Spatial memory in the Morris water maze and activation of cyclic AMP response element-binding (CREB) protein within the mouse hippocampus

Learning and Memory

Volumn 15, Issue 12, 2008, Pages 885-894

  Porte, Yves ^a   Buhot, Marie Christine ^a   Mons, Nicole E ^a  

^a UMR 5287   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; ELECTROENCEPHALOGRAM; ENZYME ACTIVATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LEARNING; LIMBIC CORTEX; MALE; MAZE TEST; MENTAL TASK; MORRIS WATER MAZE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REFERENCE MEMORY; SPATIAL MEMORY; TRAINING;

ANIMALS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EARLY GROWTH RESPONSE PROTEIN 1; GENE EXPRESSION REGULATION; HIPPOCAMPUS; LINEAR MODELS; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; SPACE PERCEPTION; TIME FACTORS;

EID: 57349198937     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.1094208     Document Type: Article

References (68)

1. Abraham, W.C., Logan, B., Greenwood, J.M., and Dragunow, M. 2002. Induction and experience-dependent consolidation of stable long-term potentiation lasting months in the hippocampus. J. Neurosci. 22: 9626-9634.
2. Balschun, D., Wolfer, D.P., Gass, P., Mantamadiotis, T., Welzl, H., Schutz, G., Frey, J.U., and Lipp, H.P. 2003. Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory? J. Neurosci. 23: 6304-6314.
3. Bekinschtein, P., Cammarota, M., Igaz, L.M., Bevilaqua, L.R., Izquierdo, I., and Medina, J.H. 2007. Persistence of long-term memory storage requires a late protein synthesis- and BDNF-dependent phase in the hippocampus. Neuron 53: 261-277.
4. Bernabeu, R., Bevilaqua, L., Ardenghi, P., Bromberg, E., Schmitz, P., Bianchin, M., Izquierdo, I., and Medina, J.H. 1997. Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proc. Natl. Acad. Sci. 94: 7041-7046.
5. Bilang-Bleuel, A., Rech, J., De Carli, S., Holsboer, F., and Reul, J.M. 2002. Forced swimming evokes a biphasic response in CREB phosphorylation in extrahypothalamic limbic and neocortical brain structures in the rat. Eur. J. Neurosci. 15: 1048-1060.
6. Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G., and Silva, A.J. 1994. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79: 59-68.
7. Bozon, B., Davis, S., and Laroche, S. 2003a. A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40: 695-701.
8. Bozon, B., Kelly, A., Josselyn, S.A., Silva, A.J., Davis, S., and Laroche, S. 2003b. MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358: 805-814.
9. Brightwell, J.J., Smith, C.A., Neve, R.L., and Colombo, P.J. 2007. Long-term memory for place learning is facilitated by expression of cAMP response element-binding protein in the dorsal hippocampus. Learn. Mem. 14: 195-199.
10. Brightwell, J.J., Smith, C.A., Neve, R.L., and Colombo, P.J. 2008. Transfection of mutant CREB in the striatum, but not the hippocampus, impairs long-term memory for response learning. Neurobiol. Learn. Mem. 89: 27-35.
11. Broadbent, N.J., Squire, L.R., and Clark, R.E. 2007. Rats depend on habit memory for discrimination learning and retention. Learn. Mem. 14: 145-151.
12. Brun, V.H., Otnass, M.K., Molden, S., Steffenach, H.A., Witter, M.P., Moser, M.B., and Moser, E.I. 2002. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296: 2243-2246.
13. Cammarota, M., Bevilaqua, L.R., Ardenghi, P., Paratcha, G., Levi de Stein, M., Izquierdo, I., and Medina, J.H. 2000. 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. Brain Res. Mol. Brain Res. 76: 36-46.
14. Cammarota, M., Bevilaqua, L.R., Kohler, C., Medina, J.H., and Izquierdo, I. 2005. Learning twice is different from learning once and from learning more. Neuroscience 132: 273-279.
15. Cohen-Matsliah, S.I., Brosh, I., Rosenblum, K., and Barkai, E. 2007. A novel role for extracellular signal-regulated kinase in maintaining long-term memory-relevant excitability changes. J. Neurosci. 27: 12584-12589.
16. Colombo, P.J., Brightwell, J.J., and Countryman, R.A. 2003. Cognitive strategy-specific increases in phosphorylated cAMP response element-binding protein and c-Fos in the hippocampus and dorsal striatum. J. Neurosci. 23: 3547-3554.
17. Countryman, R.A., Orlowski, J.D., Brightwell, J.J., Oskowitz, A.Z., and Colombo, P.J. 2005. CREB phosphorylation and c-Fos expression in the hippocampus of rats during acquisition and recall of a socially transmitted food preference. Hippocampus 15: 56-67.
18. Davis, H.P. and Squire, L.R. 1984. Protein synthesis and memory: A review. Psychol. Bull. 96: 518-559.
19. Desmedt, A., Hazvi, S., and Dudai, Y. 2003. Differential pattern of cAMP response element-binding protein activation in the rat brain after conditioned aversion as a function of the associative process engaged: Taste versus context association. J. Neurosci. 23: 6102-6110.
20. Dudai, Y. 1996. Consolidation: Fragility on the road to the engram. Neuron 17: 367-370.
21. Florian, C., Mons, N., and Roullet, P. 2006. CREB antisense oligodeoxynucleotide administration into the dorsal hippocampal CA3 region impairs long- but not short-term spatial memory in mice. Learn. Mem. 13: 465-472.
22. Franklin, B.J. and Paxinos, G. 1997. The mouse brain in stereotaxic coordinates. Academic Press, San Diego, CA.
23. Gill, K.M., Bernstein, I.L., and Mizumori, S.J. 2007. Immediate early gene activation in hippocampus and dorsal striatum: Effects of explicit place and response training. Neurobiol. Learn. Mem. 87: 583-596.
24. Goldbart, A., Row, B.W., Kheirandish, L., Schurr, A., Gozal, E., Guo, S.Z., Payne, R.S., Cheng, Z., Brittian, K.R., and Gozal, D. 2003. Intermittent hypoxic exposure during light phase induces changes in cAMP response element binding protein activity in the rat CA1 hippocampal region: Water maze performance correlates. Neuroscience 122: 585-590.
25. Grunbaum, L. and Muller, U. 1998. Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee. J. Neurosci. 18: 4384-4392.
26. 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.
27. Guzowski, J.F., Setlow, B., Wagner, E.K., and McGaugh, J.L. 2001. Experience-dependent gene expression in the rat hippocampus after spatial learning: A comparison of the immediate-early genes Arc, c-fos, and zif268. J. Neurosci. 21: 5089-5098.
28. Guzowski, J.F., Miyashita, T., Chawla, M.K., Sanderson, J., Maes, L.I., Houston, F.P., Lipa, P., McNaughton, B.L., Worley, P.F., and Barnes, C.A. 2006. Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. Proc. Natl. Acad. Sci. 103: 1077-1082.
29. Impey, S., Smith, D.M., Obrietan, K., Donahue, R., Wade, C., and Storm, D.R. 1998. Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat. Neurosci. 1: 595-601.
30. Izquierdo, I. and Medina, J.H. 1997. Memory formation: The sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 68: 285-316.
31. Izquierdo, L.A., Viola, H., Barros, D.M., Alonso, M., Vianna, M.R., Furman, M., Levi de Stein, M., Szapiro, G., Rodrigues, C. , Choi, H., et al. 2001. Novelty enhances retrieval: Molecular mechanisms involved in rat hippocampus. Eur. J. Neurosci. 13: 1464-1467.
32. Kesner, R.P., Lee, I., and Gilbert, P. 2004. A behavioral assessment of hippocampal function based on a subregional analysis. Rev. Neurosci. 15: 333-351.
33. 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.
34. Kogan, I. and Richter-Levin, G. 2008. Activation pattern of the limbic system following spatial learning under stress. Eur. J. Neurosci. 27: 715-722.
35. Malleret, G., Hen, R., Guillou, J.L., Segu, L., and Buhot, M.C. 1999. 5-HT1B receptor knock-out mice exhibit increased exploratory activity and enhanced spatial memory performance in the Morris water maze. J. Neurosci. 19: 6157-6168.
36. Martel, G., Millard, A., Jaffard, R., and Guillou, J.L. 2006. Stimulation of hippocampal adenylyl cyclase activity dissociates memory consolidation processes for response and place learning. Learn. Mem. 13: 342-348.
37. Martel, G., Blanchard, J., Mons, N., Gastambide, F., Micheau, J., and Guillou, J.L. 2007. Dynamic interplays between memory systems depend on practice: The hippocampus is not always the first to provide solution. Neuroscience 150: 743-753.
38. Matthies, H. 1989. In search of cellular mechanisms of memory. Prog. Neurobiol. 32: 277-349.
39. McGaugh, J.L. 1966. Time-dependent processes in memory storage. Science 153: 1351-1358.
40. McGaugh, J.L. 2000. Memory - a century of consolidation. Science 287: 248-251.
41. Miyashita, T., Kubik, S., Lewandowski, G., and Guzowski, J.F. 2008. Networks of neurons, networks of genes: An integrated view of memory consolidation. Neurobiol. Learn. Mem. 89: 269-284.
42. Mizuno, M., Yamada, K., Maekawa, N., Saito, K., Seishima, M., and Nabeshima, T. 2002. CREB phosphorylation as a molecular marker of memory processing in the hippocampus for spatial learning. Behav. Brain Res. 133: 135-141.
43. Moncada, D. and Viola, H. 2006. Phosphorylation state of CREB in the rat hippocampus: A molecular switch between spatial novelty and spatial familiarity? Neurobiol. Learn. Mem. 86: 9-18
44. Morris, R. 1984. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11: 47-60.
45. Morris, R.G., Garrud, P., Rawlins, J.N., and O'Keefe, J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297: 681-683.
46. Muller, U. 2000. Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27: 159-168.
47. Packard, M.G. and McGaugh, J.L. 1992. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: Further evidence for multiple memory systems. Behav. Neurosci. 106: 439-446.
48. Packard, M.G. and Teather, L.A. 1997. Double dissociation of hippocampal and dorsal-striatal memory systems by posttraining intracerebral injections of 2-amino-5-phosphonopentanoic acid. Behav. Neurosci. 111: 543-551.
49. Packard, M.G., Hirsh, R., and White, N.M. 1989. Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: Evidence for multiple memory systems. J. Neurosci. 9: 1465-1472.
50. Packard, M.G., Cahill, L., and McGaugh, J.L. 1994. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc. Natl. Acad. Sci. 91: 8477-8481.
51. Pittenger, C., Huang, Y.Y., Paletzki, R.F., Bourtchuladze, R., Scanlin, H., Vronskaya, S., and Kandel, E.R. 2002. Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 34: 447-462.
52. Poirier, G.L., Amin, E., and Aggleton, J.P. 2008. Qualitatively different hippocampal subfield engagement emerges with mastery of a spatial memory task by rats. J. Neurosci. 28: 1034-1045.
53. Porte, Y., Buhot, M.C., and Mons, N. 2008. Alteration of CREB phosphorylation and spatial memory deficits in aged 129T2/Sv mice. Neurobiol. Aging 29: 1533-1546.
54. Ramirez-Amaya, V., Vazdarjanova, A., Mikhael, D., Rosi, S., Worley, P.F., and Barnes, C.A. 2005. Spatial exploration-induced Arc mRNA and protein expression: Evidence for selective, network-specific reactivation. J. Neurosci. 25: 1761-1768.
55. Remondes, M. and Schuman, E.M. 2004. Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 431: 699-703.
56. Roozendaal, B., Hahn, E.L., Nathan, S.V., de Quervain, D.J., and McGaugh, J.L. 2004. Glucocorticoid effects on memory retrieval require concurrent noradrenergic activity in the hippocampus and basolateral amygdala. J. Neurosci. 24: 8161-8169.
57. Schulz, S., Siemer, H., Krug, M., and Hollt, V. 1999. Direct evidence for biphasic cAMP responsive element-binding protein phosphorylation during long-term potentiation in the rat dentate gyrus in vivo. J. Neurosci. 19: 5683-5692.
58. Silva, A.J., Kogan, J.H., Frankland, P.W., and Kida, S. 1998. CREB and memory. Annu. Rev. Neurosci. 21: 127-148.
59. Stanciu, M., Radulovic, J., and Spiess, J. 2001. Phosphorylated cAMP response element binding protein in the mouse brain after fear conditioning: Relationship to Fos production. Brain Res. Mol. Brain Res. 94: 15-24.
60. Sutherland, R.J., Weisend, M.P., Mumby, D., Astur, R.S., Hanlon, F.M., Koerner, A., Thomas, M.J., Wu, Y., Moses, S.N., Cole, C., et al. 2001. Retrograde amnesia after hippocampal damage: Recent vs. remote memories in two tasks. Hippocampus 11: 27-42.
61. Swank, M.W. and Sweatt, J.D. 2001. Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning. J. Neurosci. 21: 3383-3391.
62. 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.
63. Taubenfeld, S.M., Wiig, K.A., Monti, B., Dolan, B., Pollonini, G., and Alberini, C.M. 2001. 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.
64. Teather, L.A., Packard, M.G., Smith, D.E., Ellis-Behnke, R.G., and Bazan, N.G. 2005. Differential induction of c-Jun and Fos-like proteins in rat hippocampus and dorsal striatum after training in two water maze tasks. Neurobiol. Learn. Mem. 84: 75-84.
65. Trifilieff, P., Herry, C., Vanhoutte, P., Caboche, J., Desmedt, A., Riedel, G., Mons, N., and Micheau, J. 2006. Foreground contextual fear memory consolidation requires two independent phases of hippocampal ERK/CREB activation. Learn. Mem. 13: 349-358.
66. Trifilieff, P., Calandreau, L., Herry, C., Mons, N., and Micheau, J. 2007. Biphasic ERK1/2 activation in both the hippocampus and amygdala may reveal a system consolidation of contextual fear memory. Neurobiol. Learn. Mem. 88: 424-434.
67. Vianna, M.R., Alonso, M., Viola, H., Quevedo, J., de Paris, F., Furman, M., de Stein, M.L., Medina, J.H., and Izquierdo, I. 2000. Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learn. Mem. 7: 333-340.
68. Zhang, J.J., Okutani, F., Inoue, S., and Kaba, H. 2003. Activation of the cyclic AMP response element-binding protein signaling pathway in the olfactory bulb is required for the acquisition of olfactory aversive learning in young rats. Neuroscience 117: 707-713.