A study of the mechanisms by which potassium moves through brain tissue in the rat

The flux of K+ produced by electric current across the pia-arachnoid surface of the neocortex of anaesthetized rats has been studied with K+-selective electrodes in a cup at the surface and with flame photometry. The potential differences developed across three regions of the rat brain (neocortex, cerebellum, hippocampus) have been measured as [K+] was altered in fluid at the surface. The experimental results have been related to those that would be expected (i) if K+ moved principally by diffusion in extracellular space and (ii) if current flow through cells makes a significant contribution to K+ transfer. K movement produced by current across the neocortical surface accounted for 0.06 of the transfer of electric charge with small currents in either direction (ca. 5 microA mm-2) and with larger currents out of the tissue. Large currents (ca. 20 microA mm-2) into the tissue produced less K+ movement, but still more than the fraction 0.012 expected for purely extracellular flux. Alternating current pulses (5 Hz) with zero net transfer of charge produced no flux of K+ across the surface, while alternation with unequal durations produced the same effects as the equivalent steady charge transfer. The K+ flux lagged behind the onset and cessation of current with a time constant ca. 45 sec, approximately as expected from calculations with a model of the tissue. A surface-negative potential shift averaging 2 mV was observed when [K+ ]at the brain surface was increased from 3 to 12 mM. The time for development of half of the full potential change was 20 sec, with the solution changes complete in less than 4 sec. These results are inconsistent with the hypothesis that K+ movement through brain tissue occurs principally through intercellular clefts, except where these movements involve very localized gradients. They are consistent with the conclusion that ca. 5 times as much K+ flux passes through cells (probably largely glial cells) as through extracellular space, with fluxes driven by either extracellular voltage or concentration gradients.