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The Journal of Neuroscience, February 23, 2005, 25(8):2146-2156; doi:10.1523/JNEUROSCI.4740-04.2005

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Development/Plasticity/Repair
Control of Synaptic Connection by Glutamate Receptor 2 in the Adult Cerebellum

Tomonori Takeuchi,^1 * Taisuke Miyazaki,^2 * Masahiko Watanabe,² Hisashi Mori,¹ Kenji Sakimura,³ and Masayoshi Mishina¹

¹Department of Molecular Neurobiology and Pharmacology, Graduate School of Medicine, University of Tokyo, and Solution Oriented Research for Science and Technology, Japan Science and Technology Agency, Tokyo 113-0033, Japan, ²Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060-8638, Japan, and ³Department of Cellular Neurobiology, Brain Research Institute, Niigata University, Niigata 951-8585, Japan

Precise topological matching of presynaptic and postsynaptic specializations is essential for efficient synaptic transmission. Furthermore, synaptic connections are subjected to rearrangements throughout life. Here we examined the role of glutamate receptor (GluR) 2 in the adult brain by inducible and cerebellar Purkinje cell (PC)-specific gene targeting under the pure C57BL/6 genetic background. Concomitant with the decrease of postsynaptic GluR2 proteins, presynaptic active zones shrank progressively and postsynaptic density (PSD) expanded, resulting in mismatching between presynaptic and postsynaptic specializations at parallel fiber-PC synapses. Furthermore, GluR2 and PSD-93 proteins were concentrated at the contacted portion of mismatched synapses, whereas AMPA receptors were distributed in both the contacted and dissociated portions. When GluR2 proteins were diminished, PC spines lost their synaptic contacts. We thus identified postsynaptic GluR2 as a key regulator of the presynaptic active zone and PSD organization at parallel fiber-PC synapses in the adult brain.

Key words: cerebellar Purkinje cell; conditional gene targeting; glutamate receptor 2; postsynaptic density; synaptic connection; synaptic matching

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Received Nov 19, 2004; revised January 11, 2005; accepted January 12, 2005.

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