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The Journal of Neuroscience, October 1, 2002, 22(19):8487-8503
Distal Extension of Climbing Fiber Territory and Multiple
Innervation Caused by Aberrant Wiring to Adjacent Spiny Branchlets in
Cerebellar Purkinje Cells Lacking Glutamate Receptor  2
Ryoichi
Ichikawa1, 2,
Taisuke
Miyazaki1,
Masanobu
Kano3,
Tsutomu
Hashikawa4,
Haruyuki
Tatsumi2,
Kenji
Sakimura5,
Masayoshi
Mishina6,
Yoshiro
Inoue1, and
Masahiko
Watanabe1
1 Department of Anatomy, Hokkaido University School of
Medicine, Sapporo 060-8638, Japan, 2 Department of Anatomy,
Sapporo Medical University School of Medicine, Sapporo 060-8556, Japan,
3 Department of Physiology, Kanazawa University School of
Medicine, Takara-machi, Kanazawa 920-8640, Japan,
4 Laboratory for Neural Architecture, Brain Science
Institute, RIKEN, Wako 351-0198, Japan, 5 Department
of Cellular Neurobiology, Brain Research Institute, Niigata University,
Niigata 951-8122, Japan, and 6 Department of Molecular
Neurobiology and Pharmacology, Graduate School of Medicine, University
of Tokyo, and Solution-Oriented Research for Science and
Technology, Japan Science and Technology, Tokyo 113-0033, Japan
Organized synapse formation on to Purkinje cell (PC) dendrites by
parallel fibers (PFs) and climbing fibers (CFs) is crucial for
cerebellar function. In PCs lacking glutamate receptor  2 (GluR2),
PF synapses are reduced in number, numerous free spines emerge, and
multiple CF innervation persists to adulthood. In the present study, we
conducted anterograde and immunohistochemical labelings to investigate
how CFs innervate PC dendrites under weakened synaptogenesis by PFs. In
the GluR2 knock-out mouse, CFs were distributed in the molecular
layer more closely to the pial surface compared with the wild-type
mouse. Serial electron microscopy demonstrated that CFs in the
knock-out mouse innervated all spines protruding from proximal
dendrites of PCs, as did those in the wild-type mouse. In the knock-out
mouse, however, CF innervation extended distally to spiny branchlets,
where nearly half of the spines were free of innervation in contrast to
complete synapse formation by PFs in the wild-type mouse. Furthermore,
from the end point of innervation, CFs aberrantly jumped to form
ectopic synapses on adjacent spiny branchlets, whose proximal portions were often innervated by different CFs. Without GluR2, CFs are thus
able to expand their territory along and beyond dendritic trees of the
target PC, resulting in persistent surplus CFs by innervating the
distal dendritic segment. We conclude that GluR2 is essential to
restrict CF innervation to the proximal dendritic segment, by which
territorized innervation by PFs and CFs is properly structured and the
formation of excess CF wiring to adjacent PCs is suppressed.
Key words:
cerebellum; Purkinje cell; climbing fiber; multiple
innervation; parallel fiber; glutamate receptor 2
Copyright © 2002 Society for Neuroscience 0270-6474/02/22198487-17$05.00/0
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