Is the potassium channel distribution in glial cells optimal for spatial buffering of potassium?

Abstract

Glial cells in the nervous system are believed to reduce changes of extracellular potassium concentration ([K+]o), caused by neural activity, by carrying out spatial buffering of potassium. In the case of retinal glial cells (Müller cells), light-evoked increases of [K+]o within the retina are reduced by K ions flowing through the Müller cell to the vitreous fluid of the eye. We have calculated the optimal way to distribute the potassium conductance of the Müller cell to maximize spatial buffering to the vitreous fluid. The best distribution is with half the potassium conductance in the outer part of the cell, where K+ enters, and half the conductance in the vitreal endfoot, where K+ leaves the cell. This calculated distribution is very different from the actual distribution measured by Newman (1984, Nature [Lond.], 309: 155-157), where only 6% of the Müller cell conductance is in the outer cell and 94% is in the endfoot. The experimentally observed distribution gives less than a quarter of the spatial buffering that would be produced by the optimal distribution. The possible advantages of this arrangement are discussed.