Upstairs/downstairs revisited: Spatial pretraining-induced rescue of normal spatial learning during selective blockade of hippocampal N-methyl-d-aspartate receptors

European Journal of Neuroscience

Volumn 37, Issue 5, 2013, Pages 718-727

  Inglis, Jennifer ^a   Martin, Stephen J ^a   Morris, Richard G M ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cognitive map; Glutamate receptors; Long term potentiation; Pretraining; Spatial learning; Watermaze

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; IN VIVO STUDY; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; NERVE CELL PLASTICITY; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; RAT; SPATIAL LEARNING; SPATIAL MEMORY; TASK PERFORMANCE;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; DENTATE GYRUS; EXCITATORY AMINO ACID ANTAGONISTS; INFUSIONS, INTRAVENTRICULAR; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MEMORY; RATS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84874543548     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12087     Document Type: Article

References (50)

1. Andersen, P., Morris, R.G.M., Amaral, D.G., Bliss, T.V.P. & O'Keefe, J. (2007) The Hippocampus Book. Oxford University Press, Oxford.
2. Bannerman, D.M., Good, M.A., Butcher, S.P., Ramsay, M. & Morris, R.G.M. (1995) Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature, 378, 182-186.
3. Bannerman, D.M., Rawlins, J.N. & Good, M.A. (2006) The drugs don't work-or do they? Pharmacological and transgenic studies of the contribution of NMDA and GluR-A-containing AMPA receptors to hippocampal-dependent memory. Psychopharmacology, 188, 552-566.
4. Bannerman, D.M., Bus, T., Taylor, A., Sanderson, D.J., Schwarz, I., Jensen, V., Hvalby, Ø., Rawlins, J.N., Seeburg, P.H. & Sprengel, R. (2012) Dissecting spatial knowledge from spatial choice by hippocampal NMDA receptor deletion. Nat. Neurosci., 15, 1153-1159.
5. Bast, T., Wilson, I.A., Witter, M.P. & Morris, R.G.M. (2009) From rapid place learning to behavioral performance: a key role for the intermediate hippocampus. PLoS Biol., 7, e1000089.
6. Bliss, T.V.P. & Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361, 31-39.
7. Cain, D.P. (1998) Testing the NMDA, long-term potentiation, and cholinergic hypotheses of spatial learning. Neurosci. Biobehav. Rev., 22, 181-193.
8. Cain, D.P., Saucier, D., Hall, J., Hargreaves, E.L. & Boon, F. (1996) Detailed behavioral analysis of water maze acquisition under APV or CNQX: contribution of sensorimotor disturbances to drug-induced acquisition deficits. Behav. Neurosci., 110, 86-102.
9. Cain, D.P., Saucier, D. & Boon, F. (1997) Testing hypotheses of spatial learning: the role of NMDA receptors and NMDA-mediated long-term potentiation. Behav. Brain Res., 84, 179-193.
10. Clayton, N.S. & Dickinson, A. (1998) Episodic-like memory during cache recovery by scrub jays. Nature, 395, 272-274.
11. Collingridge, G.L., Kehl, S.J. & McLennan, H. (1983) Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J. Physiol., 334, 33-46.
12. Danysz, W., Zajaczkowski, W. & Parsons, C.G. (1995) Modulation of learning processes by ionotropic glutamate receptor ligands. Behav. Pharmacol., 6, 455-474.
13. Davis, S., Butcher, S.P. & Morris, R.G.M. (1992) The NMDA receptor antagonist D-2-amino-5-phosphonopentanoate (D-AP5) impairs spatial learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro. J. Neurosci., 12, 21-34.
14. Day, M., Langston, R. & Morris, R.G.M. (2003) Glutamate-receptor-mediated encoding and retrieval of paired-associate learning. Nature, 424, 205-209.
15. Gallistel, C. (1980) The Organisation of Action: A New Synthesis. Laurence Erlbaum Associates, Hillsdale, USA.
16. Griffiths, D., Dickinson, A. & Clayton, N. (1999) Episodic memory: what can animals remember about their past? Trends Cogn. Sci., 3, 74-80.
17. Gruart, A., Munoz, M.D. & Delgado-Garcia, J.M. (2006) Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J. Neurosci., 26, 1077-1087.
18. Hardt, O., Wang, S.H. & Nader, K. (2009) Storage or retrieval deficit: the yin and yang of amnesia. Learn. Mem., 16, 224-230.
19. Hoh, T., Beiko, J., Boon, F., Weiss, S. & Cain, D.P. (1999) Complex behavioral strategy and reversal learning in the water maze without NMDA receptor-dependent long-term potentiation. J. Neurosci., 19, RC2.
20. Martin, S.J. & Morris, R.G.M. (2002) New life in an old idea: the synaptic plasticity and memory hypothesis revisited. Hippocampus, 12, 609-636.
21. Martin, S.J., Grimwood, P.D. & Morris, R.G.M. (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci., 23, 649-711.
22. Mayford, M. (2012) Navigating uncertain waters. Nat. Neurosci., 15, 1056-1057.
23. Morris, R.G.M. (1981) Spatial localization does not require the presence of local cues. Learn. Motiv., 12, 239-249.
24. Morris, R.G.M. (2006) Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur. J. Neurosci., 23, 2829-2846.
25. Morris, R.G.M., Anderson, E., Lynch, G.S. & Baudry, M. (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature, 319, 774-776.
26. Morris, R.G.M., Inglis, J., Ainge, J.A., Olverman, H.J., Tulloch, J., Dudai, Y. & Kelly, P.A. (2006) Memory reconsolidation: sensitivity of spatial memory to inhibition of protein synthesis in dorsal hippocampus during encoding and retrieval. Neuron, 50, 479-489.
27. Morris, R.G.M., Steele, R.J., Bell, J.E. & Martin, S.J. (2012) N-methyl-D-aspartate receptors, learning and memory: chronic intraventricular infusion of the NMDA receptor antagonist D-AP5 interacts directly with the neural mechanisms of spatial learning. Eur. J. Neurosci., in press.
28. Moser, M.B. & Moser, E.I. (1998) Functional differentiation in the hippocampus. Hippocampus, 8, 608-619.
29. Nakazawa, K., McHugh, T.J., Wilson, M.A. & Tonegawa, S. (2004) NMDA receptors, place cells and hippocampal spatial memory. Nat. Rev. Neurosci., 5, 361-372.
30. O'Keefe, J. & Nadel, L. (1978) The Hippocampus as a Cognitive Map. Clarendon Press, Oxford.
31. Olton, D.S., Becker, J.T. & Handelmann, G.E. (1979) Hippocampus, space, and memory. Brain Behav. Sci., 2, 313-365.
32. Reisel, D., Bannerman, D.M., Schmitt, W.B., Deacon, R.M.J., Flint, J., Borchardt, T., Seeburg, P.H. & Rawlins, J.N.P. (2002) Spatial memory dissociations in mice lacking GluR1. Nat. Neurosci., 5, 868-873.
33. Riedel, G., Platt, B. & Micheau, J. (2003) Glutamate receptor function in learning and memory. Behav. Brain Res., 140, 1-47.
34. Rioult-Pedotti, M.S., Friedman, D. & Donoghue, J.P. (2000) Learning-induced LTP in neocortex. Science, 290, 533-536.
35. Rumpel, S., LeDoux, J., Zador, A. & Malinow, R. (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science, 308, 83-88.
36. Sakimura, K., Kutsuwada, T., Ito, I., Manabe, T., Takayama, C., Kushiya, E., Yagi, T., Aizawa, S., Inoue, Y., Sugiyama, H. & Mishina, M. (1995) Reduced hippocampal long-term potentiation and spatial learning of mice defective in the E1 subunit of the NMDA receptor channel. Nature, 373, 151-155.
37. Sanders, M.J. & Fanselow, M.S. (2003) Pre-training prevents context fear conditioning deficits produced by hippocampal NMDA receptor blockade. Neurobiol. Learn. Mem., 80, 123-129.
38. Saucier, D. & Cain, D.P. (1995) Spatial learning without NMDA receptor dependent long-term potentiation. Nature, 378, 186-189.
39. Saucier, D., Hargreaves, E.L., Boon, F., Vanderwolf, C.H. & Cain, D.P. (1996) Detailed behavioural analysis of water maze acquisition under systemic NMDA or muscarinic antagonism: nonspatial pretraning eliminates spatial learning deficits. Behav. Neurosci., 110, 103-116.
40. Spooner, R.I., Thomson, A., Hall, J., Morris, R.G.M. & Salter, S.H. (1994) The Atlantis platform: a new design and further developments of Buresova's on-demand platform for the water maze. Learn. Mem., 1, 203-211.
41. Steele, R.J. & Morris, R.G.M. (1999) Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5. Hippocampus, 9, 118-136.
42. Tse, D., Langston, R.F., Kakeyama, M., Bethus, I., Spooner, P.A., Wood, E.R., Witter, M.P. & Morris, R.G. (2007) Schemas and memory consolidation. Science, 316, 76-82.
43. Tse, D., Langston, R.F., Bethus, I., Wood, E.R., Witter, M.P. & Morris, R.G.M. (2008) Does assimilation into schemas involve systems or cellular consolidation? It's not just time. Neurobiol. Learn. Mem., 89, 361-365.
44. Tsien, J.Z., Chen, D.F., Gerber, D., Tom, C., Mercer, E.H., Anderson, D.J., Mayford, M., Kandel, E.R. & Tonegawa, S. (1996) Subregion- and cell type-restricted gene knockout in mouse brain. Cell, 87, 1317-1326.
45. Uekita, T. & Okaichi, H. (2009) Pretraining does not ameliorate spatial learning deficits induced by intrahippocampal infusion of AP5. Behav. Neurosci., 123, 520-526.
46. Von Engelhardt, J., Doganci, B., Jensen, V., Hvalby, Ø., Göngrich, C., Taylor, A., Barkus, C., Sanderson, D.J., Rawlins, J.N., Seeburg, P.H., Bannerman, D.M. & Monyer, H. (2008) Contribution of hippocampal and extra-hippocampal NR2B-containing NMDA receptors to performance on spatial learning tasks. Neuron, 60, 846-860.
47. Wang, S.H., Finnie, P.S., Hardt, O. & Nader, K. (2012) Dorsal hippocampus is necessary for novel learning but sufficient for subsequent similar learning. Hippocampus, 22, 2157-2170.
48. Whishaw, I.Q. (1998) Place learning in hippocampal rats and the path integration hypothesis. Neurosci. Biobehav. Rev., 22, 209-220.
49. Whitlock, J.R., Heynen, A.J., Shuler, M.G. & Bear, M.F. (2006) Learning induces long-term potentiation in the hippocampus. Science, 313, 1093-1097.
50. Wiltgen, B.J., Zhou, M., Cai, Y., Balaji, J., Karlsson, M.G., Parivash, S.N., Li, W. & Silva, A.J. (2010) The hippocampus plays a selective role in the retrieval of detailed contextual memories. Curr. Biol., 20, 1336-1344.