Memory formation and the regulation of gene expression

Cellular and Molecular Life Sciences

Volumn 55, Issue 4, 1999, Pages 575-592

  Stork, O ^a   Welzl, H ^b  

^a NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Consolidation; Gene transcription; Long term memory; Neuronal plasticity; Protein synthesis

Indexed keywords

ION CHANNEL;

GENE EXPRESSION; GENETIC TRANSCRIPTION; INVERTEBRATE; LEARNING; LONG TERM MEMORY; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN SYNTHESIS; REVIEW; SYNAPTIC TRANSMISSION; VERTEBRATE;

ANIMALS; BIRDS; GENE EXPRESSION REGULATION; MEMORY;

EID: 0032897880     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s000180050316     Document Type: Review

References (221)

1. James W. (1890) The Principles of Psychology (2 vols), Holt, Rinehart and Winston, New York
2. Davis H. P. and Squire L. R. (1984) Protein synthesis and memory: a review. Psychol. Bull. 96: 518-559
3. Lee K. S., Schottler F., Oliver M. and Lynch G. (1980) Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus. J. Neurophysiol. 44: 247-258
4. Chang F. F. and Greenough W. T. (1984) Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice. Brain Res. 309: 35-46
5. Bailey C. H. and Kandel E. R. (1993) Structural changes accompanying memory storage. Ann. Rev. Physiol. 55: 397-426
6. Moser M.-B., Trommald M. and Andersen P. (1994) An increase in dendritic spine densitiy on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc. Natl. Acad. Sci. USA 91: 12673-12675
7. Atwood H. L., Dixon D. and Wojtowicz J. M. (1989) Rapid introduction of long-lasting synaptic changes at crustacean neuromuscular junctions. J. Neurophysiol. 20: 373-385
8. Wojtowicz J. M., Marin L. and Atwood H. L. (1989) Synaptic restructuring during long-term facilitation at the crayfish neuromuscular junction. Can. J. Physiol. Pharmacol. 67: 167-171
9. Tobin A. J. (1994) Gene expression in the mammalian nervous system. In: Basic Neurochemistry, pp. 493-513, Siegel C. J., Agranoff B. W., Albers R. W., Fisher S. K., Uhler M. D. et al. (eds). Raven Press, New York
10. Silva A. J., Kogan J., Frankland P. W. and Kida S. (1998) CREB and memory. Annu. Rev. Neurosci. 21: 127-148
11. Sceburg P. H., Higuchi M. and Sprengel R. (1998) RNA editing of brain glutamte receptor channels: mechanism and physiology. Brain Res. Rev. 26: 217-229
12. Garner C. C., Tucker R. and Matus A. (1988) Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature 336: 674-677
13. Tucker R. P., Garner C. and Matus A. (1989) In situ localization of microtubule-associated protein mRNA in the developing and adult rat brain. Neuron 2: 1245-1256
14. Link W., Konietzko U., Kauselmann G., Krug M., Schwanke B., Frey U. et al. (1995) Somatodendritic expression of immediate early gene is regulated by synaptic activity. Proc. Natl. Acad. Sci. USA 92: 5734-5738
15. Nakova B., Kvetnansky R., McMahon A., Viskupic E., Hiremagalur B., Frankle G. et al. (1994) Induction of tyrosine hydroxylase gene expression by a nonneuronal nonpituitary-mediated mechanism in immobilization stress. Proc. Natl. Acad. Sci. USA 91: 5937-5941
16. Smeyne R. J., Schilling K., Robertson L., Luk D., Oberdick J., Curran T. et al. (1992) fos-IacZ transgenic mice: mapping sites of gene induction in the central nervous system. Neuron 8: 13-23
17. Anokhin K. V., Mileusnic R., Shamakina I. Y. and Rose S. P. R. (1991) Effects of early experience on c-fos gene expression in the chick forebrain. Brain Res. 544: 101-107
18. Anokhin K. V. and Rose S. P. R. (1991) Learning-induced increase of immediate early gene messenger RNA in the chick forebrain. Eur. J. Neurosci. 3: 162-167
19. Campeau S., Hayward M. D., Hope B. T., Rosen J. B., Nestler E. J. and Davis M. (1991) Induction of the c-fos proto-oncogene in rat amygdala during unconditioned and conditoned fear. Brain Res. 565: 349-352
20. Campeau S., Falls W., Cullinan W. E., Helmreich D. L., Davis M. and Watson S. J. (1997) Elicitation and reduction of fear: behavioural and neuroendocrine indices and brain induction of the immediate-early gene c-fos. Neurosci. 78: 1087-1104
21. Berger T. S. C., Kraushaar U. and Monyer H. (1998) Dentate gyrus basket cell GABAA receptors are blocked by Zn2 + via changes of their desensitization kinetics: an in situ patch-clamp and single-cell PCR study. J. Neurosci. 18: 2437-2448
22. Mack K. J., Yi S.-D., Chang S., Millan N. and Mack P. (1995) NGFI-C expression is affected by physiological stimulation and seizure in the somatosensory cortex. Mol. Brain Res. 29: 140-146
23. Singh T. D., Mizuno K., Kohno T. and Nakamura S. (1997) BDNF ad trkB mRNA expression in neurons of the neonatal mouse barrel field cortex: normal development and plasticity after cauterizing facial vibrissae. Neurochem. Res. 22: 791-797
24. Rodger J., Davis S., Laroche S., Mallet J. and Hicks A. (1998) Induction of long-term potentiation in vivo regulates alternate splicing to alter syntaxin 3 isoform expression in rat dentate gyrus. J. Neurochem. 71: 666-675
25. Diatchenko L., Lau Y. F., Campbell A. P., Chenchik A., Moqadam F., Huang B. et al. (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl. Acad. Sci. USA 93: 6025-6030
26. Nedivi E., Hevroni D., Naot D., Israeli D. and Citri Y. (1993) Numerous canditate plasticity-related genes revealed by differential cDNA cloning. Nature 363: 718-722
27. Douglass J., McKinzie A. A. and Couceyro P. (1995) PCR differential display identifies a rat brain mRNA that is transcriptionally regulated by cocaine and amphetamine. J. Neurosci. 15: 2471-2481
28. Huang A. M., Wang H., Tang Y. P. and Lee E. H. (1998) Impression of integrin-associated protein gene associated with memory formation in rats. J. Neurosci. 18: 4305-4513
29. Wan J., Sharp S. J., Poirier G. M.-C., Wagaman P. C., Chambers J., Pyati J. et al. (1996) Cloning differentially expressed mRNAs. Nature Biotech. 14: 1685-1691
30. Barzilai A., Kennedy T. E., Sweatt J. D. and Kandel E. R. (1989) 5-HT modulates protein synthesis and the expression of specific proteins during long-term facilitation in Aplysia sensory neurons. Neuron 2: 1577-1586
31. Beck C. H. M. and Fibiger H. C. (1995) Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment. J. Neurosci. 15: 709-720
32. Bailey C. H., Chen M., Keller F. and Kandel E. R. (1992) Serotonin-mediated endocytosis of apCAM: an early step of learning-related synaptic growth in Aplysia. Science 256: 645-649
33. Schuster T., Krug M., Hassan H. and Schachner M. (1998) Increase in proportion of hippocampal spine synapses expressing neural cell adhesion molecule NCAM180 following long-term potentiation. J. Neurobiol. 37: 359-372
34. Rose S. P. R. (1995) Cell-adhesion molecules, glucocorticoids and long-term-memory formation. Trends Neurosci. 18: 502-506
35. Doyle E., Nolan P. M., Bell R. and Regan C. M. (1992) Hippocampal NCAM 180 transiently increases sialylation during the acquisition and consolidation of a passive avoidance response in the adult rat. J. Neurosci. Res. 31: 513-523
36. Gale E. F., Cundliffe E., Reynolds P. E., Richmond M. H. and Waring M. J. (1981) The Molecular Basis of Antibiotic Action, 2nd ed., John Wiley, London
37. Reich E. (1963) Biochemistry of actinomycins. Cancer Res. 23: 1428-1441
38. Chabner B. A., Allegra C. J., Curt G. A. and Calabresi P. (1995) Antineoplastic agents. In: Goodman & Gilman's The Pharmacological Basis of Therapeutics, 9th ed., pp. 1233-1287, Hardman J. G., Limbird L. E., Molinoff P. B., Ruddon R. W. and Goodman Gilman A. (eds), McGraw-Hill, New York
39. Squire L. R. and Barondes S. H. (1970) Actinomycin-D: effects on memory at different times after training. Nature 225: 649-650
40. Flood J. F., Rosenzweig M. R., Bennett E. L. and Orme A. E. (1973) The influence of duration of protein synthesis inhibition on memory. Physiol. Behav. 10: 555-562
41. Pestka S. (1971) Inhibitors of ribosome function. Ann. Rev. Microbiol. 25: 487-562
42. Flood J. F., Rosenzweig M. R., Bennett E. L. and Orme A. E. (1972) Influence of training strength on amnesia induced by pretraining injections of cycloheximide. Physiol. Behav. 9: 589-600
43. Tsien J. Z., Chen D. F., Gerber D., Tom C., Mercer E. H., Anderson D. J. et al. (1996) Subregion-and cell type-restricted gene knockout in mouse brain. Cell 87: 1317-1326
44. Kojima N., Wang J., Mansuy I. M., Grant S. G., Mayford M. and Kandel E. R. (1997) Rescuing impairment of long-term potentiation in fyn-deficient mice by introducing Fyn transgene. Proc. Natl. Acad. Sci. USA 94: 4761-4765
45. Mansuy I. M., Mayford M., Jacob B., Kandel E. R. and Bach M. E. (1998) Restricted and regulated overexpression reveals calcineurin as a key component in the transition from short-term to long-term memory. Cell 92: 39-49
46. Olson E. N., Arnold H.-H., Rigby P. W. J. and Wold B. J. (1996) Know your neighbors: three phenotypes in null mutnats of the myogenic bHLH gene MRF4. Cell 85: 1-4
47. Crusio W. E. (1996) Gene-targeting studies: new methods, old problems. Trends Neurosci. 19: 186-187
48. Gerlai R. (1996) Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends Neurosci. 19: 177-181
49. Shockett P., Difillippantonio M., Hellman N. and Schatz D. G. (1995) A modified tetracycline-regulated system provides autoregulatory, inducible gene expression in cultured cells and transgenic mice. Proc. Natl. Acad. Sci. USA 92: 6522-6526
50. Saez E., No D., West A. and Evans R. M. (1997) Inducible gene expression in mammalian cells and transgenic mice. Curr. Opin. Biotechnol. 8: 608-616
51. Tischmeyer W., Grimm R., Schicknick H., Brysch W. and Schlingensiepen K. H. (1994) Sequence-specific impairment of learning by c-jun antisense oligonucleotides. Neuroreport 5: 1501-1504
52. Lamprecht R., Hazvi S. and Dudai Y. (1997) cAMP response element-binding protein in the amygdala is required for long-but not short-term conditioned taste aversion memory. J. Neurosci. 17: 8443-8450
53. Pettit D. L., Perlman S. and Malinow R. (1994) Potentiated transmission and prevention of further LTP by increased CaMKII activity in postsynaptic hippocampal slice neurons. Science 266: 1881-1885
54. Korte M., Griesbeck O., Gravel C., Carroll P., Staiger V., Thoenen H. et al. (1996) Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. Proc. Natl. Acad. Sci. USA 93: 12547-12552
55. NcNamara J. O., Bonhaus D. W. and Shin C. (1993) The kindling model of epilepsy. In: Epilepsy: Models, Mechanisms and Concepts, pp. 27-47, Schwartzkroin P. A. (ed.). Cambridge University Press, Cambridge
56. Sutula T., Xiao-Xian H., Cavazos J. and Scott G. (1988) Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 239: 1147-1150
57. Cavazos J. E., Golarai G. and Sutula T. P. (1991) Mossy fibre synaptic reorganization induced by kindling: time course of development, progression and permanence. J. Neurosci. 11: 2795-2803
58. Cain D. P., Corcoran M. E. and Staines W. A. (1980) Effects of protein synthesis inhibition on kindling in the mouse. Exp. Neurol. 68: 409-419
59. Jones L. S., Grooms S. Y., Lapadula D. M. and Lewis D. V. (1992) Protein synthesis inhibition blocks maintenance but not induction of epileptogenesis in hippocampal slice. Brain Res. 599: 338-344
60. Morgan J. I. and Curran T. (1991) Proto-oncogene transcription factors and epilepsy. Trends Pharmacol. Sci. 12: 343-349
61. Labiner D. M., Butler L. S., Cao Z., Hosford D. A., Shin C. and McNamara J. O. (1993) Induction of c-fos mRNA by kindled seizures: complex relationship with neuronal burst firing. J. Neurosci. 13: 744-751
62. Qian Z., Gilbert M. E., Colicos M. A., Kandel E. R. and Kuhl D. (1993) Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 361: 453-457
63. Ernfors P., Bengzon J., Kokaia Z., Persson H. and Lindvall O. (1991) Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron 7: 165-176
64. Bengzon J., Kokaia Z., Ernfors P., Kokaia M., Leanza G., Nilsson O. G. et al. (1993) Regulation of neurotrophin and trkA, trkB and trkC tyrosine kinase receptor messenger RNA expression in kindling. Neurosci. 53: 433-446
65. Schwarzer C., Sperk G., Samanin R., Rizzi M., Gariboldi M. and Vezzani A. (1996) Neuropeptides-immunoreactivity and their mRNA expression in kindling: functional implications for limbic epileptogenesis. Brain Res. Rev. 22: 27-50
66. Pratt G. D., Kokaia M., Bengzon J., Kokaia Z., Fritschy J.-M., Möhler H. et al. (1993) Differential regulation of N-methyl-D-aspartate receptor subunit messenger RNAs in kindling-induced epileptogenesis. Neurosci. 57: 307-318
67. Clark M., Smith M. A., Weiss S. R. B. and Post R. M. (1994) Modulation of hippocampal glucocorticoid and mineralocorticoid receptor mRNA expression by amygdaloid kindling. Neuroendocrinol. 59: 451-456
68. Kamphuis W., De Rijk T. C., Talamini L. M. and Lopes da Silva F. H. (1994) Rat hippocampal kindling induces changes in the glutamate receptor mRNA expression patterns in dentate granule neurons. Eur. J. Neurosci. 6: 1119-1127
69. Kamphuis W. and da Silva F. (1995) Editing status of the Q R site of glutamate receptor-A, -B, -5 and -6 subunit mRNA in the hippocampal kindling model of epilepsy. Mol. Brain Res. 29: 35-42
70. A receptor subunit mRNA levels in dentate gyrus granule cells following recurrent kindling-induced seizures. Mol. Brain Res. 23: 323-332
71. Akbar M. T., Rattray M., Powell J. F. and Meldrum B. S. (1996) Altered expression of group I metabotropic glutamate receptors in the hippocampus of amygdala-kindled rats. Mol. Brain Res. 43: 105-116
72. Elmer E., Alm P., Kokaia Z., Kokaia M., Larsson B., Andersson K. E. et al. (1996) Regulation of neuronal nitric oxide synthase mRNA levels in rat brain by seizure activity. Neuroreport 7: 1335-1339
73. Bliss T. V. P. and Collingridge G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39
74. Richter-Levin G., Collingridge L. and Bliss T. V. (1995) Long-term potentiation and glutamate release in the dentate gyrus: links to spatial learning. Behav. Brain Res. 66: 37-40
75. Maren S. and Fanselow M. (1995) Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J. Neurosci. 15: 7548-7564
76. Rogan M. T., Staubli U. and LeDoux J. E. (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390: 604-607
77. Frey U., Krug M., Reymann K. G. and Matthies H. (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res. 452: 57-65
78. Stanton P. K. and Sarvey J. M. (1984) Blockade of long-term potentiation in rat hippocampal CAI region by inhibitors of protein synthesis. J. Neurosci. 4: 3080-3088
79. Huang Y.-Y., Li X.-C. and 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
80. Nguyen P. V., Abel T. and Kandel E. R. (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265: 1104-1107
81. Namgung U., Valcourt E. and Routtenberg A. (1995) Long-term potentiation in vivo in the intact mouse hippocampus. Brain Res. 689: 85-92
82. Linden D. J. (1996) A protein synthesis-dependent late phase of cerebellar long-term depression. Neuron 17: 483-490
83. Frey U. and Morris R. G. M. (1998) Synaptic tagging: implications for late maintainance of hippocampal long-term potentiation. Trends Neurosci. 21: 181-188
84. Otani S., Marshall C. J., Tate W. P., Goddard G. V. and Abraham W. C. (1989) Maintenance of long-term potentiation in rat dentate gyrus requires protein synthesis but not messenegr RNA synthesis immediately post-tetanization. Neurosci. 28: 519-526
85. Steward O. and Levy W. B. (1982) Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dendate gyrus. J. Neurosci. 2: 284-291
86. Steward O. and Reeves T. M. (1988) Protein-synthetic machinery beneath postsynaptic sites on CNS neurons: association between polyribosomes and other organelles at the synaptic site. J. Neurosci. 8: 176-184
87. Impey S., Mark M., Villacres E. C., Poser S., Chavkin C. and 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
88. Abel T., Nguyen P. V., Barad M., Deuel T. A. S., Kandel E. R. and Bourtchouladze R. (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88: 615-626
89. Bourtchuladze R., Frenguelli B., Blendy J., Cioffi D., Schutz G. and 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
90. Abraham W. C., Dragunow M. and Tate W. P. (1991) The role of immediate early genes in the stabilization of long-term potentiation. Mol. Neurobiol. 5: 297-314
91. Williams J., Dragunow M., Lawlor P., Mason S., Abraham W. C., Leah J. et al. (1995) Krox20 may play a key role in the stabilization of long-term potentiation. Mol. Brain Res. 28: 87-93
92. Castrén E., Pitkänen M., Sirviö J., Parsadanian A., Lindholm D., Thoenen H. et al. (1993) The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. Neuroreport 4: 895-898
93. Bramham C. R., Sourthard T., Sarvey J. M., Herkenham M. and Brady L. S. (1996) Unilateral LTP triggers bilateral increases in hippocampal neurotrophin and trk receptor mRNA expression in behaving rats: evidence for interhemispheric communication. J. Comp. Neurol. 368: 371-382
94. Dragunow M., Hughes P., Mason-Parker S. E., Lawlor P. and Abraham W. C. (1997) TrkB expression in dentate granule cells is associated with a late phase of long-term potentiation. Mol. Brain Res. 46: 274-280
95. Roberts L. A., Large C. H., O'Shaughnessy C. T. and Morris B. J. (1997) Long-term potentiation in perforant path, granule cell synapses is associated with a post-synaptic induction of proenkephalin gene expression. Neurosci. Lett. 227: 205-208
96. Smirnova T., Laroche S., Errington M. L., Hicks A. A., Bliss T. V. P. and Mallet J. (1993) Transsynaptic expression of a presynaptic glutamate receptor during hippocampal long-term potentiation. Science 262: 433-436
97. Nayak A., Zastrov D. J., Lickteig R., Zahniser N. R. and Browning M. D. (1998) Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature 394: 680-683
98. Korte M., Kang H. Bonhoeffer T. and Schuman E. (1998) A role for BDNF in the late-phase of hippocampal long-term potentiation. Neuropharmacol. 37: 553-559
99. Korte M., Caroll P., Wolf E., Brem G., Thoenen H. and Bonhoeffer T. (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA 92: 8856-8860
100. Martin K. C., Casadio A., Zhu H., Yaping E., Rose J. C., Chen M. et al. (1997) 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. Castellucci V. F., Blumenfeld H., Goelet P. and Kandel E. R. (1989) Inhibitor of protein synthesis blocks long-term behavioral sensitization in the isolated gill-withdrawal reflex in Aplysia. J. Neurobiol. 20: 1-9
102. Montarolo P. G., Goelet P., Castellucci V. F., Morgan J., Kandel E. R. and Schacher S. (1986) A critical period of macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234: 1249-1254
103. Bailey C. H., Montarolo P., Chen M., Kandel E. R. and Schacher S. (1992) Inhibitors of protein and RNA synthesis block structural changes that accompany long-term heterosynaptic plasticity in Aplysia. Neuron 9: 749-758
104. O'Leary F. A., Byrne J. H. and Cleary L. J. (1995) Long-term structural remodeling in Aplysia sensory neurons requires de novo protein synthesis during a critical time period. J. Neurosci. 15: 3519-3525
105. Mayford M., Barzilai A., Keller F., Schacher S. and Kandel E. R. (1992) Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in Aplysia. Science 256: 638-644
106. Castellucci V. F., Kennedy T. E., Kandel E. R. and Goelet P. (1988) A quantitative analysis of 2-D gels identifies proteins in which labeling is increased following long-term sensitization in Aplysia. Neuron 1: 321-328
107. Alberini C., Ghirardi M., Metz R. and Kandel E. R. (1994) CEBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76: 1099-1114
108. Hedge A. N., Inokuchi K., Pei W., Casadio A., Ghirardi M., Chain D. G. et al. (1997) Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89: 115-126
109. Zwartjes R. E., West H., Hattar S., Ren X., Noel F., Nuñez-Regueiro M. et al. (1998) Identification of specific mRNAs affected by treatments producing long-term facilitation in Aplysia. Learn. Mem. 4: 478-495
110. Kuhl D., Kennedy T. E., Barzilai A. and Kandel E. R. (1992) Long-term sensitization training in Aplysia leads to an increase in the expression of BiP, the major protein chaperon of the ER. J. Cell Biol. 119: 1069-1076
111. Hu Y., Barzilai A., Chen M., Bailey C. H. and Kandel E. R. (1993) 5-HT and cAMP induce the formation of coated pits and vesicles and increase the expression of clathrin light chain in sensory neurons of Aplysia. Neuron 10: 921-929
112. Noel F., Nuñez-Regueiro M., Cook R., Byrne J. H. and Eskin A. (1993) Long-term changes in synthesis of intermediate filament protein, actin and other proteins in pleural sensory neurons of Aplysia produced by an in vitro analogue of sensitization training. Mol. Brain Res. 19: 203-210
113. Kennedy T. E., Kuhl D., Barzilai A., Sweatt J. D. and Kandel E. R. (1992) Long-term sensitization training in Aplysia leads to an increase in calreticulin, a major presynaptic calcium-binding protein. Neuron 9: 1013-1024
114. Trudeau L. E. and Castellucci V. F. (1995) Postsynaptic modifications in long-term facilitation in Aplysia: upregulation of excitatory amino acid receptors. J. Neurosci. 15: 1275-1284
115. Alkon D. L., Ikeno H., Dworkin J., McPhie D. L., Olds J. L., Lederhendler I. et al. (1990) Contraction of neuronal branching volume: an anatomical correlate of Pavlovian conditioning. Proc. Natl. Acad. Sci. USA 87: 1611-1614
116. Ramirez R. R., Gandhi C. C., Muzzio I. A. and Matzel L. D. (1998) Protein synthesis-dependent memory and neuronal enhancement in Hermissenda are contingent on parameters of training and retention. Learn. Mem. 4: 462-477
117. Crow T. and Forrester J. (1990) Inhibition of protein synthesis blocks long-term enhancement of generator potentials produced by one-irial in vivo conditioning in Hermissenda. Proc. Natl. Acad. Sci. USA 87: 4490-4494
118. Crow T., Siddiqi V. and Dash P. K. (1997) Long-term enhancement but not short-term in Hermissenda is dependent upon mRNA synthesis. Neurobiol. Learn. Mem. 68: 343-350
119. Nelson T. J. and Alkon D. L. (1988) Prolonged RNA changes in the Hermissenda eye induced by classical conditioning. Proc. Natl. Acad. Sci. USA 85: 7800-7804
120. Nelson T. J. and Alkon D. L. (1990) Specific high molecular weight mRNAs induced by associative learning in Hermissenda. Proc. Natl. Acad. Sci. USA 87: 269-273
121. Nelson T. J., Collin C. and Alkon D. L. (1990) Isolation of a G protein that is modified by learning and reduces potassium currents in Hermissenda. Science 247: 1479-1483
122. Tully T., Preat T., Boynton S. C. and Del Vecchio M. (1994) Genetic dissection of consolidated memory in Drosophila melanogaster. Cell 79: 35-47
123. Yin J. C., Wallach J., Del Vecchio M., Wilder E. L., Zhou H., Quinn W. G. et al. (1994) Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79: 49-58
124. Yin J. C., Del Vecchio M., Zhou H. and 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
125. Schuster C. M., Davis G. W., Fetter R. D. and Goodman C. S. (1996) Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron 17: 641-654
126. Davis G. W., Schuster C. M. and 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
127. Schuster C. M., Davis G. W., Fetter R. D. and 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
128. Jaffe K. (1980) Effect of cycloheximide on protein synthesis and memory in praying mantis. Physiol. Behav. 25: 367-371
129. Wittstock S., Kaatz H.-H. and Menzel R. (1993) Inhibition of brain protein synthesis by cycloheximide does not affect formation of long-term memory in honeybees after olfactory conditioning. J. Neurosci. 13: 1379-1386
130. Wittstock S. and Menzel R. (1994) Color learning and memory in honey bees are not affected by protein synthesis inhibition. Behav. Neural Biol. 62: 224-229
131. Grünbaum L. and Müller U. (1998) Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honey bee. J. Neurosci. 18: 4384-4392
132. Gibbs M. E. and Lecanuet J.-P. (1981) Disruption of imprinting by memory inhibitors. Anim. Behav. 29: 572-580
133. Horn G., Bradley P. and McCabe B. J. (1985) Changes in the structure of synapses associated with learning. J. Neurosci. 5: 3161-3168
134. Bateson P. P. G., Horn G. and Rose S. P. R. (1969) Effects of an imprinting procedure on regional incorporation of tritiated leucine into proteins of chick brain. Nature 223: 534-535
135. Horn G., McCabe B. J. and Bateson P. P. G. (1979) An autoradiographic study of the chick brain after imprinting. Brain Res. 168: 361-373
136. Rose S. P. R. (1977) Early visual experience, learning and neurochemical plasticity in the rat and chick. Phil. Trans. R. Soc. London B 278: 307-318
137. Brown M. W. and Horn G. (1990) Are specific proteins implicated in the learning process of imprinting? Dev. Brain Res. 52: 294-297
138. McCabe B. J. and Horn G. (1994) Learning-related changes in Fos-like immunoreactivity in the chick forebrain alter imprinting. Proc. Natl. Acad. Sci. USA 91: 11417-11421
139. Meberg P. J., McCabe B. J. and Routtenberg A. (1996) MARCKS and protein F1/GAP-43 mRNA in chick brain: effects of imprinting. Mol. Brain Res. 35: 149-156
140. Ambalavanar R., McCabe B. J. and Horn G. (1993) Fos-like immunoreactivity in γ-aminobutyric acid (GABA)-containing neurones in a forebrain region of the domestic chick. J. Physiol. 467: 350P
141. Ambalavanar R., Van der Zee E. A., Bolhuis J. J., McCabe B. J. and Horn G. (1993) Co-expression of Fos immunoreactivity in protein kinase (PKCγ)-positive neurones: quantitative analysis of a brain region involved in learning. Brain Res. 606: 315-318
142. A receptor γ4-subunit gene: anatomical distribution of the corresponding mRNA in the domestic chick fort-brain and the effect of imprinting training. Eur. J. Neurosci. 10: 3024-3028
143. Solomonia R. O., McCabe B. J., Jackson A. P. and Horn G. (1997) Clathrín proteins and recognition memory. Neurosci. 80: 59-67
144. Godard R. (1991) Long-term memory of individual neighbours in a migratory songbird. Nature 350: 228-229
145. Chew S. J., Vicario D. S. and Nottebohm F. (1996) Quantal duration of auditory memories. Science 274: 1909-1914
146. Mello C. V., Vicario D. S. and Clayton D. F. (1992) Song presentation induces gene expression in the songbird forebrain. Proc. Natl. Acad. Sci. USA 89: 6818-6822
147. Mello C., Nottebohm F. and Clayton D. (1995) Repeated exposure to one song leads to a rapid and persistent decline in an immediate early gene's response to that song in zebra finch telencephalon. J. Neurosci. 15: 6919-6925
148. Nastiuk K. L., Mello C. V., George J. M. and Clayton D. F. (1994) Immediate-early gene responses in the avian song control system: cloning and expression analysis of the canary c-jun cDNA. Mol. Brain Res. 27: 299-309
149. Chew S. J., Mello C., Nottebohm F., Jarvis E. and Vicario D. S. (1995) Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain. Proc. Natl. Acad. Sci. USA 92: 3406-3410
150. Vicario D. S. and Nottebohm F. (1998) Quantal memory durations: observations not reproduced. Science 279: 1437
151. Rose S. P. R. (1991) How chicks make memories: the cellular cascade from c-fos to dendritic remodelling. Trends Neurosci. 14: 390-397
152. Sojka M., Davies H. A., Harrison E. and Stewart M. G. (1995) Long-term increases in synaptic density in chick CNS after passive avoidance training are blocked by an inhibitor of protein synthesis. Brain Res. 684: 209-214
153. Stewart M. G. (1991) Changes in dendritic and synaptic structure in chick forebrain consequent on passive avoidance learning. In: Neural and Behavioural Plasticity, pp. 305-328, Andrew R. J. (ed.), Oxford University Press, Oxford
154. Freeman F. M., Rose S. P. R. and 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
155. Tiunova A., Anokhin K. V., Rose S. P. R. and Mileusnic R. (1996) Involvement of glutamate receptors, protein kinases and protein synthesis in memory for visual discrimination in the young chick. Neurobiol. Learn. Mem. 65: 233-243
156. Tiunova A., Anokhin K. V. and Rose S. P. R. (1998) Two critical periods of protein and glycoprotein synthesis in memory consolidation for visual categorization learning in chicks. Learn. Mem. 4: 401-410
157. Mileusnic R., Rose S. P. R. and Tillson P. (1980) Passive avoidance learníng results in region-specific changes in concentration of and incorporation into colehicine-binding proteins in chick forebrain. J. Neurochem. 34: 1007-1015
158. 3H]fucose into chick brain glycoproteins following training on a passive avoidance task. J. Neurochem. 34: 1000-1006
159. Bullock S., Rose S. P. R. and Zamani R. (1992) Characterisation and regional localisation of pre-and postsynaptic glycoproteins of the chick forebrain showing changed fucose incorporation following passive avoidance training. J. Neurochem. 58: 2145-2154
160. Scholey A. B., Rose S. P. R., Zamani M. R., Bock E. and Schachner M. (1993) A role for the neural cell adhesion molecule in a late, consolidating phase of glycoprotein synthesis six hours following passive avoidance training of the young chick. Neurosci. 55: 499-509
161. Scholey A. B., Mileusnic R., Schachner M. and Rose S. P. R. (1995) A role for a chicken homolog of the neural cell adhesion molecule L1 in consolidation of memory for a passive avoidance task in the chick. Learn. Mem. 2: 17-25
162. Sandi C. and Rose S. P. R. (1992) Protein synthesis-and fucosylation-dependent mechanisms in corticosterone facilitation of long-term memory in the chick. Behav. Neurosci. 111: 1098-1104
163. Rose S. P. R. and Jork R. (1987) Long-term memory in the chick is blocked by 2-deoxygalactose, a fucose analogue. Behav. Neural Biol. 48: 246-258
164. Bourne R. C., Davies D. C., Stewart M. G., Csillag A. and Cooper M. (1991) Cerebral glycoprotein synthesis and long-term memory formation in chick (Gallus domesticus) following passive avoidance training depends on the nature of the aversive stimulus. Europ. J. Neurosci. 3: 243-248
165. Quatermain D. and McEwen B. S. (1970) Temporal characteristics of amnesia induced by protein synthesis inhibitor: determination by shock level. Nature 228: 677-678
166. Quinton E. E. and Kramarcy N. R. (1977) Memory impairment correlates closely with cycloheximide dose and degree of inhibition of protein synthesis. Brain Res. 131: 184-190
167. Stäubli U., Faraday R. and Lynch G. (1985) Pharmacological dissociation of memory: anisomycin, a protein synthesis inhibitor, and leupeptin, a protease inhibitor, block different learning tasks. Behav. Neural Biol. 43: 287-297
168. Lee E. H. Y., Hung H. C., Lu K. T., Chen W. H. and Chen H. Y. (1992) Protein synthesis in the hippocampus associated with memory facilitation by corticotropin-releasing factor in rats. Peptides 13: 927-937
169. Berman R. F., Kesner R. P. and Partlow L. M. (1978) Passive avoidance impairment in rats following cycloheximide injection into the amygdala. Brain Res. 158: 171-188
170. Flood J. F., Bennett E. L., Orme A. E. and Rosenzweig M. R. (1975) Effects of protein synthesis inhibition on memory for active avoidance. Physiol. Behav. 14: 177-184
171. Flood J. F., Jarvik M. E., Bennett E. L., Orme A. E. and Rosenzweig M. R. (1977) Protein synthesis inhibition and memory for pole jump active avoidance and extinction. Pharmacol. Biochem. Behav. 7: 71-77
172. Nikolaev E., Kaminska B., Tischmeyer W., Matthies H. and Kaczmarek L. (1992) Induction of expression of genes encoding transcription factors in the rat brain elicited by behavioral training. Brain Res. Bull. 28: 479-484
173. Squire L. R. and Barondes S. H. (1974) Anisomycin, like other inhibitors of cerebral protein synthesis, impairs 'long-term' memory of a discrimination task. Brain Res. 66: 301-308
174. Malefant S. A., Barry M. and Fleming A. S. (1991) Effects of cycloheximide on the retention of olfactory learning and maternal experience effects in postpartum rats. Physiol. Behav. 49: 289-294
175. Grecksch G. and Matthies H. (1980) Two sensitive periods for the amnesíc effect of anisomycin. Pharmacol. Biochem. Behav. 12: 663-665
176. Grimm R. and Tischmeyer W. (1997) Complex patterns of immediate early gene induction in rat brain following brightness discrimination training and pseudotraining. Behav. Brain Res. 84: 109-116
177. 3H]fucose into rat hippocampus after acquisition of a brightness discrimination reaction. An electrophoretic study. Neurosci. 5: 161-167
178. Meiri N. and Rosenblum K. (1998) Lateral ventricle injection of the protein synthesis inhibitor anisomycin impairs long-term memory in a spatial memory task. Brain Res. 789: 48-55
179. Guzowski J. F. and McGaugh J. L. (1997) Antisense ologideoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc. Natl. Acad. Sci. USA 94: 2693-2698
180. Paylor R., Johnson R., Papaioannou V., Spiegelman B. M. and Wehner J. M. (1994) Behavioral assessment of c-fos mutant mice. Brain Res 651: 275-282
181. Cavallaro S., Meiri N., Yi C.-L., Musco S., Ma W., Goldberg J. et al. (1997) Late memory-related genes in the hippocampus revealed by RNA fingerprinting. Proc. Natl. Acad. Sci. USA 94: 9669-9673
182. Murphy K. J., O'Connell A. W. and Regan C. M. (1996) Repetitive and transient increases in hippocampal neural cell adhesion molecule polysialylation state following multitrial spatial training. J. Neurochem. 67: 1268-1274
183. O'Connell A. W., Fox G. B., Barry T., Murphy K. J., Fichera G., Foley A. G. et al. (1997) Spatial learning activates neural cell adhesion molecule polysialylation in a corticohippocampal pathway within the medial temporal lobe. J. Neurochem. 68: 2538-2546
184. Davis S., Rodger J., Hicks A., Mallet J. and Laroche S. (1996) Brain structure and task-specific increases in expression of the gene encoding syntaxin 1B during learning in the rat: a potential molecular marker for learning-induced synaptic plasticity in neural networks. Eur. J. Neurosci. 8: 2068-2074
185. Schmaltz G. and Marcant P. (1983) Transient aversion and long-lasting amnesia following cycloheximide injection in the rat. Physiol. Behav. 30: 845-852
186. Kogan J. H., Frankland P. W., Blendy J. A., Coblentz J., Marowitz Z., Schutz G. et al. (1997) Spaced training induces normal long-term memory in CREB mutant mice. Curr. Biol. 7: 1-11
187. Milanovic S., Radulovic J., Laban O., Stiedl O., Henn F. and Spiess J. (1998) Production of the Fos protein after contextual fear conditioning of C57BL/6N mice. Brain Res. 784: 37-47
188. Rosen J. B., Fanselow M., Young S. L., Siteoske M. and Maren S. (1998) Immediate-early gene expression in the amygdala following footshock stress and contextual fear conditioning. Brain Res. 796: 132-142
189. Sterneck E., Paylor R., Jackson-Lewis V., Libbey M., Przedborski S., Tessarollo L. et al. (1998) Selectively enhanced contextual fear conditioning in mice lacking the transcriptional regulator CCAAT/enhancer binding protein delta. Proc. Natl. Acad. Sci. USA 95: 10908-10913
190. Tucker A. and Gibbs M. (1976) Cycloheximide-induced amnesia for taste aversion memory in rats. Pharmacol. Biochem. Behav. 4: 181-184
191. Rosenblum K., Meiri N. and Dudai Y. (1993) Taste memory: the role of protein synthesis in gustatory cortex. Behav. Neural Biol. 59: 49-56
192. Bartsch D. G. M., Skehel P. A., Karl K. A., Herder S. P., Chen M., Bailey C. H. et al. (1995) Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 83: 979-992
193. Kandel E. R. and O'Dell T. J. (1992) Are adult learning mechanisms also used for development? Science 258: 243-245
194. Castrén E., Zafra F., Thoenen H. and Lindholm D. (1992) Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex. Proc. Natl. Acad. Sci. USA 89: 9444-9448
195. Rocamora N., Welker E., Pascual M. and Soriano E. (1996) Upregulation of BDNF mRNA expression in the barrel cortex of adult mice after sensory stimulation. J. Neurosci. 16: 4411-4419
196. Tiunova A., Anokhin K. V., Schachner M. and Rose S. P. R. (1998) Three time windows for amnestic effect of antibodies to cell adhesion molecule L1 in chicks. Neuroreport 9: 1645-1648
197. Sheng M. and Greenberg M. E. (1990) The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4: 477-485
198. Lapchak P. A., Araujo D. and Hefti F. (1993) BDNF and trkB mRNA expression in the rat hippocampus following entorhinal cortex lesions. Neuroreport 4: 191-194
199. Falkenberg T., Mohammed A. K., Henriksson B., Persson H., Winblad B. and Lindefors N. (1992) Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neurosci. Lett. 138: 153-156
200. Thoenen H. (1995) Neurotrophins and neuronal plasticity. Science 270: 593-598
201. Tongiorgi E., Righi M. and Cattaneo A. (1997) Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J. Neurosci. 17: 9492-9505
202. Sharp F. R., Gonzales M., Hisanaga K., Mobley W. C. and Sagar S. M. (1989) Induction of the c-fos gene product in rat forebrain following cortical lesions and NGF injections. Neurosci. Lett. 100: 117-122
203. Carnahan J and Nawa H (1995) Regulation of neuropeptide expression in the brain by neurotrophins. Potential role in vivo. Mol. Neurobiol. 10: 135-139
204. Lüthi A., Laurent S. P., Figurov A., Müller D. and Schachner M. (1994) Hippocampal long-term potentiation and neural cell adhesion molecules I.1 and NCAM. Nature 372: 777-779
205. Cremer H., Lange R., Christoph A., Plomann M., Vopper G., Roes J. et al. (1994) Inactivation of the NCAM gene in mice results in size-reduction of the olfactory bulb and deficts in spatial learning. Nature 367: 455-459
206. Jucker M., Mondadori C., Mohajeri H., Bartsch U. and Schachner M. (1995) Transient upregulation of NCAM mRNA in astrocytes in response to entorhinal cortex lesions and ischemia. Mol. Brain Res. 28: 149-156
207. Arami S., Jucker M., Schachner M. and Welzl H. (1996) The effect of continuous intraventricular infusion of I.1 and NCAM antibodies on spatial learning in rats. Behav. Brain Res. 81: 81-87
208. Rutishauser U. and Landmesser L. (1996) Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions. Trends Neurosci. 19: 422-427
209. Jacobsson G., Piehl F., Bark I. C., Zhang X. and Meister B. (1996) Differential subcellular localization of SNAP-25a and SNAP-25b RNA transcripts in spinal motoneurons and plasticity in expression after nerve injury. Mol. Brain Res. 37: 49-62
210. Collet J., Fehrat L., Pollard H., de Pouplana L. R., Charton G., Bernard A. et al. (1997) Developmentally regulated alternative splicing of mRNAs encoding N-terminal tau variants in the rat hippocampus: structural and functional implications. Eur. J. Neurosci. 9: 2723-2733
211. Yamaguchi S. and Nakanishi S. (1998) Regional expression and regulation of alternative forms of mRNAs derived from two distinct transcription initiation sites of the rat mGluR5 gene. J. Neurochem. 71: 60-68
212. Fields R. D. and Itoh K. (1996) Neural cell adhesion molecules in activity-dependent development and synaptic plasticity. Trends Neurosci. 19: 473-480
213. Kashiwabuchi N., Ikeda K., Araki K., Hirano T., Shibuki K., Takayama C. et al. (1995) Impairment of motor coordination, Purkinje cell synapse formation and cerebellar long-term depression in GluR delta 2 mutant mice. Cell 81: 245-252
214. Mayford M., Baranes D., Podsypanina K. and Kandel E. R. (1994) The 3'-untranslated region of CaMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc. Natl. Acad. Sci. USA 93: 13250-13255
215. Gelot A., Moreau J., Ben Ari Y. and Pollard H. (1996) Alpha-brain spectrin mRNA belongs to the population of intradendritically transported mRNAs. Neurereport 8: 113-116
216. Steward O. (1993) Molecular sorting in neurons: cell biological processes that play a role in synapse growth and plasticity. In: Synaptic Plasticity, pp. 13-43, Baudry M., Thompson R. F. and Davis J. L. (eds), Bradford Book, MIT Press, Cambridge, MA
217. Morris B. J. (1997) Stabilization of dendritic mRNAs by nitric oxide allows localized, activity-dependent enhancement of hippocampal protein synthesis. Eur. J. Neurosci. 9: 2334-2339
218. Martin K. C. and Kandel E. R. (1996) Cell adhesion molecules, CREB and the formation of new synaptic connections. Neuron 17: 567-570
219. Tully T. (1996) Discovery of genes involved with learning and memory: an experimental synthesis of Hirschian and Benzerian perspectives. Proc. Natl. Acad. Sci. USA 93: 13460-13467
220. Wehner J. M., Bowers B. and Paylor R. (1996) The use of null mutant mice to study complex learning and memory processes. Behav. Genet. 23: 301-312
221. Lopatina N. G., Sharagina L. and Chesnokova E. G. (1997) Genetic approaches to the study of memory in insects. Neurosci. Behav. Physiol. 27: 250-253