Electrical coupling between astrocytes and between oligodendrocytes studied in mammalian cell cultures

Abstract

The characteristics of electrical coupling between astrocytes and between oligodendrocytes were analyzed in cell cultures derived from rodent central nervous system. Experiments were carried out by impaling one member of a glial pair with separate voltage recording and current passing electrodes (cell 1) and the other cell, a measured distance from the first, with a voltage‐recording electrode (cell 2). Astrocyte pairs within 300 μm of one another were always coupled. The coupling ratio was determined for 23 astrocytic pairs various distances apart, and decreased with distance in a roughly exponential manner. The average coupling ratio of astrocytes within 100 μm of each other was 0.44 ± 0.32. Oligodendrocytes were less strongly coupled to each other than astrocytes. Even cells immediately adjacent to one another were often uncoupled. Among coupled oligodendrocytes within 100 μm of each other, the average coupling ratio was 0.11 ± 0.1. Current passage between pairs of astrocytes and pairs of oligodendrocytes was nonrectifying. Application of 0.5 mM BaCl₂ or 44.6 mM CsCl (substituted for NaCl) depolarized and increased the input resistance of astrocytes and oligodendrocytes. These ions also increased the coupling ratio in astrocyte pairs and oligodendrocyte pairs; this effect was rapid in onset and completely reversible. Ba⁺⁺ and Cs⁺ appear to block resting K⁺ conductance in glia and probably increase the coupling ratio by increasing the effective length constant of the glial membrane without any direct effect on junctional resistance. In three cases, oligodendrocyte pairs that appear uncoupled in normal solution exhibited coupling in the presence of BaCl₂ or CsCl. This suggests that oligodendrocytes may be widely coupled by junctions that provide only weak electrical interaction; such junctions might be important for the exchange of small metabolically active molecules. The strong electrical coupling among astrocytes, in concert with their K⁺‐selective membrane conductance, would provide for an electrical syncytium well designed to transport K⁺ away from areas of focal extracellular accumulation (i.e., the spatial buffer mechanism), and these cells, more than oligodendrocytes, may provide this function.