Extinction and reacquisition of a fear-motivated memory require activity of the Src family of tyrosine kinases in the CA1 region of the hippocampus

Pharmacology Biochemistry and Behavior

Volumn 81, Issue 1, 2005, Pages 139-145

  Bevilaqua, Lia R M ^b   Da Silva, Weber N ^b   Medina, Jorge H ^b   Izquierdo, Iván ^b   Cammarota, Martín ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b NONE

Author keywords

CA1; Consolidation; Extinction; Hippocampus; Learning; Memory; PP2; PP3; Reacquisition; Reconsolidation; Src; Tyrosine kinase

Indexed keywords

4 AMINO 7 PHENYLPYRAZOL[3,4 D]PYRIMIDINE; 4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; DIMETHYL SULFOXIDE; PP 3; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; PYRIMIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; ENZYME ACTIVITY; FEAR; HIPPOCAMPUS; LEARNING; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; MENTAL TASK; MOTIVATION; NONHUMAN; PRIORITY JOURNAL; RAT; REACTION TIME; TASK PERFORMANCE;

ANIMALS; EXTINCTION, PSYCHOLOGICAL; FEAR; HIPPOCAMPUS; MALE; MEMORY; PYRIMIDINES; RATS; RATS, WISTAR; REACTION TIME; SRC-FAMILY KINASES;

ANIMALIA;

EID: 19344365980     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbb.2005.03.005     Document Type: Article

References (71)

1. D.W. Ali, and M.W. Salter NMDA receptor regulation by Src kinase signalling in excitatory synaptic transmission and plasticity Curr Opin Neurobiol 11 2001 336 342
2. K.V. Anokhin, A.A. Tiunova, and S.P. Rose 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 2002 1759 1765
3. D. Berman, and Y. Dudai Memory extinction, learning anew and learning the new: dissociations in the molecular machinery of learning in cortex Science 291 2001 2417 2419
4. L.R. Bevilaqua, J.I. Rossato, J.H. Medina, I. Izquierdo, and M. Cammarota Src kinase activity is required for avoidance memory formation and recall Behav Pharmacol 14 2003 649 652
5. L.R. Bevilaqua, D.S. Kerr, J.H. Medina, I. Izquierdo, and M. Cammarota Inhibition of hippocampal Jun N-terminal kinase enhances short-term memory but blocks long-term memory formation and retrieval of an inhibitory avoidance task Eur J Neurosci 17 2003 897 902
6. J.S. Bonini, L. Rodrigues, D.S. Kerr, L.R. Bevilaqua, M. Cammarota, and I. Izquierdo AMPA/kainate and group-I metabotropic receptor antagonists infused into different brain areas impair memory formation of inhibitory avoidance in rats Behav Pharmacol 14 2003 161 166
7. V.H. Brun, K. Ytterbo, R.G. Morris, M.B. Moser, and E.I. Moser Retrograde amnesia for spatial memory induced by NMDA receptor-mediated long-term potentiation J Neurosci 21 2001 356 362
8. M. Cammarota, L.R. Bevilaqua, P. Ardenghi, G. Paratcha, M. Levi de Stein, and I. Izquierdo Learning-associated activation of nuclear MAPK, CREB and Elk-1, along with Fos production, in the rat hippocampus after a one-trial avoidance learning: abolition by NMDA receptor blockade Mol Brain Res 76 2000 36 46
9. M. Cammarota, M.L. de Stein, G. Paratcha, L.R. Bevilaqua, I. Izquierdo, and J.H. Medina Rapid and transient learning-associated increase in NMDA NR1 subunit in the rat hippocampus Neurochem Res 25 2000 567 572
10. M. Cammarota, L.R. Bevilaqua, D. Kerr, J.H. Medina, and I. Izquierdo Inhibition of mRNA and protein synthesis in the CA1 region of the dorsal hippocampus blocks reinstallment of an extinguished conditioned fear response J Neurosci 23 2003 737 741
11. M. Cammarota, L.R. Bevilaqua, J.H. Medina, and I. Izquierdo Retrieval does not induce reconsolidation of inhibitory avoidance memory Learn Mem 11 2004 572 578
12. S.Y. Choi, J.J. Hwang, and J.Y. Koh NR2A induction and NMDA receptor-dependent neuronal death by neurotrophin-4/5 in cortical cell culture J Neurochem 88 2004 708 716
13. A.J. Crossthwaite, H. Valli, and R.J. Williams Inhibiting Src family tyrosine kinase activity blocks glutamate signalling to ERK1/2 and Akt/PKB but not JNK in cultured striatal neurones J Neurochem 88 2004 1127 1139
14. G. Daoudal, and D. Debanne Long-term plasticity of intrinsic excitability: learning rules and mechanisms Learn Mem 10 2003 456 465
15. M. Davis Role of NMDA receptors and MAP kinase in the amygdala in extinction of fear: clinical implications for exposure therapy Eur J Neurosci 16 2002 395 398
16. M. Davis, D.L. Walker, and KM. Myers Role of the amygdala in fear extinction measured with potentiated startle Ann N Y Acad Sci 985 2003 218 232
17. P. Derkinderen, M. Toutant, G. Kadare, C. Ledent, M. Parmentier, and J.A. Girault Dual role of Fyn in the regulation of FAK + 6,7 by cannabinoids in hippocampus J Biol Chem 276 2001 38289 38296
18. P. Derkinderen, E. Valjent, M. Toutant, J.C. Corvol, H. Enslen, and C. Ledent Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus J Neurosci 23 2003 2371 2382
19. W.K. Estes Statistical theory of spontaneous recovery and regression Psychol Rev 62 1955 145 154
20. W.A. Falls, M.J. Miserendino, and M. Davis Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala J Neurosci 12 1992 854 863
21. A. Fischer, F. Sananbenesi, C. Schrick, J. Spiess, and J. Radulovic Distinct roles of hippocampal de novo protein synthesis and actin rearrangement in extinction of contextual fear J Neurosci 24 2004 1962 1966
22. R. Gerlai Hippocampal LTP and memory in mouse strains: is there evidence for a causal relationship? Hippocampus 12 2002 657 666
23. S.G. Grant, T.J. O'Dell, K.A. Karl, P.L. Stein, P. Soriano, and E.R. Kandel Impaired long-term potentiation, spatial learning, and hippocampal development in Fyn mutant mice Science 258 1992 1903 1910
24. D. Grosshans, and M. Browning Protein kinase C activation induces tyrosine phosphorylation of the NR2A and NR2B subunits of the NMDA receptor J Neurochem 76 2001 737 744
25. J. Hanke, J. Gardner, R. Dow, P. Changelian, W. Brissette, and E. Weringer Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck and Fyn-dependent T cell activation J Biol Chem 271 1996 695 701
26. Y. Huang, W. Lu, D.W. Ali, K.A. Pelkey, G.M. Pitcher, and Y.M. Lu CAKbeta/Pyk2 kinase is a signaling link for induction of long-term potentiation in CA1 hippocampus Neuron 29 2001 485 496
27. H. Husi, and S.G. Grant Isolation of 2000-kDa complexes of N-methyl-D-aspartate receptor and postsynaptic density 95 from mouse brain J Neurochem 77 2001 281 291
28. I. Izquierdo, W. Wyrwicka, G. Sierra, and J.P. Segundo Etablissement de reflexes conditionne's de trace pendant le someil naturel chez le chat Actualite's Neurophysiologiques 6 1965 277 296
29. L.A. Izquierdo, D.M. Barros, J.H. Medina, and I. Izquierdo Novelty enhances retrieval of one-trial avoidance learning in rats 1 or 31 days after training unless the hippocampus is inactivated by different receptor antagonists and enzyme inhibitors Behav Brain Res 117 2000 215 220
30. I. Izquierdo, M. Cammarota, M.R. Vianna, and L.R. Bevilaqua The inhibition of acquired fear Neurotox Res 6 2004 175 188
31. S.A. Josselyn, S. Kida, and A.J. Silva Inducible repression of CREB function disrupts amygdala-dependent memory Neurobiol Learn Mem 82 2004 159 163
32. L.V. Kalia, and M.W. Salter Interactions between Src family protein tyrosine kinases and PSD-95 Neuropharmacology 45 2003 720 728
33. L.V. Kalia, J.R. Gingrich, and M.W. Salter Src in synaptic transmission and plasticity Oncogene 23 2004 8007 8016
34. Y. Kawasaki, T. Kohno, Z.Y. Zhuang, G.J. Brenner, H. Wang, and C. Van Der Meer Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization J Neurosci 24 2004 8310 8321
35. T.Y. Kim, J.J. Hwang, S.H. Yun, M.W. Jung, and J.Y. Koh Augmentation by zinc of NMDA receptor-mediated synaptic responses in CA1 of rat hippocampal slices: mediation by Src family tyrosine kinases Synapse 46 2002 49 56
36. G. Kohr, and P.H. Seeburg Subtype-specific regulation of recombinant NMDA receptor-channels by protein tyrosine kinases of the Src family J Physiol 492 1996 445 452
37. J. Konorski Conditioned reflexes and neuronal organization 1948 Cambridge UP London
38. K.M. Lattal, and T. Abel Different requirements for protein synthesis in acquisition and extinction of spatial preferences and context-evoked fear J Neurosci 21 2001 5773 5780
39. K.M. Lattal, S. Honarvar, and T. Abel Effects of post-session injections of anisomycin on the extinction of a spatial preference and on the acquisition of a spatial reversal preference Behav Brain Res 153 2004 327 339
40. C.H. Lin, S.H. Yeh, H.Y. Lu, and P.W. Gean The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory J Neurosci 23 2003 8310 8317
41. S. Lissek, and O. Gunturkun Dissociation of extinction and behavioral disinhibition: the role of NMDA receptors in the pigeon associative forebrain during extinction J Neurosci 23 2003 8119 8124
42. S. Lissek, B. Diekamp, and O. Gunturkun Impaired learning of a color reversal task after NMDA receptor blockade in the pigeon (Columba livia) associative forebrain (neostriatum caudolaterale) Behav Neurosci 116 2002 523 529
43. Y.M. Lu, J.C. Roder, J. Davidow, and M.W. Salter Src activation in the induction of long-term potentiation in CA1 hippocampal neurons Science 279 1998 1363 1367
44. K.T. Lu, D.L. Walker, and M. Davis Mitogen-activated protein kinase cascade in the basolateral nucleus of amygdala is involved in extinction of fear-potentiated startle J Neurosci 21 2001 RC162
45. M.A. Lynch Long-term potentiation and memory Physiol Rev 84 2004 87 136
46. S.J. Martin, P.D. Grimwood, and R.G. Morris Synaptic plasticity and memory: an evaluation of the hypothesis Annu Rev Neurosci 23 2000 649 711
47. M.R. Mehta Cooperative LTP can map memory sequences on dendritic branches Trends Neurosci 27 2004 69 72
48. K.M. Myers, and M. Davis Behavioral and neural analysis of extinction Neuron 36 2002 567 584
49. I.P. Pavlov Conditioned reflexes 1927 Oxford University Press Oxford UK
50. G. Paxinos, and C. Watson The rat brain in stereotaxic coordinates 1986 Academic Press San Diego
51. B. Perazzona, G. Isabel, T. Preat, and R.L. Davis The role of cAMP response element-binding protein in Drosophila long-term memory J Neurosci 24 2004 8823 8828
52. A.L. Purcell, and T.J. Carew Tyrosine kinases, synaptic plasticity and memory: insights from vertebrates and invertebrates Trends Neurosci 26 2003 625 630
53. R.A. Rescorla Aspects of the reinforcer learned in second-order Pavlovian conditioning J Exp Psychol, Anim Behav Processes 5 1979 79 95
54. R.A. Rescorla Retraining of extinguished Pavlovian stimuli J Exp Psychol, Anim Behav Processes 27 2001 115 124
55. R.A. Rescorla Spontaneous recovery Learn Mem 11 2004 501 509
56. M.J. Ribeiro, Z. Serfozo, A. Papp, I. Kemenes, M. O'Shea, and J.C. Yin Cyclic AMP response element-binding (CREB)-like proteins in a molluscan brain: cellular localization and learning-induced phosphorylation Eur J Neurosci 18 2003 1223 1234
57. R. Richardson, L. Ledgerwood, and J. Cranney Facilitation of fear extinction by d-cycloserine: theoretical and clinical implications Learn Mem 11 2004 510 516
58. J.A. Rostas, V.A. Brent, K. Voss, M.L. Errington, T.V. Bliss, and J.W. Gurd Enhanced tyrosine phosphorylation of the 2B subunit of the N-methyl-D-aspartate receptor in long-term potentiation Proc Natl Acad Sci U S A 93 1996 10452 10456
59. M.W. Salter Src, N-methyl-d-aspartate (NMDA) receptors, and synaptic plasticity Biochem Pharmacol 56 1998 789 798
60. P.P. Sanna, F. Berton, M. Cammalleri, M.K. Tallent, G.R. Siggins, and F.E. Bloom A role for Src kinase in spontaneous epileptiform activity in the CA3 region of the hippocampus Proc Natl Acad Sci U S A 97 2000 8653 8657
61. E. Santini, R.U. Muller, and G.J. Quirk Consolidation of extinction learning involves transfer from NMDA-independent to NMDA-dependent memory J Neurosci 21 2001 9009 9017
62. E. Santini, H. Ge, K. Ren, S. Pena de Ortiz, and G.J. Quirk Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex J Neurosci 24 2004 5704 5710
63. L.J. Shanley, A.J. Irving, and J. Harvey Leptin enhances NMDA receptor function and modulates hippocampal synaptic plasticity J Neurosci 21 2001 RC186
64. T. Suzuki, and K. Okumura-Noji NMDA receptor subunits epsilon 1 (NR2A) and epsilon 2 (NR2B) are substrates for Fyn in the postsynaptic density fraction isolated from the rat brain Biochem Biophys Res Commun 216 1995 582 588
65. G. Szapiro, M.R. Vianna, J.L. McGaugh, J.H. Medina, and I. Izquierdo The role of NMDA glutamate receptors, PKA, MAPK, and CaMKII in the hippocampus in extinction of conditioned fear Hippocampus 13 2003 53 58
66. M.R. Vianna, G. Szapiro, J.L. McGaugh, J.H. Medina, and I. Izquierdo Retrieval of memory for fear-motivated training initiates extinction requiring protein synthesis in the rat hippocampus Proc Natl Acad Sci U S A 98 2001 12251 12254
67. O.N. Walikonis, M. Jensen, D.W. Mann, J.A. Provance Jr, and M.B. Kennedy Identification of proteins in the postsynaptic density fraction by mass spectrometry J Neurosci 20 2000 4069 4080
68. D.L. Walker, and M. Davis The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction Pharmacol Biochem Behav 71 2002 379 392
69. Y.T. Wang, and M.W. Salter Regulation of NMDA receptors by tyrosine kinases and phosphatases Nature 369 1994 233 235
70. X. Wu, D. Zhu, X. Jiang, P. Okagaki, K. Mearow, and G. Zhu AMPA protects cultured neurons against glutamate excitotoxicity through a phosphatidylinositol 3-kinase-dependent activation in extracellular signal-regulated kinase to upregulate BDNF gene expression J Neurochem 90 2004 807 818
71. W. Zhao, S. Cavallaro, P. Gusev, and D.L. Alkon Nonreceptor tyrosine protein kinase pp60c-src in spatial learning: synapse-specific changes in its gene expression, tyrosine phosphorylation, and protein-protein interactions Proc Natl Acad Sci U S A 97 2000 8098 8103