Consolidation of CS and US representations in associative fear conditioning

Hippocampus

Volumn 14, Issue 5, 2004, Pages 557-569

  Frankland, Paul W ^a,b   Josselyn, Sheena A ^a,b   Anagnostaras, Stephan G ^a,c   Kogan, Jeffrey H ^a,d   Takahashi, Eiki ^a   Silva, Alcino J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Memory Pharmaceuticals Corporation   (United States)

Author keywords

CaMKII; CREB; Epinephrine; Hippocampus; NMDA; Protein synthesis

Indexed keywords

ADRENALIN; ANISOMYCIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; N METHYL DEXTRO ASPARTIC ACID; PROTEIN KINASE (CALCIUM,CALMODULIN) II; TRANSCRIPTION FACTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ASSOCIATION; CONDITIONING; CONTROLLED STUDY; CYTOLOGY; FEAR; FEMALE; GENE DISRUPTION; HORMONAL REGULATION; IMMOBILIZATION; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW;

ANIMALS; ASSOCIATION LEARNING; AVOIDANCE LEARNING; BRAIN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CONDITIONING, CLASSICAL; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ELECTRIC STIMULATION; EPINEPHRINE; EXCITATORY AMINO ACID ANTAGONISTS; FEAR; FEMALE; HIPPOCAMPUS; MALE; MEMORY; MICE; MICE, INBRED C57BL; MUTATION; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; RECEPTORS, N-METHYL-D-ASPARTATE; STRESS, PSYCHOLOGICAL;

EID: 4243054993     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.10208     Document Type: Review

References (66)

1. Abel T, Nguyen PV, Barad M, Deuel TAS, 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. Agnihotri NT, Hawkins RD, Kandel ER, Kentros C. 2001. Protein synthesis inhibition selectively abolishes the long-term stability of new hippocampal place cell maps. Soc Neurosci Abs 27:836.
3. Alberini CM. 1999. Genes to remember. J Exp Biol 202:2887-2891.
4. Anagnostaras SG, Gale GD, Fanselow MS. 2001. Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 11:8-17.
5. Anagnostaras SG, Josselyn SA, Frankland PW, Silva AJ. 2000. Computer-assisted behavioral assessment of Pavlovian fear conditioning in mice. Learn Mem 7:58-72.
6. Anagnostaras SG, Maren S, Fanselow MS. 1999. Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. J Neurosci 19:1106-1114.
7. Barrientos RM, O'Reilly RC, Rudy JW. 2002. Memory for context is impaired by injecting anisomycin into dorsal hippocampus following context exploration. Behav Brain Res 134:299-306.
8. 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.
9. Bevins RA, Ayres JJB. 1995. One-trial context fear conditioning as a function of the interstimulus interval. Anim Learn Behav 23:400-410.
10. Blendy JA, Kaestner KH, Schmid W, Gass P, Schutz G. 1996. Targeting of the CREB gene leads to up-regulation of a novel CREB mRNA isoform. EMBO J 15:1098-1106.
11. Bourtchouladze R, Abel T, Berman N, Gordon R, Lapidus K, Kandel ER. 1998. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn Mem 5:365-374.
12. 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.
13. Cahill L, McGaugh JL. 1996. Modulation of memory storage. Curr Opin Neurobiol 6:237-242.
14. - mice. Science 279:867-869.
15. Davis HP, Squire LR. 1984. Protein synthesis and memory: a review. Psychol Bull 96:518-559.
16. -/- mutant mice. Behav Neurosci 114: 998-1004.
17. Fanselow MS. 1980. Conditional and unconditional components of post-shock freezing. Integr Physiol Behav Sci 15:177-182.
18. Fanselow MS. 1986. Associative vs topographical accounts of the immediate shock freezing deficit in rats: implications for the response selection rules governing species-specific defensive reactions. Learn Motiv 17:16-39.
19. Fanselow MS. 1990. Factors governing one-trial contextual conditioning. Anim Learn Behav 18:264-270.
20. Fanselow MS. 2000. Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 110:73-81.
21. Fanselow MS, Decola JP, Young SL. 1993. Mechanisms responsible for reduced contextual conditioning with massed unsignaled unconditional stimuli. J Exp Psychol Anim Behav Process 19:121-137.
22. Fanselow MS, Gale GD. 2003. The amygdala, fear, and memory. Ann NY Acad Sci 985:125-134.
23. Frankland PW, Cestari V, Filipkowski R, McDonald RJ, Silva AJ. 1998. The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 112:863-874.
24. Gallistel CR, Gibbon J. 2000. Time, rate, and conditioning. Psychol Rev 107:289-344.
25. Gass P, Wolfer DP, Balschun D, Rudolph D, Frey U, Lipp H-P, Schuetz G. 1998. Deficits in memory tasks of mice with CREB mutations depend on gene dosage. Learn Mem 5:274-288.
26. Giese KP, Fedorov NB, Filipkowski RK, Silva AJ. 1998. Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279:870-873.
27. Guthrie ER. 1935. The psychology of learning. New York: Harper. 258 p.
28. Kandel ER, Pittenger C. 1999. The past, the future and the biology of memory storage. Philos Trans R Soc Lond B Biol Sci 354:2027-2052.
29. Kida S, Josselyn SA, Pena de Ortiz S, Kogan JH, Chevere I, Masushige S, Silva AJ. 2002. CREB required for the stability of new and reactivated fear memories. Nature Neurosci 5:348-355.
30. Kiernan MJ, Westbrook RF. 1993. Effects of exposure to a to-be-shocked environment upon the rat's freezing response: evidence for facilitation, latent inhibition, and perceptual learning. QJ Exp Psychol B 46:271-288.
31. Kiernan MJ, Westbrook RF, Cranney J. 1995. Immediate shock, passive avoidance and potentiated startle: implications for the unconditioned response to shock. Anim Learn Behav 23:22-30.
32. Kiyama Y, Manabe T, Sakimura K, Kawakami F, Mori H, Mishina M. 1998. Increased thresholds for long-term potentiation and contextual learning in mice lacking the NMDA-type glutamate receptor epsilon 1 subunit. J Neurosci 18:6704-6712.
33. Kobayashi K, Yasoshima Y. 2001. The central noradrenaline system and memory consolidation. Neuroscientist 7:371-376.
34. Kogan JH, Frankland PW, Blendy JA, Coblentz J, Marowitz Z, Schuetz G, Silva AJ. 1997. Spaced training induces normal long-term memory in CREB mutant mice. Curr Biol 7:1-11.
35. Konorski J. 1967. Integrative activity of the brain; an interdisciplinary approach. Chicago: University of Chicago Press. p xii.
36. Lattal KM, Abel T. 2001a. Different requirements for protein synthesis in acquisition and extinction of spatial preferences and context-evoked fear. J Neurosci 21:5773-5780.
37. Lattal KM, Abel T. 2001b. An immediate-shock freezing deficit with discrete cues: a possible role for unconditioned stimulus processing mechanisms. J Exp Psychol Anim Behav Process 27:394-406.
38. LeDoux JE. 2000. Emotion circuits in the brain. Annu Rev Neurosci 23:155-184.
39. Lee HJ, Berger SY, Stiedl O, Spiess J, Kim JJ. 2001. Post-training injections of catecholaminergic drugs do not modulate fear conditioning in rats and mice. Neurosci Lett 303:123-126.
40. Liang KC, Juler RG, McGaugh JL. 1986. Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system. Brain Res 368:125-133.
41. Lisman J, Schulman H, Cline H. 2002. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175-190.
42. Maren S. 2001. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897-931.
43. Martin SJ, Grimwood PD, Morris RGM. 2000. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23: 649-711.
44. Martinez JL, Jr., Jensen RA, McGaugh JL. 1981. Attenuation of experimentally-induced amnesia. Prog Neurobiol 16:155-186.
45. McGaugh JL. 2002. Memory consolidation and the amygdala: a systems perspective. Trends Neurosci 25:456-461.
46. McGaugh JL, Roozendaal B. 2002. Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12:205-210.
47. Meiri N, Rosenblum K. 1998. Lateral ventricle injection of the protein synthesis inhibitor anisomycin impairs long-term memory in a spatial memory task. Brain Res 789:48-55.
48. Milanovic S, Radulovic J, Laban O, Stiedl O, Henn F, Spiess J. 1998. Production of the Fos protein after contextual fear conditioning of C57BL/6N mice. Brain Res 784:37-47.
49. Morris RG, Moser EI, Riedel G, Martin SJ, Sandin J, Day M, O'Carroll C. 2003. Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 358:773-786.
50. Ohno M, Frankland PW, Chen AP, Costa RM, Silva AJ. 2001. Inducible, pharmacogenetic approaches to the study of learning and memory. Nat Neurosci 4:1238-1243.
51. O'Reilly RC, Rudy JW. 2001. Conjunctive representations in learning and memory: principles of cortical and hippocampal function. Psychol Rev 108:311-345.
52. Pavlov IP. 1927. Conditioned reflexes; an investigation of the physiological activity of the cerebral cortex. Translated and edited by G.V. Anrep. London: Oxford University Press.
53. Paylor R, Tracy R, Wehner J, Rudy JW. 1994. DBA/2 and C57BL/6 mice differ in contextual fear but not auditory fear conditioning. Behav Neurosci 108:810-817.
54. Pittenger C, Huang YY, Paletzki RF, Bourtchouladze R, Scanlin H, Vronskaya S, Kandel ER. 2002. Reversible inhibition of CREB/ ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 34:447-462.
55. Rosenblum K, Meiri N, Dudai Y. 1993. Taste memory: the role of protein synthesis in gustatory cortex. Behav Neural Biol 59:49-56.
56. Rudy JW, Barrientos RM, O'Reilly RC. 2002. Hippocampal formation supports conditioning to memory of a context. Behav Neurosci 116: 530-538.
57. Rudy JW, O'Reilly RC. 1999. Contextual fear conditioning, conjunctive representations, pattern completion, and the hippocampus. Behav Neurosci 113:867-880.
58. Rudy JW, O'Reilly RC. 2001. Conjunctive representations, the hippocampus, and contextual fear conditioning. Cognit Affect Behav Neurosci 1:66-82.
59. 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.
60. Schauz C, Koch M. 2000. Blockade of NMDA receptors in the amygdala prevents latent inhibition of fear-conditioning. Learn Mem 7:393-399.
61. Shaywitz AJ, Greenberg ME. 1999. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68:821-861.
62. Silva AJ, Kogan JH, Frankland PW, Kida S. 1998. CREB and memory. Annu Rev Neurosci 21:127-148.
63. Stanciu M, Radulovic J, Spiess J. 2001. Phosphorylated cAMP response element binding protein in the mouse brain after fear conditioning: relationship to Fos production. Mol Brain Res 94:15-24.
64. Stiedl O, Palve M, Radulovic J, Birkenfeld K, Spiess J. 1999. Differential impairment of auditory and contextual fear conditioning by protein synthesis inhibition in C57BL/6N mice. Behav Neurosci 113:496-506.
65. Wiltgen BJ, Sanders MJ, Behne NS, Fanselow MS. 2001. Sex differences, context preexposure, and the immediate shock deficit in Pavlovian context conditioning with mice. Behav Neurosci 115:26-32.
66. Yin JCP, Tully T. 1996. CREB and the formation of long-term memory. Curr Opin Neurobiol 6:264-268.