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The Journal of Neuroscience, June 15, 1998, 18(12):4425-4438
Functional Specialization and Topographic Segregation of
Hippocampal Astrocytes
Raimondo
D'Ambrosio1,
Jurgen
Wenzel1,
Philip A.
Schwartzkroin1, 2,
Guy M.
McKhann II1, and
Damir
Janigro1
Departments of 1 Neurological Surgery and
2 Physiology and Biophysics, University of Washington,
Harborview Medical Center, Seattle, Washington 98104
Astrocytes have been suggested to play several roles in the complex
control of brain microenvironment. However, they have been generally
considered to constitute a homogeneous population of cells. Here we
show that at least three electrophysiologically distinct types of
astrocytes can be found in the mature hippocampus. These subpopulations
of glia were characterized by expression of different ion currents. In
astrocytes exposed to elevated K+,
Cs+ prevented influx of K+ only
in cells with inwardly rectifying currents
(IIR). The topographic distribution
of glia with Cs+-sensitive inward rectifying
currents (involved in K+ buffering) was nonuniform.
Cs+-sensitive astrocytes were predominantly found in
CA3 radiatum, whereas most CA1 astrocytes were
Cs+-insensitive. Functional significance of the
spatial segregation of glial cells with inward rectification was
addressed in slices that were bathed in
Cs+-containing media. Under these conditions,
neuronal stimulation induced spontaneous epileptiform activity, which
first appeared in CA3 and was then synaptically propagated to CA1.
Intracellular labeling of astrocytes with biocytin revealed that CA1
astrocytes are characterized by a high degree of cell-to-cell coupling;
in contrast, cell labeling in CA3 revealed smaller groups and
occasionally individual cells. Three individual biocytin-labeled cells
had electrophysiological properties indistinguishable from
Cs+-sensitive astrocytes but had morphology typical
of oligodendroglia. These results provide evidence for a role of
K+ uptake via IIR into
astrocytes. The segregated expression of potassium channels in a
subpopulation of astrocytes suggests that functionally specialized cell
types are involved in K+ homeostasis.
Key words:
glia neuronal interactions; oligodendroglia; cell-to-cell
coupling; ion homeostasis; extracellular space; patch clamp
Copyright © 1998 Society for Neuroscience 0270-6474/98/18124425-14$05.00/0
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