The Role of Cells in the Dispersal of Brain Extracellular Potassium

Abstract

What is the fate of potassium which is released into the extracellular space around active neurons? A lot of information relevant to this has appeared in the last ten years, much of it obtained through the use of K+-selective microelectrodes. But there are many questions which remain unsettled and perhaps controversial (Gardner-Medwin, 1980). Potassium released into the extracellular (EC) space is ultimately restored to the neurons which have lost it; so one question centres round the time course of this restoration process and its relation to the dynamics of other processes. Potassium may also enter other cells temporarily, which thus act to ‘buffer’ the changes of K⁺ concentration in the EC space. The extent and time course of such buffering processes are uncertain (Gardner-Medwin, 1980). A third type of process is that of dispersal to less affected regions of EC space, or to fluid ventricles: this may occur either by diffusion or by the action of currents flowing through cell membrane causing the cells (probably especially glial cells) to take up K⁺ in one region and to release it elsewhere. This last process is known as the ‘spatial buffer’ mechanism and was originally suggested by Orkand, Nicholls and Kuffler in 1966. My own recent work in collaboration with various colleagues (Gardner-Medwin, 1977; Gardner-Medwin, and Nicholson, 1978; Gardner-Medwin et al., 1979; Gardner-Medwin and Coles, 1980) has suggested that the spatial buffer mechanism may be more important in relation to diffusion than was earlier appreciated. In this article I shall examine the consequences that the spatial buffer and uptake mechanisms may have in some of the situations that have been studied by other authors and in situations where it may be important for nervous systems to minimise a disturbance of EC K concentration. We cannot straightforwardly turn these components of K⁺ dynamics on and off in an experimental situation to determine their effect: but once we know or can guess at their parameters, we can do calculations to see what the effect of such a hypothetical experiment would be.