Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze

Neuropharmacology

Volumn 64, Issue , 2013, Pages 65-73

  Dong, Zhifang ^a   Bai, Yanrui ^a   Wu, Xiaoyan ^a   Li, Hongjie ^a   Gong, Bo ^b   Howland, John G ^c   Huang, Yan ^a   He, Wenting ^a   Li, Tingyu ^a   Wang, Yu Tian ^a,b  

^a CHILDREN S HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

AMPA receptor; Hippocampus; Interference peptide; NMDA receptor; Stress

Indexed keywords

4 BENZYL ALPHA (4 HYDROXYPHENYL) BETA METHYL 1 PIPERIDINEPROPANOL; AMPA RECEPTOR; PEPTIDE;

ADULT ANIMAL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; ENDOCYTOSIS; HIPPOCAMPAL CA1 REGION; IN VIVO STUDY; LEARNING; LONG TERM DEPRESSION; MALE; MAZE TEST; MORRIS WATER MAZE; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL LEARNING; STRESS;

ANIMALS; BEHAVIOR, ANIMAL; CA1 REGION, HIPPOCAMPAL; EXCITATORY AMINO ACID ANTAGONISTS; HIPPOCAMPUS; INFUSIONS, INTRAVENTRICULAR; INJECTIONS, INTRAPERITONEAL; LONG-TERM SYNAPTIC DEPRESSION; MALE; MAZE LEARNING; NEURONS; NOOTROPIC AGENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; RETENTION (PSYCHOLOGY); REVERSAL LEARNING; SPATIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 84866426198     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.06.027     Document Type: Article

References (50)

1. G. Ahmadian, W. Ju, L. Liu, M. Wyszynski, S.H. Lee, A.W. Dunah, C. Taghibiglou, Y. Wang, J. Lu, T.P. Wong, M. Sheng, and Y.T. Wang Tyrosine phosphorylation of GluR2 is required for insulin-stimulated AMPA receptor endocytosis and LTD EMBO J. 23 2004 1040 1050
2. T.E. Bartlett, N.J. Bannister, V.J. Collett, S.L. Dargan, P.V. Massey, Z.A. Bortolotto, S.M. Fitzjohn, Z.I. Bashir, G.L. Collingridge, and D. Lodge Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-week old rat hippocampus Neuropharmacology 52 2007 60 70
3. T.V. Bliss, and G.L. Collingridge A synaptic model of memory: long-term potentiation in the hippocampus Nature 361 1993 31 39
4. K. Brebner, T.P. Wong, L. Liu, Y. Liu, P. Campsall, S. Gray, L. Phelps, A.G. Phillips, and Y.T. Wang Nucleus accumbens long-term depression and the expression of behavioral sensitization Science 310 2005 1340 1343
5. D.S. Bredt, and R.A. Nicoll AMPA receptor trafficking at excitatory synapses Neuron 40 2003 361 379
6. B.N. Cazakoff, and J.G. Howland Acute stress disrupts paired pulse facilitation and long-term potentiation in rat dorsal hippocampus through activation of glucocorticoid receptors Hippocampus 20 2010 1327 1331
7. G.L. Collingridge, J.T. Isaac, and Y.T. Wang Receptor trafficking and synaptic plasticity Nat. Rev. Neurosci. 5 2004 952 962
8. G.L. Collingridge, S. Peineau, J.G. Howland, and Y.T. Wang Long-term depression in the CNS Nat. Rev. Neurosci. 11 2010 459 473
9. D.M. Diamond, M. Fleshner, and G.M. Rose Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats Behav. Brain Res. 62 1994 1 9
10. D.M. Diamond, M. Fleshner, N. Ingersoll, and G.M. Rose Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function Behav. Neurosci. 110 1996 661 672
11. D.M. Diamond, C.R. Park, K.L. Heman, and G.M. Rose Exposing rats to a predator impairs spatial working memory in the radial arm water maze Hippocampus 9 1999 542 552
12. Z. Dong, H. Han, M. Wang, L. Xu, W. Hao, and J. Cao Morphine conditioned place preference depends on glucocorticoid receptors in both hippocampus and nucleus accumbens Hippocampus 16 2006 809 813
13. Z. Dong, W. Zhong, M. Tian, H. Han, J. Cao, T. Xu, J. Luo, and L. Xu Stress evoked by opiate withdrawal facilitates hippocampal LTP in vivo Hippocampus 16 2006 1017 1025
14. S.M. Dudek, and M.F. Bear Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-d-aspartate receptor blockade Proc. Natl. Acad. Sci. U. S. A. 89 1992 4363 4367
15. S. Duffy, V. Labrie, and J.C. Roder D-serine augments NMDA-NR2B receptor-dependent hippocampal long-term depression and spatial reversal learning Neuropsychopharmacology 33 2008 1004 1018
16. C.J. Fox, K.I. Russell, Y.T. Wang, and B.R. Christie Contribution of NR2A and NR2B NMDA subunits to bidirectional synaptic plasticity in the hippocampus in vivo Hippocampus 16 2006 907 915
17. C.J. Fox, K. Russell, A.K. Titterness, Y.T. Wang, and B.R. Christie Tyrosine phosphorylation of the GluR2 subunit is required for long-term depression of synaptic efficacy in young animals in vivo Hippocampus 17 2007 600 605
18. Y. Ge, Z. Dong, R.C. Bagot, J.G. Howland, A.G. Phillips, T.P. Wong, and Y.T. Wang Hippocampal long-term depression is required for the consolidation of spatial memory Proc. Natl. Acad. Sci. U. S. A. 107 2010 16697 16702
19. C. Graybeal, M. Feyder, E. Schulman, L.M. Saksida, T.J. Bussey, J.L. Brigman, and A. Holmes Paradoxical reversal learning enhancement by stress or prefrontal cortical damage: rescue with BDNF Nat. Neurosci. 14 2011 1507 1509
20. A. Gruart, M.D. Munoz, and J.M. Delgado-Garcia Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice J. Neurosci. 26 2006 1077 1087
21. A.W. Hendricson, C.L. Miao, M.J. Lippmann, and R.A. Morrisett Ifenprodil and ethanol enhance NMDA receptor-dependent long-term depression J. Pharmacol. Exp. Ther. 301 2002 938 944
22. Y. Izumi, Y.P. Auberson, and C.F. Zorumski Zinc modulates bidirectional hippocampal plasticity by effects on NMDA receptors J. Neurosci. 26 2006 7181 7188
23. A. Kemp, and D. Manahan-Vaughan Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition Proc. Natl. Acad. Sci. U. S. A. 101 2004 8192 8197
24. A. Kemp, and D. Manahan-Vaughan Passive spatial perception facilitates the expression of persistent hippocampal long-term depression Cereb. Cortex 2011 [Epub ahead of print]
25. J.J. Kim, M.R. Foy, and R.F. Thompson Behavioral stress modifies hippocampal plasticity through N-methyl-d-aspartate receptor activation Proc. Natl. Acad. Sci. U. S. A. 93 1996 4750 4753
26. J.J. Kim, J.W. Koo, H.J. Lee, and J.S. Han Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory J. Neurosci. 25 2005 1532 1539
27. L. Liu, T.P. Wong, M.F. Pozza, K. Lingenhoehl, Y. Wang, M. Sheng, Y.P. Auberson, and Y.T. Wang Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity Science 304 2004 1021 1024
28. C. Luscher, H. Xia, E.C. Beattie, R.C. Carroll, M. von Zastrow, R.C. Malenka, and R.A. Nicoll Role of AMPA receptor cycling in synaptic transmission and plasticity Neuron 24 1999 649 658
29. M.A. Lynch Long-term potentiation and memory Physiol. Rev. 84 2004 87 136
30. R.C. Malenka, and M.F. Bear LTP and LTD: an embarrassment of riches Neuron 44 2004 5 21
31. R.C. Malenka, and R.A. Nicoll Long-term potentiation-a decade of progress? Science 285 1999 1870 1874
32. R. Malinow, and R.C. Malenka AMPA receptor trafficking and synaptic plasticity Annu. Rev. Neurosci. 25 2002 103 126
33. H.Y. Man, J.W. Lin, W.H. Ju, G. Ahmadian, L. Liu, L.E. Becker, M. Sheng, and Y.T. Wang Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization Neuron 25 2000 649 662
34. D. Manahan-Vaughan, and K.H. Braunewell Novelty acquisition is associated with induction of hippocampal long-term depression Proc. Natl. Acad. Sci. U. S. A. 96 1999 8739 8744
35. S.J. Martin, P.D. Grimwood, and R.G. Morris Synaptic plasticity and memory: an evaluation of the hypothesis Annu. Rev. Neurosci. 23 2000 649 711
36. W. Morishita, W. Lu, G.B. Smith, R.A. Nicoll, M.F. Bear, and R.C. Malenka Activation of NR2B-containing NMDA receptors is not required for NMDA receptor-dependent long-term depression Neuropharmacology 52 2007 71 76
37. R.M. Mulkey, and R.C. Malenka Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus Neuron 9 1992 967 975
38. R.E. Nicholls, J.M. Alarcon, G. Malleret, R.C. Carroll, M. Grody, S. Vronskaya, and E.R. Kandel Transgenic mice lacking NMDAR-dependent LTD exhibit deficits in behavioral flexibility Neuron 58 2008 104 117
39. P.K. Stanton LTD, LTP, and the sliding threshold for long-term synaptic plasticity Hippocampus 6 1996 35 42
40. U. Staubli, and J. Scafidi Studies on long-term depression in area CA1 of the anesthetized and freely moving rat J. Neurosci. 17 1997 4820 4828
41. T. Tsumoto Long-term depression in cerebral cortex: a possible substrate of "forgetting" that should not be forgotten Neurosci. Res. 16 1993 263 270
42. M. Wang, Y. Yang, Z. Dong, J. Cao, and L. Xu NR2B-containing N-methyl-d-aspartate subtype glutamate receptors regulate the acute stress effect on hippocampal long-term potentiation/long-term depression in vivo Neuroreport 17 2006 1343 1346
43. J.R. Whitlock, A.J. Heynen, M.G. Shuler, and M.F. Bear Learning induces long-term potentiation in the hippocampus Science 313 2006 1093 1097
44. T.P. Wong, J.G. Howland, J.M. Robillard, Y. Ge, W. Yu, A.K. Titterness, K. Brebner, L. Liu, J. Weinberg, B.R. Christie, A.G. Phillips, and Y.T. Wang Hippocampal long-term depression mediates acute stress-induced spatial memory retrieval impairment Proc. Natl. Acad. Sci. U. S. A. 104 2007 11471 11476
45. N.H. Woo, H.K. Teng, C.J. Siao, C. Chiaruttini, P.T. Pang, T.A. Milner, B.L. Hempstead, and B. Lu Activation of p75NTR by proBDNF facilitates hippocampal long-term depression Nat. Neurosci. 8 2005 1069 1077
46. J.C. Woodson, D. Macintosh, M. Fleshner, and D.M. Diamond Emotion-induced amnesia in rats: working memory-specific impairment, corticosterone-memory correlation, and fear versus arousal effects on memory Learn. Mem. 10 2003 326 336
47. L. Xu, R. Anwyl, and M.J. Rowan Behavioural stress facilitates the induction of long-term depression in the hippocampus Nature 387 1997 497 500
48. L. Xu, R. Anwyl, and M.J. Rowan Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus Nature 394 1998 891 894
49. L. Xu, C. Holscher, R. Anwyl, and M.J. Rowan Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress Proc. Natl. Acad. Sci. U. S. A. 95 1998 3204 3208
50. C.H. Yang, C.C. Huang, and K.S. Hsu Behavioral stress enhances hippocampal CA1 long-term depression through the blockade of the glutamate uptake J. Neurosci. 25 2005 4288 4293