The past, the future and the biology of memory storage

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 354, Issue 1392, 1999, Pages 2027-2052

  Kandel, Eric R ^a   Pittenger, Christopher ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Explicit; Implicit; Memory

Indexed keywords

ANIMALIA;

EID: 0033616145     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.1999.0542     Document Type: Article

References (164)

1. Abel, T. & Kandel, E. 1998 Positive and negative regulatory mechanisms that mediate long-term memory storage. Brain Res. Rev. 26, 360-378.
2. Adams, R. D., Victor, M. & Ropper, A. H. 1997 Principles of neurology. New York: McGraw-Hill.
3. Agranoff, B. W. 1976 Biochemical concomitants of the storage of behavioral information. Biochem. Sensory Funct. 597-623.
4. Ahn, S., Ginty, D. D. & Linden, D. J. 1999 A late phase of cerebellar long-term depression requires activation of CaMKIV and CREB. Neuron 23, 559-568.
5. Alberini, C. M., Ghirardi, M., Metz, R. & Kandel, E. R. 1994 C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76, 1099-1114.
6. Alheid, G. F., de Olmos, J. S. & Beltramino, C. A. 1995 Amygdala and extended amygdala. In The rat nervous system (ed. G. Paxinos). San Diego, CA: Academic Press.
7. Anagnostaras, S. G., Maren, S. & Fanselow, M. S. 1999 Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. J. Neurosci. 19, 1106-1114.
8. Arancio, O., Kicbler, M., Lee, C. J., Lev-Ram, V., Tsien, R. Y., Kandel, E. R. & Hawkins, R. D. 1996 Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87, 1025-1035.
9. Atkins, C. M., Selcher, J. C., Petraitis, J. J., Trzaskos, J. M. & Sweatt, J. D. 1998 The MAPK cascade is required for mammalian associative learning. Nature Neurosci. 1, 602-609.
10. Bach, M. E., Barad, M., Son, H., Zhuo, M., Lu, Y. F., Shih, R., Mansuy, I., Hawkins, R. D. & Kandel, E. R. 1999 Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc. Natl Acad. Sci. USA 96, 5280-5285.
11. Bacskai, B. J., Hochner, B., Mahaut-Smith, M., Adams, S. R., Kaang, B. K., Kandel, E. R. & Tsien, R. Y. 1993 Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science 260, 222-226.
12. Bailey, C. H. & Kandel, E. R. 1993 Structural changes accompanying memory storage. A. Rev. Physiol. 55, 397-426.
13. Barnes, C. A. 1979 Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 93, 74-104.
14. Bartsch, D., Ghirardi, M., Skehel, P. A., Karl, K. A., Herder, S. P., Chen, M., Bailey, C. H. & Kandel, E. R. 1995 Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 83, 979-92.
15. Bartsch, D., Casadio, A., Karl, K. A., Serodio, P. & Kandel, E. R. 1998 CREB1 encodes a nuclear activator, a repressor, and a cytoplasmic modulator that form a regulatory unit critical for long-term facilitation. Cell 95, 211-23.
16. Bartsch, D., Bourtchouladze, R., Patterson, S., Karl, K. A., Chen, A., Till, S., Gordon, R., Osman, M. & Kandel, E. R. 1999 Toward a model of the learning and memory deficit in Down syndrome: transgenic mice with tetracycline regulated minibrain kinase expression in the hippocampus. Soc. Neurosci. Abstr. (In the press.)
17. Bergson, H. 1913 Matter and memory. New York: Macmillan.
18. Blendy, J. A., Kaestner, K. H., Schmid, W., Gass, P. & Schutz, G. 1996 Targeting of the gene leads to up-regulation of a novel CREB mRNA isoform. EMBO J. 15, 1098-106.
19. Bliss, T. V. & Lømo, T. 1973 Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331-356.
20. Bolshakov, V. Y. & Siegelbaum, S. A. 1995 Regulation of hippocampal transmitter release during development and long-term potentiation. Science 269, 1730-1734.
21. Bolshakov, V. Y., Golan, H., Kandel, E. R. & Siegelbaum, S. A. 1997 Recruitment of new sites of synaptic transmission during the cAMP-dependent late phase of LTP at CA3-CA1 synapses in the hippocampus. Neuron 19, 635-651.
22. Bontempi, B., Laurent-Demir, C., Destrade, C. & Jaffard, R. 1999 Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature 400, 671-675.
23. Bourtchouladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G. & Silva, A. J. 1994 Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79, 59-68.
24. Bourtchouladze, R., Abel, T., Berman, N., Gordon, R., Lapidus, K. & Kandel, E. R. 1998 Different training procedures recruit one or two critical periods for context memory consolidation, each of which requires proteins synthesis and PKA. Learn. Mem. 5, 365-374.
25. Braha, O., Dale, N., Hochner, B., Klein, M., Abrams, T. W. & Kandel, E. R. 1990 Second messengers involved in the two processes of presynaptic facilitation that contribute to sensitization and dishabituation in Aplysia sensory neurons. Proc. Natl Acad. Sci. USA 87, 2040-2044.
26. Broca, P. 1865 Sur le siége de la faculté du langage articulé. Bull. Soc. Anthropol. 6, 377-393.
27. Brogden, W. J. & Gantt, W. H. 1937 Cerebellar conditioned reflexes. Am. J. Physiol. 119, 277-278.
28. Brunelli, M., Castellucci, V. & Kandel, E. R. 1976 Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. Science 194, 1178-1181.
29. Burkner, R. L., Kelley, W. M. & Petersen, S. E. 1999 Frontal cortex contributes to human memory formation. Nature Neurosci. 2, 311-314.
30. Byrne, J. H. & Kandel, E. R. 1996 Presynaptic facilitation revisited: state and time dependence. J. Neurosci. 16, 425-435.
31. Cahill, L., Prins, B., Weber, M. & McGaugh, J. L. 1994 Beta-adrenergic activation and memory for emotional events. Nature 371, 702-704.
32. Cajal, S. R. y 1893 Neue Darstellung vom Histologischen Bau des Centralnervensystem. Arch. Anat. Entwick. 319-428.
33. Calabresi, P., Pisani, A., Centonze, D. & Bernardi, G. 1997 Synaptic plasticity and physiological interactions between dopamine and glutamate in the striatum. Neurosci. Biobehav. Rev. 21, 519-523.
34. Carew, T. J. & Sahley, C. L. 1986 Invertebrate learning and memory: from behavior to molecules. A. Rev. Neurosci. 9, 435-487.
35. Castellucci, V. & Kandel, E. R. 1976 Presynaptic facilitation as a mechanism for behavioral sensitization in Aplysia. Science 194, 1176-1178.
36. Castellucci, V. F., Frost, W. N., Goelet, P., Montarolo, P. G., Schacher, S., Morgan, J. A., Blumenfeld, H. & Kandel, E. R. 1986 Cell and molecular analysis of long-term sensitization in Aplysia. J. Physiol. 81, 349-357.
37. Clugnet, M. C. & LeDoux, J. E. 1990 Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body. J. Neurosci. 10, 2818-2824.
38. Cooter, R. 1984 The cultural meaning of popular science: phrenology and hte organization of consent in nineteenth-century Britain. New York: Cambridge University Press.
39. Copplestone, F. 1977 Modern philosophy. A history of philosophy. New York: Doubleday.
40. Corkin, S. 1965 Tactually guided maze learning in man: effects of unilateral cortical excisions and bilateral hippocampal lesions. Neuropsychologia 3, 339-351.
41. Crick, F. & Mitchison, G. 1983 The function of dream sleep. Nature 304, 111-114.
42. Davis, G. W., Schuster, C. M. & Goodman, C. S. 1996 Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron 17, 669-679.
43. Davis, R. L. 1996 Physiology and biochemistry of Drosophila learning mutants. Physiol. Rev. 76, 299-317.
44. De Zeeuw, C. I., Hansel, C., Bian, F., Koekkoek, S. K., Van Alphen, A. M., Linden, D. J. & Oberdick, J. 1998 Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20, 495-508.
45. Denk, W., Yuste, R., Svoboda, K. & Tank, D. W. 1996 Imaging calcium dynamics in dendritic spines. Curr. Opin. Neurobiol. 6, 372-378.
46. Ebbinghaus, H. 1913 Memory: a contribution to experimental psychology. New York: Columbia University Teachers College.
47. Editorial 1999 Probing the brain with DNA chips. Nature Neurosci. 2, 1.
48. Elbert, T., Pantev, C., Wienbruch, C., Rockstroh, B. & Taub, E. 1995 Increased cortical representation of the fingers of the left hand in string players. Science 270, 305-307.
49. English, J. D. & Sweatt, J. D. 1996 Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J. Biol. Chem. 271, 24329-24332.
50. Ferrier, D. 1890 The Croonian lectures on cerebral localization. London: Smith, Elder.
51. Flexner, L. B., Flexner, J. B., De La Haba, G. & Roberts, R. B. 1965 Loss of memory as related to inhibition of cerebral protein synthesis. J. Neurochem. 12, 535-541.
52. Flourens, P. 1893 Récherches expérimentales. Archiv. Gén.de Méd. II, 321-370.
53. Freeman, F. M., Rose, S. P. & Scholey, A. B. 1995 Two time windows of anisomycin-induced amnesia for passive avoidance training in the day-old chick. Neurobiol. Learn. Mem. 63, 291-295.
54. Frey, U. & Morris, R. G. 1997 Synaptic tagging and long-term potentiation. Nature 385, 533-536.
55. Gaffan, D. 1998 Idiothetic input into object-place configuration as the contribution to memory of the monkey and human hippocampus: a review. Exp. Brain Res. 123, 201-209.
56. Gall, F. J. & Spurzheim, G. 1810 Anatomie et physiologie due systeme nerveux en general, et du cerveau en particulier, avec des observations sur la possibilite de reconnoitre plusieurs disopsitions intellectuelles et morales de l'homme et des animaux, par la configuration de leurs tetes. Paris: Schoell.
57. Gallagher, M. & Pelleymounter, M. A. 1988 An age-related spatial learning deficit: choline uptake distinguishes 'impaired' and 'unimpaired' rats. Neurobiol. Aging 9, 363-369.
58. Giese, K. P., Fedorov, N. B., Filipkowski, R. K. & Silva, A. J. 1998 Autophosphorylation at Thr28G of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279, 870-873.
59. Glanzman, D. L. 1995 The cellular basis of classical conditioning in Aplysia californica it's less simple than you think. Trends Neurosci. 18, 30-36.
60. Graybiel, A. M. 1995 Building action repertoires: memory and learning functions of the basal ganglia. Curr. Opin. Neurobiol. 5, 733-741.
61. Graybiel, A. M. 1998 The basal ganglia and chunking of action repertoires. Neurobiol. Learn. Mem. 70, 119-36,
62. Grotewiel, M. S., Beck, C. D., Wu, K. H., Zhu, X. R. & Davis, R. L. 1998 Integrin-mediated short-term memory in Drosophila. Nature 391, 455-460.
63. Gu, Q. A., Bear, M. F. & Singer, W. 1989 Blockade of NMDA-receptors prevents ocularity changes in kitten visual cortex after reversed monocular deprivation. Brain Res. Dev. Brain Res. 47, 281-288.
64. Hawkins, R. D., Kandel, E. R. & Siegelbaum, S. A. 1993 Learning to modulate transmitter release: themes and variations in synaptic plasticity. A. Rev. Neurosci. 16, 625-665.
65. Hebb, D. O. 1949 The organization of behavior. New York: Wiley.
66. Hegde, A. N., Inokuchi, K., Pei, W., Casadio, A., Ghirardi, M., Chain, D. G., Martin, K. C., Kandel, E. R. & Schwartz, J. H. 1997 Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89, 115-126.
67. Hegde, A. N., Casadio, A., Martin, K., Inokuchi, K., Pei, W., Giustetto, M., Kandel, E. R. & Schwartz, J. H. 1999 Induction of the polypeptide chain elongation factor EFla is required for the late long-term facilitation in Aplysia. Soc. Neurosci. Abstr. (In the press.)
68. Hevroni, D. (and 15 others) 1998 Hippocampal plasticity involves extensive gene induction and multiple cellular mechanisms. J. Mol. Neurosci. 10, 75-98.
69. Huang, Y. Y. & Kandel, E. R. 1998 Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21, 169-178.
70. Huang, Y. Y., Li, X. C. & Kandel, E. R. 1994 cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79, 69-79.
71. Huang, Y. Y., Kandel, E. R., Varshavsky, L., Brandon, E. P., Qi, M., Idzerda, R. L., McKnight, G. S. & Bourtchouladze, R. 1995 A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell 83, 1211-1222.
72. Hummler, E., Cole, T. J., Blendy, J. A., Ganss, R., Aguzzi, A., Schmid, W., Beermann, F. & Schutz, G. 1994 Targeted mutation of the CREB gene: compensation within the CREB/ATF family of transcription factors. Proc. Natl Acad. Sci. USA 91, 5647-5651.
73. Impey, S., Mark, M., Villacres, E. C., Poser, S., Chavkin, C. & Storm, D. R. 1996 Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 16, 973-982.
74. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation, Neuron 21, 869-883.
75. Impey, S., Smith, D. M., Obrietan, K., Donahue, R., Wade, C. & Storm, D. R. 1998b Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nature Neurosci. 1, 595-601.
76. Jackson, J. H. 1884 The Croonian lectures on evolution and dissolution of the nervous system. Br. Med. J. 1, 591-593; 660-663; 703-707.
77. James, W. 1890 The principles of psychology. New York: Henry Holt (1890). New York: Dover Publications (1950).
78. Jenkins, W. M., Merzenich, M. M., Ochs, M. T., Allard, T. & Guic-Robles, E. 1990 Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. J. Neurophysiol. 63, 82-104.
79. Kaas, J. H., Merzenich, M. M. & Killackey, H. P. 1983 The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. A. Rev. Neurosci. 6, 325-356.
80. Kandel, E. R. 1976 Cellular basis of behavior: an introduction to behavioral biology. San Francisco, CA: W. H. Freeman & Co.
81. Kandel, E. R., Schwanz, J. H. & Jessell, T. M. 1995 Essentials of neural science and behavior. Stamford, CT: Appleton & Lange.
82. Kang, H. & Schuman, E. M. 1995 Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658-1662.
83. Kentros, C., Hargreaves, E., Hawkins, R. D., Kandel, E. R., Shapiro, M. & Muller, R. V. 1998 Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280, 2121-2126.
84. Lashley, K. S. 1929 Brain mechanisms and intelligence: a quantitative study of injuries to the brain. Chicago University Press.
85. LeDoux, J. E. 1998 Fear and the brain: where have we been, and where are we going? Biol. Psychiat. 44, 1229-1238.
86. LeDoux, J. E. 1996 The emotional brain: the mysterious underpinnings of emotional life. New York: Simon & Schuster.
87. Liao, D., Hessler, N. A. & Malinow, R. 1995 Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400-404.
88. Lin, X. Y. & Glanzman, D. L. 1994 Hebbian induction of long-term potentiation of Aplysia sensorimotor synapses: partial requirement for activation of an NMDA-related receptor. Proc. R. Soc. Lond. B 255, 215-221.
89. Linden, D. J. 1999 The return of the spike: postsynaptic action potentials and the induction of LTP and LTD. Neuron 22, 661-666.
90. Linden, D. J. & Connor, J. A. 1995 Long-term synaptic depression. A. Rev. Neurosci. 18, 319-357.
91. Lisman, J. E., Fellous, J. M. & Wang, X. J. 1998 A role for NMDA-receptor channels in working memory. Nature Neurosci. 1, 273-275.
92. 2+/calmodulin-dependent protein kinase molecules of the postsynaptic density. Proc. Natl Acad. Sci. USA 85, 5320-5324.
93. Llinás, R. & Walton, K. D. 1998 Cerebellum. In The synaptic organization of the brain (ed. G. Shepherd). New York: Oxford University Press.
94. McHugh, T. J., Blum, K. I., Tsien, J. Z., Tonegawa, S. & Wilson, M. A. 1996 Impaired hippocampal representation of spare in CA1-specific NMDAR1 knockout mice. Cell 87, 1339-1349.
95. Maguire, E. A., Frackowiak, R. S. J. & Frith, C. D. 1997 Recalling routes around London: activation of the right hippocampus in taxi drivers. J. Neurosci. 17, 7103-7110.
96. Maletic-Savatic, M., Malinow, R. & Svoboda, K. 1999 Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923-1927.
97. Marr, D. 1969 A theory of cerebellar cortex. J. Physiol. 202, 437-470.
98. Marr, D. 1971 Simple memory: a theory for archicortex. Phil. Trans. R. Soc. Lond. B 262, 23-81.
99. Mars, W. M., Zarnegar, R. & Michalopoulos, G. K. 1993 Activation of hepatocyte growth factor by the plasminogen activators uPA and tPA. Am. J. Pathol. 143, 949-958.
100. Martin, K. C., Casadio, A., Zhu, H., E, Y., Rose, J. C., Chen, M., Bailey, C. H. & Kandel, E. R. 1997a Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91, 927-938.
101. Martin, K. C., Michael, D., Rose, J. C., Barad, M., Casadio, A., Zhu, H. & Kandel, E. R. 1997b MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18, 899-912.
102. Mayford, M., Barzilai, A., Keller, F., Schacher, S. & Kandel, E. R. 1992 Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in Aplysia. Science 256, 638-644.
103. Mayford, M., Mansuy, I. M., Muller, R. U. & Kandel, E. R. 1997 Memory and behavior: a second generation of genetically modified mice. Curr. Biol. 7, R580-R589.
104. Merzenich, M. M., Nelson, R. J., Stryker, M. P., Cynader, M. S., Schoppmann, A. & Zook, J. M. 1984 Somatosensory cortical map changes following digit amputation in adult monkeys. J. Comp. Neurol. 224, 591-605.
105. Michael, D., Martin, K. C., Seger, R., Ning, M. M., Baston, R. & Kandel, E. R. 1998 Repeated pulses of serotonin required for long-term facilitation activate mitogen-activated protein kinase in sensory neurons of Aplysia. Proc. Natl Acad. Sci. USA 95, 1864-1869.
106. Milner, B., Squire, L. R. & Kandel, E. R. 1998 Cognitive neuroscience and the study of memory. Neuron 20, 445-468.
107. Montarolo, P. G., Goelet, P., Castellucci, V. F., Morgan, J., Kandel, E. R. & Schacher, S. 1986 A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234, 1249-1254.
108. Muller, D. 1997 Ultrastructural plasticity of excitatory synapses. Rev. Neurosci. 8, 77-93.
109. Muller, R. U. & Kubie, J. L. 1987 The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 1951-968.
110. Muller, R. U., Kubie, J. L. & Ranck Jr, J. B. 1987 Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935-1950.
111. Murphy, G. G. & Glanzman, D. L. 1997 Mediation of classical conditioning in Aplysia californica by long-term potentiation of sensorimotor synapses. Science 278, 467-471.
112. Nguyen, P. V. & Kandel, E. R. 1996 A macromolecular synthesis-dependent late phase of long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. J. Neurosci. 16, 3189-3198.
113. Nibuya, M., Nestler, E. J. & Duman, R. S. 1996 Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J. Neurosci. 16, 2365-2372.
114. Nicoll, R. A. & Malenka, R. C. 1999 Expression mechanisms underlying NMDA receptor-dependent long-term potentiation. Ann. NY Acad. Sci. 868, 515-525.
115. O'Keefe, J. & Nadel, L. 1978 The hippocampus as a cognitive map. Oxford, UK: Clarendon.
116. Patterson, S. L., Grover, L. M., Schwartzkroin, P. A. & Bothwell, M. 1992 Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 9, 1081-1088.
117. Patterson, S. L., Abel, T., Deuel, T. A., Martin, K. C., Rose, J. C. & Kandel, E. R. 1996 Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16, 1137-1145.
118. Patterson, S. L. et al. 2000 (In preparation.)
119. Penfield, W. & Perot, P. 1963 The brain's record of auditory and visual experience. Brain 86, 595-696.
120. Pham, T. A., Impey, S., Storm, D. R. & Stryker, M. P. 1999 CRE-mediated gene transcription in neocortical neuronal plasticity during the developmental critical period. Neuron 22, 63-72.
121. Pittenger, C. & Kandel, E. 1998 A genetic switch for long-term memory. C. R. Acad. Sci. III 321, 91-96.
122. Pittenger, C., Scanlin, H., Winder, D. & Kandel, K. E. 1999 Expression of a dominant negative CREB mutant restricted to striatum and pyriform cortex reveals a role for CREB in procedural memory for striatum-based tasks. Soc. Neurosci. Abstr. (In the press.)
123. Posner, M. I. & Raichle, M. E. 1998 The neuroimaging of human brain function. Proc Natl Acad. Sci. USA 95, 763-764.
124. Qian, Z., Gilbert, M. E., Colicos, M. A., Kandel, E. R. & Kuhl, D. 1993 Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 361, 453-457.
125. Rempel-Clower, N. L., Zola, S. M., Squire, L. R. & Amaral, D. G. 1996 Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. J. Neurosci. 16, 5233-5255.
126. Robbins, T. W. & Everitt, B. J. 1999 Drug addiction: bad habits add up. Nature 398, 567-570.
127. Rogan, M. T., Staubli, U. V. & LeDoux, J. E. 1997 Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390, 604-607. (Erratum published in Nature 391, 818.)
128. Rolls, E. T. & Treves, A. 1998 Neural networks and brain function. New York: Oxford.
129. Rotenberg, A., Mayford, M., Hawkins, R. D., Kandel, E. R. & Muller, R. U. 1996 Mice expressing activated CaMKII lack low frequency LTP and do not form stable place cells in the CA1 region of the hippocampus. Cell 87, 1351-1361.
130. Rotenberg, A., Abel, T., Kandel, E. R. & Muller, R. U. 1997 The firing fields of place cells in mice with impaired late-phase LTP are crisp but move to unpredictable locations. Soc. Neurosci. Abstr. (In the press.)
131. Rudolph, D., Tafuri, A., Gass, P., Hammerling, G. J., Arnold, B. & Schutz, G. 1998 Impaired fetal T cell development and perinatal lethality in mice lacking the cAMP response clement binding protein. Proc. Natl Acad. Sci. USA 95, 4481-4486.
132. Ryle, G. 1949 The concept of mind. University of Chicago Press.
133. Sanes, J. R. & Lichtman, J. W. 1999 Can molecules explain long-term potentiation? Nature Neurosci. 2, 597-604.
134. Schacter, D. L. 1996 Searching for memory: the brain, the mind, and the past. New York: BasicBooks.
135. Schuster, C. M., Davis, G. W., Fetter, R. D. & Goodman, C. S. 1996 Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 17, 655-667.
136. Scoville, W. B. & Milner, B. 1957 Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiat. 20, 11-21.
137. Selkoe, D. J. 1999 Translating cell biology into therapeutic advances in Alzheimer's disease. Nature 399, A23-A31.
138. Sgambato, V., Pages, C., Rogard, M., Besson, M. J. & Caboche, J. 1998 Extracellular signal-regulated kinase (ERK) controls immediate early gene induction on corticostriatal stimulation. J. Neurosci. 18, 8814-8825.
139. Skaggs, W. E. & McNaughton, B. L. 1996 Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271, 1870-1873.
140. Skoulakis, E. M. & Davis, R. L. 1998 14-3-3 proteins in neuronal development and function. Mol. Neurobiol. 16, 269-284.
141. Smith, E. E. & Jonides, J. 1999 Storage and executive processes in the frontal lobes. Science 283, 1657-1661.
142. Sorra, K. E. & Harris, K. M. 1998 Stability in synapse number and size at 2 hr after long-term potentiation in hippocampal area CA1. J. Neurosci. 18, 658-671.
143. Spencer, W. A. & Kandel, E. R. 1961 Electrophysiology of hippocampal neurons. IV. Fast prepotentials. J. Neurophysiol. 24, 260-271.
144. Squire, L. R. & Kandel, E. R. 1999 Memory: from mind to molecules. Scientific American Library. New York: Scientific American.
145. Squire, L. R. & Zola-Morgan, S. 1991 The medial temporal lobe memory system. Science 253, 1380-1386.
146. Swain, R. A. H., Shinkman, P. G., Nordholm, A. F. & Thompson, R. F. 1992 Cerebellar stimulation as an unconditioned stimulus in classical conditioning. Behav. Neurosci. 106, 739-750.
147. Teng, E. & Squire, L. R. 1999 Memory for places learned long ago is intact after hippocampal damage. Nature 400, 675-677.
148. Thompson, R. F., Thompson, J. K., Kim, J. J., Krupa, D. J. & Shinkman, P. G. 1998 The nature of reinforcement in cerebellar learning. Neurobiol. Learn. Mem. 70, 150-176.
149. Tulving, E. 1972 Episodic and semantic memory. In Organization of memory (ed. E. Tulving & W. Donaldson), pp. 607-628. New York: Academic Press.
150. Tulving, E., Schacter, D. L. & Stark, H. 1982 Priming effects in word-fragment completion are independent of recognition memory. J. Exp. Psychol.: Learn. Mem. Cogn 8, 336-342.
151. Tulving, E., Schacter, D. L., McLachlan, D. R. & Moscovitch, M. 1988 Priming of semantic autobiographical knowledge: a case study of retrograde amnesia. Brain Cogn 8, 3-20.
152. Uttl, B. & Graf, P. 1993 Episodic spatial memory in adulthood. Pychol. Aging 8, 257-273.
153. Vargha-Khadem, F., Gadian, D. G., Watkins, K. E., Connelly, A., Van Paesschen, W. & Mishkin, M. 1997 Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376-380. (Erratum published in Science 277, 1117.)
154. Weiner, J. 1999 Time, love, memory: a great biologist and his quest for the origins of behavior. New York: Knopf.
155. Weiskrantz, L. 1956 Behavioral changes associated with ablation of teh amygdaloid complex in monkeys. J. Comp. Physiol. Psychol. 49, 381-391.
156. Wernicke, K. 1908 The symptom-complex of aphasia. In Diseases of the nervous system (ed. A. Church), pp. 265-324. New York: Appleton.
157. Winder, D. G., Martin, K. C., Muzzo, I., Rohrer, D., Chruscinski, A., Kobilka, B. & Kandel, E. R. 1999 ERK plays a regulatory role in the induction of LTP by theta frequency stimulation and its modulation by β-adrenergic receptors. Neuron 24, 1-20.
158. Yin, J. C., Wallach, J. S., Del Vecchio, M., Wilder, E. L., Zhou, H., Quinn, W. G. & Tully, T. 1994 Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79, 49-58.
159. Yin, J. C., Del Vecchio, M., Zhou, H. & Tully, T. 1995 CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81, 107-115.
160. Young, R. M. 1970 Mind, brain, and adaptation in the nineteenth century. Oxford: Clarendon Press.
161. Zamanillo, D. (and 16 others) 1999 Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284, 1805-1811.
162. Zeki, S. 1993 A vision of the brain. Boston, MA: Oxford.
163. Zola-Morgan, S., Squire, L. R. & Amaral, D. G. 1986 Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J. Neurosci. 6, 2950-2967.
164. Zubin, J. & Barrera, S. E. 1941 Effect of electric convulsive therapy on memory. Proc. Soc. Exp. Biol. Med. 48, 596-597.