Mouse models of impaired fear memory exhibit deficits in amygdalar LTP

Hippocampus

Volumn 15, Issue 4, 2005, Pages 502-517

  Schimanski, Lesley A ^a   Nguyen, Peter V ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Extinction; Fear conditioning; Hippocampus; Long term potentiation; Synaptic plasticity

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BRAIN ELECTROPHYSIOLOGY; CONDITIONING; CORRELATION ANALYSIS; FEAR; FEMALE; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MEMORY DISORDER; MOUSE; MOUSE STRAIN; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REINFORCEMENT; REVIEW;

AMYGDALA; ANIMALS; DISEASE MODELS, ANIMAL; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HIPPOCAMPUS; LONG-TERM POTENTIATION; MEMORY; MEMORY DISORDERS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PERFORANT PATHWAY; SPECIES SPECIFICITY; SYNAPTIC TRANSMISSION;

EID: 21444446346     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.20075     Document Type: Review

References (113)

1. Abe K. 2001. Modulation of hippocampal long-term potentiation by the amygdala: a synaptic mechanism linking emotion and memory. Jpn J Pharmacol 86:18-22.
2. 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.
3. Adams JP, Roberson ED, English JD, Selcher JC, Sweatt JD. 2000. MAPK regulation of gene expression in the central nervous system. Acta Neurobiol Exp 60:377-394.
4. Adams B, Fitch T, Chaney S, Gerlai R. 2002. Altered performance characteristics in cognitive tasks: comparison of the albino ICR and CD1 mouse strains. Behav Brain Res 133:351-361.
5. Andersen P, Sundberg SH, Sveen O, Wigstrom H. 1977. Specific, long-lasting potentiation of synaptic transmission in hippocampal slices. Nature 266:736-737.
6. Bailey CH, Bartsch D, Kandel ER. 1996. Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci USA 93:13445-13452.
7. Balogh SA, Wehner JM. 2003. Inbred mouse strain differences in the establishment of long-term fear memory. Behav Brain Res 140:97-106.
8. Barnes CA, Jung MW, McNaughton BL, Korol DL, Andreasson K, Worley PF. 1994. LTP saturation and spatial learning disruption: effects of task variables and saturation levels. J Neurosci 14:5793-5806.
9. 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.
10. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
11. Bliss TV, Lømo T. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331-356.
12. Bolivar VJ, Pooler O, Flaherty L. 2001. Inbred strain variation in contextual and cued fear conditioning behavior. Mamm Genome 12:651-656.
13. Bourtchouladze 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.
14. Bouton ME. 1993. Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol Bull 114:80-99.
15. Bowers BJ, Christensen SC, Pauley JR, Paylor R, Yuva L, Dunbar SE, Wehner JM. 1995. Protein and molecular characterization of hippocampal protein kinase C in C57BL/6 and DBA/2 mice. J Neurochem 64:2737-2746.
16. Brun VH, Ytterbo K, Morris RG, Moser MB, Moser EI. 2001. Retrograde amnesia for spatial memory induced by NMDA receptor-mediated long-term potentiation. J Neurosci 21:356-362.
17. Capocchi G, Zampolini M, Larson J. 1992. Theta burst stimulation is optimal for induction of LTP at both apical and basal dendritic synapses on hippocampal CA1 neurons. Brain Res 591:332-336.
18. Chapman PF, Ramsay MF, Krezel W, Knevett SG. 2003. Synaptic plasticity in the amygdala: comparisons with hippocampus. Ann NY Acad Sci 985:114-124.
19. Chen C, Tonegawa S. 1997. Molecular genetic analysis of synaptic plasticity, activity-dependent neural development, learning, and memory in the mammalian brain. Annu Rev Neurosci 20:157-184.
20. Chen C, Kim JJ, Thompson RF, Tonegawa S. 1996. Hippocampal lesions impair contextual fear conditioning in two strains of mice. Behav Neurosci 110:1177-1180.
21. Colino A, Malenka RC. 1993. Mechanisms underlying induction of long-term potentiation in rat medial and lateral perforant paths in vitro. J Neurophysiol 69:1150-1159.
22. Collingridge GL, Kehl SJ, McLennan H. 1983. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol 334:33-46.
23. Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, Hitzemann RJ, Maxson SC, Miner LL, Silva AJ, Wehner JM, Wynshaw-Boris A, Paylor R. 1997. Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl) 132:107-124.
24. Deadwyler SA, Dunwiddie T, Lynch G. 1987. A critical level of protein synthesis is required for long-term potentiation. Synapse 1:90-95.
25. Doyere V, Laroche S. 1992. Linear relationship between the maintenance of hippocampal LTP and retention of an associative memory. Hippocampus 2:39-48.
26. Doyere V, Schafe GE, Sigurdsson T, LeDoux JE. 2003. Long-term potentiation in freely-moving rats reveals asymmetries in thalamic and cortical inputs to the lateral amygdala. Eur J Neurosci 17:2703-2715.
27. Eichenbaum H, Cohen NJ. 2001. From conditioning to conscious recollection. Oxford, UK: Oxford University Press.
28. Fanselow MS, Kim JJ. 1994. Acquisition of contextual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist D, L-2-amino-5-phosphonovaleric acid to the basolateral amygdala. Behav Neurosci 108:210-212.
29. Festing MW. 1998. Inbred strains of mice [Online]. Available: http://www.informatics.jax.org/external/festing/mouse/STRAINS.shtml [15 Dec 2004].
30. Fischer A, Sananbenesi F, Schrick C, Spiess J, Radulovic J. 2004. Distinct roles of hippocampal de novo protein synthesis and actin rearrangement in extinction of contextual fear. J Neurosci 24:1962-1966.
31. Flood JF, Jarvik ME, Bennett EL, Orme AE, Rosenzweig MR. 1977. Protein synthesis inhibition and memory for pole jump active avoidance and extinction. Pharmacol Biochem Behav 7:71-77.
32. Francis DD, Zaharia MD, Shanks N, Anisman H. 1995. Stress-induced disturbances in Morris-water maze performance: interstrain variability. Physiol Behav 58:57-65.
33. Francis DD, Szegda K, Campbell G, Martin WD, Insel TR. 2003. Epigenetic sources of behavioral differences in mice. Nat Neurosci 6:445-446.
34. Frey U, Krug M, Reymann KG, Matthies H. 1988. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in hippocampal CA1 region in vitro. Brain Res 452:57-65.
35. Frey U, Huang YY, Kandel ER. 1993. Effects of cAMP stimulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
36. Frohardt RJ, Guarraci FA, Bouton ME. 2000. The effects of neurotoxic hippocampal lesions on two effects of context after fear extinction. Behav Neurosci 114:227-240.
37. Genoux D, Haditsch U, Knobloch M, Michalon A, Storm D, Mansuy IM. 2002. Protein phosphatase 1 is a molecular constraint on learning and memory. Nature 418:970-975.
38. Hanse E, Gustafsson B. 1992. Long-term potentiation and field EPSPs in the lateral and medial perforant paths in the dentate gyrus in vitro: a comparison. Eur J Neurosci 4:1191-1201.
39. Huang YY, Kandel ER. 1994. Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn Mem 1:74-82.
40. Huang YY, Nguyen PV, Abel T, Kandel ER. 1996. Long-lasting forms of synaptic potentiation in the mammalian hippocampus. Learn Mem 3:74-85.
41. Impey S, Mark M, Villacres EC, Poser S, Chavkin C, Storm DR. 1996. Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 16:973-982.
42. Izquierdo I, McGaugh JL. 2000. Behavioural pharmacology and its contribution to the molecular basis of memory consolidation. Behav Pharmacol 11:517-534.
43. Izquierdo I, Medina JH, Vianna MR, Izquierdo LA, Barros DM. 1999. Separate mechanisms for short- and long-term memory. Behav Brain Res 103:1-11.
44. Izquierdo LA, Barros DM, Vianna MR, Coitinho A, deDavid e Silva T, Choi H, Moletta B, Medina JH, Izquierdo I. 2002. Molecular pharmacological dissection of short- and long-term memory. Cell Mol Neurobiol 22:269-287.
45. Jackson Laboratory. 2004. Jax® Mice Strain Information [Online]. http://jaxmice.jax.org/jaxmicedb/html/inbred.shtml (17 Sept. 2004).
46. Jax Notes. Spring 2002. Genetic background effects: can your mice see [Online]. The Jackson Laboratory. http://jaxmice.jax.org/library/notes/485.pdf [22 Aug. 2003].
47. Johnston D, Wu S. 1995. Foundations of cellular neurophysiology. Cambridge, MA: MIT Press.
48. Jones MW, Errington ML, French PJ, Fine A, Bliss TVP, Garel S, Charnay P, Bozon B, Laroche S, Davis S. 2001. A requirement for the IEG zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4:289-296.
49. Kandel ER. 2001. The molecular biology of memory storage: a dialogue between genes and synapses [Nobel Lecture]. Science 294: 1030-1038.
50. Katz B, Miledi R. 1968. The role of calcium in neuromuscular facilitation. J Physiol 195:481-492.
51. Kim JJ, Fanselow MS. 1992. Modality-specific retrograde amnesia of fear. Science 256:675-677.
52. Kim JJ, Rison RA, Fanselow MS. 1993. Effects of amygdala, hippocampus and periaqueductal gray lesions on short- and long-term contextual fear. Behav Neurosci 107:1093-1098.
53. Larson J, Wong D, Lynch G. 1986. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368:347-350.
54. LeDoux JE. 2000. Emotion circuits in the brain. Annu Rev Neurosci 23:155-184.
55. Lee H, Kim JJ. 1998. Amygdalar NMDA receptors are critical for new fear learning in previously fear-conditioned rats. J Neurosci 18:8444-8454.
56. Lømo T. 1966. Frequency potentiation of excitatory synaptic activity in the dentate area of the hippocampal formation. Acta Physiol Scand 68(suppl 277):128.
57. Lyon M, Searle A. 1989. Genetic variants and strains of the laboratory mouse. Oxford, UK: Oxford University Press.
58. Malinow R, Schulman H, Tsien RW. 1989. Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245:862-866.
59. Manahan-Vaughan D. 2000a. Group III metabotropic glutamate receptors modulate long-term depression in the hippocampal CA1 region of two rat strains in vivo. Neuropharmacology 39: 1952-1958.
60. Manahan-Vaughan D. 2000b. Long-term depression in freely moving rats is dependent upon strain variation, induction protocol and behavioral state. Cereb Cortex 10:482-487.
61. Manahan-Vaughan D, Braunewell KH. 1999. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc Natl Acad Sci USA 96:8739-8744.
62. Maren S. 2000. Auditory fear conditioning increases CS-elicited spike firing in lateral amygdala neurons even after extensive overtraining. Eur J Neurosci 12:4047-4054.
63. Maxen S. 2001. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897-931.
64. Martin SJ, Grimwood PD, Morris RGM. 2000. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
65. Matsushita M, Tomizawa K, Moriwaki A, Li ST, Terada H, Matsui H. 2001. A high-efficiency protein transduction system demonstrating the role of PKA in long-lasting LTP. J Neurosci 21:6000-6007.
66. Matthies H, Reymann KG. 1993. Protein kinase-A inhibitors prevent the maintenance of hippocampal LTP. NeuroReport 4:712-714.
67. McClive PJ, Huang D, Morahan G. 1994. C57BL/6 and C57BL/10 inbred mouse strains differ at multiple loci on chromosome 4. Immunogenetics 39:286-288.
68. McGaugh JL. 2004. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1-28.
69. McGaugh JL, McIntyre CK, Power AE. 2002. Amygdala modulation of memory consolidation: interaction with other brain systems. Neurobiol Learn Mem 78:539-552.
70. McKernan MG, Shinnick-Gallagher P. 1997. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390:607-611.
71. McNaughton BL. 1980. Evidence for two physiologically distinct perforant pathways to the fascia dentata. Brain Res 199:1-19.
72. Micheau J, Riedel G. 1999. Protein kinases: which one is the memory molecule? Cell Mol Life Sci 55:534-548.
73. Miczek KA, Maxson SC, Fish EW, Faccidomo S. 2001. Aggressive behavioral phenotypes in mice. Behav Brain Res 125:167-181.
74. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
75. Morris RG, Anderson E, Lynch GS, Baudry M. 1986. Selective impairment of learning and blockade of long-term potentiation by an N-ethyl-D-aspartate receptor antagonist, AP5. Nature 319:774-776.
76. Moser EI, Krobert KA, Moser MB, Morris RG. 1998. Impaired spatial learning after saturation of long-term potentiation. Science 281:2038-2042.
77. Nguyen PV, Kandel ER. 1996. A macromolecular synthesis-dependent late phase of long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. J Neurosci 16:3189-3198.
78. Nguyen PV, Abel T, Kandel ER. 1994. Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265:1104-1107.
79. Nguyen PV, Abel T, Kandel ER, Bourtchouladze R. 2000a. Strain-dependent differences in LTP and hippocampus-dependent memory in inbred mice. Learn Mem 7:170-179.
80. Nguyen PV, Duffy SN, Young JZ. 2000b. Differential maintenance and frequency-dependent tuning of LTP at hippocampal synapses of specific strains of inbred mice. J Neurophysiol 5:2484-2493.
81. Otto T, Eichenbaum H, Weiner SI, Weible CG. 1991. Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus 1:181-192.
82. Owen EH, Logue SF, Rasmussen DL, Wehner JM. 1997. Assessment of learning by the Morris water task and fear conditioning in inbred mouse strains and F1 hybrids: implications of genetic background for single gene mutations and quantitative trait loci analyses. Neuroscience 80:1087-1099.
83. Pavlov I. 1927. Conditioned reflexes. Oxford, UK: Oxford University Press.
84. 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.
85. Paylor R, Baskall-Baldini L, Yuva L, Wehner JM. 1996. Developmental differences in place-learning performance between C57BL/6 and DBA/2 mice parallel the ontogeny of hippocampal protein kinase C. Behav Neurosci 110:1415-1425.
86. Phillips RG, LeDoux JE. 1992. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106:274-285.
87. Radulovic J, Kammermeier J, Spiess J. 1998. Generalization of fear responses in C57BL/6N mice subjected to one-trial foreground contextual fear conditioning. Behav Brain Res 95:179-189.
88. Richter-Levin G. 2004. The amygdala, the hippocampus, and emotional modulation of memory. Neuroscientist 10:31-39.
89. Rogan MT, Staubli UV, LeDoux JE. 1997. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390:604-607.
90. Royle SJ, Collins FC, Rupniak HT, Barnes JC, Anderson R. 1999. Behavioural analysis and susceptibility to CNS injury of four inbred strains of mice. Brain Res 816:337-349.
91. Sacchetti B, Lorenzini CA, Baldi E, Bucherelli C, Roberto M, Tassoni G, Brunelli M. 2002. Time-dependent inhibition of hippocampal LTP in vitro following contextual fear conditioning in the rat. Eur J Neurosci 15:143-150.
92. 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.
93. Schaeffer K. 1892. Beitrag zur histologie der Ammonshornformation. Arch Mikr Anat 39:4. x
94. Schafe GE, Nader K, Blair HT, LeDoux JE. 2001. Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective. Trends Neurosci 24:540-546.
95. Schimanski LA, Nguyen PV. 2004. Multidisciplinary approaches for investigating the mechanisms of hippocampus-dependent memory: a focus on inbred mouse strains. Neurosci Biobehav Rev 28:463-483.
96. Schimanski LA, Nguyen PV. 2005. Impaired fear memories are correlated with subregion-specific deficits in hippocampal and amygdalar LTP. Behav Neurosci 119:38-54.
97. Schimanski LA, Wahlsten D, Nguyen PV. 2002. Selective modification of short-term hippocampal synaptic plasticity and impaired memory extinction in mice with a congenitally reduced hippocampal commissure. J Neurosci 22:8277-8286.
98. Seidenbecher T, Laxmi TR, Stork O, Pape HC. 2003. Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301:846-850.
99. Shors TJ, Matzel RD. 1997. Long-term potentiation: what's learning got to do with it? Behav Brain Sci 20:597-614.
100. Silva AJ, Stevens CF, Tonegawa S, Wang Y. 1992. Deficient hippocampal LTP in CaMK-II mutant mice. Science 257:201-206.
101. Stanton PK, Sarvey JM. 1984. Blockade of long-term potentiation in rat hippocampal slices by inhibitors of protein synthesis. J Neurosci 4:3080-3088.
102. Stiedl O, Birkenfeld K, Palve M, Spiess J. 2000. Impairment of conditioned contextual fear of C57BL/6J mice by intracerebral injections of the NMDA receptor antagonist APV. Behav Brain Res 116:157-168.
103. Szapiro G, Vianna MR, McGaugh JL, Medina JH, Izquierdo I. 2003. The role of NMDA glutamate receptors, PKA, MAPK, and CAMKII in the hippocampus in extinction of conditioned fear. Hippocampus 13:53-58.
104. Tsien JZ, Huerta PT, Tonegawa S. 1996. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87:1327-1338.
105. Tsvetkov E, Carlezon WA, Benes FM, Kandel ER, Bolshakov VY. 2002. Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 34:289-300.
106. Upchurch M, Wehner JM. 1988. Differences between inbred strains of mice in Morris water maze performance. Behav Genet 18:55-68.
107. 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.
108. Wehner JM, Sleight S, Upchurch M. 1990. Hippocampal protein kinase C activity is reduced in poor spatial learners. Brain Res 523:181-187.
109. Wilson A, Brooks DC, Bouton ME. 1995. The role of the rat hippocampal system in several effects of context in extinction. Behav Neurosci 109:828-836.
110. Wu J, Rush A, Rowan MJ, Anwyl R. 2001. NMDA receptor- and metabotropic glutamate receptor-dependent synaptic plasticity induced by high-frequency stimulation in the rat dentate gyrus in vitro. J Physiol 533:745-755.
111. Yaniv D, Vouimba RM, Diamond DM, Richter-Levin G. 2003. Simultaneous induction of long-term potentiation in the hippocampus and the amygdala by entorhinal cortex activation: mechanistic and temporal profiles. Neuroscience 120:1125-1135.
112. Yoshida M, Goto K, Watanabe S. 2001. Task-dependent strain difference of spatial learning in C57BL/6N and BALB/c mice. Physiol Behav 73:37-42.
113. Zola-Morgan S, Squire LR, Amaral DG. 1986. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of hippocampus. J Neurosci 6:2950-2967.