Memory consolidation in humans: New evidence and opportunities

Experimental Physiology

Volumn 99, Issue 3, 2014, Pages 471-486

  Maguire, Eleanor A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTIC METHOD; ARTICLE; AUTOBIOGRAPHICAL MEMORY; BRAIN REGION; CONCEPTUAL FRAMEWORK; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; KNOWLEDGE; MEMORY; MEMORY CONSOLIDATION; NEUROIMAGING; VENTROMEDIAL PREFRONTAL CORTEX; VOXEL BASED MORPHOMETRY;

HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MEMORY; MEMORY, EPISODIC; PREFRONTAL CORTEX;

EID: 84895175045     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2013.072157     Document Type: Article

References (125)

1. Aimone JB, Deng W & Gage FH (2011). Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70, 589-596.
2. Alvernhe A, Van Cauter T, Save E & Poucet B (2008). Different CA1 and CA3 representations of novel routes in a shortcut situation. J Neurosci 28, 7324-7333.
3. Amaral DG & Lavenex P (2007). Hippocampal neuroanatomy. In The Hippocampus Book, ed. Anderson P, Morris R, Amaral D, Bliss T & O'Keefe J, pp. 37-114. Oxford University Press, New York.
4. Andelman F, Hoofien D, Goldberg I, Aizenstein O & Neufeld MY (2010). Bilateral hippocampal lesion and a selective impairment of the ability for mental time travel. Neurocase 16, 426-435.
5. Bajo A, Fleminger S & Kopelman MD (2010). Confabulations are emotionally charged, but not always for the best. J Int Neuropsychol Soc 16, 975-983.
6. Barron HC, Dolan RJ & Behrens TE (2013). Online evaluation of novel choices by simultaneous representation of multiple memories. Nat Neurosci 16, 1492-1498.
7. Bechara A, Damasio AR, Damasio H & Anderson SW (1994). Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50, 7-15.
8. Bechara A, Damasio H, Tranel D & Anderson SW (1998). Dissociation of working memory from decision making within the human prefrontal cortex. J Neurosci 18, 428-437.
9. Beckmann M, Johansen-Berg H & Rushworth MFS (2009). Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J Neurosci 29, 1175-1190.
10. Bird CM, Castelli F, Malik O, Frith U & Husain M (2004). The impact of extensive frontal lobe damage on 'Theory of Mind' and cognition. Brain 127, 914-928.
11. Bonnici HM, Chadwick MJ, Lutti A, Hassabis D, Weiskopf N & Maguire EA (2012). Detecting representations of recent and remote autobiographical memories in vmPFC and hippocampus. J Neurosci 32, 16982-16991.
12. Bonnici HM, Chadwick MJ & Maguire EA (2013a). Representations of recent and remote autobiographical memories in hippocampal subfields. Hippocampus 23, 849-854.
13. Bonnici HM, Sidhu M, Chadwick MJ, Duncan JS & Maguire EA (2013b). Assessing hippocampal functional reserve in temporal lobe epilepsy: a multi-voxel pattern analysis of fMRI data. Epilepsy Res 105, 140-149.
14. Bontempi B, Laurent-Demir C, Destrade C & Jaffard R (1999). Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature 400, 671-675.
15. Bullmore E & Sporns O (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10, 186-198.
16. Burgess PW & Shallice T (1996). Response suppression, initiation and strategy use following frontal lobe lesions. Neuropsychologia 34, 263-273.
17. Chadwick MJ, Bonnici HM & Maguire EA (2012). Decoding information in the human hippocampus: a user's guide. Neuropsychologia 50, 3107-3121.
18. Chadwick MJ, Hassabis D, Weiskopf N & Maguire EA (2010). Decoding individual episodic memory traces in the human hippocampus. Curr Biol 20, 544-547.
19. Clayton NC, Bussey TJ & Dickinson A (2003). Can animals recall the past and plan for the future? Nat Rev Neurosci 4, 685-691.
20. Corballis MC (2013). The wandering rat: response to Suddendorf. Trends Cogn Sci 17, 152.
21. Della Sala S, Laiacona M, Spinnler H & Trivelli C (1993). Autobiographical recollection and frontal damage. Neuropsychologia 31, 823-839.
22. Dudai Y (2004). The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55, 51-86.
23. Dudai Y (2012). The restless engram: consolidations never end. Annu Rev Neurosci 35, 227-247.
24. Evensmoen HR, Lehn H, Xu J, Witter MP, Nadel L & Håberg AK (2013). The anterior hippocampus supports a coarse, global environmental representation and the posterior hippocampus supports fine-grained, local environmental representations. J Cogn Neurosci 25, 1908-1925.
25. Fellows LK (2011). Orbitofrontal contributions to value-based decision making: evidence from humans with frontal lobe damage. Ann NY Acad Sci 1239, 51-58.
26. Frankland PW & Bontempi B (2005). The organization of recent and remote memories. Nat Rev Neurosci 6, 119-130.
27. Gilbert PE & Brushfield AM (2009). The role of the CA3 hippocampal subregion in spatial memory: a process oriented behavioral assessment. Prog Neuropsychopharm Biol Psychiatry 33, 774-781.
28. Gilboa A & Moscovitch M (2002). The cognitive neuroscience of confabulation: a review and a model. In Handbook of Memory Disorders, 2nd edition, ed. Baddeley AD, Kopelman MD & Wilson BA, pp. 315-342. John Wiley & Sons, London.
29. Gilboa A & Verfaellie M (2010). Telling it like it isn't: the cognitive neuroscience of confabulation. J Int Neuropsychol Soc 16, 961-966.
30. Gilboa A, Winocur G, Grady CL, Hevenor SJ & Moscovitch M (2004). Remembering our past: functional neuroanatomy of recollection of recent and very remote personal events. Cereb Cortex 14, 1214-1225.
31. Goel V & Dolan RJ (2003). Reciprocal neural response within lateral and ventral medial prefrontal cortex during hot and cold reasoning. Neuroimage 20, 2314-2321.
32. Goshen I, Brodsky M, Prakash R, Wallace J, Gradinaru V, Ramakrishnan C & Deisseroth K (2011). Dynamics of retrieval strategies for remote memories. Cell 147, 678-689.
33. Graham KS, Barense MD & Lee AC (2010). Going beyond LTM in the MTL: a synthesis of neuropsychological and neuroimaging findings on the role of the medial temporal lobe in memory and perception. Neuropsychologia 48, 831-853.
34. Gupta R, Tranel D & Duff MC (2012). Ventromedial preftonal cortex damage does not impair the development and use of common ground in social interaction: implications for cognitive theory of mind. Neuropsychologia 50, 145-152.
35. Hardt O, Nader K & Nadel L (2013). Decay happens: the role of active forgetting in memory. Trends Cogn Sci 17, 110-120.
36. Hassabis D, Chu C, Rees G, Weiskopf N, Molyneux PD & Maguire EA (2009). Decoding neuronal ensembles in the human hippocampus. Curr Biol 19, 546-554.
37. Hassabis D, Kumaran D & Maguire EA (2007a). Using imagination to understand the neural basis of episodic memory. J Neurosci 27, 14365-14374.
38. Hassabis D, Kumaran D, Vann SD & Maguire EA (2007b). Patients with hippocampal amnesia cannot imagine new experiences. Proc Natl Acad Sci USA 104, 1726-1731.
39. Hassabis D & Maguire EA (2007). Deconstructing episodic memory with construction. Trends Cogn Sci 11, 299-306.
40. Hassabis D & Maguire EA (2009). The construction system of the brain. Philos Trans R Soc Lond B Biol Sci 364, 1263-1271.
41. Haynes JD & Rees G (2006). Decoding mental states from brain activity in humans. Nat Rev Neurosci 7, 523-534.
42. Hebb DO (1949). The Organization of Behavior. Wiley & Sons, New York.
43. Hunsaker MR & Kesner RP (2008). Evaluating the differential roles of the dorsal dentate gyrus, dorsal CA3, and dorsal CA1 during a temporal ordering for spatial locations task. Hippocampus 18, 955-964.
44. Jocham G, Hunt LT, Near J & Behrens TE (2012). A mechanism for value-guided choice based on the extinction-inhibition balance in prefrontal cortex. Nat Neurosci 15, 960-961.
45. Kesner RP, Lee I & Gilbert P (2004). A behavioral assessment of hippocampal function based on a subregional analysis. Rev Neurosci 15, 333-352.
46. Klein SB, Loftus J & Kihlstrom JF (2002). Memory and temporal experience: the effects of episodic memory loss on an amnesic patient's ability to remember the past and imagine the future. Soc Cogn 20, 353-379.
47. Kopelman MD (1999). Varieties of false memories. Cogn Neuropsychol 16, 197-214.
48. Kopelman MD, Lasserson D, Kingsley DR, Bello F, Rush C, Stanhope N, Stevens TG, Goodman G, Buckman JR, Heilpern G, Kendall BE & Colchester AC (2003). Retrograde amnesia and the volume of critical brain structures. Hippocampus 13, 879-891.
49. Kopelman MD, Stanhope N & Kingsley D (1999). Retrograde amnesia in patients with diencephalic, temporal lobe or frontal lesions. Neuropsychologia 37, 939-958.
50. Kumaran D, Summerfield JJ, Hassabis D & Maguire EA (2009). Tracking the emergence of conceptual knowledge during human decision making. Neuron 63, 889-901.
51. Lashley KS (1950). In search of the engram. Society of Experimental Biology, Symposium 4, 454-482.
52. Lee AC, Yeung LK & Barense MD (2012). The hippocampus and visual perception. Front Hum Neurosci 6, 91.
53. Lee I, Yoganarasimha D, Rao G & Knierim JJ (2004). Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430, 456-459.
54. Leutgeb JK, Leutgeb S, Moser MB & Moser EI (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315, 961-966.
55. Leutgeb S & Leutgeb JK (2007). Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map. Learn Mem 14, 745-757.
56. Leutgeb S, Leutgeb JK, Treves A, Moser MB & Moser EI (2004). Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305, 1295-1298.
57. Levine B (2004). Autobiographical memory and the self in time: brain lesions effects, functional neuroanatomy, and lifespan development. Brain Cogn 55, 54-58.
58. Levine B, Black SE, Cabeza R, Sinden M, Mcintosh AR, Toth JP, Tulving E & Stuss DT (1998). Episodic memory and the self in a case of isolated retrograde amnesia. Brain 121, 1951-1973.
59. Lorente de No R (1934). Studies on the structure of the cerebral cortex II. Continuation of the study of the ammonic system. J Psychol Neurol 46, 113-117.
60. McClelland JL & Goddard NH (1996). Considerations arising from a complementary learning systems perspective on hippocampus and neocortex. Hippocampus 6, 654-665.
61. McClelland JL, McNaughton BL & Reilly RC (1995). 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 102, 419-457.
62. Maguire EA (2001). Neuroimaging studies of autobiographical event memory. Philos Trans R Soc Lond B Biol Sci 356, 1441-1451.
63. Maguire EA & Frith CD (2003). Lateral asymmetry in the hippocampal response to the remoteness of autobiographical memories. J Neurosci 23, 5302-5307.
64. Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RS & Frith CD (2000). Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci USA 97, 4398-4403.
65. Maguire EA, Henson RN, Mummery CJ & Frith CD (2001). Activity in prefrontal cortex, not hippocampus, varies parametrically with the increasing remoteness of memories. Neuroreport 12, 441-444.
66. Maguire EA & Mullally SL (2013). The hippocampus: a manifesto for change. J Exp Psychol Gen 142, 1180-1189.
67. Maguire EA, Nannery R & Spiers HJ (2006). Navigation around London by a taxi driver with bilateral hippocampal lesions. Brain 129, 2894-2907.
68. Mangels JA, Gershberg FB & Shimamura AP (1996). Impaired retrieval from remote memory in patients with frontal lobe damage. Neuropsychology 10, 31-41.
69. Marr D (1971). Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262, 23-81.
70. Mayes AR (1988). Human Organic Memory Disorders. Cambridge University Press, Cambridge, UK.
71. Moscovitch M (1989). Confabulation and the frontal systems: strategic versus associative retrieval in neuropsychological theories of memory. In Varieties of Memory and Consciousness: Essays in Honor of Endel Tulving, ed. Roediger HL & Craik FI, pp. 133-160. Lawrence Erlbaum Associates, Hillsdale, NJ, USA.
72. Moscovitch M & Melo B (1997). Strategic retrieval and the frontal lobes: evidence from confabulation and amnesia. Neurospychologia 35, 1017-1034.
73. Moser MB & Moser EI (1998). Functional differentiation in the hippocampus. Hippocampus 8, 608-619.
74. Mullally SL, Intraub H & Maguire EA (2012). Attenuated boundary extension produces a paradoxical memory advantage in amnesic patients. Curr Biol 22, 261-268.
75. Nadel L, Campbell J & Ryan L (2007a). Autobiographical memory retrieval and hippocampal activation as a function of repetition and the passage of time. Neural Plast 2007, 90472.
76. Nadel L, Hupbach A, Gomez R & Newman-Smith K (2012). Memory formation, consolidation and transformation. Neurosci Biobeh Rev 36, 1640-1645.
77. Nadel L & Moscovitch M (1997). Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol 7, 217-227.
78. Nadel L, Winocur G, Ryan L & Moscovitch M (2007b). Sytems consolidation and the hippocampus: two views. Debates in Neuroscience 1, 55-66.
79. Nahum L, Ptak R, Leemann B & Schnider A (2009). Disorientation, confabulation, and extinction capacity: clues on how the brain creates reality. Biol Psychiatry 65, 966-972.
80. Nieuwenhuis IL & Takashima A (2011). The role of the ventromedial prefrontal cortex in memory consolidation. Behav Brain Res 218, 325-334.
81. Niki K & Luo J (2002). An fMRI study on the time-limited role of the medial temporal lobe in long-term topographical autobiographic memory. J Cogn Neurosci 14, 500-507.
82. Norman KA, Polyn SM, Detre GJ & Haxby JV (2006). Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn Sci 10, 424-430.
83. O'Reilly RC, Bhattacharyya R, Howard MD & Ketz N (2011). Complementary learning systems. Cogn Sci, doi: 10.1111/j.1551-6709.2011.01214.x
84. O'Reilly RC & McClelland JL (1994). Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 4, 661-682.
85. O'Reilly RC & Rudy JW (2000). Computational principles of learning in the neocortex and hippocampus. Hippocampus 10, 389-397.
86. Passingham RE & Wise SP (2012). The Neurobiology of the Prefrontal Cortex. Oxford University Press, Oxford, UK.
87. Penfield W & Mathieson G (1974). Memory. Autopsy findings and comments on the role of the hippocampus in experiential recall. Arch Neurol 31, 145-154.
88. Petrides M & Pandya DN (1999). Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and macaque brain and corticocortical connection patterns. Eur J Neurosci 11, 1011-1036.
89. Piefke M, Weiss PH, Zilles K, Markowitsch HJ & Fink GR (2003). Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory. Brain 126, 650-668.
90. Piolino P, Desgranges B, Belliard S, Matuszewski V, Lalevee C, De La Sayette V & Eustache F (2003). Autobiographical memory and autonoetic consciousness: triple dissociation in neurodegenerative diseases. Brain 126, 2203-2219.
91. Piolino P, Giffard-Quillon G, Desgranges B, Chetelat G, Baron JC & Eustache F (2004). Re-experiencing old memories via hippocampus: a PET study of autobiographical memory. Neuroimage 22, 1371-1383.
92. Poppenk J, Evensmoen HR, Moscovitch M & Nadel L (2013). Long-axis specialization of the human hippocampus. Trends Cogn Sci 17, 230-240.
93. Race E, Keane MM & Verfaellie M (2011). Medial temporal lobe damage causes deficits in episodic memory and episodic future thinking not attributable to deficits in narrative construction. J Neurosci 31, 10262-10269.
94. Rekkas PV & Constable RT (2005). Evidence that autobiographic memory retrieval does not become independent of the hippocampus: an fMRI study contrasting very recent with remote events. J Cogn Neurosci 17, 1950-1961.
95. Rolls ET (2010). A computational theory of episodic memory formation in the hippocampus. Behav Brain Res 215, 180-196.
96. Rolls ET, Hornak J, Wade D & McGrath J (1994). Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. J Neurol Neurosurg Psychiatry 57, 1518-1524.
97. Rosenbaum RS, Gilboa A, Levine B, Winocur G & Moscovitch M (2009). Amnesia as an impairment of detail generation and binding: evidence from personal, fictional, and semantic narratives in K.C. Neuropsychologia 47, 2181-2187.
98. Ryan L, Nadel L, Keil K, Putnam K, Schnyer D, Trouard T & Moscovitch M (2001). Hippocampal complex and retrieval of recent and very remote autobiographical memories: evidence from functional magnetic resonance imaging in neurologically intact people. Hippocampus 11, 707-714.
99. Saleem KS, Kondo H & Price JL (2008). Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular and opercular cortex in the macaque monkey. J Comp Neurol 506, 659-693.
100. Schnider A & Ptak R (1999). Spontaneous confabulators fail to suppress currently irrelevant memory traces. Nat Neurosci 2, 677-681.
101. Scoville WB & Milner B (1957). Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20, 11-21.
102. Shallice T & Burgess PW (1991). Deficits in strategy application following frontal lobe damage in man. Brain 114, 727-741.
103. Shimamura AP, Janowsky JS & Squire LR (1990). Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients. Neuropsychologia 28, 803-813.
104. Söderlund H, Moscovitch M, Kumar N, Mandic M & Levine B (2012). As time goes by: hippocampal connectivity changes with remoteness of autobiographical memory retrieval. Hippocampus 22, 670-679.
105. Spiers HJ, Maguire EA & Burgess N (2001). Hippocampal amnesia. Neurocase 7, 357-382.
106. Squire LR (1992). Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99, 195-231.
107. Squire LR & Wixted JT (2011). The cognitive neuroscience of human memory since H.M. Ann Rev Neurosci 34, 259-288.
108. Steinvorth S, Corkin S & Halgren E (2006). Ecphory of autobiographical memories: an fMRI study of recent and remote memory retrieval. Neuroimage 30, 285-298.
109. Suddendorf T (2013). Mental time travel: continuities and discontinuities. Trends Cogn Sci 17, 151-152.
110. Summerfield JJ, Hassabis D & Maguire EA (2009). Cortical midline involvement in autobiographical memory. Neuroimage 44, 1188-1200.
111. Svoboda E & Levine B (2009). The effects of rehearsal on the functional neuroanatomy of episodic autobiographical and semantic remembering: a functional magnetic resonance imaging study. J Neurosci 29, 3073-3082.
112. Svoboda E, McKinnon MC & Levine B (2006). The functional neuroanatomy of autobiographical memory: a meta-analysis. Neuropsychologia 44, 2189-2208.
113. Takashima A, Nieuwenhuis ILC, Jensen O, Talamini LM, Rijpkema M & Fernández G (2009). Shift from hippocampal to neocortical centred retrieval network with consolidation. J Neurosci 29, 10087-10093.
114. Teyler TJ & DiScenna P (1985). The role of hippocampus in memory: a hypothesis. Neurosci Biobehav Rev 9, 377-389.
115. Thomas BC, Croft KE & Tranel D (2011). Harming kin to save strangers: further evidence for abnormally utilitarian moral judgments after ventromedial prefrontal damage. J Cogn Neurosci 23, 2186-2196.
116. Treves A & Rolls ET (1994). Computational analysis of the role of the hippocampus in memory. Hippocampus 4, 374-391.
117. Tse D, Takeuchi T, Kakeyama M, Kajii Y, Okuno H, Tohyama C, Bito H & Morris RG (2011). Schema-dependent gene activation and memory encoding in neocortex. Science 333, 891-895.
118. Tulving E (1985). Memory and consciousness. Canadian Psychology/Pychologie Canadienne 26, 1-12.
119. van Kesteren MT, Beul SF, Takashima A, Henson RN, Ruiter DJ & Fernández G (2013). Differential roles for the medial prefrontal and medial temporal cortices in schema-dependent encoding: from congruent to incongruent. Neuropsychologia 51, 2352-2359.
120. Vazdarjanova A & Guzowski JF (2004). Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24, 6489-6496.
121. Viard A, Piolino P, Desgranges B, Chetelat G, Lebreton K, Landeau B, Young A, De La Sayette V & Eustache F (2007). Hippocampal activation for autobiographical memories over the entire lifetime in healthy aged subjects: an fMRI study. Cereb Cortex 17, 2453-2467.
122. Watanabe T, Kimura HM, Hirose S, Wada H, Imai Y, Machida T, Shirouzu I, Miyashita Y & Konishi S (2012). Functional dissociation between anterior and posterior temporal cortical regions during retrieval of remote memory. J Neurosci 32, 9659-9670.
123. Wills TJ, Lever C, Cacucci F, Burgess N & O'Keefe J (2005). Attractor dynamics in the hippocampal representation of the local environment. Science 308, 873-876.
124. Winocur G & Moscovitch M (2011). Memory transformation and systems consolidation. J Int Neuropsychol Soc 17, 766-780.
125. Yarkoni T, Poldrack RA, Nichols TE, Van Essen DC & Wager TD (2011). Large-scale automated synthesis of human functional neuroimaging data. Nat Methods 8, 665-670.