Potassium activity and changes in glial and neuronal membrane potentials during initiation and spread of afterdischarge in cerebral cortex of cat

Abstract

Trains of electrical stimuli of increasing intensity were applied to the surface of the anterior suprasylvian gyrus to produce afterdischarges (AD) that remained localized or spread to a recording site 2 cm posteriorly in the same gyrus. The local afterdischarge was associated with a negative steady potential (SP) shift and increases in [K +] 0 that were maximal at or near the surface and gradually decreased in magnitude at deeper layers of the cortex. During spreading AD, recordings at the stimulus site showed a secondary increase in both the SP shift and [K +] 0 at about 400 to 1400 μm below the cortical surface. As the AD invaded the distant recording site it was associated with a comparable negative SP shift and increase in [K+]o. Neither the appearance of local AD nor its spread to the distant recording site were contingent upon critical elevations of [K +] 0. During secondary increases in [K+]o glial depolarizations were less than would be predicted if the membrane potential were determined solely by changes in the ratio of intra- to extracellular [K +]. Smaller deviations from the Nernst equation also occurred during the repolarizing phase of glial depolarization produced by weaker stimuli that did not produce a secondary increase in [ K +] 0. Only immediately after the stimulus train did the relationship between glial depolarization and [K +] 0 approach the expected slope of a K + electrode. Simultaneous intracellular recording of neurons and [K +] 0 did not show an increase in neuronal firing rate or membrane depolarization to account for the additional increase in [K +] 0 during spreading AD. The possible sources of the secondary increase in [K +] 0 and the significance of the failure of glia to depolarize to levels predicted by the Nernst equation are discussed.