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 followed by large tail currents (Itail) after the offset of a voltage jump. The aim of the present study was to characterize the properties of Itail in astrocytes, oligodendrocytes, and their respective precursors in the gray matter of spinal cord slices. Studies were carried out on 5- to 11-day-old rats, using the whole-cell patch clamp technique. The reversal potential (Vrev) of Itail evoked by membrane depolarization was significantly more positive in oligodendrocytes (-31.7+/-2.58 mV, n = 53) than in astrocytes (-57.9+/-2.43 mV, n = 21), oligodendrocyte precursors (-41.2+/-3.44 mV, n = 36), or astrocyte precursors (-52.1+/-1.32 mV, n = 43). Analysis of the Itail (using a variable amplitude and duration of the de- and hyperpolarizing prepulses as well as an analysis of the time constant of the membrane currents during voltage steps) showed that the Itail in oligodendrocytes arise from a larger shift of K+ across their membrane than in other cell types. As calculated from the Nernst equation, changes in Vrev revealed significantly larger accumulation of the extracellular K+ concentration ([K+]e) around oligodendrocytes than around astrocytes. The application of 50 mM K+ or hypotonic solution, used to study the effect of cell swelling on the changes in [K+]e evoked by a depolarizing prepulse, produced in astrocytes an increase in [K+]e of 201% and 239%, respectively. In oligodendrocytes, such increases (22% and 29%) were not found. We conclude that K+ tail currents, evoked by a larger accumulation of K+ in the vicinity of the oligodendrocyte membrane, could result from a smaller extracellular space (ECS) volume 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 contribute to efficient K+ homeostasis.