CHANGES IN GLIAL K-MATTER( CURRENTS WITH DECREASED EXTRACELLULAR VOLUME IN DEVELOPING RAT WHITE)

Whole cell patch-clamp recordings of K+ currents from oligodendrocyte precursors in 10-day-old rats (P10) and, following myelination, in mat ure oligodendrocytes from 20-day-old rats (P20) were correlated with e xtracellular space (ECS) diffusion parameters measured by the local di ffusion of iontophoretically injected tetramethylammonium ions (TMA(+) ). The aim of this study was to find an explanation for the changes in glial currents that occur with myelination. Oligodendrocyte precursor s (P10) in slices from corpus callosum were characterized by the prese nce of A-type K+ currents, delayed and inward rectifier currents, and lack of tail currents after the offset of a voltage jump. Mature oligo dendrocytes in corpus callosum slices from P20 rats were characterized by passive, decaying currents and large tail currents after the offse t of a voltage jump. Measurements of the reversal potential for the ta il currents indicate that they result from increases in [K+](e) by an average of 32 mM during a 20 msec 100 mV voltage step. Concomitant wit h the change in oligodendrocyte electrophysiological behavior after my elination there is a decrease in the ECS of the corpus callosum. ECS v olume decreases from 36% (P9-10) to 25% (P20-21) of total tissue volum e. ECS tortuosity lambda = (D/ADC)(0.5), where D is the free diffusion coefficient and ADC is the apparent diffusion coefficient of TMA(+) i n the brain, increases as measured perpendicular to the axons from 1.5 3 +/- 0.02 (n = 6, mean +/- SEM) to 1.70 +/- 0.02 (n = 6). TMA(+) non- specific uptake (k') was significantly larger at P20 (5.2 +/- 0.6 x 10 (-3)s(-1), n = 6) than at P10 (3.5 +/- 0.4 x 10(-3)s(-1), n = 6). It c an be concluded that membrane potential changes in mature oligodendroc ytes are accompanied by rapid changes in the K+ gradient resulting fro m K+ fluxes across the glial membrane. As a result of the reduced extr acellular volume and increased tortuosity, the membrane fluxes produce larger changes in [K+](e) in the more mature myelinated corpus callos um than before myelination. These conclusions also account for differe nces between membrane currents in cells in slices compared to those in tissue culture where the ECS is essentially infinite. The size and ge ometry of the ECS influence the membrane current patterns of glial cel ls and may have consequences for the role of glial cells in spatial bu ffering. (C) 1997 Wiley-Liss, Inc.