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The Journal of Neuroscience, October 5, 2005, 25(40):9213-9226; doi:10.1523/JNEUROSCI.2134-05.2005

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Cellular/Molecular
Target-Cell-Specific Left-Right Asymmetry of NMDA Receptor Content in Schaffer Collateral Synapses in {epsilon}1/NR2A Knock-Out Mice

Yue Wu,1,2 Ryosuke Kawakami,3 Yoshiaki Shinohara,2 Masahiro Fukaya,4 Kenji Sakimura,5 Masayoshi Mishina,6 Masahiko Watanabe,4 Isao Ito,3 and Ryuichi Shigemoto1,2,7

1Department of Physiology, School of Life Science, Graduate University for Advanced Studies (Sokendai), Okazaki, Aichi 444-8787, Japan, 2Division of Cerebral Structure, National Institute for Physiological Sciences, Okazaki, Aichi 444-8787, Japan, 3Department of Biology, Faculty of Science, Kyushu University, Fukuoka 812-8581, Japan, 4Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060-8638, Japan, 5Department of Cellular Neurobiology, Brain Research Institute, Niigata University, Niigata 951-8585, Japan, 6Department of Molecular Neurobiology and Pharmacology, School of Medicine, University of Tokyo, Tokyo 113-0033, Japan, and 7Solution-Oriented Research for Science and Technology, Japan Science and Technology Agency, Kawaguchi 332-0012, Japan

Input-dependent left-right asymmetry of NMDA receptor {epsilon}2 (NR2B) subunit allocation was discovered in hippocampal Schaffer collateral (Sch) and commissural fiber pyramidal cell synapses (Kawakami et al., 2003). To investigate whether this asymmetrical{epsilon}2 allocation is also related to the types of the postsynaptic cells, we compared postembedding immunogold labeling for {epsilon}2 in left and right Sch synapses on pyramidal cells and interneurons. To facilitate the detection of {epsilon}2 density difference, we used {epsilon}1 (NR2A) knock-out (KO) mice, which have a simplified NMDA receptor subunit composition.

The labeling density for {epsilon}2 but not {zeta}1 (NR1) and subtype 2/3 glutamate receptor (GluR2/3) in Sch-CA1 pyramidal cell synapses was significantly different between the left and right hippocampus with opposite directions in strata oriens and radiatum; the left to right ratio of{epsilon}2 labeling density was 1:1.50 in stratum oriens and 1.44:1 in stratum radiatum. No significant difference, however, was detected in CA1 stratum radiatum between the left and right Sch-GluR4-positive (mostly parvalbumin-positive) and Sch-GluR4-negative interneuron synapses. Consistent with the anatomical asymmetry, the amplitude ratio of NMDA EPSCs to non-NMDA EPSCs in pyramidal cells was approximately two times larger in right than left stratum radiatum and vice versa in stratum oriens of {epsilon}1 KO mice. Moreover, the amplitude of long-term potentiation in the Sch-CA1 synapses of left stratum radiatum was significantly larger than that in the right corresponding synapses. These results indicate that the asymmetry of {epsilon}2 distribution is target cell specific, resulting in the left-right difference in NMDA receptor content and plasticity in Sch-CA1 pyramidal cell synapses in {epsilon}1 KO mice.

Key words: NMDA receptor; hippocampus; pyramidal cell; interneuron; asymmetry; NR2B; GluR4; NR2A; NR2D; postembedding; knockout; LTP

Received May 27, 2005; revised August 22, 2005; accepted August 25, 2005.




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