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 delta [TMA+] and delta [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+]0 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.

Potassium channel Kir4.1 macromolecular complex in retinal glial cells

“…There is also evidence that AQP4 is involved in [K 1 ] o buffering. First, the volume of the extracellular space in brain appears to be negatively correlated with [K 1 ] o , suggesting the involvement of a water transport mechanism (Dietzel et al, 1980;Holthoff and Witte, 2000). Second, a-syntrophin null mice show an impairment of both water transport and K 1 buffering in brain resulting from a redistribution of AQP4 away from astrocytic endfeet (AmiryMoghaddam et al, 2003b(AmiryMoghaddam et al, , 2004.…”

Model of potassium dynamics in the central nervous system

“…Variations in [K+]i may alter the magnitude of spatial buffer currents. 3) The model does not take account of the movement of water between extracellular and intracellular compartments, a process accompanying passive K + uptake (Dietzel et al, 1980). The movement of water leads to changes in (Y and thus to variations in [K+], (Dietzel et al, 1980).…”

Exclusive potassium dependence of the membrane potential in cultured mouse oligodendrocytes

“…The accumulation of potassium in glial cells may be substantially greater than documented by our activity measurements assuming a swelling of the cells during potassium uptake as proposed by several investigators, e.g., Nicholson (1980). In situ the described potassium uptake mechanisms can effectively contribute to the regulation of [K'],,, especially under the consideration that the glial volume in brain is larger than that of the extracellular space (Dietzel et al, 1980). At present, it is unclear whether this intracellular potassium accumulation results from passive ion fluxes or active transport.…”