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Volume 17, Number 19, Issue of October 1, 1997 pp. 7278-7287
Copyright ©1997 Society for Neuroscience

Intracellular Calcium Transients and Potassium Current Oscillations Evoked by Glutamate in Cultured Rat Astrocytes

Received May 21, 1997; revised July 17, 1997; accepted July 18, 1997.

Jianguo Chen, Kurt H. Backus, and Joachim W. Deitmer

Abteilung für Allgemeine Zoologie, FB Biologie, Universität Kaiserslautern, D-67653 Kaiserslautern, Germany

Glutamate responses in cultured rat astrocytes from cerebella of neonatal rats were investigated using the perforated-patch configuration to record membrane currents without rundown of intracellular messenger cascades, and microfluorometric measurements to measure the intracellular Ca²⁺ concentration ([Ca²⁺]_i) and intracellular pH (pH_i) with fura-2 AM and 2,7-bis-(2-carboxyethyl)-5,6-carboxyfluorescein acetoxy methylester respectively. In the perforated-patch mode, glutamate evoked single or multiple outward current transients in 82% of the cells, which disappeared when the recording technique was converted into a conventional whole-cell mode. The outward current transients were accompanied by [Ca²⁺]_i transients, whereas pH_i fell monophasically, without any sign of oscillation. Pharmacological analysis of the glutamate-induced responses indicated that ionotropic receptor activation evoked an inward current but no outward current transients, and metabotropic receptor activation (of the mGluR1/5 type) elicited outward current transients but no inward current. The outward current transients were reduced in frequency, or even abolished, after depletion of the intracellular Ca²⁺-stores by the Ca²⁺-ATPase inhibitor cyclopiaconic acid (10 µM). They reversed near 85 mV and were reduced by tetraethylammonium (10 mM), suggesting that they were caused by K⁺ channel activation. It is concluded that glutamate evoked these K⁺ outward current transients by oscillatory Ca²⁺ release mediated by mGluR activation. The corresponding membrane potential waves across the astroglial syncytium could provide spatial and temporal dynamics to the glial K⁺ uptake capacity and other voltage-dependent processes.

Key words: glutamate; perforated patch-clamp; gramicidin; current oscillation; [Ca²⁺]_i oscillations; Ca²⁺-activated K⁺ channels; rat

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