mantle shelf of Aplysia. J. Neurophysiol. 37: 1041-1064.
40. Cammalleri, M., R. Lutjens, F. Berton, A. R. King, C. Simpson, W. Francesconi, and P. P. Sanna. 2003. 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.
41. Carew, T. J., and C. L. Sahley. 1986. Invertebrate learning and memory: from behavior to molecules. Annu. Rev. Neurosci. 9: 435-487.
42. Carew, T. J., V. F. Castellucci, and E. R. Kandel. 1971. An analysis of dishabituation and sensitization of the gill-withdrawal reflex in Aplysia. Int. J. Neurosci. 2: 79-98.
43. Carew, T. J., E. T. Walters, and E. R. Kandel. 1981. Classical conditioning in a simple withdrawal reflex in Aplysia californica. J. Neurosci. 1: 1426-1437.
44. Carew, T. J., R. D. Hawkins, and E. R. Kandel. 1983. Differential classical conditioning of a defensive withdrawal reflex in Aplysia californica. Science 219: 397-400.
45. Carew, T. J., R. D. Hawkins, T. W. Abrams, and E. R. Kandel. 1984. A test of Hebb's postulate at identified synapses which mediate classical conditioning in Aplysia. J. Neurosci. 4: 1217-1224.
46. Casadio, A., K. C. Martin, M. Giustetto, H. Zhu, M. Chen, D. Bartsch, C. H. Bailey, and E. R. Kandel. 1999. A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99: 221-237.
47. Castellucci, V., H. Pinsker, I. Kupfermann, and E. R. Kandel. 1970. Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167: 1745-1748.
48. Castellucci, V. F., W. N. Frost, P. Goelet, P. G. Montarolo, S. Schacher, J. A. Morgan, H. Blumenfeld, and E. R. Kandel. 1986. Cell and molecular analysis of long-term sensitization in Aplysia. J. Physiol. 81: 349-357.
49. Chitwood, R. A., Q. Li, and D. L. Glanzman. 2001. Serotonin facilitates AMPA-type responses in isolated siphon motor neurons of Aplysia in culture. J. Physiol. 534: 501-510.
50. Clark, G. A., R. D. Hawkins, and E. R. Kandel. 1994. Activity dependent enhancement of presynaptic facilitation provides a cellular mechanism for the temporal specificity of classical conditioning in Aplysia. Learn. Mem. 1: 243-257.
51. Cohen-Cory, S. 2002. The developing synapse: construction and modulation of synaptic structures and circuits. Science 298: 770-776.
52. Colwill, R. M., R. A. Absher, and M. L. Roberts. 1988a. Context US learning in Aplysia californica. J. Neurosci. 8: 4434-4439.
53. Colwill, R. M., R. A. Absher, and M. L. Roberts. 1988b. Conditional discrimination learning in Aplysia californica. J. Neurosci. 8: 4440-4444.
54. Conrad, P., F. Wu, and S. Schacher. 1999. Changes in functional glutamate receptors on a postsynaptic neuron accompany formation and maturation of an identified synapse. J Neurobiol. 39: 237-248.
55. Dale, N., and E. R. Kandel. 1993. L-glutamate may be the fast excitatory transmitter of Aplysia sensory neurons. Proc. Natl. Acad. Sci. USA 90: 7163-7167.
56. Dale, N., S. Schacher, and E. R. Kandel. 1988. Long-term facilitation in Aplysia involves increase in transmitter release. Science 239: 282-285.
57. Dash, P. K., B. Hochner, and E. R. Kandel. 1990. Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345: 718-721.
58. Dudai, Y., Y. N. Jan, D. Byers, W. G. Quinn, and S. Benzer. 1976. Dunce, a mutant of Drosophila deficient in learning. Proc. Natl. Acad. Sci. USA 73: 1684-1688.
59. Dudek, S. M., and R. D. Fields. 2002. Somatic action potentials are sufficient for late-phase LTP-related cell signaling. Proc. Natl. Acad. Sci. USA 99: 3962-3967.
60. Duerr, J. S., and W. G. Quinn. 1982. Three Drosophila mutations that block associative learning also affect habituation and sensitization. Proc. Natl. Acad. Sci. USA 79: 3646-3650.
61. Eliot, L. S., R. D. Hawkins, E. R. Kandel, and S. Schacher. 1994. Pairing-specific, activity-dependent presynaptic facilitation at Aplysia sensory-motor neuron synapses in isolated cell cultures. J Neurosci. 14: 368-383.
62. Engert, F., and T. Bonhoeffer. 1999. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399: 66-70.
63. Frey, U., and R. G. Morris. 1997. Synaptic tagging and long-term potentiation. Nature 385: 533-536.
64. Frey, U., and R. G. Morris. 1998. Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37: 545-552.
65. Frost, L., S.W. Kaplan, T.E. Cohen, V. Henzi, E.R. Kandel, and R.D. Hawkins. 1997. A simplified preparation for relating cellular events to behavior: contribution of LE and unidentified siphon sensory neurons to mediation and habituation of the Aplysia gill- and siphon-withdrawal reflex. J. Neurosci. 17: 2900-2913.
66. Frost, W. N., and E. R. Kandel. 1995. Structure of the network mediating siphon-elicited siphon withdrawal in Aplysia. J. Neurophysiol. 73: 2413-2427.
67. Ghirardi, M., P. G. Montarolo, and E. R. Kandel. 1995. A novel intermediate stage in the transition between short- and long-term facilitation in the sensory to motor neuron synapse of Aplysia. Neuron 14: 413-420.
68. Glanzman, D. L., S. L. Mackey, R. D. Hawkins, A. M. Dyke, P. E. Lloyd, and E. R. Kandel. 1989. Depletion of serotonin in the nervous system of Aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by tail shock. J. Neurosci. 9: 4200-4213.
69. Glanzman, D. L., E. R. Kandel, and S. Schacher. 1990. Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. Science 249: 799-802.
70. Guan, Z., M. Giustetto, S. Lomvardas, J. H. Kim, M. C. Miniaci, J. H. Schwartz, D. Thanos, and E. R. Kandel. 2002. Integration of long-term-memory- related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111: 483-493.
71. Guan, Z., J. H. Kim, S. Lomvardas, K. Holick, S. Xu, E. R. Kandel, and J. H. Schwartz. 2003. p38 MAP kinase mediates both short-term and long-term synaptic depression in Aplysia. J. Neurosci. 23: 7317-7325.
72. Han, J. H., C. S. Lim, Y. S. Lee, E. R. Kandel, and B. K. Kaang. 2004. Role of Aplysia cell adhesion molecules during 5-HT-induced long-term functional and structural changes. Learn. Mem. 11: 421-435.
73. Hatada, Y., F. Wu, Z.-Y. Sun, S. Schacher, and D. J. Goldberg. 2000. Presynaptic morphological changes associated with long-term synaptic facilitation are triggered by actin polymerization at preexisting varicosities. J. Neurosci. 20: RC82.
74. Hawkins, R. D., and S. Schacher. 1989. Identified facilitator neurons L29 and L28 are excited by cutaneous stimuli used in dishabituation, sensitization, and classical conditioning of Aplysia. J. Neurosci. 9: 4236-4245.
75. Hawkins, R. D., T. W. Abrams, T. J. Carew, and E. R. Kandel. 1983. A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science 219: 400-415.
76. Hawkins, R. D., T. J. Carew, and E. R. Kandel. 1986. Effects of interstimulus interval and contingency on classical conditioning of the Aplysia siphon withdrawal reflex. J. Neurosci. 6: 1695-1701.
77. Hawkins, R. D., N. Lalevic, G. A. Clark, and E. R. Kandel. 1989. Classical conditioning of the Aplysia siphon-withdrawal reflex exhibits response specificity. Proc. Natl Acad. Sci. USA 86: 7620-7624.
78. Hawkins, R. D., E. R. Kandel, and S. A. Siegelbaum. 1993. Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annu. Rev. Neurosci. 16: 625-665.
79. Hawkins, R. D., W. Greene, and E. R. Kandel. 1998. Classical conditioning, differential conditioning, and second-order conditioning of the Aplysia gill-withdrawal reflex in a simplified mantle organ preparation. Behav. Neurosci. 112: 636-645.
80. Hawkins, R. D., T. E. Cohen, and E. R. Kandel. 2006. Dishabituation in Aplysia can involve either reversal of habituation or superimposed sensitization. Learn. Mem. (In press), doi: 10.1101/lm.49706 [Published online 16 May 2006].
81. Hegde, A. N., K. Inokuchi, W. Pei, A. Casadio, M. Ghirardi, D. G. Chain, K. C. Martin, E. R. Kandel, and J. H. Schwartz. 1997. Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89: 115-126.
82. Hsieh, J., and F. H. Gage. 2005. Chromatin remodeling in neural development and plasticity. Curr. Opin. Cell Biol. 17: 664-671.
83. Huang, Y. S., M. Y. Jung, M. Sarkissian, and J. D. Richter. 2002. N-methyl-D-aspartate receptor signaling results in Aurora kinase-catalyzed CPEB phosphorylation and alpha CaMKII mRNA polyadenylation at synapses. EMBO. J. 21: 2139-2148.
84. Izquierdo, I., and M. Cammarota. 2004. Zif and the survival of memory. Science 304: 829-830.
85. Jessell, T. M., and E. R. Kandel. 1993. Synaptic transmission: a bidirectional and self-modifiable form of cell-cell communication. Cell 72/
86. Neuron 10 (Suppl.): 1-30.
87. Jin, I., and R. D. Hawkins. 2003. Presynaptic and postsynaptic mechanisms of a novel form of homosynaptic potentiation at Aplysia sensory-motor neuron synapses. J. Neurosci. 23: 7288-7297.
88. Jin, I., H. Udo, E. R. Kandel, and R. D. Hawkins. 2003. Rapid increase in synaptophysin puncta at onset of homosynaptic potentiation in Aplysia. Soc. Neurosci. Abstr. 291.22 [Online].
89. Jin, I., E. R. Kandel, and R. D. Hawkins. 2004. Pre- and postsynaptic mechanisms of facilitation at Aplysia sensory-motor synapses: time and state dependence revisited. Soc. Neurosci. Abstr. 515.4 [Online].
90. Jin, I., E. R. Kandel, and R. D. Hawkins. 2005. The roles of PKA, PKC, and CamKII in facilitation at Aplysia sensory-motor neuron synapses depend on the duration of exposure to 5HT. Soc. Neurosci. Abstr. 540.5 [Online].
91. Kandel, E. R. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294: 1030-1038.
92. Kandel, E. R., T. Abrams, L. Bernier, T. J. Carew, R. D. Hawkins, and J. H. Schwartz. 1983. Classical conditioning and sensitization share aspects of the same molecular cascade in Aplysia. Cold Spring Harbor Symp. Quant. Biol. 48: 821-830.
93. Kim, J. H., H. Udo, H. L. Li, T. Y. Youn, M. Chen, E. R. Kandel, and C. H. Bailey. 2003. Presynaptic activation of silent synapses and growth of new synapses contribute to intermediate and long-term facilitation in Aplysia. Neuron 40: 151-165.
94. Klein, M., J. Camardo, and E. R. Kandel. 1982. Serotonin modulates a specific potassium current in the sensory neurons that show presynaptic facilitation in Aplysia. Proc. Natl. Acad. Sci. USA 79: 5713-5717.
95. Lamprecht, R., and J. LeDoux. 2004. Structural plasticity and memory. Nat. Rev. Neurosci. 5: 45-54.
96. Levenson, J. M., and J. D. Sweatt. 2005. Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci. 6: 108-118 [Online].
97. Li, H., B. S. H. Huang, and E. R. Kandel. 2004. Innervation-dependent clustering of glutamate receptors during regeneration and plasticity-associated synaptogenesis in Aplysia. Soc. Neurosci. Abstr. 614.18 [Online].
98. + from postsynaptic intracellular stores, postsynaptic exocytosis, and modulation of postsynaptic AMPA receptor efficacy. J. Neurosci. 25: 5623-5637.
99. Lin, X. Y., and D. L. Glanzman. 1994a. Hebbian induction of long-term potentiation of Aplysia sensorimotor synapses: partial requirement for activation of a NMDA-related receptor. Proc. R. Soc. Lond. B 255: 215-221.
100. Lin, X. Y., and D. L. Glanzman. 1994b. Long-term potentiation of Aplysia sensorimotor synapses in cell culture: regulation by postsynaptic voltage. Proc. R. Soc. Lond. B 255: 113-118.
101. Lonze, B. E., and D. D. Ginty. 2002. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35: 605-623.
102. 2+ and CamKII contribute to LTP at synapses between individual CA3 neurons. Proc. Natl. Acad. Sci. USA 103: 4264-4269.
103. Mackey, S. L., E. R. Kandel, and R. D. Hawkins. 1989. Identified serotonergic neurons LCB1 and RCB1 in the cerebral ganglia of Aplysia produce presynaptic facilitation of siphon sensory neurons. J. Neurosci. 9: 4227-4235.
104. Maletic-Savatic, M., R. Malinow, and K. Svoboda. 1999. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283: 1923-1927.
105. Malgaroli, A., A. E. Ting, B. Wendland, A. Bergamaschi, A. Villa, R. W. Tsien, and R.H. Scheller. 1995. Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science 268: 1624-1628.
106. Malinow, R., and R. C. Malenka. 2002. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25: 103-126.
107. Malinow, R., Z. F. Mainen, and Y. Hayashi. 2000. LTP mechanisms: from silence to four-lane traffic. Can. Opin. Neurobiol. 10: 352-357.
108. Marcus, E. A., T. G. Nolen, C. H. Rankin, and T. J. Carew. 1988. Behavioral dissociation of dishabituation, sensitization, and inhibition in Aplysia. Science 241: 210-213.
109. Marinesco, S., and T. J. Carew. 2002. Serotonin release evoked by tail nerve stimulation in the CNS of Aplysia: characterization and relationship to heterosynaptic plasticity. J. Neurosci. 22: 2299-2312.
110. Martin, K. C., D. Michael, J. C. Rose, M. Barad, A. Casadio, H. Zhu, and E. R. Kandel. 1997a. MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18: 899-912.
111. Martin, K. C., A. Casadio, H. Zhu, E. Yaping, J. C. Rose, M. Chen, C. H. Bailey, and E. R. Kandel. 1997b. Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91: 927-938.
112. Martin, S. J., P. D. Grimwood, and R. G. Morris. 2000. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23: 649-711.
113. Matsuzaki, M., N. Honkura, G. C. R. Ellis-Davies, and H. Kasai. 2004. Structural basis of long-term potentiation in single dendritic spines. Nature 429: 761-766.
114. Mauelshagen, J., G. R. Parker, and T. J. Carew. 1996. Dynamics of induction and expression of long-term synaptic facilitation in Aplysia. J. Neurosci. 16: 7099-7108.
115. Mayford, M., A. Barzilai, F. Keller, S. Schacher, and E. R. Kandel. 1992. Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in Aplysia. Science 256: 638-644.
116. Miesenbock, G., D. A. De Angelis, and J. E. Rothman. 1998. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394: 192-195.
117. Milner, B. 1985. Memory and the human brain. Pp. 1864-1869 in How We Know, M. Shafto, ed. Harper and Rowe, San Francisco.
118. Montarolo, P. G., P. Goelet, V. F. Castellucci, J. Morgan, E. R. Kandel, and S. Schacher. 1986. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234: 1249-1254.
119. 2+. Proc. Natl. Acad. Sci. USA 93: 9931-9936.
120. Murphy, G. G., and D. L. Glanzman. 1997. Mediation of classical conditioning in Aplysia californica by long-term potentiation of sensorimotor synapses. Science 278: 467-471.
121. Murphy, G. G., and D. L. Glanzman. 1999. Cellular analog of differential classical conditioning in Aplysia: disruption by the NMDA receptor antagonist DL-2-amino-5-phosphono-valerate. J. Neurosci. 19: 10595-10602.
122. Nakanishi, K., F. Zhang, D. A. Baxter, A. Eskin, and J. H. Byrne. 1997. Role of calcium-calmodulin-dependent protein kinase II in modulation of sensorimotor synapses in Aplysia. J. Neurophysiol. 78: 409-416.
123. Nikonenko, I., P. Jourdain, and D. Muller. 2003. Presynaptic remodeling contributes to activity-dependent synaptogenesis. J. Neurosci. 24: 8498-8505.
124. Ninan, I., and O. Arancio. 2004. Presynaptic CamkII is necessary for synaptic plasticity in cultured hippocampal neurons. Neuron 42: 129-141.
125. Ocorr, K. A., E. T. Walters, and J. H. Byrne. 1985. Associative conditioning analog selectively increases cAMP levels of tail sensory neurons in Aplysia. Proc. Natl. Acad. Sci. USA 82: 2548-2552.
126. Perazzona, B., G. Isabel, T. Preat, and R. L. Davis. 2004. The role of cAMP response element-binding protein in Drosophila long-term memory. J. Neurosci. 24: 8823-8828.
127. Perlman, A. J. 1979. Central and peripheral control of siphon-withdrawal reflex in Aplysia californica. J. Neurophysiol. 42: 510-529.
128. Pinsker, H., I. Kupfermann, V. Castellucci, and E. R. Kandel. 1970. Habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167: 1740-1742.
129. Polster, M. R., L. Nadel, and D. L. Schachter. 1991. Cognitive neuroscience: an analysis of memory: a historical perspective. J. Cogn. Neurosci. 3: 95-116.
130. Purcell, A. L., S. K. Sharma, M. W. Bagnall, M. A. Sutton, and T. J. Carew. 2003. Activation of a tyrosine kinase-MAPK cascade enhances the induction of long-term synaptic facilitation and long-term memory in Aplysia. Neuron 37: 473-484.
131. Ramanan, N., Y. Shen, S. Sarsfield, T. Lemberger, G. Schutz, D. J. Linden, and D. D. Ginty. 2005. SRF mediates activity-induced gene expression and synaptic plasticity but not neuronal viability. Nat. Neurosci. 8: 759-767.
132. Roberts, A. C., and D. L. Glanzman. 2003. Learning in Aplysia: looking at synaptic plasticity from both sides. Trends Neurosci. 26: 662-670.
133. Ryan, T. A., N. E. Ziv, and S. J. Smith. 1996. Potentiation of evoked vesicle turnover at individually resolved synaptic boutons. Neuron 17: 125-134.
134. Schacher, S., F. Wu, and Z.-Y. Sun. 1997. Pathway-specific synaptic plasticity: activity-dependent enhancement and suppression of long-term heterosynaptic facilitation at converging inputs on a single target. J. Neurosci. 17: 597-606.
135. Sharma, S. K., M. W. Bagnall, M. A. Sutton, and T. J. Carew. 2003a. Inhibition of calcineurin facilitates the induction of memory for sensitization in Aplysia: requirement of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 100: 4861-4866.
136. Sharma, S. K., C. M. Sherff, J. Shobe, M. W. Bagnall, M. A. Sutton, and T. J. Carew. 2003b. Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia. J. Neurosci. 23: 3899-3907.
137. Si, K., S. Lindquist, and E. R. Kandel. 2003a. A neuronal isoform of the Aplysia CPEB has prion-like properties. Cell 115: 879-891.
138. Si, K. M. Giustetto, A. Etkin, R. Hsu, A. M. Janisiewicz, M. C. Miniaci, J. H. Kim, H. Zhu, and E. R. Kandel. 2003b. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in Aplysia. Cell 115: 893-904.
139. Squire, L. R., and S. Zola-Morgan. 1991. The medial temporal lobe memory system. Science 253: 1380-1386.
140. Steward, O., and E. M. Schuman. 2001. Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24: 299-325.
141. Steward, O., and E. M. Schuman. 2003. Compartmentalized synthesis and degradation of proteins in neurons. Neuron 40: 347-359.
142. Sutton, M. A., and T. J. Carew. 2000. Parallel molecular pathways mediate expression of distinct forms of intermediate-term facilitation at tail sensory-motor synapses in Aplysia. Neuron 26: 219-231.
143. Sutton, M. A., and E. M. Schuman. 2005. Local translational control in dendrites and its role in long-term synaptic plasticity. J. Neurobiol. 64: 116-131.
144. Sutton, M. A., S. E. Masters, M. W. Bagnall, and T. J. Carew. 2001. Molecular mechanisms underlying a unique intermediate phase of memory in Aplysia. Neuron 31: 143-154.
145. Theis, M., K. Si, and E. R. Kandel. 2003. Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus. Proc. Natl. Acad. Sci. USA 100: 9602-9607.
146. Thompson, K. R., K. O. Otis, D. Y. Chen, Y. Zhao, T. J. O'Dell, and K. C. Martin. 2004. Synapse to nucleus signaling during long-term synaptic plasticity: a role for the classical active nuclear import pathway. Neuron 44: 997-1009.
147. Tischmeyer, W., and R. Grimm. 1999. Activation of immediate early genes and memory formation. Cell. Mol. Life Sci. 55: 564-574.
148. Tompa, P., and P. Friedrich. 1998. Prion proteins as memory molecules: an hypothesis. Neuroscience 86: 1037-1043.
149. Toni, N., P. A. Buchs, I. Nikonenko, C. R. Bron, and D. Muller. 1999. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402: 421-425.
150. Trudeau, L. E., and V. F. Castellucci. 1993. Excitatory amino acid neurotransmission of sensory-motor and interneuronal synapses of Aplysia californica. J. Neurophysiol. 70: 1221-1230.
151. Udo, H., I. Jin, J. H. Kim, H. L. Li, T. Youn, R. D. Hawkins, E. R. Kandel, and C. H. Bailey. 2005. Serotonin-induced regulation of the actin network for learning-related synaptic growth requires Cdc42, N-WASP, and PAK in Aplysia sensory neurons. Neuron 45: 887-901.
152. Waddell, S., and W. G. Quinn. 2001. Flies, genes, and learning. Annu. Rev. Neurosci. 24: 1283-1309.
153. Walters, E. T. 1989. Transformation of siphon responses during conditioning of Aplysia suggests a model of primitive stimulus-response association. Proc. Natl. Acad. Sci. USA 86: 7616-7619.
154. Walters, E. T., and J. H. Byrne. 1983. Associative conditioning of single sensory neurons suggests a cellular mechanism for learning. Science 219: 405-408.
155. Wang, H.-G., F.-M. Lu, I. Jin, H. Udo, E. R. Kandel, J. de Vente, U. Walter, S. M. Lohmann, R. D. Hawkins, and I. Antonova. 2005. Presynaptic and postsynaptic roles of NO, cGK, and RhoA in long-lasting potentiation and aggregation of synaptic proteins. Neuron 45: 389-403.
156. Winder, D. G., I. M. Mansuy, M. Osman, T. M. Moallem, and E. R. Kandel. 1998. Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell 92: 25-37.
157. Yin, J. C., J. S. Wallach, M. Del Vecchio, E. L. Wilder, H. Zhou, W. G. Quinn, and T. Tully. 1994. Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79: 49-58.
158. Yin, J. C., M. Del Vecchio, H. Zhou, and T. Tully. 1995. CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81: 107-115.
159. Zakharenko, S. S., S. L. Patterson, I. Dragatsis, S. O. Zeitlin, S. A. Siegelbaum, E.R. Kandel, and A. Morozov. 2003. Presynaptic BDNF required for a presynaptic but not a postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39: 975-990.