Dissecting spatial knowledge from spatial choice by hippocampal NMDA receptor deletion

Nature Neuroscience

Volumn 15, Issue 8, 2012, Pages 1153-1159

  Bannerman, David M ^a   Bus, Thorsten ^b   Taylor, Amy ^a   Sanderson, David J ^a   Schwarz, Inna ^b   Jensen, Vidar ^c   Hvalby, Øivind ^c   Rawlins, J Nicholas P ^a   Seeburg, Peter H ^b   Sprengel, Rolf ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATIVE MEMORY; CONTROLLED STUDY; DENTATE GYRUS; EMBRYO; FEMALE; GENE; GENE DELETION; GLUN1 GENE; GRANULE CELL; GRIN1 GENE; HIPPOCAMPAL CA1 REGION; MALE; MAZE TEST; MOLECULAR BEACON; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPATIAL MEMORY;

ANIMALS; BEHAVIOR, ANIMAL; CARRIER PROTEINS; DENTATE GYRUS; HIPPOCAMPUS; MAZE LEARNING; MEMORY; MICE; NERVE TISSUE PROTEINS; SPACE PERCEPTION;

EID: 84864493623     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3166     Document Type: Article

References (54)

1. Bliss, T.V. & Collingridge, G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39 (1993).
2. Martin, S.J., Grimwood, P.D. & Morris, R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23, 649-711 (2000).
3. Neves, G., Cooke, S.F. & Bliss, T.V. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat. Rev. Neurosci. 9, 65-75 (2008).
4. Morris, R.G., Anderson, E., Lynch, G.S. & Baudry, M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-d-aspartate receptor antagonist, AP5. Nature 319, 774-776 (1986).
5. Bannerman, D.M., Good, M.A., Butcher, S.P., Ramsay, M. & Morris, R.G. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature 378, 182-186 (1995).
6. Saucier, D. & Cain, D.P. Spatial learning without NMDA receptor-dependent long-term potentiation. Nature 378, 186-189 (1995).
7. Tsien, J.Z., Huerta, P.T. & Tonegawa, S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87, 1327-1338 (1996).
8. Tsien, J.Z. et al. Subregion-and cell type-restricted gene knockout in mouse brain. Cell 87, 1317-1326 (1996).
9. Wiltgen, B.J. et al. A role for calcium-permeable AMPA receptors in synaptic plasticity and learning. PLoS ONE 5, e12818 (2010).
10. Hoeffer, C.A. et al. Removal of FKBP12 enhances mTOR-Raptor interactions, LTP, memory, and perseverative/repetitive behavior. Neuron 60, 832-845 (2008).
11. Fukaya, M., Kato, A., Lovett, C., Tonegawa, S. & Watanabe, M. Retention of NMDA receptor NR2 subunits in the lumen of endoplasmic reticulum in targeted NR1 knockout mice. Proc. Natl. Acad. Sci. USA 100, 4855-4860 (2003).
12. Brigman, J.L. et al. Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning. J. Neurosci. 30, 4590-4600 (2010).
13. Rondi-Reig, L. et al. Impaired sequential egocentric and allocentric memories in forebrain-specific-NMDA receptor knock-out mice during a new task dissociating strategies of navigation. J. Neurosci. 26, 4071-4081 (2006).
14. Niewoehner, B. et al. Impaired spatial working memory but spared spatial reference memory following functional loss of NMDA receptors in the dentate gyrus. Eur. J. Neurosci. 25, 837-846 (2007).
15. McHugh, T.J. et al. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317, 94-99 (2007).
16. Murray, A.J. et al. Parvalbumin-positive CA1 interneurons are required for spatial working but not for reference memory. Nat. Neurosci. 14, 297-299 (2011).
17. Dillon, G.M., Qu, X., Marcus, J.N. & Dodart, J.C. Excitotoxic lesions restricted to the dorsal CA1 field of the hippocampus impair spatial memory and extinction learning in C57BL/6 mice. Neurobiol. Learn. Mem. 90, 426-433 (2008).
18. Logue, S.F., Paylor, R. & Wehner, J.M. Hippocampal lesions cause learning deficits in inbred mice in the Morris water maze and conditioned-fear task. Behav. Neurosci. 111, 104-113 (1997).
19. Bannerman, D.M. et al. Double dissociation of function within the hippocampus: a comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behav. Neurosci. 113, 1170-1188 (1999).
20. Moser, M.B., Moser, E.I., Forrest, E., Andersen, P. & Morris, R.G. Spatial learning with a minislab in the dorsal hippocampus. Proc. Natl. Acad. Sci. USA 92, 9697-9701 (1995).
21. Pothuizen, H.H., Zhang, W.N., Jongen-Relo, A.L., Feldon, J. & Yee, B.K. Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: a within-subject, within-task comparison of reference and working spatial memory. Eur. J. Neurosci. 19, 705-712 (2004).
22. von Engelhardt, J. et al. Contribution of hippocampal and extra-hippocampal NR2B-containing NMDA receptors to performance on spatial learning tasks. Neuron 60, 846-860 (2008).
23. Shimshek, D.R. et al. Enhanced odor discrimination and impaired olfactory memory by spatially controlled switch of AMPA receptors. PLoS Biol. 3, e354 (2005).
24. Suchanek, B., Seeburg, P.H. & Sprengel, R. Tissue specific control regions of the N-methyl-D-aspartate receptor subunit NR2C promoter. Biol. Chem. 378, 929-934 (1997).
25. Tashiro, A., Sandler, V.M., Toni, N., Zhao, C. & Gage, F.H. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442, 929-933 (2006).
26. Lyon, L. et al. Fractionation of spatial memory in GRM2/3 (mGlu2/mGlu3) double knockout mice reveals a role for group II metabotropic glutamate receptors at the interface between arousal and cognition. Neuropsychopharmacology 36, 2616-2628 (2011).
27. Morris, R.G., Hagan, J.J. & Rawlins, J.N. Allocentric spatial learning by hippocampectomised rats: a further test of the "spatial mapping" and "working memory" theories of hippocampal function. Q. J. Exp. Psychol. B 38, 365-395 (1986).
28. Uekita, T. & Okaichi, H. Pretraining does not ameliorate spatial learning deficits induced by intrahippocampal infusion of AP5. Behav. Neurosci. 123, 520-526 (2009).
29. Brun, V.H. et al. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296, 2243-2246 (2002).
30. Steffenach, H.A., Witter, M., Moser, M.B. & Moser, E.I. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45, 301-313 (2005).
31. Morris, R.G., Schenk, F., Tweedie, F. & Jarrard, L.E. Ibotenate lesions of hippocampus and/or subiculum: dissociating components of allocentric spatial learning. Eur. J. Neurosci. 2, 1016-1028 (1990).
32. Morris, R.G., Davis, S. & Butcher, S.P. Hippocampal synaptic plasticity and NMDA receptors: a role in information storage? Phil. Trans. R. Soc. Lond. B 329, 187-204 (1990).
33. Vinogradova, O.S. Functional organization of the limbic system in the process of registration of information: facts and hypotheses. in The Hippocampus vol. 2 (eds. Isaacson, R.I. & Pribram, K.H.) 3-69 (Plenum, New York, 1975).
34. Gray, J.A. & McNaughton, N. The Neuropsychology of Anxiety (Oxford Univ. Press, Oxford, 2000).
35. Ploghaus, A. et al. Learning about pain: the neural substrate of the prediction error for aversive events. Proc. Natl. Acad. Sci. USA 97, 9281-9286 (2000).
36. Kumaran, D. & Maguire, E.A. Match mismatch processes underlie human hippocampal responses to associative novelty. J. Neurosci. 27, 8517-8524 (2007).
37. Kumaran, D. & Maguire, E.A. An unexpected sequence of events: mismatch detection in the human hippocampus. PLoS Biol. 4, e424 (2006).
38. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon, Oxford, 1978).
39. O'Keefe, J. Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51, 78-109 (1976).
40. Fyhn, M., Molden, S., Hollup, S., Moser, M.B. & Moser, E. Hippocampal neurons responding to first-time dislocation of a target object. Neuron 35, 555-566 (2002).
41. Honey, R.C., Watt, A. & Good, M. Hippocampal lesions disrupt an associative mismatch process. J. Neurosci. 18, 2226-2230 (1998).
42. Hollerman, J.R. & Schultz, W. Dopamine neurons report an error in the temporal prediction of reward during learning. Nat. Neurosci. 1, 304-309 (1998).
43. Marr, D. Simple memory: a theory for archicortex. Phil. Trans. R. Soc. Lond. B 262, 23-81 (1971).
44. Rolls, E.T. & Treves, A. Neural Networks and Brain Function (Oxford Univ. Press, Oxford, 1998).
45. Sahay, A., Wilson, D.A. & Hen, R. Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70, 582-588 (2011).
46. Lee, G. & Saito, I. Role of nucleotide sequences of loxP spacer region in Cre-mediated recombination. Gene 216, 55-65 (1998).
47. Soriano, P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71 (1999).
48. Tang, W. et al. Faithful expression of multiple proteins via 2A-peptide self-processing: a versatile and reliable method for manipulating brain circuits. J. Neurosci. 29, 8621-8629 (2009).
49. Jerecic, J. et al. Impaired NMDA receptor function in mouse olfactory bulb neurons by tetracycline-sensitive NR1 (N598R) expression. Brain Res. Mol. Brain Res. 94, 96-104 (2001).
50. Krestel, H.E., Mayford, M., Seeburg, P.H. & Sprengel, R. A GFP-equipped bidirectional expression module well suited for monitoring tetracycline-regulated gene expression in mouse. Nucleic Acids Res. 29, E39 (2001).
51. Jensen, V. et al. A juvenile form of postsynaptic hippocampal long-term potentiation in mice deficient for the AMPA receptor subunit GluR-A. J. Physiol. (Lond.) 553, 843-856 (2003).
52. Deacon, R.M., Bannerman, D.M., Kirby, B.P., Croucher, A. & Rawlins, J.N. Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery. Behav. Brain Res. 133, 57-68 (2002).
53. Reisel, D. et al. Spatial memory dissociations in mice lacking GluR1. Nat. Neurosci. 5, 868-873 (2002).
54. Schmitt, W.B., Deacon, R.M., Seeburg, P.H., Rawlins, J.N. & Bannerman, D.M. A within-subjects, within-task demonstration of intact spatial reference memory and impaired spatial working memory in glutamate receptor-A-deficient mice. J. Neurosci. 23, 3953-3959 (2003).