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Reconsolidation and the Dynamic Nature of Memory

  • Karim NaderEmail author
Chapter

Abstract

Research on the reconsolidation effect was greatly revitalized by the highly analytic demonstration of memory reconsolidation (Nader et al. 2000) in a well-defined behavioral protocol (auditory fear conditioning in the rat). Since this study, reconsolidation has been demonstrated in hundreds of studies over a range of species, tasks, and amnesic agents. Evidence for reconsolidation does not come solely from the behavioral level of analysis. Cellular and molecular correlates of reconsolidation have also been found. In this review I will first define the evidence on which reconsolidation is concluded to exist. I will then discuss some of the conceptual issues facing the field in determining when reconsolidation does and does not occur. Lastly I will explain the clinical implications of this effect.

Keywords

Memory stabilization Memory destabilization Memory re-stabilization Memory maintenance 

Notes

Acknowledgements

K.N. was supported by the Canadian Institutes of Health Research, Natural Sciences and Engineering Research Council of Canada, Canadian Foundation for Innovation, The Volkswagen, Alfred P. Sloan and EJL Karim Nader is a James McGill Chair.

References

  1. Anokhin KV, Tiunova AA, Rose SP (2002) Reminder effects—reconsolidation or retrieval deficit? Pharmacological dissection with protein synthesis inhibitors following reminder for a passive-avoidance task in young chicks. Eur J Neurosci 15:1759–1765CrossRefPubMedGoogle Scholar
  2. Bailey CH, Kandel ER (1993) Structural changes accompanying memory storage. Annu Rev Physiol 55:397–426Google Scholar
  3. Ben Mamou C, Gamache K, Nader K (2006) NMDA receptors are critical for unleashing consolidated auditory fear memories. Nat Neurosci 9:1237–1239CrossRefPubMedGoogle Scholar
  4. Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE (2001) Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn Mem 8:229–242CrossRefPubMedGoogle Scholar
  5. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39CrossRefPubMedGoogle Scholar
  6. Bozon B, Davis S, Laroche S (2003) A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40:695–701CrossRefPubMedGoogle Scholar
  7. Brunet A, Orr SP, Tremblay J, Robertson K, Nader K, Pitman RK (2008) Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder. J Psychiatr Res 42:503–506CrossRefPubMedGoogle Scholar
  8. Cai D, Pearce K, Chen S, Glanzman DL (2012) Reconsolidation of long-term memory in aplysia. Curr Biol 22:1783–1788CrossRefPubMedPubMedCentralGoogle Scholar
  9. Child FM, Epstein HT, Kuzirian AM, Alkon DL (2003) Memory reconsolidation in hermissenda. Biol Bull 205:218–219CrossRefPubMedGoogle Scholar
  10. De Vietti T, Holiday JH (1972) Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace: a replication. Psychonomic Sci 29:137–138CrossRefGoogle Scholar
  11. Debiec J, Ledoux JE (2004) Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 129:267–272CrossRefPubMedGoogle Scholar
  12. Debiec J, LeDoux JE, Nader K (2002) Cellular and systems reconsolidation in the hippocampus. Neuron 36:527–538CrossRefPubMedGoogle Scholar
  13. Doyere V, Debiec J, Monfils MH, Schafe GE, LeDoux JE (2007) Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala. Nat Neurosci 10:414–416PubMedGoogle Scholar
  14. Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51–86CrossRefPubMedGoogle Scholar
  15. Duncan CP (1949) The retroactive effect of electroconvulsive shock. J Comp Physiol Psychol 42:32–44CrossRefPubMedGoogle Scholar
  16. Duvarci S, Nader K, Ledoux JE (2005) Activation of extracellular signal-regulated kinase-mitogen-activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning. Eur J Neurosci 21:283–289CrossRefPubMedGoogle Scholar
  17. Duvarci S, Mamou CB, Nader K (2006) Extinction is not a sufficient condition to prevent fear memories from undergoing reconsolidation in the basolateral amygdala. Eur J Neurosci 24:249–260CrossRefPubMedGoogle Scholar
  18. Ebbinghaus M (1885) Über das Gedächtnis. K. Buehler, LeipzigGoogle Scholar
  19. Eisenberg M, Kobilo T, Berman DE, Dudai Y (2003) Stability of retrieved memory: inverse correlation with trace dominance. Science 301:1102–1104CrossRefPubMedGoogle Scholar
  20. Finnie PS, Nader K (2012) The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation. Neurosci Biobehav Rev 36:1667–1707CrossRefPubMedGoogle Scholar
  21. Flexner LB, Flexner JB, Stellar E (1965) Memory and cerebral protein synthesis in mice as affected by graded amounts of puromycin. Exp Neurol 13:264–272CrossRefPubMedGoogle Scholar
  22. Fonseca R, Nagerl UV, Bonhoeffer T (2006) Neuronal activity determines the protein synthesis dependence of long-term potentiation. Nat Neurosci 9:478–480CrossRefPubMedGoogle Scholar
  23. Glickman S (1961) Preservative neural processes and consolidation of the memory trace. Psychol Bull 58:218–233CrossRefPubMedGoogle Scholar
  24. Goelet P, Castellucci VF, Schacher S, Kandel ER (1986) The long and short of long-term memory—a molecular framework. Nature 322:419–422CrossRefPubMedGoogle Scholar
  25. Gordon WC (1977a) Similarities of recently acquired and reactivated memories in interference. Am J Psychol 90:231–242CrossRefGoogle Scholar
  26. Gordon WC (1977b) Susceptibility of a reactivated memory to the effects of strychnine: a time-dependent phenomenon. Physiol Behav 18:95–99CrossRefPubMedGoogle Scholar
  27. Gordon WC, Spear NE (1973) Effect of reactivation of a previously acquired memory on the interaction between memories in the rat. J Exp Psychol 99:349–355CrossRefPubMedGoogle Scholar
  28. Gruest N, Richer P, Hars B (2004) Memory consolidation and reconsolidation in the rat pup require protein synthesis. J Neurosci 24:10488–10492CrossRefPubMedGoogle Scholar
  29. Hernandez PJ, Kelley AE (2004) Long-term memory for instrumental responses does not undergo protein synthesis-dependent reconsolidation upon retrieval. Learn Mem 11:748–754Google Scholar
  30. Hong I, Kim J, Lee S, Ko HG, Nader K, Kaang BK, Tsien RW, Choi S (2013) AMPA receptor exchange underlies transient memory destabilization on retrieval. Proc Natl Acad Sci U S A 110:8218–8223CrossRefPubMedPubMedCentralGoogle Scholar
  31. Horne CA, Rodriguez WA, Wright TP, Padilla JL (1997) Time-dependent effects of fructose on the modulation of a reactivated memory. Prog Neuropsychopharmacol Biol Psychiatry 21:649–658CrossRefPubMedGoogle Scholar
  32. Hupbach A, Gomez R, Hardt O, Nadel L (2007) Reconsolidation of episodic memories: a subtle reminder triggers integration of new information. Learn Mem 14(1–2):47–53CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038CrossRefPubMedGoogle Scholar
  34. Kelly A, Laroche S, Davis S (2003) Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J Neurosci 23:5354–5360PubMedGoogle Scholar
  35. Kida S, Josselyn SA, de Ortiz SP, Kogan JH, Chevere I, Masushige S, Silva AJ (2002) CREB required for the stability of new and reactivated fear memories. Nat Neurosci 5:348–355CrossRefPubMedGoogle Scholar
  36. Kindt M, Soeter M, Vervliet B (2009) Beyond extinction: erasing human fear responses and preventing the return of fear. Nat Neurosci 12:256–258CrossRefPubMedGoogle Scholar
  37. Kroes MC, Tendolkar I, van Wingen GA, van Waarde JA, Strange BA, Fernandez G (2014) An electroconvulsive therapy procedure impairs reconsolidation of episodic memories in humans. Nat Neurosci 17:204–206CrossRefPubMedGoogle Scholar
  38. Lee JL (2008) Memory reconsolidation mediates the strengthening of memories by additional learning. Nat Neurosci 11:1264–1266CrossRefPubMedGoogle Scholar
  39. Lee JL (2009) Reconsolidation: maintaining memory relevance. Trends Neurosci 32:413–420CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lee JL, Everitt BJ, Thomas KL (2004) Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 304:839–843CrossRefPubMedGoogle Scholar
  41. Lee JL, Di Ciano P, Thomas KL, Everitt BJ (2005) Disrupting reconsolidation of drug memories reduces cocaine-seeking behavior. Neuron 47:795–801CrossRefPubMedGoogle Scholar
  42. Lee SH, Choi JH, Lee N, Lee HR, Kim JI, Yu NK, Choi SL, Lee SH, Kim H, Kaang BK (2008) Synaptic protein degradation underlies destabilization of retrieved fear memory. Science 319:1253–1256CrossRefPubMedGoogle Scholar
  43. Lee SH, Kwak C, Shim J, Kim JE, Choi SL, Kim HF, Jang DJ, Lee JA, Lee K, Lee CH, Lee YD, Miniaci MC, Bailey CH, Kandel ER, Kaang BK (2012) A cellular model of memory reconsolidation involves reactivation-induced destabilization and restabilization at the sensorimotor synapse in Aplysia. Proc Natl Acad Sci U S A 109:14200–14205CrossRefPubMedPubMedCentralGoogle Scholar
  44. Lewis DJ (1979) Psychobiology of active and inactive memory. Psychol Bull 86:1054–1083CrossRefPubMedGoogle Scholar
  45. Li Y, Meloni EG, Carlezon WA Jr, Milad MR, Pitman RK, Nader K, Bolshakov VY (2013) Learning and reconsolidation implicate different synaptic mechanisms. Proc Natl Acad Sci U S A 110:4798–4803CrossRefPubMedPubMedCentralGoogle Scholar
  46. Malenka RC, Nicoll RA (1999) Long-term potentiation—a decade of progress? Science 285:1870–1874CrossRefPubMedGoogle Scholar
  47. Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897–931CrossRefPubMedGoogle Scholar
  48. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649–711CrossRefPubMedGoogle Scholar
  49. McGaugh JL (1966) Time-dependent processes in memory storage. Science 153:1351–1358CrossRefPubMedGoogle Scholar
  50. McGaugh JL (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1–28CrossRefPubMedGoogle Scholar
  51. McGaugh JL, Krivanek JA (1970) Strychnine effects on discrimination learning in mice: effects of dose and time of administration. Physiol Behav 5:1437–1442CrossRefPubMedGoogle Scholar
  52. Menzies RP (2012) Propranolol, traumatic memories, and amnesia: a study of 36 cases. J Clin Psychiatry 73:129–130CrossRefPubMedGoogle Scholar
  53. Milekic MH, Alberini CM (2002) Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36(3):521–525CrossRefPubMedGoogle Scholar
  54. Miller CA, Marshall JF (2005) Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory. Neuron 47:873–884CrossRefPubMedGoogle Scholar
  55. Miller RR, Springer AD (1973) Amnesia, consolidation, and retrieval. Psychol Rev 80:69–79CrossRefPubMedGoogle Scholar
  56. Milton AL, Lee JL, Butler VJ, Gardner R, Everitt BJ (2008) Intra-amygdala and systemic antagonism of NMDA receptors prevents the reconsolidation of drug-associated memory and impairs subsequently both novel and previously acquired drug-seeking behaviors. J Neurosci 28:8230–8237CrossRefPubMedGoogle Scholar
  57. Milton AL, Merlo E, Ratano P, Gregory BL, Dumbreck JK, Everitt BJ (2013) Double dissociation of the requirement for GluN2B- and GluN2A-containing NMDA receptors in the destabilization and restabilization of a reconsolidating memory. J Neurosci 33:1109–1115Google Scholar
  58. Misanin JR, Miller RR, Lewis DJ (1968) Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science 160:203–204CrossRefGoogle Scholar
  59. Morris RG, Inglis J, Ainge JA, Olverman HJ, Tulloch J, Dudai Y, Kelly PA (2006) Memory reconsolidation: sensitivity of spatial memory to inhibition of protein synthesis in dorsal hippocampus during encoding and retrieval. Neuron 50:479–489CrossRefPubMedGoogle Scholar
  60. Müller GE, Pilzecker A (1900) Experimentelle beitrage zur lehre vom gedachtnis. Z Psychol Suppl. no.1:1Google Scholar
  61. Nader K, Hardt O (2009) A single standard for memory: the case for reconsolidation. Nat Rev Neurosci 10:224–234CrossRefPubMedGoogle Scholar
  62. Nader K, Schafe GE, Le Doux JE (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406:722–726CrossRefPubMedGoogle Scholar
  63. Nader K, Hardt O, Wang SH (2005) Response to Alberini: right answer, wrong question. Trends Neurosci 28:346–347CrossRefPubMedGoogle Scholar
  64. Nader K, Hardt O, Lanius R (2013) Memory as a new therapeutic target. Dialogues Clin Neurosci 15:475–486PubMedPubMedCentralGoogle Scholar
  65. Pederia ME, Maldonado H (2003) Protein synthesis subserves reconsolidation or extinction depending on reminder duration. Neuron 38:863–869CrossRefGoogle Scholar
  66. Pedreira ME, Perez-Cuesta LM, Maldonado H (2002) Reactivation and reconsolidation of long-term memory in the crab Chasmagnathus: protein synthesis requirement and mediation by NMDA-type glutamatergic receptors. J Neurosci 22:8305–8311PubMedGoogle Scholar
  67. Pedreira ME, Perez-Cuesta LM, Maldonado H (2004) Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction. Learn Mem 11:579–585CrossRefPubMedPubMedCentralGoogle Scholar
  68. Przybyslawski J, Sara SJ (1997) Reconsolidation of memory after its reactivation. Behav Brain Res 84:241–246CrossRefPubMedGoogle Scholar
  69. Przybyslawski J, Roullet P, Sara SJ (1999) Attenuation of emotional and nonemotional memories after their reactivation: role of beta adrenergic receptors. J Neurosci 19:6623–6628PubMedGoogle Scholar
  70. Rodrigues SM, LeDoux JE, Sapolsky RM (2009) The influence of stress hormones on fear circuitry. Annu Rev Neurosci 32:289–313CrossRefPubMedGoogle Scholar
  71. Rodriguez WA, Rodriguez SB, Phillips MY, Martinez JL Jr (1993) Post-reactivation cocaine administration facilitates later acquisition of an avoidance response in rats. Behav Brain Res 59:125–129CrossRefPubMedGoogle Scholar
  72. Rodriguez WA, Horne CA, Padilla JL (1999) Effects of glucose and fructose on recently reactivated and recently acquired memories. Prog Neuro-Psychopharmacol Biol Psychiatry 23:1285–1317CrossRefGoogle Scholar
  73. Rose JK, Rankin CH (2006) Blocking memory reconsolidation reverses memory-associated changes in glutamate receptor expression. J Neurosci 26:11582–11587CrossRefPubMedGoogle Scholar
  74. Rubin RD (1976) Clinical use of retrograde amnesia produced by electroconvulsive shock: a conditioning hypothesis. Can Psychiatr Assoc J 21:87–90CrossRefPubMedGoogle Scholar
  75. Rubin RD, Fried R, Franks CM (1969) New application of ECT. In: Rubin RD, Franks C (eds) Advances in behavior therapy, 1968. Academic, New York, pp 37–44Google Scholar
  76. Rumpel S, LeDoux J, Zador A, Malinow R (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science 308:83–88CrossRefPubMedGoogle Scholar
  77. Saladin ME, Gray KM, McRae-Clark AL, Larowe SD, Yeatts SD, Baker NL, Hartwell KJ, Brady KT (2013) A double blind, placebo-controlled study of the effects of post-retrieval propranolol on reconsolidation of memory for craving and cue reactivity in cocaine dependent humans. Psychopharmacology (Berl) 226:721–737CrossRefGoogle Scholar
  78. Sangha S, Scheibenstock A, Lukowiak K (2003) Reconsolidation of a long-term memory in Lymnaea requires new protein and RNA synthesis and the soma of right pedal dorsal 1. J Neurosci 23:8034–8040PubMedGoogle Scholar
  79. Schafe GE, LeDoux JE (2000) Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J Neurosci 20:RC96PubMedGoogle Scholar
  80. Schafe GE, Nader K, Blair HT, LeDoux JE (2001) Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective. Trends Neurosci 24:540–546CrossRefPubMedGoogle Scholar
  81. Schiller D, Monfils MH, Raio CM, Johnson DC, Ledoux JE, Phelps EA (2010) Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 463:49–53CrossRefPubMedGoogle Scholar
  82. Spear N (1973) Retrieval of memory in animals. Psychol Rev 80:163–194CrossRefGoogle Scholar
  83. Stollhoff N, Menzel R, Eisenhardt D (2005) Spontaneous recovery from extinction depends on the reconsolidation of the acquisition memory in an appetitive learning paradigm in the honeybee (Apis mellifera). J Neurosci 25:4485–4492CrossRefPubMedGoogle Scholar
  84. Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, Kida S (2004) Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24:4787–4795CrossRefPubMedGoogle Scholar
  85. Suzuki A, Mukawa T, Tsukagoshi A, Frankland PW, Kida S (2008) Activation of LVGCCs and CB1 receptors required for destabilization of reactivated contextual fear memories. Learn Mem 15:426–433CrossRefPubMedPubMedCentralGoogle Scholar
  86. Taubenfeld SM, Milekic MH, Monti B, Alberini CM (2001) The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta. Nat Neurosci 4:813–818CrossRefPubMedGoogle Scholar
  87. Tronson NC, Wiseman SL, Olausson P, Taylor JR (2006) Bidirectional behavioral plasticity of memory reconsolidation depends on amygdalar protein kinase A. Nat Neurosci 9:167–169CrossRefPubMedGoogle Scholar
  88. Tsvetkov E, Carlezon WA, Benes FM, Kandel ER, Bolshakov VY (2002) Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 34:289–300CrossRefPubMedGoogle Scholar
  89. Valjent E, Aubier B, Corbille AG, Brami-Cherrier K, Caboche J, Topilko P, Girault JA, Herve D (2006) Plasticity-associated gene Krox24/Zif268 is required for long-lasting behavioral effects of cocaine. J Neurosci 26:4956–4960CrossRefPubMedGoogle Scholar
  90. von Hertzen LS, Giese KP (2005) Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J Neurosci 25:1935–1942CrossRefGoogle Scholar
  91. Walker MP, Brakefield T, Hobson JA, Stickgold R (2003) Dissociable stages of human memory consolidation and reconsolidation. Nature 425:616–620CrossRefPubMedGoogle Scholar
  92. Wang SH, Ostlund SB, Nader K, Balleine BW (2005) Consolidation and reconsolidation of incentive learning in the amygdala. J Neurosci 25:830–835CrossRefPubMedGoogle Scholar
  93. Wang SH, de Oliveira AL, Nader K (2009) Cellular and systems mechanisms of memory strength as a constraint on auditory fear reconsolidation. Nat Neurosci 12:905–912CrossRefPubMedGoogle Scholar
  94. Xue YX, Luo YX, Wu P, Shi HS, Xue LF, Chen C, Zhu WL, Ding ZB, Bao YP, Shi J, Epstein DH, Shaham Y, Lu L (2012) A memory retrieval-extinction procedure to prevent drug craving and relapse. Science 336:241–245CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Psychology DepartmentMcGill UniversityMontrealCanada

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