Endfeet of retinal glial cells have higher densities of ion channels that mediate K+ buffering

Abstract

A major function of glial cells in the central nervous system is to buffer the extracellular potassium concentration, [K+]o. A local rise in [K+]o causes potassium ions to enter glial cells, which have membranes that are highly permeable to K+; potassium then leaves the glial cells at other locations where [K+]o has not risen. We report here the first study of the individual ion channels mediating potassium buffering by glial cells. The patch-clamp technique was employed to record single channel currents in Müller cells, the radial glia of the vertebrate retina. Those cells have 94% of their potassium conductance in an endfoot apposed to the vitreous humour, causing K+ released from active retinal neurones to be buffered preferentially to the vitreous. Recordings from patches of endfoot and cell body membrane show that a single type of inward-rectifying K+ channel mediates potassium buffering at both cell locations. The non-uniform density of K+ conductance is due to a non-uniform distribution of one type of K+ channel, rather than to the cell expressing high conductance channels at the endfoot and low conductance channels elsewhere on the cell.

cGMP‐mediated effects on the physiology of bovine and human retinal Müller (glial) cells.

“…While the cGMP analogue induced responses within 1-10 s (Fig. 1D) (Brew et al 1986;Newman, 1993;Puro & Stuenkel, 1995) (Hille, 1992). Another mechanism by which cGMP may activate Kca channels is via cGMP-dependent protein kinases as has been shown for BK channels in other cell types (White et al 1993 (Knowles et al 1989) and is likely to be synthesized by a specific population of amacrine cells (Yamamoto et al 1993).…”

“…Potassium-permeable ion channels in these glia are one of the important pathways for the redistribution of K+ from regions of the retina with higher [K+]o to areas where [K+], is lower (Newman, 1985(Newman, , 1993Brew, Gray, Mobbs & Attwell, 1986). Under usual assay conditions, the predominant potassium-permeable ion channels detected in Muller cells are of the inwardly rectifying type (Brew et al 1986;Newman, 1993;Chao et al 1994;Puro & Stuenkel, 1995 (Puro, 1991 b). Also, the depolarization induced by an influx of cations through CNG channels may help activate KCa channels directly as well as indirectly with the opening of the L-type voltage-gated calcium channels present in these glia (Puro et al 1996a).…”

Probing potassium channel function in vivo by intracellular delivery of antibodies in a rat model of retinal neurodegeneration

“…Kir subfamilies share amino acid homology but differ in mode of activation or degree of rectification (2, 3). Histological evidence of clustering of Kir4.1 channels on Müller glial cell proximal endfeet adjacent to the vitreous (4)(5)(6) and electrophysiological data (7-9) implicates Kir4.1 in "potassium siphoning" in the proximal mammalian retina (10)(11)(12). Members of Kir subfamilies are also reported on retinal neurons in the inner-nuclear (INL) and inner-plexiform (IPL) layers (13).…”

Neurovascular Coupling Is Not Mediated by Potassium Siphoning from Glial Cells

“…This influx depolarizes glial cells and drives out an equal amount of K ϩ from other cell regions . Most K ϩ efflux occurs from glial endfeet, which have a high density of K ϩ channels (Newman, 1984;Brew et al, 1986). Because glial endfeet terminate on blood vessels, most K ϩ is siphoned onto the vessels.…”