Grading gradients: Evaluating evidence for time-dependent memory reorganization in experimental animals

Journal of Experimental Neuroscience

Volumn 2009, Issue 2, 2009, Pages 13-22

  Akers, Katherine G ^a   Frankland, Paul W ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cortex; Hippocampus; Memory consolidation

Indexed keywords

ANIMAL MODEL; BRAIN CORTEX; DISEASE MODEL; EXPERIMENTAL MODEL; HIPPOCAMPUS; HUMAN; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; SLEEP;

EID: 84856785585     PISSN: None     EISSN: 11790695     Source Type: Journal    
DOI: 10.4137/jen.s2391     Document Type: Article

References (105)

1. Ribot T. Diseases of memory. Oxford: Appleton-Century-Crofts. 1882
2. Squire LR. The legacy of patient HM for neuroscience. Neuron. 2009;61:6-9
3. Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry. 1957;20:11-21
4. Salmon DP, Lasker BR, Butters N, Beatty WW. Remote memory in a patient with circumscribed amnesia. Brain Cogn. 1988;7:201-11
5. Beatty WW, Salmon DP, Bernstein N, Butters N. Remote memory in a patient with amnesia due to hypoxia. Psychol Med. 1987;17: 657-65
6. Squire LR, Slater PC, Chace PM. Retrograde amnesia: temporal gradient in very long term memory following electroconvulsive therapy. Science. 1975;187:77-9
7. Squire LR, Alvarez P. Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr Opin Neurobiol. 1995;5:169-77
8. Marr D. Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci. 1971;262:23-81
9. McClelland JL, McNaughton BL, O'Reilly RC. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev. 1995;102:419-57
10. Teyler TJ, DiScenna P. The hippocampal memory indexing theory. Behav Neurosci. 1986;100:147-54
11. Alvarez P, Squire LR. Memory consolidation and the medial temporal lobe: a simple network model. Proc Natl Acad Sci U S A. 1994; 91:7041-5
12. Squire LR. Memory and the hippocampus: a synthesis from fi ndings with rats, monkeys, and humans. Psychol Rev. 1992;99:195-231
13. Squire LR, Stark CE, Clark RE. The medial temporal lobe. Annu Rev Neurosci. 2004;27:279-306
14. Nadel L, Moscovitch M. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol. 1997;7:217-27
15. Rosenbaum RS, Winocur G, Moscovitch M. New views on old memories: re-evaluating the role of the hippocampal complex. Behav Brain Res. 2001;127:183-97
16. Winocur G. Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions. Behav Brain Res. 1990;38:145-54
17. Clark RE, Broadbent NJ, Zola SM, Squire LR. Anterograde amnesia and temporally graded retrograde amnesia for a nonspatial memory task after lesions of hippocampus and subiculum. J Neurosci. 2002;22:4663-9
18. Winocur G, McDonald RM, Moscovitch M. Anterograde and retrograde amnesia in rats with large hippocampal lesions. Hippocampus. 2001;11:18-26
19. Ross RS, Eichenbaum H. Dynamics of hippocampal and cortical activation during consolidation of a nonspatial memory. J Neurosci. 2006;26:4852-9
20. Kim JJ, Fanselow MS. Modality-specifi c retrograde amnesia of fear. Science. 1992;256:675-77
21. Anagnostaras SG, Maren S, Fanselow MS. Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. J Neurosci. 1999;9:1106-14
22. Maren S, Aharonov G, Fanselow MS. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav Brain Res. 1997;88:261-74
23. Debiec J, LeDoux JE, Nader K. Cellular and systems reconsolidation in the hippocampus. Neuron. 2002;36:527-38
24. Ward MT, Oler JA, Markus EJ. Hippocampal dysfunction during aging I: defi cits in memory consolidation. Neurobiol Aging. 1999;20: 363-72
25. Shimizu E, Tang YP, Rampon C, Tsien JZ. NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. Science. 2000;290:1170-4
26. Wang H, Shimizu E, Tang YP, Cho M, Kyin M, et al. Inducible protein knockout reveals temporal requirement of CaMKII reactivation for memory consolidation in the brain. Proc Natl Acad Sci U S A. 2003;100: 4287-92
27. Quinn JJ, Ma QD, Tinsley MR, Koch C, Fanselow MS. Inverse temporal contributions of the dorsal hippocampus and medial prefrontal cortex to the expression of long-term fear memories. Learn Mem. 2008;15:368-72
28. Cho YH, Beracochea D, Jaffard R. Extended temporal gradient for the retrograde and anterograde amnesia produced by ibotenate entorhinal cortex lesions in mice. J Neurosci. 1993;13:1759-66
29. Cho YH, Kesner RP. Involvement of entorhinal cortex or parietal cortex in long-term spatial discrimination memory in rats: retrograde amnesia. Behav Neurosci. 1996;110:436-42
30. Maviel T, Durkin TP, Menzaghi F, Bontempi B. Sites of neocortical reorganization critical for remote spatial memory. Science. 2004; 305:96-9
31. Ramos JM. Retrograde amnesia for spatial information: a dissociation between intra and extramaze cues following hippocampus lesions in rats. Eur J Neurosci. 1998;10:3295-301
32. Laurent-Demir C, Jaffard R. Temporally graded retrograde amnesia for spatial information resulting from afterdischarges induced by electrical stimulation of the dorsal hippocampus in mice. Psychobiol. 1997;25: 133-40
33. Wiig KA, Cooper LN, Bear MF. Temporally graded retrograde amnesia following separate and combined lesions of the perirhinal cortex and fornix in the rat. Learn Mem. 1996;3:313-25
34. Takehara K, Kawahara S, Kirino Y. Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. J Neurosci. 2003;23: 9897-905
35. Takehara K, Kawahara S, Takatsuki K, Kirino Y. Time-limited role of the hippocampus in the memory for trace eyeblink conditioning in mice. Brain Res. 2002;951:183-90
36. Kim JJ, Clark RE, Thompson RF. Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav Neurosci. 1995;109:195-203
37. Zola-Morgan SM, Squire LR. The primate hippocampal formation: evidence for a time-limited role in memory storage. Science.1990;250: 288-90
38. Izquierdo I, Quillfeldt JA, Zanatta MS, Quevedo J, Schaeffer E, et al. Sequential role of hippocampus and amygdala, entorhinal cortex and parietal cortex in formation and retrieval of memory for inhibitory avoidance in rats. Eur J Neurosci. 1997;9:786-93
39. Quillfeldt JA, Zanatta MS, Schmitz PK, Quevedo J, Schaeffer E, et al. Different brain areas are involved in memory expression at different times from training. Neurobiol Learn Mem. 1996;66:97-101
40. Glenn MJ, Nesbitt C, Mumby DG. Perirhinal cortex lesions produce variable patterns of retrograde amnesia in rats. Behav Brain Res. 2003;141:183-93
41. Remondes M, Schuman EM. Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature. 2004;431:699-703
42. Kubie JL, Sutherland RJ, Muller RU. Hippocampal lesions produce a temporally graded retrograde amnesia on a dry version of the Morris swimming task. Psychobiol. 1999;27:313-30
43. Yasuda M, Mayford MR. CaMKII activation in the entorhinal cortex disrupts previously encoded spatial memory. Neuron. 2006;50: 309-18
44. Mumby DG, Astur RS, Weisend MP, Sutherland RJ. Retrograde amnesia and selective damage to the hippocampal formation: memory for places and object discriminations. Behav Brain Res. 1999; 106:97-107
45. Bolhuis JJ, Stewart CA, Forrest EM. Retrograde amnesia and memory reactivation in rats with ibotenate lesions to the hippocampus or subiculum. Q J Exp Psychol B. 1994;47:129-50
46. Martin SJ, de Hoz L, Morris RG. Retrograde amnesia: neither partial nor complete hippocampal lesions in rats result in preferential sparing of remote spatial memory, even after reminding. Neuropsychologia. 2005;43:609-24
47. Gaskin S, Tremblay A, Mumby DG. Retrograde and anterograde object recognition in rats with hippocampal lesions. Hippocampus. 2003;13:962-9
48. Lehmann H, Lacanilao S, Sutherland RJ. Complete or partial hippocampal damage produces equivalent retrograde amnesia for remote contextual fear memories. Eur J Neurosci. 2007;25:1278-86
49. Lehmann H, Lecluse V, Houle A, Mumby DG. Retrograde amnesia following hippocampal lesions in the shock-probe conditioning test. Hippocampus. 2006;16:379-87
50. Mumby DG, Glenn MJ. Anterograde and retrograde memory for object discriminations and places in rats with perirhinal cortex lesions. Behav Brain Res. 2000;114:119-34
51. Sutherland RJ, O'Brien J, Lehmann H. Absence of systems consolidation of fear memories after dorsal, ventral, or complete hippocampal damage. Hippocampus. 2008;18:710-18
52. Riedel G, Micheau J, Lam AG, Roloff EL, Martin SJ, et al. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat Neurosci. 1999;2:898-905
53. Broadbent NJ, Squire LR, Clark RE. Reversible hippocampal lesions disrupt water maze performance during both recent and remote memory tests. Learn Mem. 2006;13:187-91
54. Clark RE, Broadbent NJ, Squire LR. Impaired remote spatial memory after hippocampal lesions despite extensive training beginning early in life. Hippocampus. 2005;15:340-6
55. Clark RE, Broadbent NJ, Squire LR. Hippocampus and remote spatial memory in rats. Hippocampus. 2005;15:260-72
56. Clark RE, Broadbent NJ, Squire LR. The hippocampus and spatial memory: findings with a novel modification of the water maze. J Neurosci. 2007;27:6647-54
57. Teixeira CM, Pomedli SR, Maei HR, Kee N, Frankland PW. Involvement of the anterior cingulate cortex in the expression of remote spatial memory. J Neurosci. 2006;26:7555-64
58. Winocur G, Moscovitch M, Caruana DA, Binns MA. Retrograde amnesia in rats with lesions to the hippocampus on a test of spatial memory. Neuropsychologia. 2005;43:1580-90
59. Burwell RD, Bucci DJ, Sanborn MR, Jutras MJ. Perirhinal and postrhinal contributions to remote memory for context. J Neurosci. 2004;24:11023-28
60. Sutherland RJ, Weisend MP, Mumby D, Astur RS, Hanlon FM, et al. Retrograde amnesia after hippocampal damage: recent vs. remote memories in two tasks. Hippocampus. 2001;11:27-42
61. Epp J, Keith JR, Spanswick SC, Stone JC, Prusky GT, et al. Retrograde amnesia for visual memories after hippocampal damage in rats. Learn Mem. 2008;15:214-21
62. Haijima A, Ichitani Y. Anterograde and retrograde amnesia of place discrimination in retrosplenial cortex and hippocampal lesioned rats. Learn Mem. 2008;15:477-82
63. Thornton JA, Rothblat LA, Murray EA. Rhinal cortex removal produces amnesia for preoperatively learned discrimination problems but fails to disrupt postoperative acquisition and retention in rhesus monkeys. J Neurosci. 1997;17:8536-49
64. Gaffan D. Additive effects of forgetting and fornix transfection in the temporal gradient of retrograde amnesia. Neuropsychologia. 1993;31: 1055-66
65. Winocur G, Moscovitch M, Fogel S, Rosenbaum RS, Sekeres M. Preserved spatial memory after hippocampal lesions: effects of extensive experience in a complex environment. Nat Neurosci. 2005; 8:273-5
66. Lehmann H, Sparks FT, Spanswick SC, Hadikin C, McDonald RJ, et al. (In Press) Making context memories independent of the hippocampus
67. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, et al. Schemas and memory consolidation. Science. 2007;316:76-82
68. Winocur G, Moscovitch M, Sekeres M. Memory consolidation or transformation: context manipulation and hippocampal representations of memory. Nat Neurosci. 2007;10:555-7
69. Wiltgen BJ, Silva AJ. Memory for context becomes less specifi c with time. Learn Mem. 2007;14:313-7
70. Biedenkapp JC, Rudy JW. Context preexposure prevents forgetting of a contextual fear memory: implication for regional changes in brain activation patterns associated with recent and remote memory tests. Learn Mem. 2007;14:200-3
71. Winocur G, McDonald R, Moscovitch M. Anterograde and retrograde amnesia in rats with large hippocampal lesions. Hippocampus. 2001;11:18-26
72. Wang SH, Teixeira CM, Wheeler AL, Frankland PW. The precision of remote context memories does not require the hippocampus. Nature Neurosci. In press. 2009
73. Ross R, Eichenbaum H. Dynamics of hippocampal and cortical activation during consolidation of a nonspatial memory. J Neurosci. 2006;26:4852-9
74. Bontempi B, Laurent-Demir C, Destrade C, Jaffard R. Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature. 1999;400:671-5
75. Frankland PW, Bontempi B, Talton LE, Kaczmarek L, Silva AJ. The involvement of the anterior cingulate cortex in remote contextual fear memory. Science. 2004;304:881-3
76. Smith CA, Countryman RA, Sahuque LL, Colombo PJ. Time-courses of Fos expression in rat hippocampus and neocortex following acquisition and recall of a socially transmitted food preference. Neurobiol Learn Mem. 2007;88:65-74
77. Gusev PA, Cui C, Alkon DL, Gubin AN. Topography of Arc/Arg3.1 mRNA expression in the dorsal and ventral hippocampus induced by recent and remote spatial memory recall: dissociation of CA3 and CA1 activation. J Neurosci. 2005;25:9384-97
78. Kaczmarek L, Robertson HA. Handbook of chemical neuroanatomy. Amsterdam: Elsevier. 2002
79. Takehara-Nishiuchi K, McNaughton BL. Spontaneous changes of neocortical code for associative memory during consolidation. Science. 2008;322:960-3
80. Hugues S, Garcia R. Reorganization of learning-associated prefrontal synaptic plasticity between the recall of recent and remote fear extinction memory. Learn Mem. 2007;14:520-4
81. Ding HK, Teixeira CM, Frankland PW. Inactivation of the anterior cingulate cortex blocks expression of remote, but not recent, conditioned taste aversion memory. Learn Mem. 2008;15:290-3
82. Blum S, Hebert AE, Dash PK. A role for the prefrontal cortex in recall of recent and remote memories. Neuroreport. 2006;17:341-4
83. Rudy JW, Biedenkapp JC, O'Reilly RC. Prefrontal cortex and the organization of recent and remote memories: an alternative view. Learn Mem. 2005;12:445-6
84. Louie K, Wilson MA. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron. 2001;29:145-56
85. Lee AK, Wilson MA. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron. 2002;36:1183-94
86. Ji D, Wilson MA. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci. 2007;10:100-7
87. Qin YL, McNaughton BL, Skaggs WE, Barnes CA. Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Philos Trans R Soc Lond B Biol Sci. 1997;352:1525-33
88. Siapas AG, Wilson MA. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron. 1998;21:1123-8
89. Jones MW, Errington ML, French PJ, Fine A, Bliss TV, et al. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci. 2001;4:289-96
90. Lee JL, Everitt BJ, Thomas KL. Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science. 2004;304:839-43
91. Ribeiro S, Goyal V, Mello CV, Pavlides C. Brain gene expression during REM sleep depends on prior waking experience. Learn Mem. 1999;6:500-8
92. Ribeiro S, Shi X, Engelhard M, Zhou Y, Zhang H, et al. Novel Experience Induces Persistent Sleep-Dependent Plasticity in the Cortex but not in the Hippocampus. Front Neurosci. 2007;1:43-55
93. Ribeiro S, Mello CV, Velho T, Gardner TJ, Jarvis ED, et al. Induction of hippocampal long-term potentiation during waking leads to increased extrahippocampal zif-268 expression during ensuing rapid-eye-movement sleep. J Neurosci. 2002;22:10914-23
94. Ribeiro S, Nicolelis MA. Reverberation, storage, and postsynaptic propagation of memories during sleep. Learn Mem. 2004;11:686-96
95. Frankland PW, O'Brien C, Ohno M, Kirkwood A, Silva AJ. Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature. 2001;411:309-13
96. Tanaka D, Nakada K, Takao K, Ogasawara E, Kasahara A, et al. Normal mitochondrial respiratory function is essential for spatial remote memory in mice. Mol Brain. 2008;1:21
97. Hayashi ML, Choi SY, Rao BS, Jung HY, Lee HK, et al. Altered cortical synaptic morphology and impaired memory consolidation in forebrain-specifi c dominant-negative PAK transgenic mice. Neuron. 2004;42:773-87
98. Shan Q, Chan GC, Storm DR. Type 1 adenylyl cyclase is essential for maintenance of remote contextual fear memory. J Neurosci. 2008;28:12864-7
99. White JA, McKinney BC, John MC, Powers PA, Kamp TJ, et al. Conditional forebrain deletion of the L-type calcium channel Ca V 1.2 disrupts remote spatial memories in mice. Learn Mem. 2008; 15:1-5
100. Matynia A, Anagnostaras SG, Wiltgen BJ, Lacuesta M, Fanselow MS, et al. A high through-put reverse genetic screen identifi es two genes involved in remote memory in mice. PLoS ONE. 2008;3:e2121
101. Shema R, Sacktor TC, Dudai Y. Rapid erasure of long-term memory associations in the cortex by an inhibitor of PKM zeta. Science. 2007;317:951-3
102. Cui Z, Wang H, Tan Y, Zaia KA, Zhang S, et al. Inducible and reversible NR1 knockout reveals crucial role of the NMDA receptor in preserving remote memories in the brain. Neuron. 2004;41:781-93
103. Takehara-Nishiuchi K, Nakao K, Kawahara S, Matsuki N, Kirino Y. Systems consolidation requires postlearning activation of NMDA receptors in the medial prefrontal cortex in trace eyeblink conditioning. J Neurosci. 2006;26:5049-58
104. Feng R, Rampon C, Tang YP, Shrom D, Jin J, et al. Defi cient neurogenesis in forebrain-specifi c presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron. 2001;32:911-26
105. Kitamura T, Saitoh Y, Takashima N, Murayama A, Nibori Y, et al. Adult neurogenesis is involved in the systems consolidation of memory. Society for Neuroscience Abstracts. 2008