Structural changes accompanying memory storage

Annual Review of Physiology

Volumn 55, Issue , 1993, Pages 397-426

  Bailey, Craig H ^a   Kandel, Eric R ^a  

^a New York State Psychiatric Institute ^*  (United States)

Author keywords

active zone; learning; NCAM modulation; synapse formation; synaptic plasticity

Indexed keywords

ANISOMYCIN; CYCLIC AMP; DACTINOMYCIN; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BIRD; BRAIN; CHICKEN; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; MEMORY; MOLLUSC; NONHUMAN; PRIORITY JOURNAL; RABBIT; REVIEW; SYNAPTOGENESIS;

EID: 0027538548     PISSN: 00664278     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.ph.55.030193.002145     Document Type: Review

References (216)

1. Agranoff, B. W. 1967. Agents that block memory. In The Neurosciences: A Study Program, ed. G. C. Quarton, T. Melnechuk, F. O. Schmidt, pp. 756-64. New York: The Rockefeller Univ. Press
2. Alkon, D. L., Ikeno, H., Dworkin, J., McPhie, D. L., Olds, J. L., et al. 1990. Contraction of neuronal branching volume: An anatomic correlate of Pavlovian conditioning. Proc. Natl. Acad. Sci. USA 87:1611-14
3. Anderson, B., Relucio, K., Mohr, C., Logan, C., Knowlton, B., et al. 1991. Associated eye-blink conditioning, but not unpaired conditioning, causes morphological changes in Purkinje spiny branchlets. Soc. Neurosci. Abstr. 17: 869
4. Andrew, R. J. 1991. Neural and Behavioral Plasticity. The Use of the Domestic Chick as a Model. New York: Oxford Univ. Press
5. Applegate, M. D., Kerr, D. S., Landfield, P. N. 1987. Redistribution of synaptic vesicles during long-term potentiation in the hippocampus. Brain Res. 90:3401-6
6. Applegate, M. D., Landfield, P. N. 1988. Synaptic vesicle redistribution during hippocampal frequency potentiation and depression in young and aged rats. J. Neurosci. 8:1091-111
7. Arnold, A., Jordan, C. L. 1988. Hormonal organization of neural circuits. In Frontiers in Neuroendocrinology, ed. L. Martini, W. F. Ganong, pp. 185-213. New York: Raven
8. Atwood, H. L., Dixon, D., Wojtowicz, J. M. 1989. Rapid introduction of long-lasting synaptic changes at crustacean neuromuscular junctions. J. Neurobiol. 20:373-85
9. Atwood, H. L., Govind, C. K. 1990. Activity-dependent and age-dependent recruitment and regulation of synapses in identified crustacean neurons. J. Exp. Biol. 153:105-27
10. Atwood, H. L., Lnenicka, G. A. 1986. Structure and function in synapses: Emerging correlations. Trends Neurosci. 9:248-50
11. Atwood, H. L., Wojtowicz, J. M. 1986. Short-term and long-term plasticity and physiological differentiation of crustacean motor synapses. Int. Rev. Neurobiol. 28:275-362
12. Bailey, C. H. 1991. Morphological basis of short- and long-term memory in Aplysia. In Perspectives on Cognitive Neuroscience, ed. H. Weingartner, R. Lister, pp. 76-92. New York: Oxford Univ. Press
13. Bailey, C. H. 1992. Morphological basis of learning and memory: Invertebrates. In Encyclopedia of Learning and Memory, ed. L. Squire. New York: Macmillan. In press
14. Bailey, C. H., Chen, M. 1983. Morphological basis of long-term habituation and sensitization in Aplysia. Science 220:91-93
15. Bailey, C. H., Chen, M. 1988. Morphological basis of short-term habituation in Aplysia. J. Neurosci. 8: 2452-59
16. Bailey, C. H., Chen, M. 1988. Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons. Proc. Natl. Acad. Sci. USA 85:2372-77
17. Bailey, C. H., Chen, M. 1988. Long-term sensitization in Aplysia increases the number of presynaptic contacts onto the identified gill motor neuron L7. Proc. Natl. Acad. Sci. USA 85:9356-59
18. Bailey, C. H., Chen, M. 1989. Time course of structural changes at identified sensory neuron synapses during long-term sensitization in Aplysia. J. Neurosci. 9:1774-80
19. Bailey, C. H., Chen, M. 1989. Structural plasticity at identified synapses during long-term memory in Aplysia. J. Neurobiol. 20:356-72
20. Bailey, C. H., Chen, M. 1990. Morphological alterations at identified sensory neuron synapses during long-term sensitization in Aplysia. See Ref. 184a, pp. 35-53
21. Bailey, C. H., Chen, M. 1991. Morphological aspects of synaptic plasticity in Aplysia: An anatomical substrate for long-term memory. NY Acad. Sci. 627: 181-96
22. Bailey, C. H., Chen, M. 1992. The anatomy of long-term sensitization in Aplysia: Morphological insights into learning and memory. In Memory: Organization and Locus of Change, ed. L. Squire, G. Lynch, N. Weinberger, J. McGaugh, pp. 273-300. New York: Oxford Univ. Press
23. Bailey, C. H., Chen, M., Keller, F., Kandel, E. R. 1992. Serotonin-mediated endocytosis of apCAM: An early step of learning-related synaptic growth in Aplysia. Science 256:645-49
24. Bailey, C. H., Montarolo, P. G., Chen, M., Kandel, E. R., Schacher, S. 1992. Inhibitors of protein and RNA synthesis block structural changes that accompany long-term heterosynaptic plasticity in Aplysia. Neuron. 9:749-58
25. Bailey, C. H., Thompson, E. B. 1979. Indented synapses in Aplysia. Brain Res. 173:13-20
26. Bailey, C. H., Thompson, E. B., Castellucci, V. F., Kandel, E. R. 1979. Ultrastructure of the synapses of sensory neurons that mediate the gill-withdrawal reflex in Aplysia. J. Neurocytol. 8:415-44
27. Barondes, S. H. 1975. Protein synthesis dependent and protein synthesis independent memory storage processes. In Short-Term Memory, ed. D. Deutsch, J. A. Deutsch, pp. 379-90. New York: Academic
28. Barzilai, A., Kennedy, T. E., Sweatt, J. D., Kandel, E. R. 1989. 5-HT modulates protein synthesis and the expression of specific proteins during long-term facilitation in Aplysia sensory neurons. Neuron 2:1577-86
29. Bateson, P. P. G. 1966. The characteristics and context of imprinting. Biol. Rev. 41:177-220
30. Baudry, M., Davis, J. L., eds. 1991. Long-term Potentiation: A Debate of Current Issues. Cambridge, Mass: MIT Press
31. Beaulieu, C., Colonnier, M. 1987. Effect of the richness of the environment on the cat visual cortex. J. Comp. Neurol. 266:478-94
32. Bennett, E. L., Diamond, M. C., Krech, D., Rosenzweig, M. R. 1964. Chemical and anatomical plasticity of brain. Science 146:610-19
33. Black, J. E., Isaacs, K. R., Anderson, B. J., Alcantara, A. A., Greenough, W. T. 1990. Learning causes synaptogenesis, whereas motor activity causes angiogenesis in cerebellar cortex of adult rats. Proc. Natl. Acad. Sci. USA 87:5568-72
34. Black, J. E., Zelazny, A. M., Greenough, W. T. 1991. Capillary and mitochondrial support of neural plasticity in adult rat visual cortex. Exp. Neurol. 111:204-9
35. Bradley, P. M., Galal, K. M. 1987. The effects of protein synthesis inhibition on structural changes associated with learning in the chick. Dev. Brain Res. 37:267-76
36. Brandon, J. G., Coss, R. G. 1982. Rapid dendritic spine shortening during one-trial learning: The honeybee's first orientation flight. Brain Res. 252: 51-61
37. Brenowitz, E. A., Arnold, A. P. 1986. Interspecific comparison of the size of neural song control regions and song complexity in duetting birds: Evolutionary implications. J. Neurosci. 6: 2875-79
38. Bretscher, A. 1989. Rapid phosphorylation and reorganization of ezrin and spectrin accompany morphological changes induced in A-431 cells by epidermal growth factor. J. Cell Biol. 108:921-30
39. Campbell, G., Shatz, C. J. 1992. Synapses formed by identified retrogeniculate axons during the segregation of eye input. J. Neurosci. 12:1847-58
40. Carew, T. J., Castellucci, V. F., Kandel, E. R. 1971. An analysis of dishabituation and sensitization of the gill-withdrawal reflex in Aplysia. Int. J. Neurosci. 2:79-98
41. Carew, T. J., Pinsker, H. M., Kandel, E. R. 1972. Long-term habituation of a defensive withdrawal reflex in Aplysia. Science 175:451-54
42. Carlin, P. K., Siekevitz, P. 1983. Plasticity in the central nervous system: Do synapses divide? Proc. Natl. Acad. Sci. USA 80:3517-21
43. Castellucci, V. F., Kennedy, T. E., Kandel, E. R., Goelet, P. 1988. A quantitative analysis of 2-D gels identifies proteins in which labeling is increased following long-term sensitization in Aplysia. Neuron 1:321-28
44. Chang, F.-L. F., Greenough, W. T. 1982. Lateralized effects of monocular training on dendritic branching in adult split-brain rats. Brain Res. 232:283
45. Chang, F.-L. F., 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
46. Chang, P. L., Isaacs, K. R., Greenough, W. T. 1991. Synapse formation occurs in association with the induction of long-term potentiation in two-year-old rat hippocampus in vitro. Neurobiol. Aging 12:517-22
47. Chang, R. G., Govind, C. K. 1986. Reorganization of synaptic ultrastructure at facilitated lobster neuromuscular terminals. J. Neurocytol. 15:63-74
48. Collin, C., Sakakibara, M., McPhie, D., Sanchez-Andres, J. V., Nelson, T. J., Alkon, D. L. 1991. Structural correlates of associative memory in Hermissenda neurons: The role of small G-proteins. Soc. Neurosci. Abstr. 17: 536
49. Connolly, J. L., Green, S. A., Greene, L. A. 1984. Comparison of rapid changes in surface morphology and coated pit formation of PC12 cells in response to nerve growth factor, epidermal growth factor and dibutyryl cyclic AMP. J. Cell Biol. 98:457-65
50. Corfas, G., Dudai, Y. 1991. Morphology of a sensory neuron in Drosophila is abnormal in memory mutants and changes during aging. Proc. Natl. Acad. Sci. USA 88:7252-56
51. Coss, R. G., Brandon, J. G., Globus, A. 1980. Changes in the morphology of dendritic spines on honeybee calycal interneurons associated with cumulative nursing and foraging experiences. Brain Res. 192:49-59
52. Coss, R. G., Globus, A. 1978. Spine stems on tectal interneurons in jewel fish are shortened by social stimulation. Science 200:787-90
53. Cotman, C. W., Nieto-Sampedro, M. 1982. Brain function, synapse renewal, and plasticity. Annu. Rev. Psychol. 33:371-101
54. Couteaux, R., Pecot-Dechavassine, M. 1970. Vesicules synaptiques et poches au niveau des zones actives de la jonction neuromusculaire. C. R. Acad. Sci. 271:2346-49
55. Cragg, B. G. 1975. The development of synapses in kitten visual cortex during visual deprivation. Exp. Neurol. 46:445-51
56. Crick, F. 1984. Memory and molecular turnover. Nature 312:101-2
57. Crow, T. J., Forrester, J. F. 1987. Inhibition of protein synthesis blocks long-term plasticity in identified B-photoreceptors in Hermissenda. Soc. Neurosci. Abstr. 13:389
58. Dadabay, C. Y., Patton, E., Copper, J. A., Pike, L. J. 1991. Lack of correlation between changes in polyphosphoinositide levels and actin/ gelsolin complexes in A431 cells treated with epidermal growth factor. J. Cell Biol. 112:1151-56
59. Davis, H. P., Squire, L. R. 1984. Protein synthesis and memory: A review. Physiol. Bull. 96:518-59
60. Deadwyler, S. A., Dunwiddie, T., Lynch, E. 1988. A critical period of protein synthesis is required for long-term potentiation. Synapse 1:90-95
61. Desmond, N. L., Levy, W. B. 1983. Synaptic correlates of associative potentiation/depression: An ultrastructural study in the hippocampus. Brain Res. 265:21-30
62. Desmond, N. L., Levy, W. B. 1986. Changes in the numerical density of synaptic contacts with long-term potentiation in the hippocampal dentate gyrus. J. Comp. Neurol. 253:466-75
63. Desmond, N. L., Levy, W. B. 1986. Changes in the postsynaptic density with long-term potentiation in the dentate gyrus. J. Comp. Neurol. 253:476-82
64. Desmond, N. L., Levy, W. B. 1986. More front-line synaptic vesicles with long-term synaptic potentiation in the hippocampal dentate gyrus. Soc. Neurosci. Abstr. 12:504
65. Desmond, N. L., Levy, W. B. 1988. Synaptic interface surface area increases with long-term potentiation in the hippocampal dentate gyrus. Brain Res. 453:308-14
66. Desmond, N. L., Levy, W. B. 1990. Morphological correlates of long-term potentiation imply the modification of existing synapses, not synaptogenesis in the hippocampal dentate gyrus. Synapse 5:139-43
67. DeVoogd, J. J., Nixdorf, B., Nottebohm, F. 1985. Synaptogenesis and changes in synaptic morphology related to acquisition of new behavior. Brain. Res. 329:304-8
68. Dyson, S. E., Jones, D. G. 1984. Synaptic remodeling during development and maturation: Function differentiation and splitting as a mechanism of modifying connectivity. Dev. Brain Res. 13:125-37
69. Fifkova, E. 1968. Changes in the visual cortex of rats after unilateral deprivation. Nature 220:379-81
70. Fifkova, E. 1970. Changes of axosomatic synapses in the visual cortex of monocularly deprived rats. J. Neurobiol. 1:61-71
71. Fifkova, E. 1970. The effect of monocular deprivation on the synaptic contacts of the visual cortex. J. Neurobiol. 1:285-94
72. Fifkova, E., Anderson, C. L. 1981. Stimulation-induced changes in dimensions of stalks of dendritic spines in the dentate molecular layer. Exp. Neurol. 74:621-27
73. Fifkova, E., van Harreveld, A. 1977. Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J. Neurocytol. 6:211-30
74. Flexner, J. B., Flexner, L. B., Stellar, E. 1963. Memory in mice as affected by intracerebral puromycin. Science 141:567-69
75. Floeter, M. K., Greenough, W. T. 1979. Cerebellar plasticity: Modification of Purkinje cell structure by differential rearing in monkeys. Science 206:227-29
76. Freire, M. 1979. Effects of dark rearing on dendritic spines in layer IV of the mouse visual cortex. A quantitative electron microscopical study. J. Anat. 126:193-201
77. Frey, U., Krug, M., Reymann, K. G., 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. Friedlander, M. J., Martin, K. A. C., Wassenhove-McCarthy, D. 1991. Effects of monocular visual deprivation on geniculocortical innervation of area 18 in cat. J. Neurosci. 11:3268-88
79. Frost, W. N., Castellucci, V. F., Hawkins, R. D., Kandel, E. R. 1985. Monosynaptic connections made by the sensory neurons of the gill-withdrawal and siphon-withdrawal reflex in Aplysia participate in the storage of long-term memory for sensitization. Proc. Natl. Acad. Sci. USA 82:8266-69
80. Fuchs, J. L., Montemayer, M., Greenough, W. T. 1990. Effect of environmental complexity on size of the superior colliculus. Behav. Neural Biol. 54:198-203
81. Garey, L. J., Pettigrew, J. D. 1974. Ultrastructural changes in kitten visual cortex after environmental modification. Brain Res. 66:165-72
82. Geinisman, Y., de Toledo-Morrell, L., Morrell, F. 1986. Loss of perforated synapses in the dentate gyrus: Morphological substrate of memory deficit in aged rats. Proc. Natl. Acad. Sci. USA 83:3027-31
83. Geinisman, Y., de Toledo-Morrell, L., Morrell, F. 1990. The brain's record of experience: Kindling-induced enlargement of the active zone in hippocampal perforated synapses. Brain Res. 513:175-79
84. Geinisman, Y., de Toledo-Morrell, L., Morrell, F. 1991. Induction of long-term potentiation is associated with an increase in the number of axospinous synapses with segmented postsynaptic densities. Brain Res. 566:77-88
85. Geinisman, Y., Morrell, F., de Toledo-Morrell, L. 1988. Remodelling of synaptic architecture during hippocampal "kindling." Proc. Natl. Acad. Sci. USA 85:3260-64
86. Geinisman, Y., Morrell, F., de Toledo-Morrell, L. 1990. Increase in the relative proportion of perforated axospinous synapses following hippocampal kindling is specific for the synaptic field of stimulated axons. Brain Res. 507:325-31
87. Deleted in proof
88. Glanzman, D. L., Kandel, E. R., Schacher, S. 1989. Identified target motor neuron regulates neurite outgrowth and synapse formation of Aplysia sensory neurons in vitro. Neuron 3:441-50
89. Glanzman, D. L., Kandel, E. R., Schacher, S. 1990. Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. Science 249:799-802
90. Globus, A., Rosenzweig, M. R., Bennett, E. L., Diamond, M. C. 1973. Effects of differential experience on dendritic spine counts in rat cerebral cortex. J. Comp. Physiol. Psychol. 82:175-81
91. Goelet, P., Castellucci, V. F., Schacher, S., Kandel, E. R. 1986. The long and short of long-term memory - a molecular framework. Nature 322:419-22
92. Green, E. J., Greenough, W. T., Schlumpf, B. E. 1983. Effects of complex or isolated environments on cortical dendrites of middle-aged rats. Brain Res. 264:233-40
93. Greenough, W. T. 1984. Structural correlates of information storage in the mammalian brain: A review and hypothesis. Trends Neurosci. 7:229-33
94. Greenough, W. T., Bailey, C. H. 1988. The anatomy of memory: Convergence of results across a diversity of tests. Trends Neurosci. 11:142-47
95. Greenough, W. T., Chang, F.-L. F. 1985. Synaptic structural correlates of information storage in mammalian nervous systems. In Synaptic Plasticity, ed. C. W. Cotman, pp. 335-72. New York: Guilford
96. Greenough, W. T., Chang, F.-L. F. 1988. Plasticity of synapse structure and pattern in the cerebral cortex. In Cerebral Cortex, ed. A. Peters, E. G. Jones, pp. 391-40. New York: Plenum
97. Greenough, W. T., Hwang, H.-M., Gorman, C. 1985. Evidence for active synapse formation, or altered postsynaptic metabolism, in visual cortex of rats reared in complex environments. Proc. Natl. Acad. Sci. USA 82:4549-52
98. Greenough, W. T., Juraska, J. M., Volkmar, F. R. 1979. Maze training effects on dendritic branching in occipital cortex of adult rats. Behav. Neural Biol. 26:287-97
99. Greenough, W. T., Larson, J. R., Withers, G. S. 1985. Effects of unilateral and bilateral training on dendritic branching in occipital cortex of adult rats. Behav. Neural Biol. 44: 301-14
100. Greenough, W. T., McDonald, J. W., Parnisari, R. M., Camel, J. E. 1986. Environmental conditions modulate degeneration and new dendritic growth in cerebellum of senescent rats. Brain Res. 380:136-43
101. Greenough, W. T., Volkmar, F. R. 1973. Pattern of dendritic branching in occipital cortex of rats reared in complex environments. Exp. Neurol. 40:491-504
102. Greenough, W. T., Volkmar, F. R., Juraska, J. M. 1973. Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. Exp. Neurol. 41:371-78
103. Greenough, W. T., West, R. W., DeVoogd, T. J. 1978. Subsynaptic plate perforations: Changes with age and experience in the rat. Science 202: 1096-98
104. Greenough, W. T., Withers, G. S., Wallace, C. S. 1990. Morphological changes in the nervous system arising from behavioral experience: What is the evidence that they are involved in learning and memory. See Ref. 184a, pp. 159-85
105. Gurney, M. E., Konishi, M. 1980. Hormone-induced sexual differentiation of brain and behavior in zebra finches. Science 208:1380-83
106. Han, H.-Q., Nichols, R. A., Rubin, M. R., Bähler, M., Greengard, P. 1991. Induction of formation of presynaptic terminals in neuroblastoma cells by Synapsin-IIb. Nature 349:697-700
107. Hatton, J. D., Ellisman, M. H. 1982. A restructuring of hypothalamic synapses is associated with motherhood. J. Neurosci. 2:704-7
108. Hawrylak, N., Chang, F.-L. F., Greenough, W. T. 1988. Synaptogenesis in kindling. Soc. Neurosci. Abstr. 14:881
109. Herrera, A. A., Grinnell, A. D., Wolowske, B. 1985. Ultrastructural correlates of experimentally altered transmitter release efficacy in frog motor-nerve terminals. Neuroscience 16:491-500
110. Heuser, J. E., Reese, T. S., Dennis, M. J., Jan, Y., Jan, L., Evans, L. 1979. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J. Cell Biol. 81:275-300
111. Horn, G. 1985. Memory, Imprinting and the Brain, an Inquiry into Mechanisms. Oxford: Clarendon
112. Horn, G., Bradley, P., McCabe, B. J. 1985. Changes in the structure of synapse associated with learning. J. Neurosci. 5:3161-68
113. Hu, Y., Bailey, C. H., Chen, M., Barzilai, A. 1992. Long-term facilitation in Aplysia sensory neurons is associated with an increase in the light chain of clathrin and coated vesicles. Soc. Neurosci. Abstr. 18:941
114. Hubel, D. H., Wiesel, T. W. 1963. Reception fields in striate cortex of very young, visually inexperienced kittens. J. Neurophysiol. 26:994-1002
115. Hubel, D. H., Wiesel, T. W. 1970. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. 206:419-36
116. Hubel, D. H., Wiesel, T. W., LeVay, S. 1979. Plasticity of ocular dominance columns in monkey striate cortex. Philos. Trans. R. Soc. London Ser. B 278:377-409
117. Isaacs, K. R., Marks, A., Sirevaag, A. M., Chang, F.-L. F., Greenough, W. T. 1989. Long-term potentiation alters glial process in the dentate gyms. Soc. Neurosci. Abstr. 15:610
118. Juraska, J. M., Fitch, J. M., Henderson, C., Rivers, N. 1985. Sex differences in dendritic branching of dentate granule cells following differential experience. Brain Res. 333:73-80
119. Juraska, J. M., Fitch, J. M., Washburne, D. L. 1989. The dendritic morphology of pyramidal neurons in the rat hippocampus CA3 area. II. Effects of gender and the environment. Brain Res. 479:115-19
120. Juraska, J. M., Greenough, W. T., Elliott, C., Mack, K., Berkowitz, R. 1980. Plasticity in adult rat visual cortex: An examination of several cell populations after differential rearing. Behav. Neural Biol. 29:157-67
121. Kandel, E. R., Schwartz, J. H. 1982. Molecular biology of learning: Modulation of transmitter release. Science 218:433-43
122. Katz, L. C., Gilbert, C. D., Wiesel, T. N. 1989. Local circuits and ocular dominance columns in monkey striate cortex. J. Neurosci. 9:1389-99
123. Keller, F., Schacher, S. 1990. Neuron-specific membrane glycoproteins promoting neurite fasciculation in Aplysia californica. J. Cell Biol. 111:2637-50
124. Kelly, R. B. 1991. A system for synapse control. Nature 349:650-51
125. Kennedy, T. E., Gawinowicz, M. A., Barzilai, A., Kandel, E. R., Sweatt, J. D. 1988. Sequencing of proteins from two-dimensional gels using in situ digestion and transfer of peptides to polyvinylidene difluoride membranes: Application to proteins associated with sensitization in Aplysia. Proc. Natl. Acad. Sci. USA 85: 7008-12
126. Kennedy, T. E., Kuhl, D., Barzilai, A., Kandel, E. R., Sweatt, J. D. 1989. Characterization of changes in late protein and mRNA expression during the maintenance phase of long-term sensitization. Soc. Neurosci. Abstr. 15:1117
127. Kennedy, T. E., Wager-Smith, K., Barzilai, A., Kandel, E. R., Sweatt, J. D. 1988. Sequencing proteins from acrylamide gels. Nature 336:499-500
128. Kilman, V. L., Sirevaag, A. M., Greenough, W. T. 1991. Adult rats exposed to complex environments have a greater number of synapses per neuron than individually housed rats. Soc. Neurosci. Abstr. 17:535
129. Kilman, V. L., Wallace, C. S., Withers, G. S., Greenough, W. T. 1988. Four days of differential housing alters dendritic morphology of weaning rats. Soc. Neurosci. Abstr. 14:1135
130. Koch, C., Zador, A., Brown, T. H. 1992. Dendritic spines: Convergence of theory and experiment. Science 256: 973-74
131. Konishi, M. 1989. Birdsong for neurobiologists. Neuron 3:541-49
132. Kuhl, D., Kennedy, T. E., Barzilai, A., Kandel, E. R. 1993. Long-term sensitization training in Aplysia leads to an increase in the expression of BiP, the major protein chaperon of the endoplasmic reticulum. J. Cell Biol. In press
133. Landis, D. M. D., Hall, A. K., Weinstein, L. A., Reese, T. S. 1988. The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse. Neuron 1:201-9
134. Lee, K., Oliver, M., Schottler, F., Lynch, G. 1981. Electron microscopic studies of brain slices: The effects of high-frequency stimulation on dendritic ultrastructure. In Electrophysiology of Isolated Mammalian CNS Properties, ed. G. A. Kerkut, H. V. Wheal, pp. 189-211. New York: Academic
135. Lee, K., Schottler, F., Oliver, M., Lynch, G. 1980. Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus. J. Neurophysiol. 4:247-58
136. LeVay, S., Stryker, M. P. 1979. The development of ocular dominance columns in the cat. In Aspects of Developmental Neurobiology, Society for Neuroscience Symposia, ed. J. A. Ferrendelli, 4:83-98. Bethesda, Md: Soc. Neurosci.
137. LeVay, S., Stryker, M. P., Shatz, C. J. 1978. Ocular dominance columns and their development in layer IV of the cat's visual cortex: A quantitative study. J. Comp. Neurol. 179: 223-44
138. LeVay, S., Wiesel, T. W., Hubel, D. H. 1980. The development of ocular dominance columns in normal and visually deprived monkeys. J. Comp. Neurol. 191:1-51
139. Lnenicka, G. A., Atwood, H. L., Marin, L. 1986. Morphological transformation of synaptic terminals of a phasic motoneuron by long-term tonic stimulation. J. Neurosci. 6:2252-58
140. Lnenicka, G. A., Hong, S. J., Combatti, M., LePage, S. 1988. Activity-dependent development of synaptic varicosities at crayfish motor terminals. J. Neurosci. 11:1040-48
141. Markus, E. J., Petit, T. L. 1989. Synaptic structural plasticity: Role of synaptic shape. Synapse 3:1-11
142. Marler, P. 1991. Song-learning behavior: The interface with neuroethology. Trends Neurosci. 14:199-206
143. Matthies, H. 1991. Long-lasting maintenance of long-term potentiation and macromolecular synthesis. See Ref. 29, pp. 233-43
144. Mayford, M., Barzilai, A., Keller, F., Schacher, S., Kandel, E. R. 1992. Modulation of an NCAM-related cell adhesion molecule with long-term synaptic plasticity in Aplysia. Science 256: 638-44
145. Meister, M., Wong, R. O. L., Baylor, D. A., Shatz, C. J. 1991. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252:939-43
146. Merzenich, M. M. 1984. Functional "maps" of skin sensations. In The Many Facets of Touch. The summary publication of Johnson & Johnson Pediatric Roundtable #10 - Touch, ed. C. C. Brown, pp. 15-22. Skillman, NJ: Johnson & Johnson Baby Products Co.
147. Merzenich, M. M. 1985. Sources of intraspecies and interspecies cortical map variability in mammals: Conclusions and hypotheses. In Comparative Neurobiology: Modes of Communication in the Nervous System, ed. M. J. Cohen, F. Strumwasser, pp. 105-16. New York: Wiley
148. Merzenich, M. M., Kaas, J. H., Wall, J., Nelson, R. J., Sur, M., Felleman, D. 1983. Topographic reorganization of somatosensory cortical areas 3B and 1 in adult monkeys following restricted deafferentation. Neuroscience 8:33-35
149. Merzenich, M. M., Kaas, J. H., Wall, J. T., Sur, M., Nelson, R. J., Felleman, D. 1983. Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkey. Neuroscience 10:639-65
150. Merzenich, M. M., Nelson, R. J., Stryker, M. P., Cyander, M. S., Schoppman, A., Zook, J. M. 1984. Somatosensory cortical map changes following digit amputation in adult monkeys. J. Comp. Neurol. 224:591-605
151. Merzenich, M. M., Recanzone, E. G., Jenkins, W. M., Allard, T. T., Nudo, R. J. 1988. Cortical representational plasticity. In Neurobiology of Neocortex, ed. P. Rakic, W. Singer, pp. 41-67. New York: Wiley
152. Meshul, C. K., Hopkins, W. F. 1990. Presynaptic ultrastructural correlates of long-term potentiation in the CA1 subfield of the hippocampus. Brain Res. 514:310-19
153. Meshul, C. K., Seil, F. J., Herndon, R. M. 1987. Astrocytes play a role in regulation of synaptic density. Brain Res. 402:139-45
154. Montarolo, P. G., Ghirardi, M., Kandel, E. R. 1992. Contribution of persistent protein kinase A to serotonin-induced long-term facilitation of Aplysia sensory-motor synapses in culture. Soc. Neurosci. Abstr. 18:712
155. 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 234:1249-54
156. Morrell, F., Geinisman, Y., de Toledo-Morrell, L. 1991. Kindling-induced increase in the number of axospinous synapses with segmented postsynaptic densities. Soc. Neurosci. Abstr. 17:875
157. 2+ responses. Nature 354:73-76
158. Nazif, F. A., Byrne, J. H., Cleary, L. J. 1991. cAMP induces long-term morphological changes in sensory neurons of Aplysia. Brain Res. 539:324-27
159. Nazif, F. A., Byrne, J. H., Cleary, L. J. 1991. Long-term (24 hr) morphological changes induced by cAMP in pleural sensory neurons of Aplysia are dependent on de novo protein synthesis. Soc. Neurosci. Abstr. 17:1589
160. Nieto-Sampedro, M., Hoff, S. W., Cotman, C. W. 1982. Perforated post-synaptic densities: Probable intermediates in synapse turnover. Proc. Natl. Acad. Sci. USA 79:5718-22
161. Nottebohm, F. 1980. Brain pathways for vocal learning in birds: A review of the first 10 years. Prog. Psychobiol. Physiol. 9:85-124
162. Nottebohm, F. 1981. A brain for all seasons: Cyclical anatomical changes in song control nuclei of the canary brain. Science 214:1368-70
163. Nottebohm, F. 1991. Reassessing the mechanisms and origins of vocal learning in birds. Trends Neurosci. 14:206-11
164. Nottebohm, F., Kelley, P. B., Paton, J. A. 1982. Connections of vocal control nuclei in the canary telencephalon. J. Comp. Neurol. 207:344-57
165. Nottebohm, F., Stokes, T. M., Leonard, C. M. 1976. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165:457-86
166. Parnavelas, J. G., Globus, A., Kaups, P. 1973. Continuous illumination from birth affects spine density of neurons in the visual cortex of the rat. Exp Neurol. 40:742-47
167. Patel, S. N., Rose, S. P. R., Stewart, M. G. 1988. Training-induced spine density changes are specifically related to memory formation processes in the chick, Gallus domesticus. Brain Res. 463:168-73
168. Patel, S. N., Stewart, M. G. 1988. Changes in the number and structure of dendritic spines, 25 hrs after passive avoidance training in the domestic chick, Gallus domesticus. Brain Res. 449:34-46
169. Pelham, H. 1988. Heat shock proteins: Coming in from the cold. Nature 332:776-77
170. Pinsker, H. M., Hening, W. A., Carew, T. J., Kandel, E. R. 1973. Long-term sensitization of a defensive withdrawal reflex in Aplysia. Science 182:1039-42
171. Pinsker, H. M., Kupfermann, I., Castellucci, V. F., Kandel, E. R. 1970. Habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167:1740-42
172. Purves, D., Lichtman, J. W. 1985. Principles of Neural Development. Sunderland, Mass: Sinauer
173. Pysh, J. J., Weiss, M. 1979. Exercise during development induces an increase in Purkinje cell dendritic tree size. Science 206:230-32
174. Pysh, J. J., Wiley, R. G. 1972. Morphologic alterations of synapses in electrically stimulated superior cervical ganglia of the cat. Science 176:191-93
175. Deleted in proof
176. Rose, S. P. R. 1991. How chicks make memories: The cellular cascade from c-fos to dendritic remodelling. Trends Neurosci. 14:390-97
177. Rose, S. P. R. 1991. Biochemical mechanisms involved in memory formation in the chick. See Ref. 4, pp. 277-304
178. Rosenzweig, M. R., Bennett, E. L. 1978. Experiential influences on the brain anatomy and brain chemistry in rodents. In Studies on the Development of Behavior and the Nervous System, ed. G. Gottlieb, 4:289-327. New York: Academic
179. Rosenzweig, M. R., Bennett, E. L., Diamond, M. C. 1972. Chemical and anatomical plasticity of brain: Replication and extensions. In Macromolecules and Behavior, ed. J. Gaito, 2:205-78. New York: Appleton-Century-Crofts
180. Rothblat, L. A., Schwartz, M. 1979. The effect of monocular deprivation on dendritic spines in visual cortex of young and adult albino rats: Evidence for a sensitive period. Brain. Res. 161:156-61
181. Schneider, W. D., Johnson, E. M. Jr. 1989. Neurotrophic molecules. Ann. Neurol. 26:489
182. Schuster, T., Krug, M., Wenzel, J. 1990. Spinules in axospinous synapses of the rat dentate gyrus: Changes in density following long-term potentiation. Brain Res. 523:171-74
183. Shatz, C. J. 1990. Competitive interactions between retinal ganglion cells during prenatal development. J. Neurobiol. 21:197-211
184. Shatz, C. J. 1990. Impulse activity and the patterning of connections during CNS development. Neuron 5:745-56
185. Sirevaag, A. M., Greenough, W. T. 1987. Differential rearing effects on rat visual cortex synapses. III. Neuronal and glial nuclei, boutons, dendrites and capillaries. Brain. Res. 424:320-32
186. Sirevaag, A. M., Greenough, W. T. 1991. Plasticity of GFAP-immunoreactive astrocyte size and number in visual cortex of rats reared in complex environments. Brain Res. 540:273-78
187. Squire, L. R. 1987. Memory and Brain. New York: Oxford Univ. Press
188. Squire, L. R., Lindenlaub, E., eds. 1990. The Biology of Memory, Vol. 23. Stuttgart/New York: Shattauer Verlag
189. Sretavan, D. W., Shatz, C. J. 1986. Prenatal development of retinal ganglion cell axons: Segregation into eye-specific layers. J. Neurosci. 6: 234-51
190. Stanton, P. K., Sarvey, J. M. 1984. Blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis. J. Neurosci. 4:3080-88
191. Stewart, M. G. 1990. Morphological correlates of long-term memory in the chick forebrain consequent on passive-avoidance learning. See Ref. 184a, pp. 93-220
192. Stewart, M. G. 1991. Changes in dendritic and synaptic structure in chick forebrain consequent on passive avoidance learning. See Ref. 4, pp. 305-20
193. Stewart, M. G., Csillag, A., Rose, S. P. R. 1987. Alterations in synaptic structure in the paleostriatal complex of the domestic chick, Gallus domesticus, following passive avoidance training. Brain Res. 426:69-81
194. Stewart, M. G., Rose, S. P. R., King, T. S., Gabbott, P. L. A., Bourne, R. 1984. Hemispheric asymmetry of synapses in chick medial hyperstriatum ventrale following passive avoidance training: A stereological investigation. Dev. Brain Res. 12:261-69
195. Stryker, M. P. 1991. Activity-dependent reorganization of afferents in the developing mammalian visual system. In Development of the Visual System, ed. D. M.-K. Lam, C. J. Shatz, pp. 267-87. Cambridge, Mass: MIT Press
196. Stryker, M. P., Harris, W. A. 1986. Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. J. Neurosci. 6:2117-33
197. Stryker, M. P., Strickland, S. L. 1984. Physiological segregation of ocular dominance columns depends on the pattern of afferent electrical activity. Invest. Ophthalmol. Visual Sci. 25:278 (Suppl.) (ARVO Abstr.)
198. Sweatt, D., Kandel, E. R. 1989. Persistent and transcriptionally-dependent increase in protein phosphorylation in long-term facilitation of Aplysia sensory neurons. Nature 339:51-54
199. Tieman, S. B. 1984. Effects of monocular deprivation on geniculocortical synapses in the cat. J. Comp. Neurol. 222:166-76
200. Tieman, S. B. 1985. The anatomy of geniculocortical connections in monocularly deprived cats. Cell Mol. Neurobiol. 5:35-45
201. Trommald, M., Vaaland, J. L., Blackstad, T. W., Andersen, P. 1990. Dendritic spine changes in rat dentate granule cells associated with long-term potentiation. In Neurotoxicity of Excit-atory Amino Acids, ed. A. Guidotti, pp. 163-79. New York: Raven
202. Turner, A. M., Greenough, W. T. 1985. Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron. Brain Res. 329:195-203
203. Tweedle, C. D., Hatton, G. I. 1984 Synaptic formation and disappearance in adult rat supraoptic nucleus during different hydration states. Brain Res. 309:373-76
204. Valverde, F. 1967. Apical dendritic spines of the visual cortex and light deprivation in the mouse. Exp. Brain Res. 3:337-52
205. Valverde, F. 1971. Rate and extent of recovery from dark rearing in the mouse. Brain. Res. 33:1-11
206. van Harreveld, A., Fifkova, E. 1975. Swelling of dendritic spines in the fascia dentata after stimulation of the perforant fibers as a mechanism of post-tetanic potentiation. Exp. Neurol. 49:736-49
207. Volkmar, F. R., Greenough, W. T. 1972. Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science 176:1445-47
208. Vrensen, G., Cardozo, J. N. 1981. Changes in size and shape of synaptic connections after visual training: An ultrastructural approach of synaptic plasticity. Brain Res. 218:79-97
209. Vrensen, G., DeGroot, D. 1974. The effect of dark-rearing and its recovery on synaptic terminals in the visual cortex of rabbits: A quantitative electron miscroscopic study. Brain Res. 78:263-78
210. Vrensen, G., DeGroot, D. 1975. The effect of monocular deprivation on synaptic terminals in the visual cortex of rabbits: A quantitative electron miscroscopic study. Brain Res. 93:15-24
211. Wallace, C. S., Hawrylak, N., Greenough, W. T. 1991. Studies of synaptic structural modifications after long-term potentiation and kindling: Context for a molecular morphology. See Ref. 29, pp. 189-232
212. Wenzel, J., Matthies, H. 1985. Morphological changes in the hippocampal formation accompanying memory function and long-term potentiation. In Memory Systems of the Brain, ed. N. M. Weinberger, J. L. McGaugh, G. Lynch, pp. 151-70. New York: Guilford
213. Wesa, J. M., Chang, F.-L. F., Greenough, W. T., West, R. W. 1982. Synaptic contact curvature: Effects of differential rearing on rat occipital cortex. Dev. Brain Res. 4:253-57
214. West, R. W., Greenough, W. T. 1972. Effect of environmental complexity on cortical synapses of rats: Preliminary results. Behav. Biol. 7:279-84
215. Withers, G. S., Greenough, W. T. 1989. Reach training selectively alters dendritic branching in subpopulations of layer II-III pyramids in rat motor-somatosensory forelimb cortex. Neuropsychologia 27:61-69
216. Wojtowicz, J. M., Marin, L., Atwood, H. L. 1989. Synaptic restructuring during long-term facilitation at the crayfish neuromuscular junction. Can. J. Physiol. Pharmacol. 67:167-71