A mismatch-based model for memory reconsolidation and extinction in attractor networks

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Osan, Remus ^a,b   Tort, Adriano B L ^c,d   Amaral, Olavo B ^e  

^a BOSTON UNIVERSITY   (United States)

^b USA   (United States)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

^d Edmond and Lily Safra International Institute of Neuroscience of Natal   (Brazil)

^e FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ARTIFICIAL NEURAL NETWORK; ASSOCIATION; BRAIN FUNCTION; HIPPOCAMPUS; LEARNING; MEDICAL RESEARCH; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; PROTEIN SYNTHESIS; REINFORCEMENT; SIMULATION; SYNAPSE; SYNAPTIC TRANSMISSION; HUMAN; MEMORY; THEORETICAL MODEL;

HUMANS; MEMORY; MODELS, THEORETICAL;

EID: 79961045218     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023113     Document Type: Article

References (94)

1. Misanin JR, Miller RR, Lewis DJ, (1968) Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science 160: 554-555.
2. Nader K, Hardt O, (2009) A single standard for memory: the case for reconsolidation. Nat Rev Neurosci 10: 224-234.
3. Milekic MH, Alberini CM, (2002) Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36: 521-525.
4. Nader K, Schafe GE, LeDoux JE, (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406: 722-726.
5. Berman DE, Dudai Y, (2001) Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex. Science 291: 2417-2419.
6. Vianna MRM, 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.
7. Eisenberg M, Kobilo T, Berman DE, Dudai Y, (2003) Stability of retrieved memory: inverse correlation with trace dominance. Science 301: 1102-1104.
8. Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, et al. (2004) Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24: 4787-4795.
9. Biedenkapp JC, Rudy JW, (2004) Context memories and reactivation: constraints on the reconsolidation hypothesis. Behav Neurosci 118: 956-964.
10. Cammarota M, Bevilaqua LR, Medina JH, Izquierdo I, (2004) Retrieval does not induce reconsolidation of inhibitory avoidance memory. Learn Mem 11: 572-578.
11. Dudai Y, (2006) Reconsolidation: the advantage of being refocused. Curr Opin Neurobiol 16: 174-178.
12. Tronson NC, Taylor JR, (2007) Molecular mechanisms of memory reconsolidation. Nat Rev Neurosci 8: 262-275.
13. Lee JLC, (2009) Reconsolidation: maintaining memory relevance. Trends Neurosci 32: 413-420.
14. 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: 579-585.
15. Morris RG, Inglis J, Ainge JA, Olverman HJ, Tulloch J, et al. (2006) Memory reconsolidation: sensitivity of spatial memory to inhibition of protein synthesis in dorsal hippocampus during encoding and retrieval. Neuron 50: 479-489.
16. Bustos SG, Maldonado H, Molina VA, (2009) Disruptive effect of midazolam on fear memory reconsolidation: decisive influence of reactivation time span and memory age. Neuropsychopharmacology 34: 446-457.
17. Brunet A, Orr SP, Tremblay J, Robertson K, Nader K, et al. (2008) Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder. J Psychiatr Res 42: 503-506.
18. Ressler KJ, Rothbaum BO, Tannenbaum L, Anderson P, Graap K, et al. (2004) Cognitive enhancers as adjuncts to psychotherapy: use of D-cycloserine in phobic individuals to facilitate extinction of fear. Arch Gen Psychiatry 61: 1136-1144.
19. 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.
20. Colgin LL, Leutgeb S, Jezek K, Leutgeb JK, Moser EI, et al. (2010) Attractor-map versus autoassociation based attractor dynamics in the hippocampal network. J Neurophysiol 104: 35-50.
21. Miyashita Y, Chang HS, (1988) Neuronal correlate of pictorial short-term memory in the primate temporal cortex. Nature 331: 68-70.
22. Niessing J, Friedrich RW, (2010) Olfactory pattern classification by discrete neuronal network states. Nature 465: 47-52.
23. Cohen M, Grossberg S, (1983) Absolute stability of global pattern-formation and parallel memory storage by competitive neural networks. IEEE Trans Syst Man Cybern 13: 815-826.
24. Hopfield JJ, (1982) Neural networks and physical systems with emergent collective computational abilities. Proc Natl Acad Sci USA 79: 2554-2558.
25. Rolls ET, (2007) An attractor network in the hippocampus: Theory and neurophysiology. Learn Mem 14: 714-731.
26. Tsodyks M, (1999) Attractor neural network models of spatial maps in hippocampus. Hippocampus 9: 481-489.
27. Anishchenko A, Treves A, (2006) Autoassociative memory retrieval and spontaneous activity bumps in small-world networks of integrate-and-fire neurons. J Physiol Paris 100: 225-236.
28. Bush D, Philippides A, Husbands P, O'Shea M, (2010) Dual coding with STDP in a spiking recurrent neural network model of the hippocampus. PLoS Comput Biol 6: e1000839.
29. Blumenfeld B, Preminger S, Sagi D, Tsodyks M, (2006) Dynamics of memory representations in networks with novelty-facilitated synaptic plasticity. Neuron 52: 383-394.
30. Amaral OB, Osan R, Roesler R, Tort ABL, (2008) A synaptic reinforcement-based model for transient amnesia following disruptions of memory consolidation and reconsolidation. Hippocampus 18: 584-601.
31. Wittenberg GM, Sullivan MR, Tsien JZ, (2002) Synaptic reentry reinforcement based network model for long-term memory consolidation. Hippocampus 12: 637-647.
32. Tronson NC, Schrick C, Guzman YF, Huh KH, Srivastava DP, et al. (2009) Segregated populations of hippocampal principal CA1 neurons mediating conditioning and extinction of contextual fear. J Neurosci 29: 3387-3394.
33. Herry C, Ciocchi S, Senn V, Demmou L, Muller C, et al. (2008) Switching on and off fear by distinct neuronal circuits. Nature 454: 600-606.
34. Eisenhardt D, Menzel R, (2007) Extinction learning, reconsolidation and the internal reinforcement hypothesis. Neurobiol Learn Mem 87: 167-173.
35. Lee JLC, (2008) Memory reconsolidation mediates the strengthening of memories by additional learning. Nat Neurosci 11: 1264-1266.
36. Lee SH, Choi JH, Lee N, Lee HR, Kim JI, et al. (2008) Synaptic protein degradation underlies destabilization of retrieved fear memory. Science 319: 1253-1256.
37. Hernandez PJ, Abel T, (2008) The role of protein synthesis in memory consolidation: progress amid decades of debate. Neurobiol Learn Mem 89: 293-311.
38. Treves A, Rolls ET, (1991) What determines the capacity of autoassociative memories in the brain? Network 2: 371-397.
39. Golomb D, Rubin N, Sompolinsky H, (1990) Willshaw model: associate memory with sparse coding and low fire rates. Phys Rev A 41: 1843-1854.
40. Schafe GE, Nadel NV, Sullivan GM, Harris A, Le Doux JE, (1999) Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP kinase. Learn Mem 6: 97-110.
41. Lagasse F, Devaud J-M, Mery F, (2009) A switch from cycloheximide-resistant consolidated memory to cycloheximide-sensitive reconsolidation and extinction in Drosophila. J Neurosci 29: 2225-2230.
42. Lee JLC, Milton AL, Everitt BJ, (2006) Reconsolidation and extinction of conditioned fear: inhibition and potentiation. J Neurosci 26: 10051-10056.
43. Doyère V, Debiec J, Monfils MH, Schafe G, LeDoux JE, (2007) Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala. Nat Neurosci 10: 414-416.
44. Wang SH, de Oliveira Alvares L, Nader K, (2009) Cellular and systems mechanisms of memory strength as a constraint on auditory fear reconsolidation. Nat Neurosci 12: 905-912.
45. Zhang XL, Sullivan JA, Moskal JR, Stanton PK, (2008) A NMDA receptor glycine site partial agonist, GLYX-13, simultaneously enhances LTP and reduces LTD at Schaffer collateral-CA1 synapses in hippocampus. Neuropharmacology 55: 1238-1250.
46. Tronson NC, Wiseman SL, Olausson P, Taylor JR, (2006) Bidirectional behavioral plasticity of memory reconsolidation depends on amygdalar protein kinase A. Nat Neurosci 9: 167-169.
47. Artinian J, McGauran AT, De Jaeger X, Mouledous L, Frances B, et al. (2008) Protein degradation, as with protein synthesis, is required during not only long-term spatial memory consolidation but also reconsolidation. Eur J Neurosci 27: 3009-3019.
48. Lopez-Salon M, Alonso M, Vianna MRM, Viola H, Mello e Souza T, et al. (2001) The ubiquitin-proteasome cascade is required for mammalian long-term memory formation. Eur J Neurosci 14: 1820-1826.
49. Merlo E, Romano A, (2007) Long-term memory consolidation depends on proteasome activity in the crab Chasmagnathus. Neuroscience 147: 46-52.
50. Rossato JI, Bevilaqua LR, Medina JH, Izquierdo I, Cammarota M, (2006) Retrieval induces hippocampal-dependent reconsolidation of spatial memory. Learn Mem 13: 431-440.
51. Rossato JI, Bevilaqua LR, Myskiw JC, Medina JH, Izquierdo I, et al. (2007) On the role of hippocampal protein synthesis in the consolidation and reconsolidation of object recognition memory. Learn Mem 14: 36-46.
52. Hupbach A, Hardt O, Gomez R, Nadel L, (2008) The dynamics of memory: Context-dependent updating. Learn Mem 15: 574-579.
53. Lopez J, Vasconcelos AP, Cassel JC, (2008) Differential sensitivity of recent vs. remote memory traces to extinction in a water-maze task in rats. Neurobiol Learn Mem 90: 460-466.
54. Lattal KM, Abel T, (2004) Behavioral impairments caused by injections of the protein synthesis inhibitor anisomycin after contextual retrieval reverse with time. Proc Natl Acad Sci USA 101: 4667-4672.
55. Amaral OB, Luft T, Cammarota M, Izquierdo I, Roesler R, (2007) Temporary inactivation of the dorsal hippocampus induces a transient impairment in retrieval of aversive memory. Behav Brain Res 180: 113-118.
56. 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.
57. Przybyslawski J, Sara SJ, (1997) Reconsolidation of memory after its reactivation. Behav Brain Res 84: 241-246.
58. Mamou CB, Gamache K, Nader K, (2006) NMDA receptors are critical for unleashing consolidated auditory fear memories. Nat Neurosci 9: 1237-1239.
59. Colledge M, Snyder EM, Crozier RA, Soderling JA, Jin Y, et al. (2003) Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression. Neuron 40: 595-607.
60. Kauderer BS, Kandel ER, (2000) Capture of a protein synthesis-dependent component of long-term depression. Proc Natl Acad Sci USA 97: 13342-13347.
61. Naie K, Manahan-Vaughan D, (2005) Investigations of the protein synthesis dependency of mGluR-induced long-term depression in the dentate gyrus of freely moving rats. Neuropharmacology 49: 35-44.
62. Zhang L, Meng K, Li YH, Han TZ, (2009) NR2A-containing NMDA receptors are required for L-LTP induction and depotentiation in CA1 region of hippocampal slices. Eur J Neurosci 29: 2137-2144.
63. Wagner JJ, Alger BE, (1996) Homosynaptic LTD and depotentiation: Do they differ in name only? Hippocampus 6: 24-29.
64. Bi GQ, Poo MM, (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18: 10464-10472.
65. Markram H, Lubke J, Frotscher M, Sakmann B, (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275: 213-215.
66. Izhikevich EM, Desai NS, (2003) Relating STDP to BCM. Neural Comput 15: 1511-1523.
67. Gilson M, Burkitt A, van Hemmen LJ, (2010) STDP in recurrent neuronal networks. Front Comput Neurosci 4: 12.
68. McNaughton BL, Morris RGM, (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10: 408-415.
69. Marr D, (1971) Simple memory: a theory for archicortex. Philos Trans R Soc Lond B 262: 23-81.
70. Gold AE, Kesner RP, (2005) The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat. Hippocampus 15: 808-814.
71. McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, et al. (2007) Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317: 94-99.
72. Nakazawa K, Quirk MC, Chitwood RA, Watanabe M, Yeckel MF, et al. (2002) Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297: 211-218.
73. Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI, (2004) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305: 1295-1298.
74. Kesner RP, (2007) A behavioral analysis of dentate gyrus function. Prog Brain Res 163: 567-576.
75. Amit DJ, Brunel N, (1997) Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. Cereb Cortex 7: 237-252.
76. Johnson LR, Hou M, Ponce-Alvarez A, Gribelyuk L, Alphs H, et al. (2008) A recurrent network in the lateral amygdala: a mechanism for coincidence detection. Front Neural Circuits 2: 3.
77. Mamiya N, Fukushima H, Suzuki A, Matsuyama Z, Homma S, et al. (2009) Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J Neurosci 29: 402-413.
78. Rolls ET, Stringer SM, (2001) A model of the interaction between mood and memory. Network 12: 89-109.
79. Pedreira ME, Maldonado H, (2003) Protein synthesis subserves reconsolidation or extinction depending on reminder duration. Neuron 38: 863-869.
80. Hasselmo ME, Wyble BP, (1997) Free recall and recognition in a network model of the hippocampus: simulating effects of scopolamine on human memory function. Behav Brain Res 89: 1-34.
81. Lisman JE, Grace AA, (2005) The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46: 703-713.
82. Clarke JR, Cammarota M, Gruart A, Izquierdo I, Delgado-García JM, (2010) Plastic modifications induced by object recognition memory processing. Proc Natl Acad Sci USA 107: 2652-2657.
83. Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, et al. (2005) Progressive transformation of hippocampal neuronal representations in "morphed" environments. Neuron 48: 345-358.
84. Moita MAP, Rosis S, Zhou Y, LeDoux JE, Blair HT, (2004) Putting fear in its place: remapping of hippocampal place cells during fear conditioning. J Neurosci 24: 7015-7023.
85. Rossato JI, Bevilaqua LR, Izquierdo I, Medina JH, Cammarota M, (2010) Retrieval induces reconsolidation of fear extinction memory. Proc Natl Acad Sci USA 107: 1017-1020.
86. de Oliveira Alvares L, Pasqualini Genro B, Diehl F, Molina VA, Quillfeldt JA, (2008) Opposite action of hippocampal CB1 receptors in memory reconsolidation and extinction. Neuroscience 154: 1648-1655.
87. Merlo E, Romano A, (2008) Memory extinction entails the inhibition of the transcription factor NF-kappaB. PLoS ONE 3: e3687.
88. Yamada D, Zushida K, Wada K, Sekiguchi M, (2009) Pharmacological discrimination of extinction and reconsolidation of contextual fear memory by a potentiator of AMPA receptors. Neuropsychopharmacology 34: 2574-2584.
89. Tsodyks MV, Feigel'man MV, (1988) The enhanced storage capacity in neural networks with low activity level. Europhys Lett 6: 101-105.
90. Wilson RC, (2009) Parallel Hopfield networks. Neural Comput 21: 831-850.
91. Osan R, Zhu L, Shoham S, Tsien JZ, (2007) Subspace projection approaches to classification and visualization of neural network-level encoding patterns. PLoS ONE 2: e404.
92. Rolls ET, Treves A, Foster D, Perez-Vicente C, (1997) Simulation studies of the CA3 hippocampal subfield modelled as an attractor network. Neural Netw 9: 1559-1569.
93. Simmen MW, Treves A, Rolls ET, (1996) Pattern retrieval in threshold-linear associative nets. Network 7: 109-122.
94. Urcelay GP, Wheeler DS, Miller RR, (2009) Spacing extinction trials alleviates renewal and spontaneous recovery. Learn Behav 37: 60-73.