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J. Biol. Chem., Vol. 277, Issue 7, 4945-4950, February 15, 2002

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Diversity of Neuron-specific K⁺-Cl Cotransporter Expression and Inhibitory Postsynaptic Potential Depression in Rat Motoneurons^*

Tsuyoshi Ueno, Akihito Okabe^§, Norio Akaike, Atsuo Fukuda^§, and Junichi Nabekura^¶

From the  Department of Cellular and System Physiology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan and ^§ Department of Physiology, Hamamatsu University School of Medicine, 20-1 Handayama 1-chome, Hamamatsu, Shizuoka 431-3192, Japan

Motoneurons receive a robust recurrent synaptic inhibition by -aminobutyric acid and glycine, which activate Cl channels. Thus, Cl homeostasis determines the efficacy of synaptic inhibition in the motoneurons. In situ hybridization reveals that the neuronal K⁺-Cl cotransporter isoform 2 (KCC2), a major mechanism in maintaining a low Cl concentration in neurons, is abundantly expressed in the facial, hypoglossal (XII), and spinal motoneurons innervating striated muscle, whereas the dorsal vagal motoneurons (DMVs) controlling smooth muscle exhibited little expression of KCC2. This raises a general interest in the correlation between KCC2 expression and inhibitory postsynaptic potential (IPSP) performance in the native circuits. Intracellular and whole-cell patch recordings revealed that an activity-dependent depression of IPSPs and positive shift of IPSP reversal potentials were more prominent in the DMV than in the XII. Cl influx through Cl channels was extruded more potently in the XII than in the DMV, suggesting that differences in Cl extrusion account for these dynamic differences of IPSP. Cl extrusion was inhibited by either furosemide or an increase in extracellular potassium concentrations. Thus, the rigid maintenance of IPSP and rapid Cl extrusion in the XII reflects an intense expression of KCC2. KCC2 expression may strongly influence the IPSP depression and functional properties of the motoneurons innervating striated muscles.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) U55816.

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