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The Journal of Neuroscience, October 10, 2007, 27(41):10947-10956; doi:10.1523/JNEUROSCI.2603-07.2007

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Cellular/Molecular
A Pathway-Specific Function for Different AMPA Receptor Subunits in Amygdala Long-Term Potentiation and Fear Conditioning

Yann Humeau,^1,2 * Daniel Reisel,^3 * Alexander W. Johnson,^4 * Thilo Borchardt,⁵ Vidar Jensen,⁶ Christine Gebhardt,¹ Verena Bosch,⁵ Peter Gass,⁷ David M. Bannerman,³ Mark A. Good,⁴ Øivind Hvalby,⁶ Rolf Sprengel,⁵ and Andreas Lüthi¹

¹Friedrich Miescher Institute for Biomedical Research, CH-4058 Basel, Switzerland, ²Unité Mixte de Recherche 7168, Centre National de la Recherche Scientifique, F-67084 Strasbourg, France, ³Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom, ⁴School of Psychology, Cardiff University, Cardiff CF10 3YG, United Kingdom, ⁵Department of Molecular Neurobiology, Max Planck Institute for Medical Research, D-69120 Heidelberg, Germany, ⁶Molecular Neurobiology Research Group, Institute of Basic Medical Sciences, University of Oslo, N-0317 Oslo, Norway, and ⁷Central Institute of Mental Health Mannheim, J5, D-68159 Mannheim, Germany

Correspondence should be addressed to Andreas Lüthi, Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, CH-4058 Basel, Switzerland. Email: andreas.luthi{at}fmi.ch

The AMPA receptor subunit glutamate receptor 1 (GluR1 or GluR-A) contributes to amygdala-dependent emotional learning. It remains unclear, however, to what extent different amygdala pathways depend on GluR1, or other AMPA receptor subunits, for proper synaptic transmission and plasticity, and whether GluR1-dependent long-term potentiation (LTP) is necessary for auditory and contextual fear conditioning. Here, we dissected the role of GluR1 and GluR3 (GluR-C) subunits in AMPA receptor-dependent amygdala LTP and fear conditioning using knock-out mice (GluR1^–/– and GluR3^–/–). We found that, whereas LTP at thalamic inputs to lateral amygdala (LA) projection neurons and at glutamatergic synapses in the basal amygdala was completely absent in GluR1^–/– mice, both GluR1 and GluR3 contributed to LTP in the cortico-LA pathway. Because both auditory and contextual fear conditioning were selectively impaired in GluR1^–/– but not GluR3^–/– mice, we conclude that GluR1-dependent synaptic plasticity is the dominant form of LTP underlying the acquisition of auditory and contextual fear conditioning, and that plasticity in distinct amygdala pathways differentially contributes to aversive conditioning.

Key words: lateral amygdala; basal amygdala; fear conditioning; synaptic transmission; LTP; GluR1; GluR3

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Received June 7, 2007; revised Aug. 22, 2007; accepted Aug. 26, 2007.

Correspondence should be addressed to Andreas Lüthi, Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, CH-4058 Basel, Switzerland. Email: andreas.luthi{at}fmi.ch

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