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Science 11 June 1999:
Vol. 284. no. 5421, pp. 1805 - 1811
DOI: 10.1126/science.284.5421.1805
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Research Articles

Importance of AMPA Receptors for Hippocampal Synaptic Plasticity But Not for Spatial Learning

Daniel Zamanillo, 1* Rolf Sprengel, 1dagger Øivind Hvalby, 2 Vidar Jensen, 2 Nail Burnashev, 1 Andrei Rozov, 1 Katharina M. M. Kaiser, 1 Helmut J. Köster, 1 Thilo Borchardt, 1 Paul Worley, 3 Joachim Lübke, 4 Michael Frotscher, 4 Peter H. Kelly, 5 Bernd Sommer, 5 Per Andersen, 2 Peter H. Seeburg, 1 Bert Sakmann 1

Gene-targeted mice lacking the L-alpha -amino-3-hydroxy-5-methylisoxazole-4-propionate (AMPA) receptor subunit GluR-A exhibited normal development, life expectancy, and fine structure of neuronal dendrites and synapses. In hippocampal CA1 pyramidal neurons, GluR-A-/- mice showed a reduction in functional AMPA receptors, with the remaining receptors preferentially targeted to synapses. Thus, the CA1 soma-patch currents were strongly reduced, but glutamatergic synaptic currents were unaltered; and evoked dendritic and spinous Ca2+ transients, Ca2+-dependent gene activation, and hippocampal field potentials were as in the wild type. In adult GluR-A-/- mice, associative long-term potentiation (LTP) was absent in CA3 to CA1 synapses, but spatial learning in the water maze was not impaired. The results suggest that CA1 hippocampal LTP is controlled by the number or subunit composition of AMPA receptors and show a dichotomy between LTP in CA1 and acquisition of spatial memory.

1 Departments of Molecular Neuroscience and Cell Physiology, Max-Planck Institute for Medical Research, Jahnstrasse 29, 69120 Heidelberg, Germany.
2 Department of Physiology, Institute of Basic Medical Sciences, University of Oslo, Norway.
3 Departments of Neuroscience and Neurology, Johns Hopkins University, School of Medicine, Baltimore MD 21205, USA.
4 Department of Anatomy, University of Freiburg, Albertstrasse 17, D-79104 Freiburg, Germany.
5 NS Research Novartis Pharma AG, Basel, Switzerland.
*   Present address: Laboratorios Doctor Esteve, Avenida Mare de Deu de Montserrat 221, 08041 Barcelona, Spain.

dagger    To whom correspondence should be addressed. E-mail: sprengel{at}mpimf-heidelberg.mpg.de

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Science 292, 2501-2504
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Morphine-Induced Dependence and Sensitization Are Altered in Mice Deficient in AMPA-Type Glutamate Receptor-A Subunits.
O. Y. Vekovischeva, D. Zamanillo, O. Echenko, T. Seppala, M. Uusi-Oukari, A. Honkanen, P. H. Seeburg, R. Sprengel, and E. R. Korpi (2001)
J. Neurosci. 21, 4451-4459
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Impaired Synaptic Plasticity and cAMP Response Element-Binding Protein Activation in Ca2+/Calmodulin-Dependent Protein Kinase Type IV/Gr-Deficient Mice.
N. Ho, J. A. Liauw, F. Blaeser, F. Wei, S. Hanissian, L. M. Muglia, D. F. Wozniak, A. Nardi, K. L. Arvin, D. M. Holtzman, et al. (2000)
J. Neurosci. 20, 6459-6472
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Protein Phosphatase-1 Regulation in the Induction of Long-Term Potentiation: Heterogeneous Molecular Mechanisms.
P. B. Allen, O. Hvalby, V. Jensen, M. L. Errington, M. Ramsay, F. A. Chaudhry, T. V. P. Bliss, J. Storm-Mathisen, R. G. M. Morris, P. Andersen, et al. (2000)
J. Neurosci. 20, 3537-3543
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Caspase-Mediated Degradation of AMPA Receptor Subunits: A Mechanism for Preventing Excitotoxic Necrosis and Ensuring Apoptosis.
G. W. Glazner, S. L. Chan, C. Lu, and M. P. Mattson (2000)
J. Neurosci. 20, 3641-3649
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Dissection of behavior and psychiatric disorders using the mouse as a model.
L. Tarantino and M. Bucan (2000)
Hum. Mol. Genet. 9, 953-965
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NMDA Receptor-Mediated Subthreshold Ca2+ Signals in Spines of Hippocampal Neurons.
Y. Kovalchuk, J. Eilers, J. Lisman, and A. Konnerth (2000)
J. Neurosci. 20, 1791-1799
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Of Mice and Memory.
E. B. Han and C. F. Stevens (1999)
Learn. Mem. 6, 539-541
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Silent Synapses in Neural Plasticity: Current Evidence.
H. L. Atwood and J. M. Wojtowicz (1999)
Learn. Mem. 6, 542-571
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Unilateral GluR2(B) Hippocampal Knockdown: A Novel Partial Seizure Model in the Developing Rat.
L. K. Friedman and A. R. Koudinov (1999)
J. Neurosci. 19, 9412-9425
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Long-Term Potentiation--A Decade of Progress?.
R. C. Malenka and a. R. A. Nicoll (1999)
Science 285, 1870-1874
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Toward a Molecular Explanation for Long-Term Potentiation.
J. D. Sweatt (1999)
Learn. Mem. 6, 399-416
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Cellular Signaling through Multifunctional Ca2+/Calmodulin-dependent Protein Kinase II.
T. R. Soderling, B. Chang, and D. Brickey (2001)
J. Biol. Chem. 276, 3719-3722
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