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The Journal of Neuroscience, December 15, 2001, 21(24):9701-9712
Roles of Glutamate Receptor  2 Subunit (GluR2) and
Metabotropic Glutamate Receptor Subtype 1 (mGluR1) in Climbing
Fiber Synapse Elimination during Postnatal Cerebellar Development
Kouichi
Hashimoto1,
Ryoichi
Ichikawa2,
Hajime
Takechi3,
Yoshiro
Inoue4,
Atsu
Aiba5,
Kenji
Sakimura6,
Masayoshi
Mishina7,
Tsutomu
Hashikawa8,
Arthur
Konnerth9,
Masahiko
Watanabe4, and
Masanobu
Kano1
1 Department of Physiology, Kanazawa University School
of Medicine, Takara-machi, Kanazawa 920-8640, Japan,
2 Department of Anatomy, Sapporo Medical University,
Sapporo 060-8556, Japan, 3 Department of Gerontology, Kyoto
University Faculty of Medicine, Kyoto 606-8507, Japan,
4 Department of Anatomy, Hokkaido University School of
Medicine, Sapporo 060-8638, Japan, 5 Division of Cell
Biology, Department of Molecular and Cellular Biology, Kobe University
Graduate School of Medicine, Kobe 650-0017, Japan,
6 Department of Cellular Neurobiology, Brain Research
Institute, Niigata University, Niigata 951-8585, Japan,
7 Department of Molecular Neurobiology and Pharmacology,
Graduate School of Medicine, University of Tokyo, and Cure Research for
Evolutional Science and Technology (CREST), Japan Science and
Technology Corporation, Tokyo 113-0033, Japan, 8 Laboratory
for Neural Architecture, Brain Science Institute, RIKEN,
Wako-shi, Saitama 351-0198, Japan, and 9 Institut für
Physiologie, Ludwig-Maximilians-Universität München, 80802 München, Germany
Climbing fiber (CF) synapse formation onto cerebellar Purkinje
cells (PCs) is critically dependent on the synaptogenesis from parallel
fibers (PFs), the other input to PCs. Previous studies revealed that
deletion of the glutamate receptor  2 subunit (GluR2) gene results
in persistent multiple CF innervation of PCs with impaired PF
synaptogenesis, whereas mutation of the metabotropic glutamate receptor
subtype 1 (mGluR1) gene causes multiple CF innervation with normal PF
synaptogenesis. We demonstrate that atypical CF-mediated EPSCs
(CF-EPSCs) with slow rise times and small amplitudes coexisted with
typical CF-EPSCs with fast rise times and large amplitudes in PCs from
GluR2 mutant cerebellar slices. CF-EPSCs in mGluR1 mutant and
wild-type PCs had fast rise times. Atypical slow CF responses of
GluR2 mutant PCs were associated with voltage-dependent
Ca2+ signals that were confined to PC distal
dendrites. In the wild-type and mGluR1 mutant PCs, CF-induced
Ca2+ signals involved both proximal and distal
dendrites. Morphologically, CFs of GluR2 mutant mice extended to the
superficial regions of the molecular layer, whereas those of wild-type
and mGluR1 mutant mice did not innervate the superficial one-fifth of
the molecular layer. It is therefore likely that surplus CFs of
GluR2 mutant mice form ectopic synapses onto distal dendrites,
whereas those of wild-type and mGluR1 mutant mice innervate proximal
dendrites. These findings suggest that GluR2 is required for
consolidating PF synapses and restricting CF synapses to the proximal
dendrites, whereas the mGluR1-signaling pathway does not affect PF
synaptogenesis but is involved in eliminating surplus CF synapses at
the proximal dendrites.
Key words:
climbing fiber; parallel fiber; cerebellum; Purkinje
cell; synapse; glutamate receptor; postnatal development; mutant
mouse
Copyright © 2001 Society for Neuroscience 0270-6474/01/21249701-12$05.00/0
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