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J Neurophysiol 84: 2746-2757, 2000;
0022-3077/00 $5.00
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The Journal of Neurophysiology Vol. 84 No. 6 December 2000, pp. 2746-2757
Copyright ©2000 by the American Physiological Society

Freshly Isolated Astrocytes From Rat Hippocampus Show Two Distinct Current Patterns and Different [K+]o Uptake Capabilities

Min Zhou and Harold K. Kimelberg

Center for Neuropharmacology and Neuroscience and Division of Neurosurgery, Albany Medical College, Albany, New York 12208

Zhou, Min and Harold K. Kimelberg. Freshly Isolated Astrocytes From Rat Hippocampus Show Two Distinct Current Patterns and Different [K+]o Uptake Capabilities. J. Neurophysiol. 84: 2746-2757, 2000. Whether astrocytes predominantly express ohmic K+ channels in vivo, and how expression of different K+ channels affects [K+]o homeostasis in the CNS have been long-standing questions for how astrocytes function. In the present study, we have addressed some of these questions in glial fibrillary acidic protein [GFAP(+)], freshly isolated astrocytes (FIAs) from CA1 and CA3 regions of P7-15 rat hippocampus. As isolated, these astrocytes were uncoupled allowing a higher resolution of electrophysiological study. FIAs showed two distinct ion current profiles, with neither showing a purely linear I-V relationship. One population of astrocytes had a combined expression of outward potassium currents (IKa, IKd) and inward sodium currents (INa). We term these outwardly rectifying astrocytes (ORA). Another population of astrocytes is characterized by a relatively symmetric potassium current pattern, comprising outward IKdr, IKa, and abundant inward potassium currents (IKin), and a larger membrane capacitance (Cm) and more negative resting membrane potential (RMP) than ORAs. We term these variably rectifying astrocytes (VRA). The IKin in 70% of the VRAs was essentially insensitive to Cs+, while IKin in the remaining 30% of VRAs was sensitive. The IKa of VRAs was most sensitive to 4-aminopyridine (4-AP), while IKdr of ORAs was more sensitive to tetraethylammonium (TEA). ORAs and VRAs occurred approximately equally in FIAs isolated from the CA1 region (52% ORAs versus 48% VRAs), but ORAs were enriched in FIAs isolated from the CA3 region (71% ORAs versus 29% VRAs), suggesting an anatomical segregation of these two types of astrocytes within the hippocampus. VRAs, but not ORAs, showed robust inward currents in response to an increase in extracellular K+ from 5 to 10 mM. As VRAs showed a similar current pattern and other passive membrane properties (e.g., RMP, Rin) to "passive astrocytes"in situ (i.e., these showing linear I-V curves), such passive astrocytes possibly represent VRAs influenced by extensive gap-junction coupling in situ. Thus, our data suggest that, at least in CA1 and CA3 regions from P7-15 rats, there are two classes of GFAP(+) astrocytes which possess different K+ currents. Only VRAs seem suited to uptake of extracellular K+ via IKin channels at physiological membrane potentials and increases of [K+]o. ORAs show abundant outward potassium currents with more depolarized RMP. Thus VRAs and ORAs may cooperate in vivo for uptake and release of K+, respectively.




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