Glial depolarization evokes a larger potassium accumulation around oligodendrocytes than around astrocytes in gray matter of rat spinal cord slices

The cell membrane of astrocytes and oligodendrocytes is almost exclusively permeable for K+. Depolarizing and hyperpolarizing voltage steps produce in oligodendrocytes, but not in astrocytes, decaying passive currents followe d by large tail currents (I-tail) after the offset of a voltage jump. The a im of the present study was to characterize the properties of I-tail in ast rocytes, oligodendrocytes, and their respective precursors in the gray matt er of spinal cord slices. Studies were carried out on 5- to Ii-day-old rats , using the whole-cell patch clamp technique. The reversal potential (V-rev ) of I-tail evoked by membrane depolarization was significantly more positi ve in oligodendrocytes (-31.7 +/- 2.58 mV, n = 53) than in astrocytes (-57. 9 +/- 2.43 mV, n = 21), oligodendrocyte precursors (-41.2 +/- 3.34 mV, n = 36), or astrocyte precursors (-52.1 +/- 1.32 mV, n = 43), Analysis of the I -tail (using a variable amplitude and duration of the de-and hyperpolarizin g prepulses as well as an analysis of the time constant of the membrane cur rents during voltage steps) showed that the I-tail in oligodendrocytes aris e from a larger shift of K+ across their membrane than in other cell types. As calculated from the Nernst equation, changes in V-rev revealed signific antly larger accumulation of the extracellular K+ concentration ([K+](e)) a round oligodendrocytes than around astrocytes, The application of 50 mM Kor hypotonic solution, used to study the effect of cell swelling on the cha nges in [K+](e) evoked by a depolarizing prepulse, produced in astrocytes a n increase in [K+](e) of 201% and 239%, respectively. In oligodendrocytes, such increases (22% and 29%) were not found. We conclude that K+ tail curre nts, evoked by a larger accumulation of K+ in the vicinity of the oligodend rocyte membrane, could result from a smaller extracellular space (ECS) volu me around oligodendrocytes than around astrocytes, Thus, in addition to the clearance of K+ from the ECS performed by astrocytes, the presence of the K+ tail currents in oligodendrocytes indicates that they might also contrib ute to efficient K+ homeostasis. (C) 1999 Wiley-Liss, Inc.