Biphasic ERK1/2 activation in both the hippocampus and amygdala may reveal a system consolidation of contextual fear memory

Neurobiology of Learning and Memory

Volumn 88, Issue 4, 2007, Pages 424-434

  Trifilieff, Pierre ^a   Calandreau, Ludovic ^a   Herry, Cyril ^b   Mons, Nicole ^a   Micheau, Jacques ^a  

^a UMR 5287   (France)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Amygdala; Biphasic activation; Contextual fear conditioning; Hippocampus; MAPK ERK; Mouse

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; ENZYME ACTIVATION; FEAR; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MEMORY CONSOLIDATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; ASSOCIATION LEARNING; AVOIDANCE LEARNING; CONDITIONING, CLASSICAL; ENVIRONMENT; FEAR; HIPPOCAMPUS; MALE; MEMORY; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEURONAL PLASTICITY; STATISTICS, NONPARAMETRIC; TIME FACTORS;

EID: 34848920101     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2007.05.004     Document Type: Article

References (48)

1. Alonso M., Viola H., Izquierdo I., and Medina J.H. Aversive experiences are associated with a rapid and transient activation of ERKs in the rat hippocampus. Neurobiology of Learning and Memory 77 (2002) 119-124
2. Bailey D.J., Kim J.J., Sun W., Thompson R.F., and Helmstetter F.J. Acquisition of fear conditioning in rats requires the synthesis of mRNA in the amygdala. Behavioural Neuroscience 113 (1999) 276-282
3. Bernabeu R., Bevilaqua L., Ardenghi P., Bromberg E., Schmitz P., Bianchin M., et al. Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proceedings of the National Academy of Sciences of the United States of America 94 (1997) 7041-7046
4. Blanchard R.J., and Blanchard D.C. Passive and active reactions to fear-eliciting stimuli. Journal of Comparative and Physiological Psychology 68 (1969) 129-135
5. Bourtchouladze R., Abel T., Berman N., Gordon R., Lapidus K., and Kandel E.R. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learning & Memory 5 (1998) 365-374
6. Calandreau L., Desmedt A., Decorte L., and Jaffard R. A different recruitment of the lateral and basolateral amygdala promotes contextual or elemental conditioned association in Pavlovian fear conditioning. Learning & Memory 12 (2005) 383-388
7. Calandreau L., Trifilieff P., Mons N., Costes L., Marien M., Marighetto A., et al. Extracellular hippocampal acetylcholine level controls amygdala function and promotes adaptive conditioned emotional response. The Journal of Neuroscience 26 (2006) 13556-13566
8. Canteras N.S., and Swanson L.W. Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: A PHAL anterograde tract-tracing study in the rat. The Journal of Comparative Neurology 324 (1992) 180-194
9. Daumas S., Halley H., Frances B., and Lassalle J.M. Encoding, consolidation, and retrieval of contextual memory: Differential involvement of dorsal CA3 and CA1 hippocampal subregions. Learning & Memory 12 (2005) 375-382
10. Davis H.P., and Squire L.R. Protein synthesis and memory: A review. Psychological Bulletin 96 (1984) 518-559
11. Desmedt A., Garcia R., and Jaffard R. Differential modulation of changes in hippocampal-septal synaptic excitability by the amygdala as a function of either elemental or contextual fear conditioning in mice. The Journal of Neuroscience 18 (1998) 480-487
12. Donley M.P., Schulkin J., and Rosen J.B. Glucocorticoid receptor antagonism in the basolateral amygdala and ventral hippocampus interferes with long-term memory of contextual fear. Behavioural Brain Research 164 (2005) 197-205
13. Gale G.D., Anagnostaras S.G., Godsil B.P., Mitchell S., Nozawa T., Sage J.R., et al. Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. The Journal of Neuroscience 24 (2004) 3810-3815
14. Goosens K.A., and Maren S. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learning & Memory 8 (2001) 148-155
15. Grecksch G., and Matthies H. Two sensitive periods for the amnesic effect of anisomycin. Pharmacology Biochemistry and Behavior 12 (1980) 663-665
16. Hall J., Thomas K.L., and Everitt B.J. Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: Selective activation of hippocampal CA1 neurons during the recall of contextual memories. The Journal of Neuroscience 21 (2001) 2186-2193
17. Huff N.C., Frank M., Wright-Hardesty K., Sprunger D., Matus-Amat P., Higgins E., et al. Amygdala regulation of immediate-early gene expression in the hippocampus induced by contextual fear conditioning. The Journal of Neuroscience 26 (2006) 1616-1623
18. Igaz L.M., Vianna M.R., Medina J.H., and Izquierdo I. Two time periods of hippocampal mRNA synthesis are required for memory consolidation of fear-motivated learning. The Journal of Neuroscience 22 (2002) 6781-6789
19. Ito R., Robbins T.W., McNaughton B.L., and Everitt B.J. Selective excitotoxic lesions of the hippocampus and basolateral amygdala have dissociable effects on appetitive cue and place conditioning based on path integration in a novel Y-maze procedure. European Journal of Neuroscience 23 (2006) 3071-3080
20. Kim J.J., Koo J.W., Lee H.J., and Han J.S. Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. The Journal of Neuroscience 25 (2005) 1532-1539
21. Koo J.W., Han J.S., and Kim J.J. Selective neurotoxic lesions of basolateral and central nuclei of the amygdala produce differential effects on fear conditioning. The Journal of Neuroscience 24 (2004) 7654-7662
22. Lee I., and Kesner R.P. Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus 14 (2004) 301-310
23. Louie K., and Wilson M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29 (2001) 145-156
24. Malin E.L., and McGaugh J.L. Differential involvement of the hippocampus, anterior cingulate cortex, and basolateral amygdala in memory for context and footshock. Proceedings of the National Academy of Sciences of the United States of America 103 (2006) 1959-1963
25. Maren S. Neurotoxic basolateral amygdala lesions impair learning and memory but not the performance of conditional fear in rats. The Journal of Neuroscience 19 (1999) 8696-8703
26. Matus-Amat P., Higgins E.A., Barrientos R.M., and Rudy J.W. The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. The Journal of Neuroscience 24 (2004) 2431-2439
27. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Reviews of Neuroscience 27 (2004) 1-28
28. McGaugh J.L., McIntyre C.K., and Power A.E. Amygdala modulation of memory consolidation: Interaction with other brain systems. Neurobiology of Learning and Memory 78 (2002) 539-552
29. McIntyre C.K., Miyashita T., Setlow B., Marjon K.D., Steward O., Guzowski J.F., et al. Memory-influencing intra-basolateral amygdala drug infusions modulate expression of Arc protein in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America 102 (2005) 10718-10723
30. Muller J., Corodimas K.P., Fridel Z., and LeDoux J.E. Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli. Behavioural Neuroscience 111 (1997) 683-691
31. Nader K., Majidishad P., Amorapanth P., and LeDoux J.E. Damage to the lateral and central, but not other, amygdaloid nuclei prevents the acquisition of auditory fear conditioning. Learning & Memory 8 (2001) 156-163
32. Pape H.C. GABAergic neurons: Gate masters of the amygdala, mastered by dopamine. Neuron 48 (2005) 877-879
33. Perez-Villalba A., Teruel-Marti V., Ruiz-Torner A., and Olucha-Bordonau F. The effect of long context exposure on cued conditioning and c-fos expression in the rat forebrain. Behavioural Brain Research 161 (2005) 263-275
34. Phillips R.G., and LeDoux J.E. Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learning & Memory 1 (1994) 34-44
35. Pitkanen A., Pikkarainen M., Nurminen N., and Ylinen A. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Annals of the New York Academy of Sciences 911 (2000) 369-391
36. Quevedo J., Vianna M.R., Roesler R., de-Paris F., Izquierdo I., and Rose S.P. Two time windows of anisomycin-induced amnesia for inhibitory avoidance training in rats: Protection from amnesia by pretraining but not pre-exposure to the task apparatus. Learning & Memory 6 (1999) 600-607
37. Ramirez-Amaya V., Vazdarjanova A., Mikhael D., Rosi S., Worley P.F., and Barnes C.A. Spatial exploration-induced arc mRNA and protein expression: Evidence for selective, network-specific reactivation. The Journal of Neuroscience 25 (2005) 1761-1768
38. Ribeiro S., Gervasoni D., Soares E.S., Zhou Y., Lin S.C., Pantoja J., et al. Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biology 2 (2004) E24
39. Richardson M.P., Strange B.A., and Dolan R.J. Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nature Neuroscience 7 (2004) 278-285
40. Romanski L.M., and LeDoux J.E. Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning. The Journal of Neuroscience 12 (1992) 4501-4509
41. Rose S.P. God's organism? The chick as a model system for memory studies. Learning & Memory 7 (2000) 1-17
42. Schafe G.E., Atkins C.M., Swank M.W., Bauer E.P., Sweatt J.D., and LeDoux J.E. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of pavlovian fear conditioning. The Journal of Neuroscience 20 (2000) 8177-8187
43. Schafe G.E., and LeDoux J.E. Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. The Journal of Neuroscience 20 (2000) RC96
44. Schafe G.E., Nader K., Blair H.T., and LeDoux J.E. Memory consolidation of Pavlovian fear conditioning: A cellular and molecular perspective. Trends in Neurosciences 24 (2001) 540-546
45. Stanciu M., Radulovic J., and Spiess J. Phosphorylated cAMP response element binding protein in the mouse brain after fear conditioning: Relationship to Fos production. Brain Research Molecular Brain Research 94 (2001) 15-24
46. Swank M.W., and Sweatt J.D. Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning. The Journal of Neuroscience 21 (2001) 3383-3391
47. Trifilieff P., Herry C., Vanhoutte P., Caboche J., Desmedt A., Riedel G., et al. Foreground contextual fear memory consolidation requires two independent phases of hippocampal ERK/CREB activation. Learning & Memory 13 (2006) 349-358
48. Weitemier A.Z., and Ryabinin A.E. Subregion-specific differences in hippocampal activity between Delay and Trace fear conditioning: An immunohistochemical analysis. Brain Research 995 (2004) 55-65