Reconsolidation of human memory: Brain mechanisms and clinical relevance

Biological Psychiatry

Volumn 76, Issue 4, 2014, Pages 274-280

  Schwabe, Lars ^a   Nader, Karim ^b   Pruessner, Jens C ^b,c  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Amygdala; drug addiction; episodic memory; fear memory; hippocampus; memory reconsolidation; PTSD

Indexed keywords

BRAIN; DRUG DEPENDENCE; EPISODIC MEMORY; FEAR; HUMAN; MEMORY CONSOLIDATION; MEMORY RECONSOLIDATION; NEUROIMAGING; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; REVIEW; ANIMAL; MEMORY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN; FEAR; HUMANS; MEMORY;

EID: 84905037939     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.03.008     Document Type: Review

References (100)

1. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders: DSM-V 2013 American Psychiatric Press Washington, DC
2. M.E. Coles, and R.G. Heimberg Memory biases in the anxiety disorders: Current status Clin Psychol Rev 22 2002 587 627
3. S.E. Hyman, R.C. Malenka, and E.J. Nestler Neural mechanisms of addiction: The role of reward-related learning and memory Annu Rev Neurosci 29 2006 565 598
4. J. McGaugh Memory-a century of consolidation Science 287 2000 248 251
5. J.L.C. Lee Reconsolidation: Maintaining memory relevance Trends Neurosci 32 2009 413 420
6. K. Nader, and O. Hardt A single standard for memory: The case for reconsolidation Nat Rev Neurosci 10 2009 224 234
7. J.R. Misanin, R.R. Miller, and D.J. Lewis Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace Science 160 1968 554 555
8. A.M. Schneider, and W. Sherman Amnesia: A function of the temporal relation of foot-shock to electroconvulsive shock Science 159 1968 219 221
9. D.J. Lewis, and N.J. Bregman Source of cues for cue-dependent amnesia in rats J Comp Physiol Psychol 85 1973 421 426
10. D.J. Lewis, N.J. Bregman, and J. Mahan Cue-dependent amnesia in rats J Comp Physiol Psychol 81 1972 243 247
11. D.J. Lewis Psychobiology of active and inactive memory Psychol Bull 86 1979 1054 1083
12. N. Spear Retrieval of memory in animals Psychol Rev 80 1973 163 194
13. J. Przybyslawski, and S.J. Sara Reconsolidation of memory after its reactivation Behav Brain Res 84 1997 241 246
14. J.L. McGaugh Time-dependent processes in memory storage Science 153 1966 1351 1359
15. S. Glickman Preservative neural processes and consolidation of the memory trace Psychol Bull 58 1961 218 233
16. S.J. Sara Retrieval and reconsolidation: Toward a neurobiology of remembering Learn Mem 7 2000 73 84
17. K. Nader, G.E. Schafe, and J.E. LeDoux Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval Nature 406 2000 722 726
18. S.M. Taubenfeld, M.H. Milekic, B. Monti, and C.M. Alberini The consolidation of new but not reactivated memory requires hippocampal C/EBPβ Nat Neurosci 4 2001 813 818
19. J. Debiec, J.E. LeDoux, and K. Nader Cellular and systems reconsolidation in the hippocampus Neuron 36 2002 527 538
20. R. Fonseca, U.V. Nagerl, and T. Bonhoeffer Neuronal activity determines the protein synthesis dependence of long-term potentiation Nat Neurosci 9 2006 478 480
21. J.K. Rose, and C.H. Rankin Blocking memory reconsolidation reverses memory-associated changes in glutamate receptor expression J Neurosci 26 2006 11582 11587
22. Y. Dudai The restless engram: Consolidations never end Annu Rev Neurosci 35 2012 227 247
23. P.S.B. Finnie, and K. Nader The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation Neurosci Biobehav Rev 36 2012 1667 1707
24. J.L.C. Lee, B.J. Everitt, and K.L. Thomas Independent cellular processes for hippocampal memory consolidation and reconsolidation Science 304 2004 839 843
25. M.P. Walker, T. Brakefield, J.A. Hobson, and R. Stickgold Dissociable stages of human memory consolidation and reconsolidation Nature 425 2003 616 620
26. A. Besnard, J. Caboche, and S. Laroche Reconsolidation of memory: A decade of debate Prog Neurobiol 99 2012 61 80
27. M. Kindt, M. Soeter, and B. Vervliet Beyond extinction: Erasing human fear responses and preventing the return of fear Nat Neurosci 12 2009 256 258
28. J.L. McGaugh The amygdala modulates the consolidation of memories of emotionally arousing experiences Annu Rev Neurosci 27 2004 1 28
29. M. Soeter, and M. Kindt Stimulation of the noradrenergic system during memory formation impairs extinction learning but not the disruption of reconsolidation Neuropsychopharmacology 37 2012 1204 1215
30. M. Soeter, and M. Kindt Erasing fear for an imagined threat event Psychoneuroendocrinology 37 2012 1769 1779
31. D. Sevenster, T. Beckers, and M. Kindt Prediction error governs pharmacologically induced amnesia for learned fear Science 339 2013 830 833
32. D. Sevenster, T. Beckers, and M. Kindt Retrieval per se is not sufficient to trigger reconsolidation of human fear memory Neurobiol Learn Mem 97 2012 338 345
33. M. Soeter, and M. Kindt Dissociating response systems: Erasing fear from memory Neurobiol Learn Mem 94 2010 30 41
34. D. Schiller, and E.A. Phelps Does reconsolidation occur in humans? Front Behav Neurosci 5 2011 24
35. A. Brunet, A.R. Ashbaugh, D. Saumier, M. Nelson, R.K. Pitman, and J. Tremblay et al. Does reconsolidation occur in humans: A reply Front Behav Neurosci 5 2011 74
36. M.H. Monfils, K.K. Cowansage, E. Klann, and J.E. LeDoux Extinction-reconsolidation boundaries: Key to persistent attenuation of fear memories Science 324 2009 951 955
37. D. Schiller, M.H. Monfils, C.M. Raio, D.C. Johnson, J.E. LeDoux, and E.A. Phelps Preventing the return of fear in humans using reconsolidation update mechanisms Nature 463 2010 49 53
38. J.P. Oyarzun, D. Lopez-Barroso, L. Fuentemilla, D. Cucurell, C. Pedraza, A. Rodriguez-Fornells, and R. de Diego-Balaguer Updating fearful memories with extinction training during reconsolidation: A human study using auditory aversive stimuli PLoS One 7 2012 e38849
39. T. Agren, J. Engman, A. Frick, J. Björkstrand, E.-M. Larsson, T. Furmark, and M. Fredrikson Disruption of reconsolidation erases a fear memory trace in the human amygdala Science 337 2012 1550 1552
40. T. Agren, T. Furmark, E. Eriksson, and M. Fredrikson Human fear reconsolidation and allelic differences in serotonergic and dopaminergic genes Transl Psychiatry 2 2012 e76
41. M. Soeter, and M. Kindt Disrupting reconsolidation: Pharmacological and behavioral manipulations Learn Mem 18 2011 357 366
42. M. Kindt, and M. Soeter Reconsolidation in a human fear conditioning study: A test of extinction as updating mechanism Biol Psychol 92 2013 43 50
43. A. Golkar, M. Bellander, A. Olsson, and A. Ohman Are fear memories erasable?-reconsolidation of learned fear with fear-relevant and fear-irrelevant stimuli Front Behav Neurosci 6 2012 80
44. N.T. Warren, K.M. Anderson, C. Kwon, L. Bosshardt, T. Jovanovic, B. Bradley, and S.D. Norrholm Human fear extinction and return of fear using reconsolidation update mechanisms: The contribution of on-line expectancy ratings [published online ahead of print October 29] Neurobiol Learn Mem 2013
45. E.F. Loftus Planting misinformation in the human mind: A 30-year investigation of the malleability of memory Learn Mem 12 2005 361 366
46. B. Fischhoff Hindsight is not equal to foresight: The effect of outcome knowledge on judgment J Exp Psychol Hum Percept Perform 1 1975 288 299
47. A. Hupbach, R. Gomez, O. Hardt, and L. Nadel Reconsolidation of episodic memories: A subtle reminder triggers integration of new information Learn Mem 14 2007 47 53
48. C. Forcato, M.L. Rodriguez, M.E. Pedreira, and H. Maldonado Reconsolidation in humans opens up declarative memory to the entrance of new information Neurobiol Learn Mem 93 2010 77 84
49. J.C. Chan, and J.A. LaPaglia Impairing existing declarative memory in humans Proc Natl Acad Sci U S A 110 2013 9309 9313
50. A. Hupbach, O. Hardt, R. Gomez, and L. Nadel The dynamics of memory: Context-dependent updating Learn Mem 15 2008 574 579
51. A. Hupbach, R. Gomez, and L. Nadel Episodic memory reconsolidation: Updating or source confusion? Memory 17 2009 502 510
52. B.A. Strange, M.C. Kroes, J.E. Fan, and R.J. Dolan Emotion causes targeted forgetting of established memories Front Behav Neurosci 4 2010 175
53. C. Forcato, V.L. Burgos, P.F. Argibay, V.A. Molina, M.E. Pedreira, and H. Maldonado Reconsolidation of declarative memory in humans Learn Mem 14 2007 295 303
54. L. Schwabe, and O.T. Wolf New episodic learning interferes with the reconsolidation of autobiographical memories PLoS One 4 2009 e7519
55. C. Forcato, M.L. Rodriguez, and M.E. Pedreira Repeated labilization-reconsolidation processes strengthen declarative memory in humans PLoS One 6 2011 e23305
56. V. Coccoz, H. Maldonado, and A. Delorenzi The enhancement of reconsolidation with a naturalistic mild stressor improves the expression of a declarative memory in humans Neuroscience 185 2011 61 72
57. V. Coccoz, A.V. Sandoval, J. Stehberg, and A. Delorenzi The temporal dynamics of enhancing a human declarative memory during reconsolidation Neuroscience 246 2013 397 408
58. L. Schwabe, and O.T. Wolf Stress impairs the reconsolidation of autobiographical memories Neurobiol Learn Mem 94 2010 153 157
59. M.C.W. Kroes, I. Tendolkar, G.A. van Wingen, J.A. van Waarde, B.A. Strange, and G. Fernandez An electroconvulsive therapy procedure impairs reconsolidation of episodic memories in humans Nat Neurosci 17 2014 204 206
60. L. Schwabe, K. Nader, and J.C. Pruessner Beta-adrenergic blockade during reactivation reduces the subjective feeling of remembering associated with emotional episodic memories Biol Psychol 92 2013 227 232
61. M.L. Rodriguez, J. Campos, C. Forcato, R. Leiquarda, H. Maldonado, V.A. Molina, and M.E. Pedreira Enhancing a declarative memory in humans: The effect of clonazepam on reconsolidation Neuropharmacology 64 2013 432 442
62. L. Schwabe, K. Nader, O.T. Wolf, T. Beaudry, and J.C. Pruessner Neural signature of reconsolidation impairments by propranolol in humans Biol Psychiatry 71 2012 380 386
63. L. Cahill, R. Babinsky, H.J. Markowitsch, and J.L. McGaugh The amygdala and emotional memory Nature 377 1995 295 296
64. L. Cahill, and J.L. McGaugh Mechanisms of emotional arousal and lasting declarative memory Trends Neurosci 21 1998 294 299
65. L. Cahill, B. Prins, M. Weber, and J.L. McGaugh Beta-adrenergic activation and memory for emotional events Nature 371 1994 702 704
66. K.S. LaBar, J.C. Gatenby, J.C. Gore, J.E. LeDoux, and E.A. Phelps Human amygdala activation during conditioned fear acquisition and extinction: A mixed-trial fMRI study Neuron 20 1998 937 945
67. C. Büchel, J. Morris, R.J. Dolan, and K.J. Friston Brain systems mediating aversive conditioning: An event-related fMRI study Neuron 20 1998 947 957
68. D. Schiller, J.W. Kanen, J.E. LeDoux, M.H. Monfils, and E.A. Phelps Extinction during reconsolidation of threat memory diminishes prefrontal cortex involvement Proc Natl Acad Sci U S A 110 2013 20040 20045
69. N. Censor, E. Dayan, and L.G. Cohen Cortico-subcortical neuronal circuitry associated with reconsolidation of human procedural memories [published online ahead of print June 15] Cortex 2013
70. C. Gerloff, B. Corwell, R. Chen, M. Hallett, and L.G. Cohen Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences Brain 120 1997 1587 1602
71. S. Diekelmann, C. Büchel, J. Born, and B. Rasch Labile or stabile: Opposing consequences for memory when reactivated during waking and sleep Nat Neurosci 14 2011 381 386
72. M. Sandrini, N. Censor, J. Mishoe, and L.G. Cohen Causal role of prefrontal cortex in strengthening of episodic memories through reconsolidation Curr Biol 23 2013 2181 2184
73. R.D. Rubin, R. Fried, and C.M. Franks New applications of ECT R.D. Rubin, C.M. Franks, Advances in Behavior Therapy 1968 Academic Press New York
74. R.K. Pitman Post-traumatic stress disorder, hormones, and memory Biol Psychiatry 26 1989 221 223
75. R.K. Pitman, K.M. Sanders, R.M. Zusman, A.R. Healy, F. Cheema, and N.B. Lasko et al. Pilot study of secondary prevention of posttraumatic stress disorder with propranolol Biol Psychiatry 51 2002 189 192
76. G. Vaiva, F. Ducrocq, K. Jezequel, B. Averland, P. Lestavel, A. Brunet, and C.R. Marmar Immediate treatment with propranolol decreases posttraumatic stress disorder two months after trauma Biol Psychiatry 54 2003 947 949
77. L. McGhee, C.V. Maani, T.H. Garza, P.A. DeSocio, K.M. Gaylord, and I.H. Black The effect of propranolol on posttraumatic stress disorder in burned service members J Burn Care Res 30 2009 92 97
78. A. Brunet, S.P. Orr, J. Tremblay, K. Robertson, K. Nader, and R.K. Pitman Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder J Psychiatr Res 42 2008 503 506
79. A. Brunet, J. Poundja, J. Tremblay, E. Bui, E. Thomas, and S.P. Orr et al. Trauma reactivation under the influence of propranolol decreases posttraumatic stress symptoms and disorder: 3 open-label trials J Clin Psychopharmacol 31 2011 547 550
80. J.R. Taylor, P. Olausson, J.J. Qiunn, and M.M. Torregrossa Targeting extinction and reconsolidation mechanisms to combat the impact of drug cues on addiction Neuropharmacology 56 suppl 1 2009 186 195
81. F.H. Gawin, and H.D. Kleber Abstinence symptomatology and psychiatric diagnosis in cocaine abusers. Clinical observations Arch Gen Psychiatry 43 1986 107 113
82. H. de Wit, and J. Stewart Reinstatement of cocaine-reinforced responding in the rat Psychopharmacology (Berl) 75 1981 134 143
83. T.W. Robbins, M. Cador, J.R. Taylor, and B.J. Everitt Limbic-striatal interactions in reward-related processes Neurosci Biobehav Rev 13 1989 155 162
84. C.A. Conklin, and S.T. Tiffany Applying extinction research and theory to cue-exposure addiction treatments Addiction 97 2002 155 167
85. H.S. Crombag, and Y. Shaham Renewal of drug seeking by contextual cues after prolonged extinction in rats Behav Neurosci 116 2002 169 173
86. J.L.C. Lee, P. Di Ciano, K.L. Thomas, and B.J. Everitt Disrupting reconsolidation of drug memories reduces cocaine-seeking behavior Neuron 47 2005 795 801
87. A.L. Milton, J.L.C. Lee, and B.J. Everitt Reconsolidation of appetitive memories for both neutral and drug reinforcement is dependent on {beta}-adrenergic receptors Learn Mem 15 2008 88 92
88. L.Y. Zhao, L.L. Sun, J. Shi, P. Li, Y. Zhang, and L. Lu Effects of β-adrenergic receptor blockade on drug-related memory reconsolidation in abstinent heroin addicts Drug Alcohol Depend 118 2011 224 229
89. L.Y. Zhao, X.L. Zhang, J. Shi, D.H. Epstein, and L. Lu Psychosocial stress after reactivation of drug-related memory impairs later recall in abstinent heroin addicts Psychopharmacology (Berl) 203 2009 599 608
90. Y.X. Xue, Y.X. Luo, P. Wu, H.S. Shi, L.F. Xue, and C. Chen et al. A memory retrieval-extinction procedure to prevent drug craving and relapse Science 336 2012 241 245
91. M. Milekic, and C.M. Alberini Temporally graded requirement for protein synthesis following memory reactivation Neuron 36 2002 521 525
92. A. Suzuki, S.A. Josselyn, P.W. Frankland, S. Masushige, A.J. Silva, and S. Kida Memory reconsolidation and extinction have distinct temporal and biochemical signatures J Neurosci 24 2004 4787 4795
93. S.H. Wang, L. de Oliveira Alvares, and K. Nader Cellular and systems mechanisms of memory strength as a constraint on auditory fear reconsolidation Nat Neurosci 12 2009 905 912
94. S. Wichert, O.T. Wolf, and L. Schwabe Reactivation, interference, and reconsolidation: Are recent and remote memories likewise susceptible? Behav Neurosci 125 2011 699 704
95. C. Forcato, P.F. Argibay, M.E. Pedreira, and H. Maldonado Human reconsolidation does not always occur when a memory is retrieved: The relevance of the reminder structure Neurobiol Learn Mem 91 2009 50 57
96. S. Wichert, O.T. Wolf, and L. Schwabe Changing memories after reactivation: A one-time opportunity? Neurobiol Learn Mem 99 2013 38 49
97. S. Wichert, O.T. Wolf, and L. Schwabe Updating of episodic memories depends on the strength of new learning after memory reactivation Behav Neurosci 127 2013 331 338
98. S.G. Bustos, M. Giachero, H. Maldonado, and V.A. Molina Previous stress attenuates the susceptibility to Midazolam's disruptive effect on fear memory reconsolidation: Influence of pre-reactivation D-cycloserine administration Neuropsychopharmacology 35 2010 1097 1108
99. B.D. Winters, M.C. Tucci, and M. DaCosta-Furtado Older and stronger object memories are selectively destabilized by reactivation in the presence of new information Learn Mem 16 2009 545 553
100. N.C. Tronson, and J.R. Taylor Molecular mechanisms of memory reconsolidation Nat Rev Neurosci 8 2007 262 275