Memory - A century of consolidation

Science

Volumn 287, Issue 5451, 2000, Pages 248-251

  McGaugh, James L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMNESIA; HORMONAL REGULATION; HUMAN; LONG TERM MEMORY; MEMORY CONSOLIDATION; NEUROANATOMY; PRIORITY JOURNAL; REGULATORY MECHANISM; RETROGRADE AMNESIA; REVIEW; SHORT TERM MEMORY;

AMNESIA, RETROGRADE; AMYGDALA; ANIMALS; BRAIN; EMOTIONS; HIPPOCAMPUS; HUMANS; LONG-TERM POTENTIATION; MEMORY; MEMORY, SHORT-TERM; PROTEIN KINASES; RECEPTORS, ADRENERGIC, BETA;

EID: 0033969570     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.287.5451.248     Document Type: Review

References (102)

1. G. E. Müller and A. Pilzecker, Z. Psychol. 1, 1 (1900).
2. S. E. Glickman, Psychol. Bull. 58, 218 (1961); J. L. McGaugh and M. J. Herz, Memory Consolidation (Albion, San Francisco, 1972); H. Weingartner and E. S. Parker, Eds., Memory Consolidation (Erlbaum, Hillsdale, NJ, 1984); H. A. Lechner, L. R. Squire, J. H. Byrne, Learn. Mem. 6, 77 (1999); M. R. Polster, L. Nadel, D. L. Schacter, J. Cogn. Neurosci. 3, 95 (1991).
3. S. E. Glickman, Psychol. Bull. 58, 218 (1961); J. L. McGaugh and M. J. Herz, Memory Consolidation (Albion, San Francisco, 1972); H. Weingartner and E. S. Parker, Eds., Memory Consolidation (Erlbaum, Hillsdale, NJ, 1984); H. A. Lechner, L. R. Squire, J. H. Byrne, Learn. Mem. 6, 77 (1999); M. R. Polster, L. Nadel, D. L. Schacter, J. Cogn. Neurosci. 3, 95 (1991).
4. S. E. Glickman, Psychol. Bull. 58, 218 (1961); J. L. McGaugh and M. J. Herz, Memory Consolidation (Albion, San Francisco, 1972); H. Weingartner and E. S. Parker, Eds., Memory Consolidation (Erlbaum, Hillsdale, NJ, 1984); H. A. Lechner, L. R. Squire, J. H. Byrne, Learn. Mem. 6, 77 (1999); M. R. Polster, L. Nadel, D. L. Schacter, J. Cogn. Neurosci. 3, 95 (1991).
5. S. E. Glickman, Psychol. Bull. 58, 218 (1961); J. L. McGaugh and M. J. Herz, Memory Consolidation (Albion, San Francisco, 1972); H. Weingartner and E. S. Parker, Eds., Memory Consolidation (Erlbaum, Hillsdale, NJ, 1984); H. A. Lechner, L. R. Squire, J. H. Byrne, Learn. Mem. 6, 77 (1999); M. R. Polster, L. Nadel, D. L. Schacter, J. Cogn. Neurosci. 3, 95 (1991).
6. S. E. Glickman, Psychol. Bull. 58, 218 (1961); J. L. McGaugh and M. J. Herz, Memory Consolidation (Albion, San Francisco, 1972); H. Weingartner and E. S. Parker, Eds., Memory Consolidation (Erlbaum, Hillsdale, NJ, 1984); H. A. Lechner, L. R. Squire, J. H. Byrne, Learn. Mem. 6, 77 (1999); M. R. Polster, L. Nadel, D. L. Schacter, J. Cogn. Neurosci. 3, 95 (1991).
7. J. L. McGaugh, Science 153, 1351 (1966).
8. Y. Dudai, Neuron 17, 367 (1996).
9. T. Ribot, Diseases of Memory (Appleton, New York, 1882); W. McDougall, Mind 10, 388 (1901); W. H. Burnham, Am. J. Psychol. 14, 382 (1903).
10. T. Ribot, Diseases of Memory (Appleton, New York, 1882); W. McDougall, Mind 10, 388 (1901); W. H. Burnham, Am. J. Psychol. 14, 382 (1903).
11. T. Ribot, Diseases of Memory (Appleton, New York, 1882); W. McDougall, Mind 10, 388 (1901); W. H. Burnham, Am. J. Psychol. 14, 382 (1903).
12. C. P. Duncan, J. Comp. Physiol. Psychol. 42, 32 (1949).
13. R. W. Gerard, Am. J. Psychiatry 106, 161 (1949).
14. D. O. Hebb, The Organization of Behavior (Wiley, New York, 1949) and (7). It is of interest that Hebb did not refer to the perseveration-consolidation hypothesis in his seminal 1949 book.
15. B. W. Agranoff, R. E. Davis, J. J. Brink, Brain Res. 1, 303 (1965).
16. J. L. McGaugh, in Recent Advances in Learning and Retention, D. Bovet, F. Bovet-Nitti, A. Oliverio, Eds. (Accademia Nazionale dei Lincei, Rome, 1968), pp. 13-24.
17. J. L. McGaugh, Annu. Rev. Pharmacol. 13, 229 (1973); Brain Res. Bull. 23, 339 (1989).
18. J. L. McGaugh, Annu. Rev. Pharmacol. 13, 229 (1973); Brain Res. Bull. 23, 339 (1989).
19. T. M. Alloway and A. Routtenberg, Science 158, 1066 (1967); T. Tully, T. Preat, S. C. Boynton, M. Del Vecchio, Cell 79, 35 (1994); R. Menzel and U. Müller, Annu. Rev. Neurosci. 19, 379 (1966); U. Müller, Neuron 16, 1249 (1996).
20. T. M. Alloway and A. Routtenberg, Science 158, 1066 (1967); T. Tully, T. Preat, S. C. Boynton, M. Del Vecchio, Cell 79, 35 (1994); R. Menzel and U. Müller, Annu. Rev. Neurosci. 19, 379 (1966); U. Müller, Neuron 16, 1249 (1996).
21. T. M. Alloway and A. Routtenberg, Science 158, 1066 (1967); T. Tully, T. Preat, S. C. Boynton, M. Del Vecchio, Cell 79, 35 (1994); R. Menzel and U. Müller, Annu. Rev. Neurosci. 19, 379 (1966); U. Müller, Neuron 16, 1249 (1996).
22. T. M. Alloway and A. Routtenberg, Science 158, 1066 (1967); T. Tully, T. Preat, S. C. Boynton, M. Del Vecchio, Cell 79, 35 (1994); R. Menzel and U. Müller, Annu. Rev. Neurosci. 19, 379 (1966); U. Müller, Neuron 16, 1249 (1996).
23. C. Sandi and S. P. R. Rose, Brain Res. 647, 106 (1994).
24. P. E. Gold and J. L. McGaugh, in Short-Term Memory, D. Deutsch and J. A. Deutsch, Eds. (Academic Press, New York, 1975), pp. 355-378.
25. S.-A. Christianson, Ed., Handbook of Emotion and Memory: Current Research and Theory (Erlbaum, Hillsdale, NJ, 1992).
26. P. E. Gold and R. van Buskirk, Behav. Biol. 13, 145 (1975).
27. J. L. McGaugh and P. E. Gold, in Psychoendocrinology, R. B. Brush and S. Levine, Eds. (Academic Press, New York, 1989), pp. 305-339.
28. E. R. de Kloet, Front. Neuroendocrinol. 12, 95 (1991); _, S. Kock, V. Schild, H. D. Veldhuis, Neuroendocrinology 47, 109 (1988); B. Roozendaal, L. Cahill, J. L. McGaugh in Brain Processes and Memory, K. Ishikawa, J. L. McGaugh, H. Sakata, Eds. (Elsevier, Amsterdam, 1996), pp. 39-54.
29. E. R. de Kloet, Front. Neuroendocrinol. 12, 95 (1991); _, S. Kock, V. Schild, H. D. Veldhuis, Neuroendocrinology 47, 109 (1988); B. Roozendaal, L. Cahill, J. L. McGaugh in Brain Processes and Memory, K. Ishikawa, J. L. McGaugh, H. Sakata, Eds. (Elsevier, Amsterdam, 1996), pp. 39-54.
30. E. R. de Kloet, Front. Neuroendocrinol. 12, 95 (1991); _, S. Kock, V. Schild, H. D. Veldhuis, Neuroendocrinology 47, 109 (1988); B. Roozendaal, L. Cahill, J. L. McGaugh in Brain Processes and Memory, K. Ishikawa, J. L. McGaugh, H. Sakata, Eds. (Elsevier, Amsterdam, 1996), pp. 39-54.
31. S. J. Lupien and B. S. McEwen, Brain Res. Rev. 24, 1 (1997).
32. M. G. Packard, C. L. Williams, L. Cahill, J. L. McGaugh, in Neurobehavioral Plasticity: Learning, Development and Response to Brain Insults, N. E. Spear, L. Spear, M. Woodruff, Eds. (Erlbaum, Hillsdale, NJ, 1995), pp. 149-184; J. L. McGaugh, L. Cahill, B. Roozendaal, Proc. Natl. Acad. Sci. U.S.A. 93, 13508 (1996). There is also evidence that epinephrine influences memory through the release of glucose, which then enters the brain; however, the effects of glucose on memory differ from those mediated by the activation of vagal afferents. P. E. Gold, in Cellular Mechanisms of Conditioning and Behavioral Plasticity, C. D. Woody, D. L. Alkon, J. L. McGaugh, Eds. (Plenum, New York, 1988), pp. 329-341.
33. M. G. Packard, C. L. Williams, L. Cahill, J. L. McGaugh, in Neurobehavioral Plasticity: Learning, Development and Response to Brain Insults, N. E. Spear, L. Spear, M. Woodruff, Eds. (Erlbaum, Hillsdale, NJ, 1995), pp. 149-184; J. L. McGaugh, L. Cahill, B. Roozendaal, Proc. Natl. Acad. Sci. U.S.A. 93, 13508 (1996). There is also evidence that epinephrine influences memory through the release of glucose, which then enters the brain; however, the effects of glucose on memory differ from those mediated by the activation of vagal afferents. P. E. Gold, in Cellular Mechanisms of Conditioning and Behavioral Plasticity, C. D. Woody, D. L. Alkon, J. L. McGaugh, Eds. (Plenum, New York, 1988), pp. 329-341.
34. M. G. Packard, C. L. Williams, L. Cahill, J. L. McGaugh, in Neurobehavioral Plasticity: Learning, Development and Response to Brain Insults, N. E. Spear, L. Spear, M. Woodruff, Eds. (Erlbaum, Hillsdale, NJ, 1995), pp. 149-184; J. L. McGaugh, L. Cahill, B. Roozendaal, Proc. Natl. Acad. Sci. U.S.A. 93, 13508 (1996). There is also evidence that epinephrine influences memory through the release of glucose, which then enters the brain; however, the effects of glucose on memory differ from those mediated by the activation of vagal afferents. P. E. Gold, in Cellular Mechanisms of Conditioning and Behavioral Plasticity, C. D. Woody, D. L. Alkon, J. L. McGaugh, Eds. (Plenum, New York, 1988), pp. 329-341.
35. K. C. Liang, R. G. Juler, J. L. McGaugh, Brain Res. 368, 125 (1986).
36. B. Roozendaal and J. L. McGaugh, Neurobiol. Learn. Mem. 65, 1 (1996); T. Hatfield and J. L. McGaugh, Neurobiol. Learn. Mem. 71, 232 (1999); B. Ferry and J. L. McGaugh, Neurobiol. Learn. Mem. 72, 8 (1999).
37. B. Roozendaal and J. L. McGaugh, Neurobiol. Learn. Mem. 65, 1 (1996); T. Hatfield and J. L. McGaugh, Neurobiol. Learn. Mem. 71, 232 (1999); B. Ferry and J. L. McGaugh, Neurobiol. Learn. Mem. 72, 8 (1999).
38. B. Roozendaal and J. L. McGaugh, Neurobiol. Learn. Mem. 65, 1 (1996); T. Hatfield and J. L. McGaugh, Neurobiol. Learn. Mem. 71, 232 (1999); B. Ferry and J. L. McGaugh, Neurobiol. Learn. Mem. 72, 8 (1999).
39. G. L. Quirarte, B. Roozendaal, J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 94, 14048 (1997).
40. R. Galvez, M. Mesches, J. L. McGaugh, Neurobiol. Learn. Mem. 66, 253 (1996); G. L. Quirarte, R. Galvez, B. Roozendaal, J. L. McGaugh, Brain Res. 808, 134 (1998); C. L. Williams, D. Men, E. C. Clayton and P. E. Gold, Behav. Neurosci. 112, 1414 (1998); T. Hatfield, C. Spanis, J. L. McGaugh, Brain Res. 835, 340 (1999).
41. R. Galvez, M. Mesches, J. L. McGaugh, Neurobiol. Learn. Mem. 66, 253 (1996); G. L. Quirarte, R. Galvez, B. Roozendaal, J. L. McGaugh, Brain Res. 808, 134 (1998); C. L. Williams, D. Men, E. C. Clayton and P. E. Gold, Behav. Neurosci. 112, 1414 (1998); T. Hatfield, C. Spanis, J. L. McGaugh, Brain Res. 835, 340 (1999).
42. R. Galvez, M. Mesches, J. L. McGaugh, Neurobiol. Learn. Mem. 66, 253 (1996); G. L. Quirarte, R. Galvez, B. Roozendaal, J. L. McGaugh, Brain Res. 808, 134 (1998); C. L. Williams, D. Men, E. C. Clayton and P. E. Gold, Behav. Neurosci. 112, 1414 (1998); T. Hatfield, C. Spanis, J. L. McGaugh, Brain Res. 835, 340 (1999).
43. R. Galvez, M. Mesches, J. L. McGaugh, Neurobiol. Learn. Mem. 66, 253 (1996); G. L. Quirarte, R. Galvez, B. Roozendaal, J. L. McGaugh, Brain Res. 808, 134 (1998); C. L. Williams, D. Men, E. C. Clayton and P. E. Gold, Behav. Neurosci. 112, 1414 (1998); T. Hatfield, C. Spanis, J. L. McGaugh, Brain Res. 835, 340 (1999).
44. L. R. Squire and E. R. Kandel, Memory from Mind to Molecules (Scientific American Library, New York, 1999).
45. For example, M. G. Packard and N. M. White, Behav. Neurosci. 105, 295 (1991); M. G. Packard, R. Hirsh, N. M. White, J. Neurosci. 9, 1465 (1989).
46. For example, M. G. Packard and N. M. White, Behav. Neurosci. 105, 295 (1991); M. G. Packard, R. Hirsh, N. M. White, J. Neurosci. 9, 1465 (1989).
47. M. G. Packard, L. Cahill, J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 91, 8477 (1994); M. G. Packard and L. Teather, Neurobiol. Learn. Mem. 69, 163 (1998).
48. M. G. Packard, L. Cahill, J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 91, 8477 (1994); M. G. Packard and L. Teather, Neurobiol. Learn. Mem. 69, 163 (1998).
49. B. Roozendaal and J. L. McGaugh, Euro. J. Neurosci. 9, 76 (1997); B. Roozendaal, B.T. Nguyen, A. Power, J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 96, 11642 (1999).
50. B. Roozendaal and J. L. McGaugh, Euro. J. Neurosci. 9, 76 (1997); B. Roozendaal, B.T. Nguyen, A. Power, J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 96, 11642 (1999).
51. Y. Ikegaya, H. Saito, K. Abe, Brain Res. 671, 351 (1995); Neurosci. Res. 22, 203 (1995); _, K. Nakanishi, NeuroReport 8, 3143 (1997). BLA stimulation also induces NMDA-dependent LTP in the insular cortex, a brain region known to be important for several forms of learning [F. Bermudez-Rattoni, I. B. Introini-Collison, J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 88, 5379 (1991); M. L. Escobar, V. Chao, F. Bermudez-Rattoni, Brain Res. 779, 314 (1998); M. W. Jones, P. J. French, T. V. P. Bliss, K. Rosenblum, J. Neurosci 19, RC36 (1999)].
52. Y. Ikegaya, H. Saito, K. Abe, Brain Res. 671, 351 (1995); Neurosci. Res. 22, 203 (1995); _, K. Nakanishi, NeuroReport 8, 3143 (1997). BLA stimulation also induces NMDA-dependent LTP in the insular cortex, a brain region known to be important for several forms of learning [F. Bermudez-Rattoni, I. B. Introini-Collison, J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 88, 5379 (1991); M. L. Escobar, V. Chao, F. Bermudez-Rattoni, Brain Res. 779, 314 (1998); M. W. Jones, P. J. French, T. V. P. Bliss, K. Rosenblum, J. Neurosci 19, RC36 (1999)].
53. Y. Ikegaya, H. Saito, K. Abe, Brain Res. 671, 351 (1995); Neurosci. Res. 22, 203 (1995); _, K. Nakanishi, NeuroReport 8, 3143 (1997). BLA stimulation also induces NMDA-dependent LTP in the insular cortex, a brain region known to be important for several forms of learning [F. Bermudez-Rattoni, I. B. Introini-Collison, J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 88, 5379 (1991); M. L. Escobar, V. Chao, F. Bermudez-Rattoni, Brain Res. 779, 314 (1998); M. W. Jones, P. J. French, T. V. P. Bliss, K. Rosenblum, J. Neurosci 19, RC36 (1999)].
54. Y. Ikegaya, H. Saito, K. Abe, Brain Res. 671, 351 (1995); Neurosci. Res. 22, 203 (1995); _, K. Nakanishi, NeuroReport 8, 3143 (1997). BLA stimulation also induces NMDA-dependent LTP in the insular cortex, a brain region known to be important for several forms of learning [F. Bermudez-Rattoni, I. B. Introini-Collison, J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 88, 5379 (1991); M. L. Escobar, V. Chao, F. Bermudez-Rattoni, Brain Res. 779, 314 (1998); M. W. Jones, P. J. French, T. V. P. Bliss, K. Rosenblum, J. Neurosci 19, RC36 (1999)].
55. Y. Ikegaya, H. Saito, K. Abe, Brain Res. 671, 351 (1995); Neurosci. Res. 22, 203 (1995); _, K. Nakanishi, NeuroReport 8, 3143 (1997). BLA stimulation also induces NMDA-dependent LTP in the insular cortex, a brain region known to be important for several forms of learning [F. Bermudez-Rattoni, I. B. Introini-Collison, J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 88, 5379 (1991); M. L. Escobar, V. Chao, F. Bermudez-Rattoni, Brain Res. 779, 314 (1998); M. W. Jones, P. J. French, T. V. P. Bliss, K. Rosenblum, J. Neurosci 19, RC36 (1999)].
56. Y. Ikegaya, H. Saito, K. Abe, Brain Res. 671, 351 (1995); Neurosci. Res. 22, 203 (1995); _, K. Nakanishi, NeuroReport 8, 3143 (1997). BLA stimulation also induces NMDA-dependent LTP in the insular cortex, a brain region known to be important for several forms of learning [F. Bermudez-Rattoni, I. B. Introini-Collison, J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 88, 5379 (1991); M. L. Escobar, V. Chao, F. Bermudez-Rattoni, Brain Res. 779, 314 (1998); M. W. Jones, P. J. French, T. V. P. Bliss, K. Rosenblum, J. Neurosci 19, RC36 (1999)].
57. E. Soetens, S. Casaer, R. D'Hooge, J. E. Hueting, Psychopharmacology 119, 155 (1995).
58. L. Cahill, B. Prins, M. Weber, J. L. McGaugh, Nature 371, 702 (1994); A. H. van Stegeren, W. Everaerd, L. Cahill, J. L. McGaugh, L. J. G. Gooren, Psychopharmacology 138, 305 (1998); K. Nielson and R. Jensen, Behav. Neural Biol. 62, 190 (1994).
59. L. Cahill, B. Prins, M. Weber, J. L. McGaugh, Nature 371, 702 (1994); A. H. van Stegeren, W. Everaerd, L. Cahill, J. L. McGaugh, L. J. G. Gooren, Psychopharmacology 138, 305 (1998); K. Nielson and R. Jensen, Behav. Neural Biol. 62, 190 (1994).
60. L. Cahill, B. Prins, M. Weber, J. L. McGaugh, Nature 371, 702 (1994); A. H. van Stegeren, W. Everaerd, L. Cahill, J. L. McGaugh, L. J. G. Gooren, Psychopharmacology 138, 305 (1998); K. Nielson and R. Jensen, Behav. Neural Biol. 62, 190 (1994).
61. L. Cahill, R. Babinsky, H. J. Markowitsch, J. L. McGaugh, Nature 377, 295 (1995); R. Adolphs, L. Cahill, R. Schul, R. Babinsky, Learn. Mem. 4, 291 (1997).
62. L. Cahill, R. Babinsky, H. J. Markowitsch, J. L. McGaugh, Nature 377, 295 (1995); R. Adolphs, L. Cahill, R. Schul, R. Babinsky, Learn. Mem. 4, 291 (1997).
63. L. Cahill et al., Proc. Natl. Acad. Sci. U.S.A. 93, 8016 (1996); S. Hamann, T. Ely, S. Grafton, C. Kilts, Nature Neurosci. 2, 289 (1999).
64. L. Cahill et al., Proc. Natl. Acad. Sci. U.S.A. 93, 8016 (1996); S. Hamann, T. Ely, S. Grafton, C. Kilts, Nature Neurosci. 2, 289 (1999).
65. R. Shadmehr and H. H. Holcomb, Science 277, 821 (1997).
66. N. M. Weinberger, in The Cognitive Neurosciences, M. S. Gazzaniga, Ed. (MIT Press, Cambridge, MA, 1995), pp. 1071-1089; N. M. Weinberger, Trends Cogn. Sci. 2, 271 (1998); T. S. Bjordahl, M. A. Dimyan, N. M. Weinberger, Behav. Neurosci. 112, 467 (1998); V. V. Galvan, J. Chen, N. M. Weinberger, Soc. Neurosci. Abstr. 24, 1422 (1998).
67. N. M. Weinberger, in The Cognitive Neurosciences, M. S. Gazzaniga, Ed. (MIT Press, Cambridge, MA, 1995), pp. 1071-1089; N. M. Weinberger, Trends Cogn. Sci. 2, 271 (1998); T. S. Bjordahl, M. A. Dimyan, N. M. Weinberger, Behav. Neurosci. 112, 467 (1998); V. V. Galvan, J. Chen, N. M. Weinberger, Soc. Neurosci. Abstr. 24, 1422 (1998).
68. N. M. Weinberger, in The Cognitive Neurosciences, M. S. Gazzaniga, Ed. (MIT Press, Cambridge, MA, 1995), pp. 1071-1089; N. M. Weinberger, Trends Cogn. Sci. 2, 271 (1998); T. S. Bjordahl, M. A. Dimyan, N. M. Weinberger, Behav. Neurosci. 112, 467 (1998); V. V. Galvan, J. Chen, N. M. Weinberger, Soc. Neurosci. Abstr. 24, 1422 (1998).
69. N. M. Weinberger, in The Cognitive Neurosciences, M. S. Gazzaniga, Ed. (MIT Press, Cambridge, MA, 1995), pp. 1071-1089; N. M. Weinberger, Trends Cogn. Sci. 2, 271 (1998); T. S. Bjordahl, M. A. Dimyan, N. M. Weinberger, Behav. Neurosci. 112, 467 (1998); V. V. Galvan, J. Chen, N. M. Weinberger, Soc. Neurosci. Abstr. 24, 1422 (1998).
70. G. Winocur, Behav. Brain Res. 38, 145 (1990); S. Zola-Morgan and L. R. Squire, Science 250, 288 (1990); J. J. Kim and M. S. Fanselow, Science 256, 675 (1992); Y. H. Cho, D. Beracochea, R. Jaffard, J. Neurosci. 13, 1759 (1993); J. J. Kim, R. E. Clark, R. F. Thompson, Behav Neurosci. 109, 195 (1995); G. Reidel et al., Nature Neurosci. 3, 898 (1999).
71. G. Winocur, Behav. Brain Res. 38, 145 (1990); S. Zola-Morgan and L. R. Squire, Science 250, 288 (1990); J. J. Kim and M. S. Fanselow, Science 256, 675 (1992); Y. H. Cho, D. Beracochea, R. Jaffard, J. Neurosci. 13, 1759 (1993); J. J. Kim, R. E. Clark, R. F. Thompson, Behav Neurosci. 109, 195 (1995); G. Reidel et al., Nature Neurosci. 3, 898 (1999).
72. G. Winocur, Behav. Brain Res. 38, 145 (1990); S. Zola-Morgan and L. R. Squire, Science 250, 288 (1990); J. J. Kim and M. S. Fanselow, Science 256, 675 (1992); Y. H. Cho, D. Beracochea, R. Jaffard, J. Neurosci. 13, 1759 (1993); J. J. Kim, R. E. Clark, R. F. Thompson, Behav Neurosci. 109, 195 (1995); G. Reidel et al., Nature Neurosci. 3, 898 (1999).
73. G. Winocur, Behav. Brain Res. 38, 145 (1990); S. Zola-Morgan and L. R. Squire, Science 250, 288 (1990); J. J. Kim and M. S. Fanselow, Science 256, 675 (1992); Y. H. Cho, D. Beracochea, R. Jaffard, J. Neurosci. 13, 1759 (1993); J. J. Kim, R. E. Clark, R. F. Thompson, Behav Neurosci. 109, 195 (1995); G. Reidel et al., Nature Neurosci. 3, 898 (1999).
74. G. Winocur, Behav. Brain Res. 38, 145 (1990); S. Zola-Morgan and L. R. Squire, Science 250, 288 (1990); J. J. Kim and M. S. Fanselow, Science 256, 675 (1992); Y. H. Cho, D. Beracochea, R. Jaffard, J. Neurosci. 13, 1759 (1993); J. J. Kim, R. E. Clark, R. F. Thompson, Behav Neurosci. 109, 195 (1995); G. Reidel et al., Nature Neurosci. 3, 898 (1999).
75. G. Winocur, Behav. Brain Res. 38, 145 (1990); S. Zola-Morgan and L. R. Squire, Science 250, 288 (1990); J. J. Kim and M. S. Fanselow, Science 256, 675 (1992); Y. H. Cho, D. Beracochea, R. Jaffard, J. Neurosci. 13, 1759 (1993); J. J. Kim, R. E. Clark, R. F. Thompson, Behav Neurosci. 109, 195 (1995); G. Reidel et al., Nature Neurosci. 3, 898 (1999).
76. W. B. Scoville and B. Milner, J. Neurol. Neurosurg. Psychiatry 20, 11 (1957); B. Milner, in Amnesia, C. W. M. Whitty and O. L. Zangwill, Eds. (Butterworths, London, 1966), pp. 109-133.
77. W. B. Scoville and B. Milner, J. Neurol. Neurosurg. Psychiatry 20, 11 (1957); B. Milner, in Amnesia, C. W. M. Whitty and O. L. Zangwill, Eds. (Butterworths, London, 1966), pp. 109-133.
78. L. R. Squire and P. Alvarez, Curr. Opin. Neurobiol. 5, 169 (1995).
79. T. J. Tyler and P. DiScenna, Behav. Neurosci. 100, 147 (1986); J. L. McClelland, B. L. McNaughton, R. C. O'Reilly, Psychol. Rev. 102, 419 (1995).
80. T. J. Tyler and P. DiScenna, Behav. Neurosci. 100, 147 (1986); J. L. McClelland, B. L. McNaughton, R. C. O'Reilly, Psychol. Rev. 102, 419 (1995).
81. T. J. Shors and L. D. Matzel, Behav. Brain Sci. 20, 597 (1997).
82. R. C. Malenka and R. A. Nicoll, Science 285, 1870 (1999).
83. T. Seidenbacher, K. G. Reymann, D. Balschun, Proc. Natl. Acad. Sci U.S.A. 94, 1494 (1997)
84. U. Frey, M. Krug, K. G. Reymann, H. Matthies, Brain Res. 452, 57 (1988).
85. D. M. Barros et al., Neurobiol. Learn. Mem. 71, 94 (1999).
86. P. A. Colley, F. -S. Sheu, A. Routtenberg, J. Neurosci. 10, 3353 (1990); Y.-Y. Huang, P. A. Colley, A. Routtenberg, Neuroscience 49, 819 (1992); D. Jerusalinsky et al., Behav. Neural Biol. 61, 107 (1994).
87. P. A. Colley, F. -S. Sheu, A. Routtenberg, J. Neurosci. 10, 3353 (1990); Y.-Y. Huang, P. A. Colley, A. Routtenberg, Neuroscience 49, 819 (1992); D. Jerusalinsky et al., Behav. Neural Biol. 61, 107 (1994).
88. P. A. Colley, F. -S. Sheu, A. Routtenberg, J. Neurosci. 10, 3353 (1990); Y.-Y. Huang, P. A. Colley, A. Routtenberg, Neuroscience 49, 819 (1992); D. Jerusalinsky et al., Behav. Neural Biol. 61, 107 (1994).
89. Y.-Y. Huang and E. R. Kandel, Proc. Natl. Acad. Sci. U.S.A. 92, 2446 (1995); R. Bernabeu et al., Proc. Natl. Acad. Sci. U.S.A. 94, 7041 (1997); G. E. Schafe, N. V. Nadel, G. M. Sullivan, A. Harris, J. E. LeDoux, Learn. Mem. 6, 97 (1999).
90. Y.-Y. Huang and E. R. Kandel, Proc. Natl. Acad. Sci. U.S.A. 92, 2446 (1995); R. Bernabeu et al., Proc. Natl. Acad. Sci. U.S.A. 94, 7041 (1997); G. E. Schafe, N. V. Nadel, G. M. Sullivan, A. Harris, J. E. LeDoux, Learn. Mem. 6, 97 (1999).
91. Y.-Y. Huang and E. R. Kandel, Proc. Natl. Acad. Sci. U.S.A. 92, 2446 (1995); R. Bernabeu et al., Proc. Natl. Acad. Sci. U.S.A. 94, 7041 (1997); G. E. Schafe, N. V. Nadel, G. M. Sullivan, A. Harris, J. E. LeDoux, Learn. Mem. 6, 97 (1999).
92. J. F. Guzowski and J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 94, 2693 (1997); T. Tully, Proc. Natl. Acad. Sci. U.S.A. 94, 4239 (1997).
93. J. F. Guzowski and J. L. McGaugh, Proc. Natl. Acad. Sci. U.S.A. 94, 2693 (1997); T. Tully, Proc. Natl. Acad. Sci. U.S.A. 94, 4239 (1997).
94. A. Routtenberg, in Four Decades of Memory, P. E. Gold, and W. T. Greenough, Eds. (American Psychological Association, Washington, DC, in press); T. Abel, K. C. Martin, D. Bartsch, E. R. Kandel, Science 279, 338 (1998).
95. A. Routtenberg, in Four Decades of Memory, P. E. Gold, and W. T. Greenough, Eds. (American Psychological Association, Washington, DC, in press); T. Abel, K. C. Martin, D. Bartsch, E. R. Kandel, Science 279, 338 (1998).
96. K. J. Murphy and C. M. Regan, Neurobiol. Learn. Mem. 70, 73 (1998); P. Roullet, R. Mileusnic, S. P. R. Rose, S. J. Sara, NeuroReport 8, 1907 (1997).
97. K. J. Murphy and C. M. Regan, Neurobiol. Learn. Mem. 70, 73 (1998); P. Roullet, R. Mileusnic, S. P. R. Rose, S. J. Sara, NeuroReport 8, 1907 (1997).
98. N. J. Emptage and T. J. Carew, Science 262, 253 (1993); J. Mauelshagen, G. R. Parker, T. J. Carew, J. Neurosci. 15, 7099 (1996); U. Müller and T. J. Carew, Neuron 21, 1423 (1996).
99. N. J. Emptage and T. J. Carew, Science 262, 253 (1993); J. Mauelshagen, G. R. Parker, T. J. Carew, J. Neurosci. 15, 7099 (1996); U. Müller and T. J. Carew, Neuron 21, 1423 (1996).
100. N. J. Emptage and T. J. Carew, Science 262, 253 (1993); J. Mauelshagen, G. R. Parker, T. J. Carew, J. Neurosci. 15, 7099 (1996); U. Müller and T. J. Carew, Neuron 21, 1423 (1996).
101. I. Izquierdo, D. M. Barros, T. Mello e Souza, M. M. de Souza, L. A. Izquierdo, Nature 393, 635 (1998).
102. I thank L. Cahill, I. Izquierdo, A. Routtenberg, G. Streidter, and N. M. Weinberger for their helpful comments and N. Collett for assistance in preparation of the manuscript. Supported by National Institute of Mental Health grant MH12526.