Journal of Neurophysiology, Vol 63, Issue 5 1089-1097, Copyright © 1990 by APS

ARTICLES

Mechanism of potassium uptake in neuropile glial cells in the central nervous system of the leech

W. A. Wuttke
School of Biological Sciences, University College of Swansea, United Kingdom.

1. Ion-selective double-barreled microelectrodes (ISME) were used to measure intracellular K+ (aKi), Na+ (aNai), and Cl- (aCli) activities of neuropile glial (NG) cells in the central nervous system of the medicinal leech Hirudo medicinalis. Ion fluxes were induced by an increase in extracellular K+ concentration [( K+]o) and analyzed to elucidate the ionic mechanism of the K+ uptake occurring under such conditions. 2. In addition, the K+ concentration of the extracellular space of the nerve cell body region (NCBR) and the neuropile (N) was measured with neutral carrier K(+)-ISME. In normal saline (4 mM K+), a concentration of 4.2 mM was measured in both extracellular spaces. No differences between the K+ concentration of the bathing fluid and the extracellular spaces were found at higher (i.e., 10 and 40 mM) K+ concentrations. 3. In normal saline, the mean membrane potential (Em) was -68 mV, and the mean aKi, aNai, and aCli were found to be 77, 10, and 7 mM, respectively. The corresponding equilibrium potentials were -81, 56, and -66 mV. The chloride equilibrium potential (ECl) was similar to Em, and it is concluded that chloride is passively distributed across the NG cell membrane. 4. When [K+]o was transiently increased 10-fold (i.e., to 40 mM), aKi and a Cli increased transiently by 22 and 25 mM, respectively, and the membrane depolarized to -28 mV, which was similar to both K+ equilibrium potential (EK) and ECl. The KCl uptake was accompanied by a transient decrease in aNai to 5 mM. 5. After incubation for at least 1 h in Na(+)-free saline, NG cells accumulated K+ in the absence of extracellular Na+ to levels similar to those observed in the presence of Na+. Therefore the uptake of K+ was not dependent on external--and probably also internal--Na+. 6. Changes in cell volume induced by the increase in [K+]o were estimated by loading NG cells with choline and monitoring its intracellular concentration with Corning-K(+)-ISME. In saline containing 40 mM K+, NG cell volume increased to approximately 150% of its volume in normal saline. 7. It is concluded that the mechanism of K+ uptake in NG cells is by passive KCl and water influx, which causes cell swelling.

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