Spatial Buffering of Light-Evoked Potassium Increases by Retinal Müller (Glial) Cells

Abstract

Activity-dependent variations in extracellular potassium concentration in the central nervous system may be regulated, in part, by potassium spatial buffering currents in glial cells. The role of spatial buffering in the retina was assessed by measuring light-evoked potassium changes in amphibian eyecups. The amplitude of potassium increases in the vitreous humor was reduced to approximately 10 percent by 50 micromolar barium, while potassium increases in the inner plexiform layer were largely unchanged. The decrease in the vitreal potassium response was accurately simulated with a numerical model of potassium current flow through Müller cells, the principal glial cells of the retina. Barium also substantially increased the input resistance of Müller cells and blocked the Müller cell-generated M-wave, indicating that barium blocks the potassium channels of Müller cells. Thus, after a light-evoked potassium increase within the retina, there is a substantial transfer of potassium from the retina to the vitreous humor by potassium current flow through Müller cells.

Detecting Activity in Olfactory Bulb Glomeruli with Astrocyte Recording

“…At this concentration, Ba 2ϩ effectively blocks inward rectifier K ϩ channels (IRKs) that are highly expressed in glial cells (Newman, 1993). IRKs are thought to be involved in the spatial buffering of K ϩ released in the extracellular space during neuronal activity (Karwoski et al, 1989;Newman, 1993;Amédée et al, 1997;Kofuji and Newman, 2004). Because K ϩ accumulates in the glomerular layer after OSN stimulation (Jahr and Nicoll, 1981;Khayari et al, 1988;Friedrich and Korsching, 1998), the Ba 2ϩ -sensitive component is consistent with IRK-dependant current in response to extracellular K ϩ accumulation.…”

“…Astrocytes are thought to use IRK channels to remove K ϩ from regions with high extracellular K ϩ and release it to regions with low K ϩ , a mechanism known as spatial buffering or siphoning of K ϩ (Karwoski et al, 1989;Amédée et al, 1997;Kofuji and Newman, 2004). In the retina, Kir4.1 channels are the main channels involved in the regulation of external K ϩ (Kofuji et al, 2000).…”

Compartmentalized and Signal-Selective Gap Junctional Coupling in the Hearing Cochlea

“…The supporting cell syncitium may act as a "sink" for excess perilymphatic K ϩ . Gap junction coupling could provide extensive spatial buffering, as seen in astrocytes (Leis et al, 2005) and retinal Müller cells (Karwoski et al, 1989). The widespread localization of gap junction channels, K/Cl cotransporters (Boettger et al, 2002), and aquaporins (Huang et al, 2002) could provide a passive mechanism of K ϩ buffering and osmotic homeostasis.…”

Conditional Knock-Out of Kir4.1 Leads to Glial Membrane Depolarization, Inhibition of Potassium and Glutamate Uptake, and Enhanced Short-Term Synaptic Potentiation

“…Subsequently, this phenomenon was confirmed in a variety of nervous tissue preparations (Kettenmann et al, 1983;Coles et al, 1986;Holthoff and Witte, 2000;Amzica et al, 2002). Although several possible mediators of astrocyte K ϩ uptake have been proposed, pharmacological studies suggest that K ir channels predominate in K ϩ buffering (Ballanyi et al, 1987;Karwoski et al, 1989;Oakley et al, 1992). The first identified glia-associated K ir was the weakly rectifying K ir 4.1 (Takumi et al, 1995), found in astrocyte processes surrounding synapses and blood vessels and in oligodendrocyte cell bodies (Poopalasundaram et al, 2000;Higashi et al, 2001;Ishii et al, 2003).…”