Hippocampus and retrograde amnesia in the rat model: A modest proposal for the situation of systems consolidation

Neuropsychologia

Volumn 48, Issue 8, 2010, Pages 2357-2369

  Sutherland, Robert J ^a   Sparks, Fraser T ^a   Lehmann, Hugo ^b  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

^b TRENT UNIVERSITY   (Canada)

Author keywords

Anterograde amnesia; Distributed Reinstatement Theory; Memory overshadowing; Memory replay; Remote memory; Temporal gradient

Indexed keywords

ANTEROGRADE AMNESIA; ARTICLE; BRAIN DAMAGE; BRAIN FUNCTION; BRAIN REGION; BRAIN TISSUE; COMPETITION; DISEASE SEVERITY; FLAVOR; HIPPOCAMPUS; LEARNING; MEMORY CONSOLIDATION; NONHUMAN; ODOR; RETROGRADE AMNESIA; TASK PERFORMANCE; THEORETICAL STUDY; ANIMAL; CONDITIONING; DISEASE MODEL; HUMAN; LONG TERM MEMORY; NEUROPSYCHOLOGICAL TEST; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; RECOGNITION;

AMNESIA, RETROGRADE; ANIMALS; CONDITIONING (PSYCHOLOGY); DISEASE MODELS, ANIMAL; HIPPOCAMPUS; HUMANS; NEUROPSYCHOLOGICAL TESTS; RATS; RECOGNITION (PSYCHOLOGY); RETENTION (PSYCHOLOGY);

EID: 77954216491     PISSN: 00283932     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2010.04.015     Document Type: Article

References (110)

1. Ainge J.A., Heron-Maxwell C., Theofilas P., Wright P., de Hoz L., Wood E.R. The role of the hippocampus in object recognition in rats: Examination of the influence of task parameters and lesion size. Behavioural Brain Research 2006, 167(1):183-195.
2. Anagnostaras S.G., Gale G.D., Fanselow M.S. Hippocampus and contextual fear conditioning: Recent controversies and advances. Hippocampus 2001, 11(1):8-17.
3. Anagnostaras S.G., Maren S., Fanselow M.S. Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: Within-subjects examination. Journal of Neuroscience 1999, 19(3):1106-1114.
4. Andersen P. The hippocampus book 2007, Oxford University Press, Oxford; New York.
5. Atkins A., Mashhoon Y., Kantak K. Hippocampal regulation of contextual cue-induced reinstatement of cocaine-seeking behavior. Pharmacology, Biochemistry and Behavior 2008, 90:481-491.
6. Avis H.H., Carlton P.L. Amnesia produced by hippocampal spreading depression. Science 1968, 161(3836):73-75.
7. Biedenkapp J.C., Rudy J.W. Hippocampal and extrahippocampal systems compete for control of contextual fear: Role of ventral subiculum and amygdala. Learning & Memory 2009, 16:38-45.
8. Bohbot V., Otáhal P., Liu Z., Nadel L., Bures J. Electroconvulsive shock and lidocaine reveal rapid consolidation of spatial working memory in the water maze. Proceedings of the National Academy of Science USA 1996, 93:4016-4019.
9. Bolhuis J.J., Stewart C.A., Forrest E.M. Retrograde amnesia and memory reactivation in rats with ibotenate lesions to the hippocampus or subiculum. Quarterly Journal of Experimental Psychology B 1994, 47:129-150.
10. Broadbent N.J., Gaskin S., Squire L.R., Clark R.E. Recognition memory after hippocampal damage in rats: Anterograde and temporally graded retrograde memory impairment. Society for Neuroscience Abstracts 2008, 791:12.
11. Broadbent N.J., Squire L.R., Clark R.E. Reversible hippocampal lesions disrupt water maze performance during both recent and remote memory tests. Learning & Memory 2006, 13:187-191.
12. Broadbent N.J., Squire L.R., Clark R.E. Rats depend on habit memory for discrimination learning and retention. Learning & Memory 2007, 14:145-151.
13. Clark R.E., Broadbent N.J., Squire L.R. Hippocampus and remote spatial memory in rats. Hippocampus 2005, 15:260-272.
14. Clark R.E., Broadbent N.J., Squire L.R. Impaired remote spatial memory after hippocampal lesions despite extensive training beginning early in life. Hippocampus 2005, 15:340-346.
15. Clark R.E., Broadbent N.J., Squire L.R. The hippocampus and spatial memory: Findings with a novel modification of the watermaze. Journal of Neuroscience 2007, 27:6647-6654.
16. Clark R.E., Broadbent N.J., Zola S.M., Squire L.R. Anterograde amnesia and temporally graded retrograde amnesia for a nonspatial memory task after lesions of hippocampus and subiculum. Journal of Neuroscience 2002, 22(11):4663-4669.
17. Corcoran K.A., Desmond T.J., Frey K.A., Maren S. Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction. Journal of Neuroscience 2005, 25(39):8978-8987.
18. Corcoran K.A., Maren S. Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. Journal of Neuroscience 2001, 21(5):1720-1726.
19. Corkin S. What's new with the amnesic patient HM?. Nature Reviews Neuroscience 2002, 3:153-160.
20. Driscoll I., Howard S.R., Prusky G.T., Rudy J.W., Sutherland R.J. Seahorse wins all races: Hippocampus participates in both linear and non-linear visual discrimination learning. Behavioural Brain Research 2005, 164(1):29-35.
21. Ennaceur A., Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behavioural Brain Research 1988, 31(1):47-59.
22. Epp, J., Keith, J. R., Spanswick, S. C., Stone, J. C., Prusky, G. T., & Sutherland, R. J. (2008). Retrograde amnesia for visual memories after hippocampal damage in rats. Learning & Memory, 15, 214-221.
23. Euston D.R., Tatsuno M., McNaughton B.L. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 2007, 318:1147-1150.
24. Fanselow M.S., Poulos A.M. The neuroscience of mammalian associative learning. Annual Review of Psychology 2004, 56:207-234.
25. Fanselow M.S., Tighe T.J. Contextual conditioning with massed versus distributed unconditional stimuli in the absence of explicit conditional stimuli. Journal of Experimental Psycholology: Animal Behavior Processes 1988, 14(2):187-199.
26. Fanselow M.S., DeCola J.P., Young S.L. Mechanisms responsible for reduced contextual conditioning with massed unsignaled unconditional stimuli. Journal of Experimental Psychology: Animal Behavior Processes 1993, 19(2):121-137.
27. Frank M.J., Rudy J.W., O'Reilly R.C. Transitivity, flexibility, conjunctive representations, and the hippocampus. II. A computational analysis. Hippocampus 2003, 13(3):341-354.
28. Frankland P.W., Bontempi B. The organization of recent and remote memories. Nature Reviews Neuroscience 2005, 6(2):119-130.
29. Gaskin S., Tremblay A., Mumby D.G. Retrograde and anterograde object recognition in rats with hippocampal lesions. Hippocampus 2003, 13(8):962-969.
30. Gilboa A., Winocur G., Rosenbaum R.S., Poreh A., Gao F., Black S.E., et al. Hippocampal contributions to recollection in retrograde and anterograde amnesia. Hippocampus 2006, 16:966-980.
31. Hobin J.A., Ji J., Maren S. Ventral hippocampal muscimol disrupts context-specific fear memory retrieval after extinction in rats. Hippocampus 2006, 16:174-182.
32. Holt W., Maren S. Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory. Journal of Neuroscience 1999, 19(20):9054-9062.
33. Hughes R.A. Retrograde amnesia in rats produced by hippocampal injections of potassium chloride: Gradient of effect and recovery. Journal of Comparative and Physiological Psychology 1969, 68(4):637-644.
34. Karlsson M.P., Frank L.M. Awake replay of remote experiences in the hippocampus. Nat. Neurosci. 2009, 12:913-918.
35. Kim J.J., Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 1992, 256(5057):675-677.
36. Knowlton B.J., Fanselow M.S. The hippocampus, consolidation and online memory. Current Opinion in Neurobiology 1998, 8:293-296.
37. Kubik S., Miyashita T., Guzowski J.F. Hippocampal inactivation produces hypoactivity in a cortical circuit: A marked decrease in experience-dependent Arc gene expression in rat retrosplenial cortex. Society for Neuroscience Abstracts 2008, 389:4.
38. Kudrimoti H.S., Barnes C.A., McNaughton B.L. Reactivation of hippocampal cell assemblies: Effects of behavioral state, experience and EEG dynamics. Journal of Neuroscience 1999, 19:4090-4101.
39. Lehmann H., Carfagnini A., Yamin S., Mumby D.G. Context-dependent effects of hippocampal damage on memory in the shock-probe test. Hippocampus 2005, 15(1):18-25.
40. Lehmann H., Glenn M.J., Mumby D.G. Consolidation of object-discrimination memory is independent of the hippocampus in rats. Experimental Brain Research 2007, 180(4):755-764.
41. Lehmann H., Lacanilao S., Sutherland R.J. Complete or partial hippocampal damage produces equivalent retrograde amnesia for remote contextual fear memories. European Journal of Neuroscience 2007, 25(5):1278-1286.
42. Lehmann H., Lecluse V., Houle A., Mumby D.G. Retrograde amnesia following hippocampal lesions in the shock-probe conditioning test. Hippocampus 2006, 16(4):379-387.
43. Lehmann, H., Sparks, F. T., O'Brien, J., Robert, J., McDonald, R. J., & Sutherland, R. J. (in press). Complete, but not dorsal or ventral, hippocampal damage produces retrograde amnesia for fear-potentiated startle in rats. Neuroscience.
44. Lehmann H., Sparks F.T., Spanswick S.C., Hadikin C., McDonald R.J., Sutherland R.J. Making context memories independent of the hippocampus. Learning & Memory 2009, 16:417-420.
45. Lehmann H., Sparks F.T., Spanswick S.C., Sutherland R.J. Learning parameters mitigate retrograde amneisa after hippocampal damage. Society for Neuroscience Abstracts 2008, 295:9.
46. Lomber S. The advantages and limitations of permanent or reversible deactivation techniques in the assessment of neural function. Journal of Neuroscience Methods 1999, 86:109-117.
47. Maguire E.A., Nannery R., Spiers H.J. Navigation around London by a taxi driver with bilateral hippocampal lesions. Brain 2006, 129(11):2894-2907.
48. Maren S., Aharonov G., Fanselow M.S. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behavioural Brain Research 1997, 88(2):261-274.
49. Maren S., Holt W. The hippocampus and contextual memory retrieval in Pavlovian conditioning. Behavioural Brain Research 2000, 110:97-108.
50. Martin S.J., de Hoz L., Morris R.G. Retrograde amnesia: Neither partial nor complete hippocampal lesions in rats result in preferential sparing of remote spatial memory, even after reminding. Neuropsychologia 2005, 43(4):609-624.
51. Matus-Amat P., Higgins E., Barrientos R., Rudy J. The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. Journal of Neuroscience 2004, 24(10):2431-2439.
52. Maviel T., Durkin T.P., Menzaghi F., Bontempi B. Sites of neocortical reorganization critical for remote spatial memory. Science 2004, 305:96-99.
53. McClelland J.L., McNaughton B.L., O'Reilly R.C. Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychological Review 1995, 102(3):419-457.
54. McDonald R.J., White N.M. A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum. Behavioral Neuroscience 1993, 107(1):3-22.
55. McDonald R.J., White N.M. Parallel information processing in the water maze: Evidence for independent memory systems involving dorsal striatum and hippocampus. Behavioral & Neural Biology 1994, 61(3):260-270.
56. McDonald R.J., White N.M. Information acquired by the hippocampus interferes with acquisition of the amygdala-based conditioned-cue preference in the rat. Hippocampus 1995, 5(3):189-197.
57. Meeter M., Murre J.M. Consolidation of long-term memory: Evidence and alternatives. Psychological Bulletin 2004, 130(6):843-857.
58. Micheau J., Riedel G., Roloff E.V.L., Inglis J., Morris R.G.M. Reversible hippocampal inactivation partially dissociates how and where to search in the water maze. Behavioral Neuroscience 2004, 118(5):1022-1032.
59. Milner, B. (1959). The memory defect in bilateral hippocampal lesions (pp. 43-58). Psychiatric Research Reports, American Psychiatric Association, No 11.
60. Milner B. The medial temporal-lobe amnesic syndrome. Psychiatric Clinics of North America 2005, 28:599-611.
61. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297(5868):681-683.
62. Moscovitch M., Nadel L., Winocur G., Gilboa A., Rosenbaum R.S. The cognitive neuroscience of remote episodic, semantic and spatial memory. Current Opinion in Neurobiology 2006, 16(2):179-190.
63. Moser M.-B., Moser E.I., Forrest E., Andersen P., Morris R.G.M. Spatial learning with a minislab in the dorsal hippocampus. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:9697-9701.
64. Mumby D.G., Gaskin S., Glenn M.J., Schramek T.E., Lehmann H. Hippocampal damage and exploratory preferences in rats: Memory for objects, places, and contexts. Learning & Memory 2002, 9(2):49-57.
65. Mumby D.G., Tremblay A., Lecluse V., Lehmann H. Hippocampal damage and anterograde object-recognition in rats after long retention intervals. Hippocampus 2005, 15(8):1050-1056.
66. Nadel L., Moscovitch M. Memory consolidation, retrograde amnesia and the hippocampal complex. Current Opinion in Neurobiology 1997, 7(2):217-227.
67. O'Keefe J.M., Nadel L. The hippocampus as a cognitive map 1978, Oxford University Press, Oxford.
68. Pavlides C., Winson J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. Journal of Neuroscience 1989, 9:2907-2918.
69. Pavlov I.P., Anrep G.V. Conditioned reflexes: An investigation of the physiological activity of the cerebral cortex 1927, Oxford University Press, London.
70. Penfield W., Milner B. Memory deficits induced by bilateral lesions in the hippocampal zone. Archives of Neurology and Psychiatry 1958, 79:475-497.
71. Quinn J.J., Ma Q.D., Tinsley M.R., Koch C., Fanselow M.S. Inverse temporal contributions of the dorsal hippocampus and medial prefrontal cortex to the expression of long-term fear memories. Learning & Memory 2008, 15:368-372.
72. Rempel-Clower N.L., Zola S.M., Squire L.R., Amaral D.G. Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. Journal of Neuroscience 1996, 16(16):5233-5255.
73. Resstel L.B., Joca S.R., Corrêa F.M., Guimarães F.S. Effects of reversible inactivation of the dorsal hippocampus on the behavioral and cardiovascular responses to an aversive conditioned context. Behavioral Pharmacology 2008, 19(2):137-144.
74. Ribeiro S., Gervasoni D., Soares E.S., Zhou Y., Lin S.C., Pantoja J., et al. Long-lastingnovelty-inducedneuronalreverbera- tion during slow-wave sleep in multiple forebrain areas. PLoS Biology 2004, 2:126-137.
75. Riedel G., Micheau J., Lam A.G.M., Roloff E.N.L., Martin S.J., Bridge H., et al. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nature 1999, 2(10):898-905.
76. Ross R.S., Eichenbaum H. Dynamics of hippocampal and cortical activation during consolidation of a nonspatial memory. J Neurosci 2006, 26:4852-4859.
77. Rudy J.W., Barrientos R.M., O'Reilly R.C. Hippocampal formation supports conditioning to memory of a context. Behavioral Neuroscience 2002, 116(4):530-538.
78. Rudy J.W., O'Reilly R.C. Contextual fear conditioning, conjunctive representations, pattern completion, and the hippocampus. Behavioral Neuroscience 1999, 113(5):867-880.
79. Rudy J.W., Sutherland R.J. Is it Systems or Cellular Consolidation? Time will tell. An Alternative interpretation of The Morris Group's Recent Science Paper. Neurobiology of Learning and Memory 2008, 89:366-369.
80. Sacchetti B., Lorenzini C., Baldi E., Tassoni G., Bucherelli C. Auditory thalamus, dorsal hippocampus, basolateral amygdala, and perirhinal cortex role in the consolidation of conditioned freezing to context and to acoustic conditioned stimulus in the rat. Journal of Neuroscience 1999, 19(21):9570-9578.
81. Sara S.J. Memory deficits in rats with hippocampal or cortical lesions: Retrograde effects. Behavioral & Neural Biology 1981, 32:504-509.
82. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurochemistry 1957, 20:11-21.
83. Sherry D.F., Schacter D.L. The evolution of multiple memory systems. Psychological Review 1987, 94(4):439-454.
84. Sparks F.T., O'Brien J., Lehmann H., Sutherland R.J. Hippocampal damage produces retrograde amnesia for fear potentiated startle. Society for Neuroscience Abstracts 2005, 31(649):12.
85. Squire L.R. Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychological Review 1992, 99:195-231.
86. Squire L.R., Alvarez P. Retrograde amnesia and memory consolidation: A neurobiological perspective. Current Opinion in Neurobiology 1995, 5(2):169-177.
87. Squire L.R., Bayley P.J. The neuroscience of remote memory. Current Opinion in Neurobiology 2007, 17:185-196.
88. Squire L.R., Slater P.C., Chace P.M. Retrograde amnesia: Temporal gradient in very long term memory following electroconvulsive therapy. Science 1975, 187(4171):77-79.
89. Squire L.R., Knowlton B.J. Learning about categories in the absence of memory. Proceedings of the National Academy of Science USA 1995, 92(26):12470-12474.
90. Squire L.R., Zola S.M. Memory, memory impairment, and the medial temporal lobe. Cold Spring Harbor Symposium on Quantitative Biology 1996, 61:185-195.
91. Squire L.R., Stark C.E., Clark R.E. The medial temporal lobe. Annual Review of Neuroscience 2004, 27:279-306.
92. Steinvorth S., Levine B., Corkin S. Medial temporal lobe structures are needed to re-experience remote autobiographical memories: Evidence from H.M. and W.R. Neuropsychologia 2005, 43:479-496.
93. Sutherland R.J., Kolb B., Whishaw I.Q. Spatial mapping: Definitive disruption by hippocampal or medial frontal cortical damage in the rat. Neuroscience Letters 1982, 31:271-276.
94. Sutherland R.J., Rudy J.W. Configural association theory: The contribution of the hippocampus to learning, memory, and amnesia. Psychobiology 1989, 17(2):129-144.
95. Sutherland R.J., Lehmann H., Spanswick S.C., Sparks F.T., Melvin N.R. Growth points in research on memory and hippocampus. Canadian Journal of Experimenta Psychology 2006, 60(2):166-174.
96. Sutherland R.J., O'Brien J., Lehmann H. Absence of systems consolidation of fear memories after dorsal, ventral, or complete hippocampal damage. Hippocampus 2008, 16:417-420.
97. Sutherland R.J., Weisend M.P., Mumby D., Astur R.S., Hanlon F.M., Koerner A., et al. Retrograde amnesia after hippocampal damage: Recent vs. remote memories in two tasks. Hippocampus 2001, 11(1):27-42.
98. Takehara K., Shigenori Kawahara S., Kirino Y. Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. Journal of Neuroscience 2003, 23(30):9897-9905.
99. Tatsuno M., Lipa P., McNaughton B.L. Methodological considerations on the use of template matching to study long-lasting memory trace replay. Journal of Neuroscience 2006, 26(42):10727-10742.
100. Teixeira C.M., Pomedli S.R., Maei H.R., Kee N., Frankland P.W. Involvement of the anterior cingulate cortex in the expression of remote spatial memory. Journal of Neuroscience 2006, 26:7555-7564.
101. Tse D., Langston R.F., Bethus I., et al. Does assimilation into schemas involve systems or cellular consolidation? It's not just time. Learning & Memory 2008, 89(4):361-365.
102. Tse D., Langston R.F., Kakeyama M., Bethus I., Spooner P.A., Wood E.R., et al. Schemas and memory consolidation. Science 2007, 316(5821):76-82.
103. Travis, S. G., Fraser T. Sparks, F. T., Arnold, T., Lehmann, H., Sutherland, R. J., et al. (in press). Hippocampal damage produces retrograde but not anterograde amnesia for a cued location in a spontaneous exploratory task in rats. Hippocampus.
104. White N.M., McDonald R.J. Multiple parallel memory systems in the brain of the rat. Neurobiology of Learning & Memory 2002, 77(2):125-184.
105. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 1994, 265:676-679.
106. Wiltgen B.J., Brown R.A., Talton L.E., Silva A.J. New circuits for old memories: The role of the neocortex in consolidation. Neuron 2004, 44(1):101-108.
107. Wiltgen B.J., Sanders M.J., Anagnostaras S.G., Sage J.R., Fanselow M.S. Context fear learning in the absence of the hippocampus. Journal of Neuroscience 2006, 26(20):5484-5491.
108. Winocur G. Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions. Behavioural Brain Research 1990, 38(2):145-154.
109. Winocur G., McDonald R.M., Moscovitch M. Anterograde and retrograde amnesia in rats with large hippocampal lesions. Hippocampus 2001, 11(1):18-26.
110. Winocur G., Moscovitch M., Fogel S., Rosenbaum R.S., Sekeres M. Preserved spatial memory after hippocampal lesions: Effects of extensive experience in a complex environment. Nature Neuroscience 2005, 8(3):273-275.