Spatial buffering of potassium ions in brain extracellular space.

It has long been assumed that one important mechanism for the dissipation of local potassium gradients in the brain extracellular space is the so-called spatial buffer, generally associated with glial cells. To date, however, there has been no analytical description of the characteristic patterns of K(+) clearance mediated by such a mechanism. This study reanalyzed a mathematical model of Gardner-Medwin (1983, J. Physiol. (Lond.). 335:393-426) that had previously been solved numerically. Under suitable approximations, the transient solutions for the potassium concentrations and the corresponding membrane potentials of glial cells in a finite, parallel domain were derived. The analytic results were substantiated by numerical simulations of a detailed two-compartment model. This simulation explored the dependence of spatial buffer current and extracellular K(+) on the distribution of inward rectifier K(+) channels in the glial endfoot and nonendfoot membranes, the glial geometric length, and the effect of passive KCl uptake. Regarding the glial cells as an equivalent leaky cable, the analyses indicated that a maximum endfoot current occurs when the glial geometric length is equal to the corresponding electrotonic space constant. Consequently, a long glial process is unsuitable for spatial buffering, unless the axial space constant can match the length of the process. Finally, this study discussed whether the spatial buffer mechanism is able to efficiently transport K(+) over distances of more than several glial space constants.

[1]  U. Heinemann,et al.  Relations between slow extracellular potential changes, glial potassium buffering, and electrolyte and cellular volume changes during neuronal hyperactivity in cat brain , 1989, Glia.

[2]  J. C. Jaeger,et al.  Conduction of Heat in Solids , 1952 .

[3]  D. Attwell,et al.  Is the potassium channel distribution in glial cells optimal for spatial buffering of potassium? , 1985, Biophysical journal.

[4]  C. Nicholson,et al.  Extracellular space structure revealed by diffusion analysis , 1998, Trends in Neurosciences.

[5]  E. Newman Membrane physiology of retinal glial (Muller) cells , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  E. Newman,et al.  Model of potassium dynamics in the central nervous system , 1988, Glia.

[7]  S. W. Kuffler,et al.  Physiological properties of glial cells in the central nervous system of amphibia. , 1966, Journal of neurophysiology.

[8]  E Syková,et al.  Extracellular K+ accumulation in the central nervous system. , 1983, Progress in biophysics and molecular biology.

[9]  E. Newman,et al.  Model of electroretinogram b-wave generation: a test of the K+ hypothesis. , 1984, Journal of neurophysiology.

[10]  A. Gardner-Medwin A study of the mechanisms by which potassium moves through brain tissue in the rat. , 1983, The Journal of physiology.

[11]  A. Reichenbach,et al.  Potassium buffering by Müller cells isolated from the center and periphery of the frog retina , 1999, Glia.

[12]  B W Connors,et al.  Activity-dependent shrinkage of extracellular space in rat optic nerve: a developmental study , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  A. Robert,et al.  Potassium homeostasis and glial energy metabolism , 1997 .

[14]  C. Nicholson,et al.  Changes of extracellular potassium activity induced by electric current through brain tissue in the rat. , 1983, The Journal of physiology.

[15]  R. Orkand,et al.  Modification of potassium movement through the retina of the drone (Apis mellifera male) by glial uptake. , 1983, The Journal of physiology.

[16]  M. Tsacopoulos,et al.  Potassium activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation. , 1979, The Journal of physiology.

[17]  E. Newman,et al.  Spatial buffering of light-evoked potassium increases by retinal Müller (glial) cells. , 1989, Science.

[18]  A. R. Gardner-Medwin,et al.  Clearance of extracellular potassium: evidence for spatial buffering by glial cells in the retina of the drone , 1981, Brain Research.

[19]  H. Kettenmann,et al.  Exclusive potassium dependence of the membrane potential in cultured mouse oligodendrocytes , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  R. H. Steinberg,et al.  Spatial buffering of K+ by the retinal pigment epithelium in frog , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  G. Somjen,et al.  Extracellular potassium activity, intracellular and extracellular potential responses in the spinal cord. , 1975, The Journal of physiology.

[22]  W. Walz Role of glial cells in the regulation of the brain ion microenvironment , 1989, Progress in Neurobiology.

[23]  D. Corey,et al.  Ion channels in vertebrate glia. , 1990, Annual review of neuroscience.

[24]  Shin-Ho Chung,et al.  Permeation of ions across the potassium channel: Brownian dynamics studies. , 1999, Biophysical journal.

[25]  A. Gardner-Medwin,et al.  Analysis of potassium dynamics in mammalian brain tissue. , 1983, The Journal of physiology.

[26]  I. Reisert,et al.  Volume densities and specific surfaces of neuronal and glial tissue elements in the rat supraoptic nucleus , 1982, The Journal of comparative neurology.

[27]  E. Newman High potassium conductance in astrocyte endfeet. , 1986, Science.

[28]  E A Newman,et al.  Inward-rectifying potassium channels in retinal glial (Muller) cells , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  E. Conway,et al.  Potassium accumulation in muscle and associated changes 1 , 1941 .

[30]  P. Grafe,et al.  Ion activities and potassium uptake mechanisms of glial cells in guinea‐pig olfactory cortex slices. , 1987, The Journal of physiology.

[31]  E. Newman,et al.  Regional specialization of retinal glial cell membrane , 1984, Nature.

[32]  A. Reichenbach,et al.  Spatial buffering of potassium by retinal müller (glial) cells of various morphologies calculated by a model , 1987, Neuroscience.

[33]  D. Taylor,et al.  Probing the structure of cytoplasm , 1986, The Journal of cell biology.

[34]  B. Barres,et al.  New roles for glia , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  L. Vyklický,et al.  Potassium currents in endfeet of isolated Müller cells from the frog retina , 1995, Glia.

[36]  C. Nicholson,et al.  Ion diffusion modified by tortuosity and volume fraction in the extracellular microenvironment of the rat cerebellum. , 1981, The Journal of physiology.

[37]  H. Sontheimer Voltage‐dependent ion channels in glial cells , 1994, Glia.

[38]  S. W. Kuffler,et al.  Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. , 1966, Journal of neurophysiology.

[39]  O B Paulson,et al.  Does the release of potassium from astrocyte endfeet regulate cerebral blood flow? , 1987, Science.

[40]  A. Lehmenkühler,et al.  Extracellular space parameters in the rat neocortex and subcortical white matter during postnatal development determined by diffusion analysis , 1993, Neuroscience.

[41]  B. Oakley,et al.  Spatial buffering of extracellular potassium by Müller (glial) cells in the toad retina. , 1992, Experimental eye research.

[42]  A. R. Gardner A New Framework for Assessment of Potassium‐Buffering Mechanisms , 1986 .

[43]  M H Ellisman,et al.  Inwardly rectifying K+ channels that may participate in K+ buffering are localized in microvilli of Schwann cells , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  D. Attwell,et al.  Endfeet of retinal glial cells have higher densities of ion channels that mediate K+ buffering , 1986, Nature.