Transient changes in the size of the extracellular space in the sensorimotor cortex of cats in relation to stimulus-induced changes in potassium concentration

Abstract

The time course of local changes of the extracellular space (ES) was investigated by measuring concentration changes of repeatedly injected tetramethylammonium (TMA⁺) and choline (Ch⁺) ions for which cell membranes are largely impermeable. After stimulus-induced extracellular [K⁺] elevations the δ[TMA⁺] and δ[Ch⁺] signals recorded with nominally K⁺-selective liquid ion-exchanger microelectrodes increased by up to 100%, thus indicating a reduction of the ES down to one half of its initial size. The shrinkage was maximal at sites where the K⁺ release into the ES was also largest. At very superficial and deep layers, however, considerable increases in extracellular K⁺ concentration were not accompanied by significant reductions in the ES. These findings can be explained as a consequence of K⁺ movement through spatially extended cell structures. Calculations based on a model combining the spatial buffer mechanism of Kuffler and Nicholls (1966) to osmolarity changes caused by selective K⁺ transport through primarily K⁺ permeable membranes support this concept. Following stimulation additional iontophoretically induced [K⁺]_o rises were reduced in amplitude by up to 35%, even at sites where maximal decreases of the ES were observed. This emphasizes the importance of active uptake for K⁺ clearance out of the ES.