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The Journal of Neuroscience, September 21, 2005, 25(38):8788-8793; doi:10.1523/JNEUROSCI.1020-05.2005

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BRIEF COMMUNICATION
Differential Roles of Glial and Neuronal Glutamate Transporters in Purkinje Cell Synapses

Yukihiro Takayasu,^1,2 Masae Iino,¹ Wataru Kakegawa,¹ Hiroshi Maeno,³ Kei Watase,³ Keiji Wada,³ Dai Yanagihara,⁴ Taisuke Miyazaki,⁵ Okiru Komine,⁶ Masahiko Watanabe,⁵ Kohichi Tanaka,⁶ and Seiji Ozawa¹

Departments of ¹Neurophysiology and ²Otolaryngology–Head and Neck Surgery, Gunma University Graduate School of Medicine, Maebashi, Gunma 371-8511, Japan, ³Department of Degenerative Neurological Diseases, National Institute of Neuroscience, Kodaira, Tokyo 187-8502, Japan, ⁴Laboratory for Neurophysiology, Toyohashi University of Technology, Toyohashi, Aichi 441-8580, Japan, ⁵Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060-8638, Japan, and ⁶Laboratory of Molecular Neuroscience, School of Biomedical Science and Medical Research Institute, Tokyo Medical and Dental University, Tokyo 113-8510, Japan

Glutamate transporters are essential for terminating excitatory neurotransmission. Two distinct glutamate transporters, glutamate–aspartate transporter (GLAST) and excitatory amino acid transporter 4 (EAAT4), are expressed most abundantly in the molecular layer of the cerebellar cortex. GLAST is expressed in Bergmann glial processes surrounding excitatory synapses on Purkinje cell dendritic spines, whereas EAAT4 is concentrated on the extrasynaptic regions of Purkinje cell spine membranes. To clarify the functional significance of the coexistence of these transporters, we analyzed the kinetics of EPSCs in Purkinje cells of mice lacking either GLAST or EAAT4. There was no difference in the amplitude or the kinetics of the rising and initial decay phase of EPSCs evoked by stimulations of climbing fibers and parallel fibers between wild-type and EAAT4-deficient mice. However, long-lasting tail currents of the EPSCs appeared age dependently in most of Purkinje cells in EAAT4-deficient mice. These tail currents were never seen in mice lacking GLAST. In the GLAST-deficient mice, however, the application of cyclothiazide that reduces desensitization of AMPA receptors increased the peak amplitude of the EPSC and prolonged its decay more markedly than in both wild-type and EAAT4-deficient mice. The results indicate that these transporters play differential roles in the removal of synaptically released glutamate. GLAST contributes mainly to uptake of glutamate that floods out of the synaptic cleft at early times after transmitter release. In contrast, the main role of EAAT4 is to remove low concentrations of glutamate that escape from the uptake by glial transporters at late times and thus prevents the transmitter from spilling over to neighboring synapses.

Key words: glutamate transporters; GLAST; EAAT4; Purkinje cell; Bergmann glia; EPSC

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Received March 16, 2005; revised August 9, 2005; accepted August 9, 2005.

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