Advertisement

Memory Reconsolidation

  • Josue Haubrich
  • Karim Nader
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 37)

Abstract

Scientific advances in the last decades uncovered that memory is not a stable, fixed entity. Apparently stable memories may become transiently labile and susceptible to modifications when retrieved due to the process of reconsolidation. Here, we review the initial evidence and the logic on which reconsolidation theory is based, the wide range of conditions in which it has been reported and recent findings further revealing the fascinating nature of this process. Special focus is given to conceptual issues of when and why reconsolidation happen and its possible outcomes. Last, we discuss the potential clinical implications of memory modifications by reconsolidation.

Keywords

Memory Consolidation Reconsolidation Retrieval Storage Forgetting PTSD Drug addiction 

References

  1. Ahmadian G, Ju W, Liu L, Wyszynski M, Lee SH, Dunah AW et al (2004) Tyrosine phosphorylation of GluR2 is required for insulin-stimulated AMPA receptor endocytosis and LTD. EMBO J 23:1040–1050PubMedPubMedCentralCrossRefGoogle Scholar
  2. Alberini CM (2011) The role of reconsolidation and the dynamic process of long-term memory formation and storage. Front Behav Neurosci 5:12Google Scholar
  3. 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 15:1759–1765PubMedCrossRefGoogle Scholar
  4. Arguello AA, Ye X, Bozdagi O, Pollonini G, Tronel S, Bambah-Mukku D, et al (2013) CCAAT enhancer binding protein delta plays an essential role in memory consolidation and reconsolidation. J Neurosci 33:3646–3658Google Scholar
  5. Auber A, Tedesco V, Jones CE, Monfils MH, Chiamulera C (2013) Post-retrieval extinction as reconsolidation interference: methodological issues or boundary conditions? Psychopharmacology 226:631–647PubMedPubMedCentralCrossRefGoogle Scholar
  6. Barak S, Liu F, Hamida S Ben, Yowell Q V, Neasta J, Kharazia V, et al (2013) Disruption of alcohol-related memories by mTORC1 inhibition prevents relapse. Nat Neurosci 16:1111–1117PubMedPubMedCentralCrossRefGoogle Scholar
  7. Baratti CM, Boccia MM, Blake MG, Acosta GB (2008) Reactivated memory of an inhibitory avoidance response in mice is sensitive to a nitric oxide synthase inhibitor. Neurobiol Learn Mem 89:426–440PubMedCrossRefGoogle Scholar
  8. Barnes P, Kirtley A, Thomas KL (2012) Quantitatively and qualitatively different cellular processes are engaged in CA1 during the consolidation and reconsolidation of contextual fear memory. Hippocampus 22:149–171PubMedCrossRefGoogle Scholar
  9. Bergstrom HC, McDonald CG, Dey S, Fernandez GM, Johnson LR (2013) Neurons activated during fear memory consolidation and reconsolidation are mapped to a common and new topography in the lateral amygdala. Brain Topogr 26:468–478PubMedCrossRefGoogle Scholar
  10. Besnard A (2012) A model of hippocampal competition between new learning and memory updating. J Neurosci 32:3281–3283PubMedCrossRefGoogle Scholar
  11. Besnard A, Caboche J, Laroche S (2012) Reconsolidation of memory: a decade of debate. Prog Neurobiol 99:61–80PubMedCrossRefGoogle Scholar
  12. Bjorkstrand J, Agren T, Frick A, Engman J, Larsson EM, Furmark T, et al (2015) Disruption of Memory Reconsolidation Erases a Fear Memory Trace in the Human Amygdala: An 18-Month Follow-Up. PLoS One 10:e0129393PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bliss TV, Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331–356PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ (1994) Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:59–68PubMedCrossRefGoogle Scholar
  15. Bouton ME (2004) Context and behavioral processes in extinction. Learn Mem 11:485–494CrossRefGoogle Scholar
  16. Bouton ME, Winterbauer NE, Todd TP (2012) Relapse processes after the extinction of instrumental learning: renewal, resurgence, and reacquisition. Behav Process 90:130–141CrossRefGoogle Scholar
  17. Bozon B, Davis S, Laroche S (2003) A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40:695–701PubMedCrossRefGoogle Scholar
  18. Bredy TW, Barad M (2008) The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear. Learn Mem 15:39–45PubMedPubMedCentralCrossRefGoogle Scholar
  19. 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 42:503–506PubMedCrossRefGoogle Scholar
  20. Bustos SG, Maldonado H, Molina V a (2009) Disruptive effect of midazolam on fear memory reconsolidation: decisive influence of reactivation time span and memory age. Neuropsychopharmacology 34:446–457PubMedCrossRefGoogle Scholar
  21. Cai D, Pearce K, Chen S, Glanzman DL (2011) Protein kinase M maintains long-term sensitization and long-term facilitation in aplysia. J Neurosci 31:6421–6431PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cai D, Pearce K, Chen S, Glanzman DL (2012) Reconsolidation of long-term memory in Aplysia. Curr Biol 22:1783–1788PubMedPubMedCentralCrossRefGoogle Scholar
  23. Censor N, Dayan E, Cohen LG (2014) Cortico-subcortical neuronal circuitry associated with reconsolidation of human procedural memories. Cortex A J Devoted to Study Nerv Syst Behav 58:281–288PubMedCrossRefGoogle Scholar
  24. Chia C, Otto T (2013) Hippocampal Arc (Arg3.1) expression is induced by memory recall and required for memory reconsolidation in trace fear conditioning. Neurobiol Learn Mem 106:48–55PubMedCrossRefGoogle Scholar
  25. Child FM, Epstein HT, Kuzirian AM, Alkon DL (2003) Memory reconsolidation in Hermissenda. Biol Bull 205:218–219PubMedCrossRefGoogle Scholar
  26. Clem RL, Huganir RL (2010) Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science 330(6007):1108–1112 PubMedPubMedCentralCrossRefGoogle Scholar
  27. Chen S, Cai D, Pearce K, Sun PY, Roberts AC, Glanzman DL (2014) Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia. Elife 3:e03896Google Scholar
  28. Clarke JR, Cammarota M, Gruart A, Izquierdo I, Delgado-Garcia JM (2010) Plastic modifications induced by object recognition memory processing. Proc Natl Acad Sci USA 107:2652–2657CrossRefGoogle Scholar
  29. Contreras M, Billeke P, Vicencio S, Madrid C, Perdomo G, Gonzalez M, et al (2012) A role for the insular cortex in long-term memory for context-evoked drug craving in rats. Neuropsychopharmacology 37:2101–2108PubMedPubMedCentralCrossRefGoogle Scholar
  30. Dash PK, Hochner B, Kandel ER (1990) Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345:718–721PubMedCrossRefGoogle Scholar
  31. Davis S, Renaudineau S, Poirier R, Poucet B, Save E, Laroche S (2010) The formation and stability of recognition memory: What happens upon recall? Front Behav Neurosci 4:177Google Scholar
  32. De Oliveira Alvares L, Crestani AP, Cassini L, Haubrich J, Santana F, Quillfeldt JA (2013) Reactivation enables memory updating, precision-keeping and strengthening: exploring the possible biological roles of reconsolidation. Neuroscience: 1–7. doi: 10.1016/j.neuroscience.2013.04.005CrossRefPubMedGoogle Scholar
  33. Debiec J, LeDoux JE, Nader K (2002) Cellular and systems reconsolidation in the hippocampus. Neuron 36:527–538PubMedCrossRefGoogle Scholar
  34. Debiec J, Doyere V, Nader K, LeDoux JE, McEwen BS (2006) Directly reactivated, but not indirectly reactivated, memories undergo reconsolidation in the amygdala. PNAS Proc Natl Acad Sci USA 103:3428–3433CrossRefGoogle Scholar
  35. Descalzi G, Li X-Y, Chen T, Mercaldo V, Koga K, Zhuo M (2012) Rapid synaptic potentiation within the anterior cingulate cortex mediates trace fear learning. Mol Brain 5:6PubMedPubMedCentralCrossRefGoogle Scholar
  36. Diaz-Mataix L, Debiec J, LeDoux JE, Doyere V (2011) Sensory-specific associations stored in the lateral amygdala allow for selective alteration of fear memories. J Neurosci 31:9538–9543PubMedPubMedCentralCrossRefGoogle Scholar
  37. Diaz-Mataix L, Ruiz Martinez RC, Schafe GE, LeDoux JE, Doyere V (2013) Detection of a temporal error triggers reconsolidation of amygdala-dependent memories. Curr Biol 23:467–472PubMedPubMedCentralCrossRefGoogle Scholar
  38. Diekelmann S, Büchel C, Born J, Rasch B (2011) Labile or stable: opposing consequences for memory when reactivated during waking and sleep. Nat Neurosci 14:381–386PubMedCrossRefGoogle Scholar
  39. Diergaarde L, Schoffelmeer AN, Vries TJ De (2006) Beta-adrenoceptor mediated inhibition of long-term reward-related memory reconsolidation. Behav Brain Res 170:333–336Google Scholar
  40. Dong Z, Han H, Li H, Bai Y, Wang W, Tu M et al (2015) Long-term potentiation decay and memory loss are mediated by AMPAR endocytosis. J Clin Invest 125:234–247PubMedCrossRefGoogle Scholar
  41. Doyere V, Debiec J, Monfils MH, Schafe GE, LeDoux JE (2007) Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala. Nat Neurosci 10:414–416PubMedCrossRefGoogle Scholar
  42. Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51–86PubMedCrossRefGoogle Scholar
  43. Dudai Y (2009) Predicting not to predict too much: how the cellular machinery of memory anticipates the uncertain future. Philos Trans R Soc Lond Ser B Biol Sci 364:1255–1262CrossRefGoogle Scholar
  44. Dudai Y, Morris R (2000) To consolidate or not to consolidate: what are the questions? In: Bolhius J (ed) Brain, perception, memory: advances in cognitive sciences. Oxford University Press, Oxford, pp 149–162CrossRefGoogle Scholar
  45. Duncan CP (1949) The retroactive effect of electroshock on learning. J Comp Physiol Psychol 42:32–44PubMedCrossRefGoogle Scholar
  46. 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 21:283–289PubMedCrossRefGoogle Scholar
  47. Ebbinghaus M (1885) Über das Gedächtnis. Buehler, LeipzigGoogle Scholar
  48. Eisenberg M, Kobilo T, Berman DE, Dudai Y (2003) Stability of retrieved memory: inverse correlation with trace dominance. Science 301:1102–1104PubMedCrossRefGoogle Scholar
  49. Eisenberg M, Dudai Y (2004) Reconsolidation of fresh, remote, and extinguished fear memory in Medaka: old fears don’t die. Eur J Neurosci 20:3397–3403PubMedCrossRefGoogle Scholar
  50. Eysenck HJ (1968) A theory of the incubation of anxiety/fear responses. Behav Res Ther 6:309–321PubMedCrossRefGoogle Scholar
  51. Flavell CR, Barber DJ, Lee JLC (2011) Behavioural memory reconsolidation of food and fear memories. Nat Commun 2:504PubMedPubMedCentralCrossRefGoogle Scholar
  52. Flexner LB, Flexner JB, Stellar E (1965) Memory and cerebral protein synthesis in mice as affected by graded amounts of puromycin. Exp Neurol 13:264–272PubMedCrossRefGoogle Scholar
  53. Forcato C, Argibay PF, Pedreira ME, Maldonado H (2009) Human reconsolidation does not always occur when a memory is retrieved: the relevance of the reminder structure. Neurobiol Learn Mem 91:50–57PubMedCrossRefGoogle Scholar
  54. Forcato C, Rodríguez MLC, Pedreira ME, Maldonado H (2010) Reconsolidation in humans opens up declarative memory to the entrance of new information. Neurobiol Learn Mem 93:77–84PubMedCrossRefGoogle Scholar
  55. Forcato C, Fernandez RS, Pedreira ME (2014) Strengthening a consolidated memory: the key role of the reconsolidation process. J Physiol Paris 108:323–333PubMedCrossRefGoogle Scholar
  56. Forcato C, Rodríguez MLC, Pedreira ME (2011) Repeated labilization-reconsolidation processes strengthen declarative memory in humans. PLoS One 6:e23305PubMedPubMedCentralCrossRefGoogle Scholar
  57. Frankland PW, Ding H-KK, Takahashi E, Suzuki A, Kida S, Silva AJ (2006) Stability of recent and remote contextual fear memory. Learn Mem 13:451–457CrossRefGoogle Scholar
  58. Frankland PW, Köhler S, Josselyn SA (2013) Hippocampal neurogenesis and forgetting. Trends Neurosci 36:497–503PubMedCrossRefGoogle Scholar
  59. Frenkel L, Maldonado H, Delorenzi A (2005) Memory strengthening by a real-life episode during reconsolidation: an outcome of water deprivation via brain angiotensin II. Eur J Neurosci 22:1757–1766PubMedCrossRefGoogle Scholar
  60. Fukushima H, Zhang Y, Archbold G, Ishikawa R, Nader K, Kida S (2014) Enhancement of fear memory by retrieval through reconsolidation. Elife 2014:1–19Google Scholar
  61. Gabriel M (1968) Effects of intersession delay and training level on avoidance extinction and intertrial behavior. J Comp Physiol Psychol 66:412–416PubMedCrossRefGoogle Scholar
  62. Gahr M, Schonfeldt-Lecuona C, Spitzer M, Graf H (2014) Electroconvulsive therapy and posttraumatic stress disorder: first experience with conversation-based reactivation of traumatic memory contents and subsequent ECT-mediated impairment of reconsolidation. J Neuropsychiatry Clin Neurosci 26:E38–E39PubMedCrossRefGoogle Scholar
  63. García-DeLaTorre P, Rodriguez-Ortiz CJ, Arreguin-Martinez JL, Cruz-Castañeda P, Bermúdez-Rattoni F (2009) Simultaneous but not independent anisomycin infusions in insular cortex and amygdala hinder stabilization of taste memory when updated. Learn Mem 16:514–519CrossRefGoogle Scholar
  64. Glickman S (1961) Perseverative neural processes and consolidation of the memory trace. Psychol Bull 58:218–233PubMedCrossRefGoogle Scholar
  65. Gold PE, King RA (1974) Retrograde amnesia: storage failure versus retrieval failure. Physiol Rev 81:465–469Google Scholar
  66. Gordon WC (1977a) Similarities of recently acquired and reactivated memories in interference. Am J Psychol 90(2):231–242CrossRefGoogle Scholar
  67. Gordon WC (1977b) Susceptibility of a reactivated memory to the effects of strychnine: a time-dependent phenomenon. Physiol Behav 18(1):95–99PubMedCrossRefGoogle Scholar
  68. Gordon WC, Spear NE (1973) Effect of reactivation of a previously acquired memory on the interaction between memories in the rat. J Exp Psychol 99:349–355PubMedCrossRefGoogle Scholar
  69. Gräff J, Joseph NF, Horn ME, Samiei A, Meng J, Seo J et al (2014) Epigenetic priming of memory updating during reconsolidation to attenuate remote fear memories. Cell 156:261–276PubMedPubMedCentralCrossRefGoogle Scholar
  70. Grill-Spector K, Henson R, Martin A (2006) Repetition and the brain: Neural models of stimulus-specific effects. Trends Cogn Sci 10:14–23PubMedCrossRefGoogle Scholar
  71. Hall J, Thomas KL, Everitt BJ (2001a) Fear memory retrieval induces CREB phosphorylation and Fos expression within the amygdala. Eur J Neurosci 13:1453–1458PubMedCrossRefGoogle Scholar
  72. Hall J, Thomas KL, Everitt BJ (2001b) Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. J Neurosci 21:2186–2193Google Scholar
  73. Haubrich J, Crestani AP, Cassini LF, Santana F, Sierra RO, Alvares Lde O et al (2015) Reconsolidation allows fear memory to be updated to a less aversive level through the incorporation of appetitive information. Neuropsychopharmacology 40:315–326PubMedCrossRefGoogle Scholar
  74. Hebb DO (1949) The organization of behavior. Wiley, New York. doi: 10.2307/1418888CrossRefGoogle Scholar
  75. Hellemans KG, Everitt BJ, Lee JL (2006) Disrupting reconsolidation of conditioned withdrawal memories in the basolateral amygdala reduces suppression of heroin seeking in rats. J Neurosci 26:12694–12699PubMedCrossRefGoogle Scholar
  76. Hernandez PJ, Kelley AE (2004) Long-term memory for instrumental responses does not undergo protein synthesis-dependent reconsolidation upon retrieval. Learn Mem 11:748–754PubMedPubMedCentralCrossRefGoogle Scholar
  77. Hertzen LS von, Giese KP (2005) Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J Neurosci 25:1935–1942Google Scholar
  78. Hong I, Kim J, Kim J, Lee S, Ko H-G, Nader K et al (2013) AMPA receptor exchange underlies transient memory destabilization on retrieval. Proc Natl Acad Sci USA 110:8218–8223PubMedPubMedCentralCrossRefGoogle Scholar
  79. Hupbach A, Gomez R, Hardt O, Nadel L (2007) Reconsolidation of episodic memories: a subtle reminder triggers integration of new information. Learn Mem 14:47–53PubMedPubMedCentralCrossRefGoogle Scholar
  80. Hupbach A, Hardt O, Gomez R, Nadel L (2008) The dynamics of memory: Context-dependent updating. Learn Mem 15:574–579CrossRefGoogle Scholar
  81. Inda MC, Muravieva E V, Alberini CM (2011) Memory retrieval and the passage of time: from reconsolidation and strengthening to extinction. J Neurosci 31:1635–1643PubMedPubMedCentralCrossRefGoogle Scholar
  82. Jarome TJ, Kwapis JL, Werner CT, Parsons RG, Gafford GM, Helmstetter FJ (2012) The timing of multiple retrieval events can alter GluR1 phosphorylation and the requirement for protein synthesis in fear memory reconsolidation. Learn Mem 19:300–306CrossRefGoogle Scholar
  83. Jarome TJ, Ferrara NC, Kwapis JL, Helmstetter FJ (2015) Contextual Information Drives the Reconsolidation-Dependent Updating of Retrieved Fear Memories. Neuropsychopharmacology 40(13):3044–3052PubMedPubMedCentralCrossRefGoogle Scholar
  84. Jones B, Bukoski E, Nadel L, Fellous J-M (2012) Remaking memories: reconsolidation updates positively motivated spatial memory in rats. Learn Mem 19:91–98CrossRefGoogle Scholar
  85. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038CrossRefPubMedGoogle Scholar
  86. 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
  87. Kemenes G, Kemenes I, Michel M, Papp A, Muller U (2006) Phase-dependent molecular requirements for memory reconsolidation: differential roles for protein synthesis and protein kinase A activity. J Neurosci 26:6298–6302PubMedCrossRefGoogle Scholar
  88. Kida S, Josselyn SA, de Ortiz SP, Kogan JH, Chevere I, Masushige S et al (2002) CREB required for the stability of new and reactivated fear memories. Nat Neurosci 5:348–355PubMedCrossRefGoogle Scholar
  89. Kim J, Song B, Hong I, Kim J, Lee J, Park S, et al (2010) Reactivation of fear memory renders consolidated amygdala synapses labile. J Neurosci 30:9631–9640 PubMedCrossRefGoogle Scholar
  90. Kindt M, Soeter M, Vervliet B (2009) Beyond extinction: erasing human fear responses and preventing the return of fear. Nat Neurosci 12:256–258PubMedCrossRefGoogle Scholar
  91. Kroes MCW, Tendolkar I, van Wingen GA, van Waarde JA, Strange BA, Fernández G (2014) An electroconvulsive therapy procedure impairs reconsolidation of episodic memories in humans. Nat Neurosci 17:204–206PubMedCrossRefGoogle Scholar
  92. Kwapis JL, Jarome TJ, Lonergan ME, Helmstetter FJ (2009) Protein kinase Mzeta maintains fear memory in the amygdala but not in the hippocampus. Behav Neurosci 123:844–850PubMedPubMedCentralCrossRefGoogle Scholar
  93. Lagasse F, Devaud JM, Mery F (2009) A switch from cycloheximide-resistant consolidated memory to cycloheximide-sensitive reconsolidation and extinction in Drosophila. J Neurosci 29:2225–2230PubMedCrossRefGoogle Scholar
  94. Lee JLC (2008) Memory reconsolidation mediates the strengthening of memories by additional learning. Nat Neurosci 11:1264–1266PubMedCrossRefGoogle Scholar
  95. Lee JLC (2009) Reconsolidation: maintaining memory relevance. Trends Neurosci 32:413–420PubMedPubMedCentralCrossRefGoogle Scholar
  96. Lee JLC (2010) Memory reconsolidation mediates the updating of hippocampal memory content. Front Behav Neurosci 4:168Google Scholar
  97. Lee JLC, Everitt BJ, Thomas KL (2004) Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 304:839–843PubMedCrossRefGoogle Scholar
  98. Lee JL, Di Ciano P, Thomas KL, Everitt BJ (2005) Disrupting reconsolidation of drug memories reduces cocaine-seeking behavior. Neuron 47:795–801PubMedCrossRefGoogle Scholar
  99. Lee JLC, Milton AL, Everitt BJ (2006) Reconsolidation and extinction of conditioned fear: inhibition and potentiation. J Neurosci 26:10051–10056PubMedCrossRefGoogle Scholar
  100. Lee S, Kim J, Choi S (2011) In vitro synaptic reconsolidation in amygdala slices prepared from rat brains. Biochem Biophys Res Commun 407:339–342PubMedCrossRefGoogle Scholar
  101. Lee SH, Kwak C, Shim J, Kim JE, Choi SL, Kim HF et al (2012) A cellular model of memory reconsolidation involves reactivation-induced destabilization and restabilization at the sensorimotor synapse in Aplysia. Proc Natl Acad Sci USA 109:14200–14205PubMedPubMedCentralCrossRefGoogle Scholar
  102. Lewis DJ (1979) Psychobiology of active and inactive memory. Psychol Bull 86:1054–1083PubMedCrossRefGoogle Scholar
  103. Li Y, Meloni EG, Carlezon Jr. WA, Milad MR, Pitman RK, Nader K, et al (2013) Learning and reconsolidation implicate different synaptic mechanisms. Proc Natl Acad Sci USA 110:4798–4803CrossRefGoogle Scholar
  104. Litvin OO, Anokhin KV (2000) Mechanisms of memory reorganization during retrieval of acquired behavioral experience in chicks: the effects of protein synthesis inhibition in the brain. Neurosci Behav Physiol 30:671–678PubMedCrossRefGoogle Scholar
  105. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M et al (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304(5673):1021–1024PubMedCrossRefGoogle Scholar
  106. Lubin FD, Sweatt JD (2007) The IkappaB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron 55:942–957PubMedPubMedCentralCrossRefGoogle Scholar
  107. Lukowiak K, Fras M, Smyth K, Wong C, Hittel K (2007) Reconsolidation and memory infidelity in Lymnaea. Neurobiol Learn Mem 87:547–560PubMedCrossRefGoogle Scholar
  108. Maddox SA, Watts CS, Doyere V, Schafe GE (2013a) A naturally-occurring histone acetyltransferase inhibitor derived from Garcinia indica impairs newly acquired and reactivated fear memories. PLoS One 8:e54463Google Scholar
  109. Maddox SA, Watts CS, Schafe GE (2013b) p300/CBP histone acetyltransferase activity is required for newly acquired and reactivated fear memories in the lateral amygdala. Learn Mem 20:109–119CrossRefGoogle Scholar
  110. Maddox SA, Watts CS, Schafe GE (2014) DNA methyltransferase activity is required for memory-related neural plasticity in the lateral amygdala. Neurobiol Learn Mem 107:93–100PubMedCrossRefGoogle Scholar
  111. Mamiya N, Fukushima H, Suzuki A, Matsuyama Z, Homma S, Frankland PW, et al (2009) Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J Neurosci 29:402–413PubMedCrossRefGoogle Scholar
  112. Mamou CB, Gamache K, Nader K (2006) NMDA receptors are critical for unleashing consolidated auditory fear memories. Nat Neurosci 9:1237–1239PubMedCrossRefGoogle Scholar
  113. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649–711PubMedCrossRefGoogle Scholar
  114. McGaugh JL (1966) Time-dependent processes in memory storage. Science 153:1351–1358PubMedCrossRefGoogle Scholar
  115. McGaugh JL, Krivanek JA (1970) Strychnine effects on discrimination learning in mice: effects of dose and time of administration. Physiol Behav 5:1437–1442PubMedCrossRefGoogle Scholar
  116. Merlo E, Freudenthal R, Maldonado H, Romano A (2005) Activation of the transcription factor NF-kappaB by retrieval is required for long-term memory reconsolidation. Learn Mem 12:23–29Google Scholar
  117. Migues PV, Hardt O, Wu DC, Gamache K, Sacktor TC, Wang YT et al (2010) PKMzeta maintains memories by regulating GluR2-dependent AMPA receptor trafficking. Nat Neurosci 13:630–634PubMedCrossRefGoogle Scholar
  118. Migues PV, Liu L, Archbold GEB, Einarsson EO, Wong J, Bonasia K et al (2016) Blocking synaptic removal of GluA2-containing AMPA receptors prevents the natural forgetting of long-term memories. J Neurosci 36:3481–3494PubMedCrossRefGoogle Scholar
  119. Milekic MH, Alberini CM (2002) Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36:521–525PubMedCrossRefGoogle Scholar
  120. Miller RR, Marlin NA (1984) The physiology and semantics of consolidation: of mice and men. In: Weingartner H, Parker ES (eds) Memory consolidation: psychobiology of cognition. Erlbaum, Hillsdale, NJ, pp 85–109Google Scholar
  121. Miller CA, Marshall JF (2005) Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory. Neuron 47:873–884PubMedCrossRefGoogle Scholar
  122. Miller RR, Springer AD (1973) Amnesia, consolidation, and retrieval. Psychol Rev 80:69–79PubMedCrossRefGoogle Scholar
  123. Milton AL, Lee JLC, 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 28:8230–8237PubMedCrossRefGoogle Scholar
  124. 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 33:1109–1115PubMedPubMedCentralCrossRefGoogle Scholar
  125. Misanin JR, Miller RR, Lewis DJ (1968) Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science 160(3827):554–555PubMedCrossRefGoogle Scholar
  126. Monfils MH, Cowansage KK, Klann E, LeDoux JE (2009) Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 324(5929):951–955PubMedPubMedCentralCrossRefGoogle Scholar
  127. Morris RGM, Inglis J, Ainge J a, Olverman HJ, Tulloch J, Dudai Y, et al (2006) Memory reconsolidation: sensitivity of spatial memory to inhibition of protein synthesis in dorsal hippocampus during encoding and retrieval. Neuron 50:479–489PubMedCrossRefGoogle Scholar
  128. Müller GE, Pilzecker A (1900) Experimentelle Beitraege zur Lehre vom Gedaechtnis. Zeitschrift für Psychologie 1:1Google Scholar
  129. Nader K, Hardt O (2009) A single standard for memory: the case for reconsolidation. Nat Rev Neurosci 10:224–234PubMedCrossRefGoogle Scholar
  130. Nader K, Schafe GE, Le Doux JE (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406:722–726PubMedCrossRefGoogle Scholar
  131. Ogasawara H, Kawato M (2010) The protein kinase Mζ network as a bistable switch to store neuronal memory. BMC Syst Biol 4:181PubMedPubMedCentralCrossRefGoogle Scholar
  132. Olshavsky ME, Song BJ, Powell DJ, Jones CE, Monfils M-H, Lee HJ (2013) Updating appetitive memory during reconsolidation window: critical role of cue-directed behavior and amygdala central nucleus. Front Behav Neurosci 7, ArtID 186, 7Google Scholar
  133. Osan R, Tort AB, Amaral OB (2011) A mismatch-based model for memory reconsolidation and extinction in attractor networks. PLoS One 6:e23113PubMedPubMedCentralCrossRefGoogle Scholar
  134. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313:1141–1144PubMedCrossRefGoogle Scholar
  135. Pavlov IP (1927) Conditioned reflexes: An investigation of the physiological activity of the cerebral cortex. Book 17Google Scholar
  136. Pedreira ME, Maldonado H (2003) Protein synthesis subserves reconsolidation or extinction depending on reminder duration. Neuron 38:863–869PubMedCrossRefGoogle Scholar
  137. 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
  138. Pedreira ME, Pérez-Cuesta LM, Maldonado H (2004) Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction. Learn Mem 11:579–585CrossRefGoogle Scholar
  139. Perez-Cuesta LM, Maldonado H (2009) Memory reconsolidation and extinction in the crab: Mutual exclusion or coexistence? Learn Mem 16:714–721CrossRefGoogle Scholar
  140. Perrin G, Ferreira G, Meurisse M, Verdin S, Mouly A-M, Lévy F (2007) Social recognition memory requires protein synthesis after reactivation. Behav Neurosci 121:148–155PubMedCrossRefGoogle Scholar
  141. Pickens CL, Golden SA, Adams-Deutsch T, Nair SG, Shaham Y (2009) Long-lasting incubation of conditioned fear in rats. Biol Psychiatry 65:881–886PubMedPubMedCentralCrossRefGoogle Scholar
  142. Radiske A, Rossato JI, Kohler CA, Gonzalez MC, Medina JH, Cammarota M (2015) Requirement for BDNF in the reconsolidation of fear extinction. J Neurosci 35:6570–6574PubMedCrossRefGoogle Scholar
  143. Rao-Ruiz P, Rotaru DC, van der Loo RJ, Mansvelder HD, Stiedl O, Smit AB et al (2011) Retrieval-specific endocytosis of GluA2-AMPARs underlies adaptive reconsolidation of contextual fear. Nat Neurosci 14:1302–1308PubMedCrossRefGoogle Scholar
  144. Rehberg K, Bergado-Acosta JR, Koch JC, Stork O (2010) Disruption of fear memory consolidation and reconsolidation by actin filament arrest in the basolateral amygdala. Neurobiol Learn Mem 94:117–126PubMedCrossRefGoogle Scholar
  145. Ren ZY, Liu MM, Xue YX, Ding ZB, Xue LF, Zhai SD, et al (2013) A critical role for protein degradation in the nucleus accumbens core in cocaine reward memory. Neuropsychopharmacology 38:778–790PubMedCrossRefGoogle Scholar
  146. Rescorla RA,Wagner AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In Classical Conditioning II. Appleton-Century-Crofts, New York, pp 64–99Google Scholar
  147. Rescorla RA, Heth CD (1975) Reinstatement of fear to an extinguished conditioned stimulus. J Exp Psychol Anim Behav Process 1:88–96PubMedCrossRefGoogle Scholar
  148. Ribot T (1881) Les Maladies de la Memoire. Appleton-Century-Crofts, New YorkGoogle Scholar
  149. Robinson MJ, Franklin KB (2010) Reconsolidation of a morphine place preference: impact of the strength and age of memory on disruption by propranolol and midazolam. Behav Brain Res 213:201–207PubMedCrossRefGoogle Scholar
  150. Robinson MJF, Ross EC, Franklin KBJ (2011) The effect of propranolol dose and novelty of the reactivation procedure on the reconsolidation of a morphine place preference. Behav Brain Res 216:281–284PubMedCrossRefGoogle Scholar
  151. Rodriguez-Ortiz CJ, Bermudez-Rattoni F (2007) Memory Reconsolidation or Updating Consolidation? Neural Plast Mem From Genes to Brain Imaging at http://www.ncbi.nlm.nih.gov/pubmed/21204424
  152. Rodriguez-Ortiz CJ, la Cruz V De, Gutiérrez R, Bermudez-Rattoni F (2005) Protein synthesis underlies post-retrieval memory consolidation to a restricted degree only when updated information is obtained. Learn Mem 12:533–537CrossRefGoogle Scholar
  153. Rodriguez-Ortiz CJ, Garcia-DeLaTorre P, Benavidez E, Ballesteros MA, Bermudez-Rattoni F (2008) Intrahippocampal anisomycin infusions disrupt previously consolidated spatial memory only when memory is updated. Neurobiol Learn Mem 89:352–359PubMedCrossRefGoogle Scholar
  154. Romero-Granados R, Fontan-Lozano A, Delgado-Garcia JM, Carrion AM (2010) From learning to forgetting: behavioral, circuitry, and molecular properties define the different functional states of the recognition memory trace. Hippocampus 20:584–595CrossRefGoogle Scholar
  155. Rose JK, Rankin CH (2006) Blocking memory reconsolidation reverses memory-associated changes in glutamate receptor expression. J Neurosci 26:11582–11587PubMedCrossRefGoogle Scholar
  156. Sachser RM, Santana F, Crestani AP, Lunardi P, Pedraza LK, Quillfeldt JA et al (2016) Forgetting of long-term memory requires activation of NMDA receptors, L-type voltage-dependent Ca(2+) channels, and calcineurin. Sci Rep 6:22771PubMedPubMedCentralCrossRefGoogle Scholar
  157. Sacktor TC (2008) PKMzeta, LTP maintenance, and the dynamic molecular biology of memory storage. Prog Brain Res 169:27–40Google Scholar
  158. Sacktor TC (2011) How does PKMζ maintain long-term memory? Nat Rev Neurosci 12:9–15PubMedCrossRefGoogle Scholar
  159. Sacktor TC, Fenton AA (2012) Appropriate application of ZIP for PKMζ inhibition, LTP reversal, and memory erasure. Hippocampus 22:645–647PubMedCrossRefGoogle Scholar
  160. Sacktor TC, Osten P, Valsamis H, Jiang X, Naik MU, Sublette E (1993) Persistent activation of the zeta isoform of protein kinase C in the maintenance of long-term potentiation. Proc. Natl. Acad. Sci. USA 90:8342–8346CrossRefGoogle Scholar
  161. 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
  162. Sara SJ (2000) Retrieval and Reconsolidation: Toward a Neurobiology of Remembering. Learn Mem 7:73–84CrossRefGoogle Scholar
  163. Sartor GC, Aston-Jones G (2014) Post-retrieval extinction attenuates cocaine memories. Neuropsychopharmacology 39:1059–1065PubMedCrossRefGoogle Scholar
  164. Schiller D, Monfils M-H, Raio CM, Johnson DC, Ledoux JE, Phelps EA (2010) Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 463:49–53PubMedPubMedCentralCrossRefGoogle Scholar
  165. Schiller D, Kanen JW, LeDoux JE, Monfils M-H, Phelps EA (2013) Extinction during reconsolidation of threat memory diminishes prefrontal cortex involvement. PNAS Proc Natl Acad Sci United States Am 110:20040–20045CrossRefGoogle Scholar
  166. Schneider AM, Sherman W (1968) Amnesia: a function of the temporal relation of footshock to electroconvulsive shock. Science 159(3811):219–21PubMedCrossRefGoogle Scholar
  167. Schwabe L, Nader K, Wolf OT, Beaudry T, Pruessner JC (2012) Neural signature of reconsolidation impairments by propranolol in humans. Biol Psychiatry 71:380–386PubMedCrossRefGoogle Scholar
  168. Serrano P, Friedman EL, Kenney J, Taubenfeld SM, Zimmerman JM, Hanna J, et al (2008) PKMζ maintains spatial, instrumental, and classically conditioned long-term memories. PLoS Biol 6:2698–2706PubMedCentralCrossRefGoogle Scholar
  169. Shema R, Haramati S, Ron S, Hazvi S, Chen A, Sacktor TC et al (2011) Enhancement of consolidated long-term memory by overexpression of protein kinase Mzeta in the neocortex. Science 331:1207–1210PubMedCrossRefGoogle Scholar
  170. Sierra RO, Cassini LF, Santana F, Crestani AP, Duran JM, Haubrich J, et al (2013) Reconsolidation may incorporate state-dependency into previously consolidated memories. Learn Mem 20:379–87CrossRefGoogle Scholar
  171. Slaker M, Churchill L, Todd RP, Blacktop JM, Zuloaga DG, Raber J, et al (2015) Removal of perineuronal nets in the medial prefrontal cortex impairs the acquisition and reconsolidation of a cocaine-induced conditioned place preference memory. J Neurosci 35:4190–4202PubMedPubMedCentralCrossRefGoogle Scholar
  172. Soeter M, Kindt M (2015) An abrupt transformation of phobic behavior after a post-retrieval amnesic agent. Biol Psychiatry. doi: 10.1016/j.biopsych.2015.04.006CrossRefPubMedGoogle Scholar
  173. Spear NE (1973) Retrieval of memory in animals. Psychol Rev 80:163–194CrossRefGoogle Scholar
  174. Spear N, Mueller C (1984) Consolidation as a function of retrieval. In: Weingarten H, Parker E (eds) Memory consolidation: psychobiology of cognition. Erlbaum, London, pp 111–147Google Scholar
  175. Squire LR, Cohen NH, Nadel L (1984) The medial temporal region and memory consolidation: a new hypothesis. In: Weingartner H, Parker E (eds) Memory consolidation. Erlbaum, Hillsdale, NJ, pp 185–210Google Scholar
  176. Stern SA, Alberini CM (2013) Mechanisms of memory enhancement. Wiley Interdiscip Rev Syst Biol Med 5:37–53PubMedCrossRefGoogle Scholar
  177. 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 25:4485–4492PubMedCrossRefGoogle Scholar
  178. 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 24:4787–4795PubMedCrossRefGoogle Scholar
  179. Taubenfeld SM, Milekic MH, Monti B, Alberini CM (2001) The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta. Nat Neurosci 4:813–818PubMedPubMedCentralCrossRefGoogle Scholar
  180. Thomas KL, Arroyo M, Everitt BJ (2003) Induction of the learning and plasticity-associated gene Zif268 following exposure to a discrete cocaine-associated stimulus. Eur J Neurosci 17:1964–1972PubMedCrossRefGoogle Scholar
  181. Thomas KL, Hall J, Everitt BJ (2002) Cellular imaging with zif268 expression in the rat nucleus accumbens and frontal cortex further dissociates the neural pathways activated following the retrieval of contextual and cued fear memory. Eur J Neurosci 16:1789–1796PubMedCrossRefGoogle Scholar
  182. Tronel S, Sara SJ (2002) Mapping of olfactory memory circuits: Region-specific c-fos activation after odor-reward associative learning or after its retrieval. Learn Mem 9:105–111CrossRefGoogle Scholar
  183. Tronson NC, Taylor JR (2007) Molecular mechanisms of memory reconsolidation. Nat Rev Neurosci 8:262–275PubMedCrossRefGoogle Scholar
  184. Tronson NC, Wiseman SL, Olausson P, Taylor JR (2006) Bidirectional behavioral plasticity of memory reconsolidation depends on amygdalar protein kinase A. Nat Neurosci 9:167–169PubMedCrossRefGoogle Scholar
  185. Walker MP, Brakefield T, Hobson JA (2003) Dissociable stages of human memory consolidation and reconsolidation. Nature 425:8–12CrossRefGoogle Scholar
  186. Wang S-H, Morris RG (2010) Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu Rev Psychol 61:49–79PubMedCrossRefGoogle Scholar
  187. Wang SH, Ostlund SB, Nader K, Balleine BW (2005) Consolidation and reconsolidation of incentive learning in the amygdala. J Neurosci 25:830–835PubMedCrossRefGoogle Scholar
  188. Wang S-H, Oliveira Alvares L de, Nader K (2009) Cellular and systems mechanisms of memory strength as a constraint on auditory fear reconsolidation. Nat Neurosci 12: 905–912PubMedCrossRefGoogle Scholar
  189. Wang Y, Zhang TY, Xin J, Li T, Yu H, Li N, et al (2012) Differential involvement of brain-derived neurotrophic factor in reconsolidation and consolidation of conditioned taste aversion memory. PLoS One 7:e49942PubMedPubMedCentralCrossRefGoogle Scholar
  190. Wells AM, Arguello AA, Xie X, Blanton MA, Lasseter HC, Reittinger AM, et al (2013) Extracellular signal-regulated kinase in the basolateral amygdala, but not the nucleus accumbens core, is critical for context-response-cocaine memory reconsolidation in rats. Neuropsychopharmacology 38:753–762PubMedPubMedCentralCrossRefGoogle Scholar
  191. Wells AM, Xie X, Higginbotham JA, Arguello AA, Healey KL, Blanton M, Fuchs RA, et al (2015) Contribution of an SFK-Mediated Signaling Pathway in the Dorsal Hippocampus to Cocaine-Memory Reconsolidation in Rats. Neuropsychopharmacology 41(3):675–685PubMedPubMedCentralCrossRefGoogle Scholar
  192. Winters BD, Tucci MC, DaCosta-Furtado M (2009) Older and stronger object memories are selectively destabilized by reactivation in the presence of new information. Learn Mem 16: 545–553CrossRefGoogle Scholar
  193. Winters BD, Tucci MC, Jacklin DL, Reid JM, Newsome J, et al (2011) On the dynamic nature of the engram: evidence for circuit-level reorganization of object memory traces following reactivation. Neurosci 31:17719–28PubMedCrossRefGoogle Scholar
  194. Wirkner J, Low A, Hamm AO, Weymar M (2015) New learning following reactivation in the human brain: targeting emotional memories through rapid serial visual presentation. Neurobiol Learn Mem 119:63–68PubMedCrossRefGoogle Scholar
  195. Xue Y-X, Luo Y-X, Wu P, Shi H-S, Xue L-F, Chen C et al (2012) A memory retrieval-extinction procedure to prevent drug craving and relapse. Science 336:241–245PubMedPubMedCentralCrossRefGoogle Scholar
  196. Yin J C, Wallach J S, Del Vecchio M, Wilder E L, Zhou H, Quinn W G, Tully T (1994) Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79(1):49-58PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of PsychologyMcGill UniversityMontrealCanada
  2. 2.Federal University of Rio Grande do SulPorto AlegreBrazil

Personalised recommendations