Glial depolarization evokes a larger potassium accumulation around oligodendrocytes than around astrocytes in gray matter of rat spinal cord slices
Abstract
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 (I-tail) after the offset of a voltage jump.
The aim of the present study was to characterize the properties of I-tail in astrocytes, oligodendrocytes, and their respective precursors in the gray matter 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 positive in oligodendrocytes (-31.7 +/- 2.58 mV, n = 53) than in astrocytes (-57.9 +/- 2.43 mV, n = 21), oligodendrocyte precursors (-41.2 +/- 3.34 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 hyperpolarizing prepulses as well as an analysis of the time constant of the membrane currents during voltage steps) showed that the I-tail 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 V-rev 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.