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PMID: 10827962 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Spatial buffering of potassium ions in brain extracellular space.

Biophysical journal ·Vol. 78 ·No. 6 ·2000-06-00 ·Pages 2776-97

Chen KC, Nicholson C

Abstract

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.

MeSH Terms
Animals Brain/physiology Cell Membrane/physiology Extracellular Space/physiology Kinetics Membrane Potentials Models, Neurological Neuroglia/physiology Potassium/physiology Potassium Channels/physiology
Chemicals
Potassium Channels Potassium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Chen K C
Department of Physiology and Neuroscience, New York University Medical School, New York, NY 10016, USA.
Nicholson C
References (44)
44 references, click to expand
  1. Spatial buffering of extracellular potassium by Müller (glial) cells in the toad retina.
    Exp Eye Res. 1992 Oct;55(4):539-50 PMID: 1483500
  2. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia.
    J Neurophysiol. 1966 Jul;29(4):788-806 PMID: 5966435
  3. Model of potassium dynamics in the central nervous system.
    Glia. 1988;1(3):198-210 PMID: 2976039
  4. Spatial buffering of K+ by the retinal pigment epithelium in frog.
    J Neurosci. 1986 Nov;6(11):3197-204 PMID: 3490548
  5. Extracellular space parameters in the rat neocortex and subcortical white matter during postnatal development determined by diffusion analysis.
    Neuroscience. 1993 Jul;55(2):339-51 PMID: 8377929
  6. Spatial buffering of potassium by retinal Müller (glial) cells of various morphologies calculated by a model.
    Neuroscience. 1987 Aug;22(2):687-96 PMID: 3670605
  7. Regional specialization of retinal glial cell membrane.
    Nature. 1984 May 10-16;309(5964):155-7 PMID: 6717594
  8. Permeation of ions across the potassium channel: Brownian dynamics studies.
    Biophys J. 1999 Nov;77(5):2517-33 PMID: 10545353
  9. Activity-dependent shrinkage of extracellular space in rat optic nerve: a developmental study.
    J Neurosci. 1985 Feb;5(2):532-5 PMID: 3973681
  10. Potassium homeostasis and glial energy metabolism.
    Glia. 1997 Sep;21(1):46-55 PMID: 9298846
  11. Physiological properties of glial cells in the central nervous system of amphibia.
    J Neurophysiol. 1966 Jul;29(4):768-87 PMID: 5966434
  12. Modification of potassium movement through the retina of the drone (Apis mellifera male) by glial uptake.
    J Physiol. 1983 Jul;340:157-74 PMID: 6887045
  13. A new framework for assessment of potassium-buffering mechanisms.
    Ann N Y Acad Sci. 1986;481:287-302 PMID: 3468861
  14. Analysis of potassium dynamics in mammalian brain tissue.
    J Physiol. 1983 Feb;335:393-426 PMID: 6875885
  15. Extracellular K+ accumulation in the central nervous system.
    Prog Biophys Mol Biol. 1983;42(2-3):135-89 PMID: 6139844
  16. Relations between slow extracellular potential changes, glial potassium buffering, and electrolyte and cellular volume changes during neuronal hyperactivity in cat brain.
    Glia. 1989;2(1):25-44 PMID: 2523337
  17. Ion diffusion modified by tortuosity and volume fraction in the extracellular microenvironment of the rat cerebellum.
    J Physiol. 1981 Dec;321:225-57 PMID: 7338810
  18. Is the potassium channel distribution in glial cells optimal for spatial buffering of potassium?
    Biophys J. 1985 Nov;48(5):843-7 PMID: 2416364
  19. Model of electroretinogram b-wave generation: a test of the K+ hypothesis.
    J Neurophysiol. 1984 Jan;51(1):164-82 PMID: 6319623
  20. Role of glial cells in the regulation of the brain ion microenvironment.
    Prog Neurobiol. 1989;33(4):309-33 PMID: 2479051
  21. Membrane physiology of retinal glial (Müller) cells.
    J Neurosci. 1985 Aug;5(8):2225-39 PMID: 3874934
  22. Changes of extracellular potassium activity induced by electric current through brain tissue in the rat.
    J Physiol. 1983 Feb;335:375-92 PMID: 6875884
  23. Exclusive potassium dependence of the membrane potential in cultured mouse oligodendrocytes.
    J Neurosci. 1983 Mar;3(3):500-5 PMID: 6827306
  24. Potassium accumulation in muscle and associated changes.
    J Physiol. 1941 Aug 11;100(1):1-63 PMID: 16991506
  25. Extracellular potassium activity, intracellular and extracellular potential responses in the spinal cord.
    J Physiol. 1975 Oct;252(1):115-36 PMID: 1202194
  26. New roles for glia.
    J Neurosci. 1991 Dec;11(12):3685-94 PMID: 1720814
  27. Potassium currents in endfeet of isolated Müller cells from the frog retina.
    Glia. 1995 Sep;15(1):54-64 PMID: 8847101
  28. Endfeet of retinal glial cells have higher densities of ion channels that mediate K+ buffering.
    Nature. 1986 Dec 4-10;324(6096):466-8 PMID: 2431322
  29. Volume densities and specific surfaces of neuronal and glial tissue elements in the rat supraoptic nucleus.
    J Comp Neurol. 1982 Nov 10;211(4):427-31 PMID: 7174904
  30. Probing the structure of cytoplasm.
    J Cell Biol. 1986 Jun;102(6):2015-22 PMID: 2423529
  31. Inward-rectifying potassium channels in retinal glial (Müller) cells.
    J Neurosci. 1993 Aug;13(8):3333-45 PMID: 8340811
  32. Potassium activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation.
    J Physiol. 1979 May;290(2):525-49 PMID: 469798
  33. High potassium conductance in astrocyte endfeet.
    Science. 1986 Jul 25;233(4762):453-4 PMID: 3726539
  34. Does the release of potassium from astrocyte endfeet regulate cerebral blood flow?
    Science. 1987 Aug 21;237(4817):896-8 PMID: 3616619
  35. Inwardly rectifying K+ channels that may participate in K+ buffering are localized in microvilli of Schwann cells.
    J Neurosci. 1996 Apr 15;16(8):2421-9 PMID: 8786419
  36. Potassium buffering by Müller cells isolated from the center and periphery of the frog retina.
    Glia. 1999 Aug;27(2):171-80 PMID: 10417816
  37. Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices.
    J Physiol. 1987 Jan;382:159-74 PMID: 2442359
  38. Ion channels in vertebrate glia.
    Annu Rev Neurosci. 1990;13:441-74 PMID: 2158266
  39. Extracellular space structure revealed by diffusion analysis.
    Trends Neurosci. 1998 May;21(5):207-15 PMID: 9610885
  40. Clearance of extracellular potassium: evidence for spatial buffering by glial cells in the retina of the drone.
    Brain Res. 1981 Mar 30;209(2):452-7 PMID: 6261870
  41. Stimulus-induced changes in extracellular Na+ and Cl- concentration in relation to changes in the size of the extracellular space.
    Exp Brain Res. 1982;46(1):73-84 PMID: 6279427
  42. Spatial buffering of light-evoked potassium increases by retinal Müller (glial) cells.
    Science. 1989 May 5;244(4904):578-80 PMID: 2785716
  43. A study of the mechanisms by which potassium moves through brain tissue in the rat.
    J Physiol. 1983 Feb;335:353-74 PMID: 6875883
  44. Voltage-dependent ion channels in glial cells.
    Glia. 1994 Jun;11(2):156-72 PMID: 7523291
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2000-06-00
Pages
2776-97
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1300867
Subset
IM
Grants
NINDS NIH HHS · NS 28642 · United States
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