Memory reconsolidation and extinction have distinct temporal and biochemical signatures

Journal of Neuroscience

Volumn 24, Issue 20, 2004, Pages 4787-4795

  Suzuki, Akinobu ^a   Josselyn, Sheena A ^b,c   Frankland, Paul W ^b,c   Masushige, Shoichi ^a   Silva, Alcino J ^c   Kida, Satoshi ^a  

^a TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Consolidation; Extinction; Fear conditioning; Protein synthesis; Reconsolidation; Spatial memory

Indexed keywords

CALCIUM CHANNEL L TYPE; CANNABINOID 1 RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL;

AGE; ANIMAL EXPERIMENT; ARTICLE; CONDITIONING; CONTROLLED STUDY; FEAR; INFORMATION RETRIEVAL; MEMORY CONSOLIDATION; MOLECULAR DYNAMICS; MOUSE; NEUROBIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REINFORCEMENT; SPATIAL MEMORY; TEMPORAL LOBE;

ANIMALS; BEHAVIOR, ANIMAL; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CONDITIONING, CLASSICAL; EXCITATORY AMINO ACID ANTAGONISTS; EXTINCTION, PSYCHOLOGICAL; FEAR; MALE; MAZE LEARNING; MEMORY; MENTAL RECALL; MICE; MICE, INBRED C57BL; PIPERIDINES; PROTEIN SYNTHESIS INHIBITORS; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; TIME FACTORS;

EID: 2442699018     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5491-03.2004     Document Type: Article

References (65)

1. Abel T, Nguye PV, Barad M, Deuel TA, Kandel ER, Bourtchouladze R (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615-626.
2. Anagnostaras SG, Maren S, Fanselow MS (1999) Temporally graded retrograde amnesia of contextual fear after hippocampus damage in rat: within-subjects examination. J Neurosci 19:1106-1114.
3. Anagnostaras SG, Gale GD, Fanselow MS (2001) hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 11:8-17.
4. Anokhin KV, Tiunova AA, Rose SPR (2002) Reminder effects-reconsolidation or retrieval deficit? Pharmachological dissection with protein synthesis inhibitors following reminder for a passive-avoidance task in young chicks. Eur J Neurosci 15:1759-1765.
5. Bauer EP, Schafe GE, LeDoux JE (2002) NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J Neurosci 22:5239-5249.
6. Baum M (1988) Spontaneous recovery from the effects of flooding (exposure) in animals. Behav Res Ther 26:185-186.
7. Berman DE, Dudai Y (2001) Memory extinction, learning anew, and learning the new: dissociation in the molecular machinery of learning in cortex. Science 291:2417-2419.
8. Blanchard RJ, Blanchard DC (1969) Passive and active reactions to fear-eliciting stimuli. J Comp Physiol Psychol 68:129-135.
9. Bontempi B, Laurent-Demir C, Destrade C, Jaffard R (1999) Time-dependent reorganization of brain circuitry underlying long-term memory strage. Nature 400:671-675.
10. 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 79:59-68.
11. Bouton ME (1993) Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol Bull 114:80-99.
12. Cain C, Blouin A, Barad MG (2002) L-type voltage-gated calcium channels are required for extinction, but not for acquisition or expression, of conditioned fear in mice. J Neurosci 22:9113-9121.
13. Davis HP, Squire LR (1984) Protein synthesis and memory. Psychol Bull 96:518-559.
14. Debiec J, LeDoux JE, Nader K (2002) Cellular and systems reconsolidation in the hippocampus. Neuron 36:527-538.
15. Dudai Y (2002) Molecular bases of long-term memories: a question of persistence. Curr Opin Neurobiol 12:211-216.
16. Eichenbaum H, Otto T, Cohen NJ (1994) Two functional components of the hippocampal memory system. Behav Brain Sci 17:449-518.
17. Eisenberg M, Kobilo T, Berman DE, Dudai Y (2003) Stability of retrieved memory: inverse correlation with trace dominance. Science 301:1102-1104.
18. Fanselow MS (1980) Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci 15:177-182.
19. Flexner LB, Flexner JB, Stellar E (1965) Memory and cerebral protein synthesis in mice as affected by graded amounts of puromycin. Exp Neurol 13:264-272.
20. Flood JF, Rosenzweig MR, Bennett EL, Orme AE (1973) The influence of duration of protein synthesis inhibition on memory. Physiol Behav 10:555-562.
21. Frankland PW, O'Brien C, Ohno M, Kirkwood A, Silva AJ (2001) Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 411:309-313.
22. Judge ME, Quartermain D (1982) Alleviation of anisomycin-induced amnesia by pre-test treatment with lysine-vasopressin. Pharmacol Biochem Behav 16:463-466.
23. Kida S, Josselyn SA, deOrtiz SP, Kogan JH, Chevere I, Masushige S, Silva AJ (2002) CREB required for the stability of new and reactivated fear memories. Nat Neurosci 5:348-355.
24. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256:675-677.
25. Konorski J (1967) Some new ideas concerning the physiological mechanisms of perception. Acta Biol Exp (Warsz) 27:147-161.
26. Kraus M, Schicknick H, Wetzel W, Ohl F, Staak S, Tischmeyer W (2002) Memory consolidation for the discrimination of frequency-modulated tones in mongolian gerbils is sensitive to protein-synthesis inhibitors applied to the auditory cortex. Learn Mem 9:293-303.
27. Lattal KM, Abel T (2001) Different requirements for protein synthesis in acquisition and extinction of spatial preferences and context-evoked fear. J Neurosci 21:5773-5780.
28. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184.
29. Lewis DJ (1979) Psychobiology of active and inactive memory. Psychol Bull 86:1054-1083.
30. Mactutus CF, Riccio DC, Ferek JM (1979) Retrograde amnesia for old (reactivated) memory: some anomalous characteristics. Science 204:1319-1320.
31. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530-534.
32. McClelland JL, McNaughton BL, O'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.
33. McGaugh JL (1966) Time-dependent processes in memory storage. Science 153:1351-1358.
34. McGaugh JL (2000) Memory-a century of consolidation. Science 287:248-251.
35. Milekic MH, Alberini CM (2002) Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36:521-525.
36. Misanin JR, Miller RR, Lewis DJ (1968) Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science 160:554-555.
37. Morgan MA, LeDoux JE (1995) Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav Neurosci 109:681-688.
38. Morgan MA, LeDoux JE (1999) Contribution of ventrolateral prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Neurobiol Learn Mem 72:244-251.
39. Morgan MA, Romanski LM, LeDoux JE (1993) Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci Lett 163:109-113.
40. Morrow BA, Elsworth JD, Rasmusson AM, Roth RH (1999) The role of mesoprefrontal dopamine neurons in the acquisition and expression of conditioned fear in the rat. Neuroscience 92:553-564.
41. Myers KM, Davis M (2002) Behavioral and neural analysis of extinction. Neuron 36:567-584.
42. Nader K (2003) Memory traces unbound. Trends Neurosci 26:65-72.
43. Nader K, Schafe GE, Le Doux JE (2000a) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406:722-726.
44. Nader K, Schafe GE, Le Doux JE (2000b) The labile nature of consolidation theory. Nat Rev Neurosci 1:216-219.
45. Pavlov IP (1927) Conditioned reflexes. London: Oxford UP.
46. Pedreira ME, Maldonado H (2003) Protein synthesis subserves reconsolidation or extinction depending on reminder duration. Neuron 38:863-869.
47. 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 22:8305-8311.
48. Przybyslawski J, Sara SJ (1997) Reconsolidation of memory after its reactivation. Behav Brain Res 84:241-246.
49. Przybyslawski J, Roullet P, Sara SJ (1999) Attenuation of emotional and nonemotional memories after their reactivation: role of β adrenergic receptors. J Neurosci 19:6623-6628.
50. Quevedo J, Vianna MR, Roesler R, de-Paris F, Izquierdo I, Rose SP (1999) Two time windows of anisomycin-induced amnesia for inhibitory avoidance training in rats: protection from amnesia by pretraining but not pre-exposure to the task apparatus. Learn Mem 6:600-607.
51. Quirk GJ, Russo GK, Barron JL, Lebron K (2000) The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J Neurosci 20:6225-6231.
52. Rescorla RA (2001) Experimental extinction. In: Handbook of contemporary learning theories (Mowrer RR, Klein S, eds), pp 119-154. Mahwah, NJ: Erlbaum.
53. Rescorla RA, Heth CD (1975) Reinstatement of fear to an extinguished conditioned stimulus. J Exp Psychol Anim Behav Process 1:88-96.
54. Rinaldi-Carmona M, Barth F, Heaulme M, Shire D, Calandra B, Congy C, Martinez S, Maruani J, Neliat G, Caput D, Ferrara P, Soubrie P, Breliere JC, Le Fur G (1994) SR141716A, a potent and selective antagonist of the brain cannabinoid receptor. FEBS Lett 350:240-244.
55. Robbins SJ (1990) Mechanisms underlying spontaneous recovery in autoshaping. J Exp Psychol Anim Behav Process 16:235-249.
56. Sangha S, Scheibenstock A, Lukowiak K (2003a) Reconsolidation of a long-term memory in Lymnaea requires new protein and RNA synthesis and the soma of right pedal dorsal 1. J Neurosci 23:8034-8040.
57. Sangha S, Scheibenstock A, Morrow R, Lukowiak K (2003b) Extinction requires new RNA and protein synthesis and the soma of the cell right pedal dorsal 1 in Lymnaea stagnalis. J Neurosci 23:9842-9851.
58. Santini E, Muller RU, Quirk GJ (2001) Consolidation of extinction learning involves transfer from NMDA-independent to NMDA-dependent memory. J Neurosci 21:9009-9017.
59. Sara SJ (2000) Retrieval and reconsolidation: toward a neurobiology of remembering. Learn Mem 7:73-84.
60. Schafe GE, Nadel NV, Sullivan GM, Harris A, LeDoux JE (1999) Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP kinase. Learn Mem 6:97-110.
61. Schneider AM, Sherman W (1968) Amnesia: a function of the temporal relation of footshock to electroconvulsive shock. Science 159:219-221.
62. Squire LR, Alvarez P (1995) Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr Opin Neurobiol 5:169-177.
63. Taubenfeld SM, Milekic MH, Monti B, Alberini CM (2001) The consolidation of new but not reactivated memory requires hippocampal C/EBP-beta. Nat Neurosci 4:813-818.
64. Teich AH, McCabe PM, Gentile CC, Schneiderman LS, Winters RW, Liskowsky DR, Schneiderman N (1989) Auditory cortex lesions prevent the extinction of Pavlovian differential heart rate conditioning to tonal stimuli in rabbits. Brain Res 480:210-218.
65. Vianna MR, Szapiro G, McGaugh JL, Medina JH, Izquierdo I (2001) Retrieval of memory for fear-motivated training initiates extinction requiring protein synthesis in the rat hippocampus. Proc Natl Acad Sci USA 98:12251-12254.