Temporal requirement of C/EBP in the amygdala following reactivation but not acquisition of inhibitory avoidance

Learning and Memory

Volumn 14, Issue 7, 2007, Pages 504-511

  Milekic, Maria H ^a   Pollonini, Gabriella ^a   Alberini, Cristina M ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; INHIBITORY AVOIDANCE MEMORY; MALE; MEMORY; MEMORY CONSOLIDATION; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RAT; RECALL; TRAINING;

AMYGDALA; ANIMALS; ANISOMYCIN; AVOIDANCE LEARNING; CCAAT-ENHANCER-BINDING PROTEIN-BETA; ELECTROSHOCK; INHIBITION (PSYCHOLOGY); MALE; MEMORY; NUCLEIC ACID SYNTHESIS INHIBITORS; OLIGODEOXYRIBONUCLEOTIDES; RATS; RATS, LONG-EVANS; TIME FACTORS;

EID: 34547644831     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.598307     Document Type: Article

References (84)

1. Alberini, C.M. 1999. Genes to remember. J. Exp. Biol. 202: 2887-2891.
2. Alberini, C.M. 2005. Mechanisms of memory stabilization: Are consolidation and reconsolidation similar or distinct processes? Trends Neurosci. 28: 51-56.
3. Alberini, C.M. 2007. Reconsolidation: The Samsara of memory consolidation. Debates Neurosci. 1: 17-24.
4. Alberini, C.M., Ghirardi, M., Metz, R., and Kandel, E.R. 1994. C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76: 1099-1114.
5. Ambrogi-Lorenzini, C.G., Baldi, E., Bucherelli, C., Sacchetti, B., and Tassoni, G. 1996. Role of dorsal hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response: A tetrodotoxin functional inactivation study. Brain Res. 730: 32-39.
6. Ambrogi-Lorenzini, C.G., Baldi, E., Bucherelli, C., Sacchetti, B., and Tassoni, G. 1999. Neural topography and chronology of memory consolidation: A review of functional inactivation findings. Neurobiol. Learn. Mem. 71: 1-18.
7. Andersen, P. and Soleng, A.F. 1998. Long-term potentiation and spatial learning are both associated with the generation of new excitatory synapses. Brain Res. Brain Res. Rev. 26: 353-359.
8. Athos, J., Impey, S., Pineda, V.V., Chen, X., and Storm, D.R. 2002. Hippocampal CRE-mediated gene expression is required for contextual memory formation. Nat. Neurosci. 5: 1119-1120.
9. Bahar, A., Dorfman, N., and Dudai, Y. 2004. Amygdalar circuits required for either consolidation or extinction of taste aversion memory are not required for reconsolidation. Eur. J. Neurosci. 19: 1115-1118.
10. Bailey, C.H. and Kandel, E.R. 1993. Structural changes accompanying memory storage. Annu. Rev. Physiol. 55: 397-426.
11. Bailey, C.H., Bartsch, D., and Kandel, E.R. 1996. Toward a molecular definition of long-term memory storage. Proc. Natl. Acad. Sci. 93: 13445-13452.
12. Berman, D.E. and Dudai, Y. 2001. Memory extinction, learning a new, and learning the new: Dissociations in the molecular machinery of learning in cortex. Science 291: 2417-2419.
13. Berman, R.F., Kesner, R.P., and Partlow, L.M. 1978. Passive avoidance impairment in rats following cycloheximide injection into the amygdala. Brain Res. 158: 171-188.
14. Boccia, M.M., Blake, M.G., Acosta, G.B., and Baratti, C.M. 2006. Post-retrieval effects of icv infusions of hemicholinium in mice are dependent on the age of the original memory. Learn. Mem. 13: 376-381.
15. Bucherelli, C., Baldi, E., Mariottini, C., Passani, M.B., and Blandina, P. 2006. Aversive memory reactivation engages in the amygdala only some neurotransmitters involved in consolidation. Learn. Mem. 13: 426-430.
16. Carew, T.J. and Sutton, M.A. 2001. Molecular stepping stones in memory consolidation. Nat. Neurosci. 4: 769-771.
17. Davis, H.P. and Squire, L.R. 1984. Protein synthesis and memory: A review. Psychol. Bull. 96: 518-559.
18. Debiec, J. and LeDoux, J.E. 2004. Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 129: 267-272.
19. Debiec, J., LeDoux, J.E., and Nader, K. 2002. Cellular and systems reconsolidation in the hippocampus. Neuron 36: 527-538.
20. Dudai, Y. 2002. Molecular bases of long-term memories: A question of persistence. Curr. Opin. Neurobiol. 12: 211-216.
21. Dudai, Y. 2004. The neurobiology of consolidations, or, how stable is the engram? Annu. Rev. Psychol. 55: 51-86.
22. Dudai, Y. and Eisenberg, M. 2004. Rites of passage of the engram: Reconsolidation and the lingering consolidation hypothesis. Neuron 44: 93-100.
23. Duvarci, S. and Nader, K. 2004. Characterization of fear memory reconsolidation. J. Neurosci. 24: 9269-9275.
24. Eisenberg, M. and Dudai, Y. 2004. Reconsolidation of fresh, remote, and extinguished fear memory in Medaka: Old fears don't die. Eur. J. Neurosci. 20: 3397-3403.
25. Engert, F. and Bonhoeffer, T. 1999. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399: 66-70.
26. Frankland, P.W., Ding, H.K., Takahashi, E., Suzuki, A., Kida, S., and Silva, A.J. 2006. Stability of recent and remote contextual fear memory. Learn. Mem. 13: 451-457.
27. Gale, G.D., Anagnostaras, S.G., Godsil, B.P., Mitchell, S., Nozawa, T., Sage, J.R., Wiltgen, B., and Fanselow, M.S. 2004. Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. J. Neurosci. 24: 3810-3815.
28. Geinisman, Y., Berry, R.W., Disterhoft, J.F., Power, J.M., and Van der Zee, E.A. 2001. Associative learning elicits the formation of multiple-synapse boutons. J. Neurosci. 21: 5568-5573.
29. Guzowski, J.F. and McGaugh, J.L. 1997. Antisense oligodeoxynucleotide- mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc. Natl. Acad. Sci. 94: 2693-2698.
30. Guzowski, J.F., Lyford, G.L., Stevenson, G.D., Houston, F.P., McGaugh, J.L., Worley, P.F., and Barnes, C.A. 2000. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J. Neurosci. 20: 3993-4001.
31. Han, J.H., Kushner, S.A., Yiu, A.P., Cole, C.J., Matynia, A., Brown, R.A., Neve, R.L., Guzowski, J.F., Silva, A.J., and Josselyn, S.A. 2007. Neuronal competition and selection during memory formation. Science 316: 457-460.
32. Hellemans, K.G., Everitt, B.J., and Lee, J.L. 2006. Disrupting reconsolidation of conditioned withdrawal memories in the basolateral amygdala reduces suppression of heroin seeking in rats. J. Neurosci. 26: 12694-12699.
33. Hernandez, P.J., Sadeghian, K., and Kelley, A.E. 2002. Early consolidation of instrumental learning requires protein synthesis in the nucleus accumbens. Nat. Neurosci. 12: 1327-1331.
34. Hooper, M.L., Chiasson, B.J., and Robertson, H.A. 1994. Infusion into the brain of an antisense oligonucleotide to the immediate-early gene c-fos suppresses production of fos and produces a behavioral effect. Neuroscience 63: 917-924.
35. Izquierdo, I., Quillfeldt, J.A., Zanatta, M.S., Quevedo, J., Schaeffer, E., Schmitz, P.K., and Medina, J.H. 1997. Sequential role of hippocampus and amygdala, entorhinal cortex and parietal cortex in formation and retrieval of memory for inhibitory avoidance in rats. Eur. J. Neurosci. 9: 786-793.
36. Jasnow, A.M., Shi, C., Israel, J.E., Davis, M., and Huhman, K.L. 2005. Memory of social defeat is facilitated by cAMP response element-binding protein overexpression in the amygdala. Behav. Neurosci. 119: 1125-1130.
37. Josselyn, S.A., Shi, C., Carlezon Jr., W.A., Neve, R.L., Nestler, E.J., and Davis, M. 2001. Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J. Neurosci. 21: 2404-2412.
38. Josselyn, S.A., Kida, S., and Silva, A.J. 2004. Inducible repression of CREB function disrupts amygdala-dependent memory. Neurobiol. Learn. Mem. 82: 159-163.
39. Kandel, E.R. 2001. The molecular biology of memory storage: A dialogue between genes and synapses. Science 294: 1030-1038.
40. Kida, S., Josselyn, S.A., de Ortiz, S.P., Kogan, J.H., Chevere, I., Masushige, S., and Silva, A.J. 2002. CREB required for the stability of new and reactivated fear memories. Nat. Neurosci. 5: 348-355.
41. Koh, M.T. and Bernstein, I.L. 2003. Inhibition of protein kinase A activity during conditioned taste aversion retrieval: Interference with extinction or reconsolidation of a memory? Neuroreport 14: 405-407.
42. Lamprecht, R., Farb, C.R., and LeDoux, J.E. 2002. Fear memory formation involves p190 RhpGAP and ROCK proteins through a GRB2-mediated complex. Neuron 14: 727-738.
43. LeDoux, J.E. 2000. Emotion circuits in the brain. Annu. Rev. Neurosci. 23: 155-184.
44. Lee, J.A., Kim, H.K., Kim, K.H., Han, J.H., Lee, Y.S., Lim, C.S., Chang, D.J., Kubo, T., and Kaang, B.K. 2001. Overexpression of and RNA interference with the CCAAT enhancer-binding protein on long-term facilitation of Aplysia sensory to motor synapses. Learn. Mem. 8: 220-226.
45. Lee, J.L., Everitt, B.J., and Thomas, K.L. 2004. Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 304: 839-843.
46. Lee, J.L., Milton, A.L., and Everitt, B.J. 2006a. Cue-induced cocaine seeking and relapse are reduced by disruption of drug memory reconsolidation. J. Neurosci. 26: 5881-5887.
47. Lee, J.L., Milton, A.L., and Everitt, B.J. 2006b. Reconsolidation and extinction of conditioned fear: Inhibition and potentiation. J. Neurosci. 26: 10051-10056.
48. Liang, K.C., McGaugh, J.L., Martinez Jr., J.L., Jensen, R.A., Vasquez, B.J., and Messing, R.B. 1982. Post-training amygdaloid lesions impair retention of an inhibitory avoidance response. Behav. Brain Res. 4: 237-249.
49. Lin, H.C., Mao, S.C., and Gean, P.W. 2006. Effects of intra-amygdala infusion of CB1 receptor agonists on the reconsolidation of fear-potentiated startle. Learn. Mem. 13: 316-321.
50. Litvin, O.O. and Anokhin, K.V. 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: 671-678.
51. Maren, S., Aharonov, G., and Fanselow, M.S. 1996. Retrograde abolition of conditional fear after excitotoxic lesions in the basolateral amygdala of rats: Absence of a temporal gradient. Behav. Neurosci. 110: 718-726.
52. McGaugh, J.L. 2004. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27: 1-28.
53. Milekic, M.H. and Alberini, C.M. 2002. Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36: 521-525.
54. Milekic, M.H., Brown, S.D., Castellini, C., and Alberini, C.M. 2006. Persistent disruption of an established morphine conditioned place preference. J. Neurosci. 26: 3010-3020.
55. Munoz, C. and Grossman, S.P. 1981. Spatial discrimination, reversal and active or passive avoidance learning in rats with KA-induced neuronal depletions in dorsal hippocampus. Brain Res. Bull. 6: 399-406.
56. Nader, K., Schafe, G.E., and LeDoux, J.E. 2000a. The labile nature of consolidation theory. Nat. Rev. Neurosci. 1: 216-219.
57. Nader, K., Schafe, G.E., and Le Doux, J.E. 2000b. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406: 722-726.
58. O'Malley, A., O'Connell, C., and Regan, C.M. 1998. Ultrastructural analysis reveals avoidance conditioning to induce a transient increase in hippocampal dentate spine density in the 6 hour post-training period of consolidation. Neuroscience 87: 607-613.
59. O'Malley, A., O'Connell, C., Murphy, K.J., and Regan, C.M. 2000. Transient spine density increases in the mid-molecular layer of hippocampal dentate gyrus accompany consolidation of a spatial learning task in the rodent. Neuroscience 99: 229-232.
60. Pall, M., Hellberg, P., Brannstrom, M., Mikuni, M., Peterson, C.M., Sundfeldt, K., Norden, B., Hedin, L., and Enerback, S. 1997. The transcription factor C/EBP-β and its role in ovarian function; evidence for direct involvement in the ovulatory process. EMBO J. 16: 5273-5279.
61. Parent, M.B. and McGaugh, J.L. 1994. Posttraining infusion of lidocaine into the amygdala basolateral complex impairs retention of inhibitory avoidance training. Brain Res. 661: 97-103.
62. Perazzona, B., Isabel, G., Preat, T., and Davis, R.L. 2004. The role of cAMP response element-binding protein in Drosophila long-term memory. J. Neurosci. 24: 8823-8828.
63. Phillips, R.G. and LeDoux, J.E. 1995. Lesions of the fornix but not the entorhinal or perirhinal cortex interfere with contextual fear conditioning. J. Neurosci. 15: 5308-5315.
64. Salinska, E., Bourne, R.C., and Rose, S.P. 2004. Reminder effects: The molecular cascade following a reminder in young chicks does not recapitulate that following training on a passive avoidance task. Eur. J. Neurosci. 19: 3042-3047.
65. Sara, S.J. 2000. Retrieval and reconsolidation: Toward a neurobiology of remembering. Learn. Mem. 7: 73-84.
66. Schafe, G.E. and LeDoux, J.E. 2000. Memory consolidation of auditory Pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J. Neurosci. 20: RC96.
67. Schafe, G.E., Atkins, C.M., Swank, M.W., Bauer, E.P., Sweatt, J.D., and LeDoux, J.E. 2000. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear conditioning. J. Neurosci. 20: 8177-8187.
68. Silva, A.J., Kogan, J.H., Frankland, P.W., and Kida, S. 1998. CREB and memory. Annu. Rev. Neurosci. 21: 127-148.
69. Steward, O. and Worley, P. 2002. Local synthesis of proteins at synaptic sites on dendrites: Role in synaptic plasticity and memory consolidation? Neurobiol. Learn. Mem. 78: 508-527.
70. Suzuki, A., Josselyn, S.A., Frankland, P.W., Masushige, S., Silva, A.J., and Kida, S. 2004. Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J. Neurosci. 24: 4787-4795.
71. Taubenfeld, S.M., Wiig, K.A., Bear, M.F., and Alberini, C.M. 1999. A molecular correlate of memory and amnesia in the hippocampus. Nat. Neurosci. 2: 309-310.
72. Taubenfeld, S.M., Milekic, M.H., Monti, B., and Alberini, C.M. 2001a. The consolidation of new but not reactivated memory requires hippocampal C/EBPβ. Nat. Neurosci. 4: 813-818.
73. Taubenfeld, S.M., Wiig, K.A., Monti, B., Dolan, B., Pollonini, G., and Alberini, C.M. 2001b. Fornix-dependent induction of hippocampal CCAAT enhancer-binding protein β and δ co-localizes with phosphorylated cAMP response element-binding protein and accompanies long-term memory consolidation. J. Neurosci. 21: 84-91.
74. Tronel, S. and Sara, S.J. 2002. Mapping of olfactory memory circuits: Region-specific c-fos activation after odor-reward associative learning or after its retrieval. Learn. Mem. 3: 105-111.
75. Tronel, S., Milekic, M.H., and Alberini, C.M. 2005. Linking new information to a reactivated memory requires consolidation and not reconsolidation mechanisms. PLoS Biol. 3: 1630-1638.
76. Tronson, N.C., Wiseman, S.L., Olausson, P., and Taylor, J.R. 2006. Bidirectional behavioral plasticity of memory reconsolidation depends on amygdalar protein kinase A. Nat. Neurosci. 9: 167-169.
77. von Hertzen, L.S. and Giese, K.P. 2005. Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J. Neurosci. 25: 1935-1942.
78. Wang, S.H., Ostlund, S.B., Nader, K., and Balleine, B.W. 2005. Consolidation and reconsolidation of incentive learning in the amygdala. J. Neurosci. 25: 830-835.
79. Widnell, K.L., Self, D.W., Lane, S.B., Russell, D.S., Vaidya, V.A., Miserendino, M.J., Rubin, C.S., Duman, R.S., and Nestler, E.J. 1996. Regulation of CREB expression: in vivo evidence for a functional role in morphine action in the nucleus accumbens. J. Pharmacol. Exp. Ther. 276: 306-315.
80. Wilensky, A.E., Schafe, G.E., and LeDoux, J.E. 2000. The amygdala modulates memory consolidation of fear-motivated inhibitory avoidance learning but not classical fear conditioning. J. Neurosci. 20: 7059-7066.
81. Yim, A.J., Moraes, C.R., Ferreira, T.L., and Oliveira, M.G. 2006. Protein synthesis inhibition in the basolateral amygdala following retrieval does not impair expression of morphine-associated conditioned place preference. Behav. Brain Res. 171: 162-169.
82. Yin, J.C. and Tully, T. 1996. CREB and the formation of long-term memory. Curr. Opin. Neurobiol. 6: 264-268.
83. Yin, J.C., Del Vecchio, M., Zhou, H., and Tully, T. 1995. CREB as a memory modulator: Induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81: 107-115.
84. Zanatta, M.S., Quillfeldt, J.H., Schaeffer, E., Schmitz, P.K., Quevedo, J., Medina, J.H., and Izquierdo, I. 1997. Involvement of the hippocampus, amygdala, entorhinal cortex and posterior parietal cortex in memory consolidation. Braz. J. Med. Biol. Res. 30: 235-240.