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The Journal of Neuroscience, May 17, 2006, 26(20):5438-5447; doi:10.1523/JNEUROSCI.0037-06.2006
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Behavioral/Systems/Cognitive
The Impact of Astrocytic Gap Junctional Coupling on Potassium Buffering in the Hippocampus
Anke Wallraff,1 Rüdiger Köhling,2 Uwe Heinemann,3 Martin Theis,5 Klaus Willecke,4 andChristian Steinhäuser1 1Department of Experimental Neurobiology, Neurosurgery, University of Bonn, 53105 Bonn, Germany, 2Institute of Physiology, University of Rostock, 18057 Rostock, Germany, 3Institute of Neurophysiology, Charité Universitätsmedizin Berlin, 10117 Berlin, Germany, 4Institute of Genetics, University of Bonn, 53117 Bonn, Germany, and 5Howard Hughes Medical Institute, Center for Neurobiology and Behavior, Columbia University, New York, New York 10032
Correspondence should be addressed to Dr. Christian Steinhäuser, Department of Experimental Neurobiology, Neurosurgery, University of Bonn, Sigmund-Freud-Strasse 25, D-53125 Bonn, Germany. Email: christian.steinhaeuser{at}ukb.uni-bonn.de
Astrocytic gap junctions have been suggested to contribute to spatial buffering of potassium in the brain. Direct evidence has been difficult to gather because of the lack of astrocyte-specific gap junction blockers. We obtained mice with coupling-deficient astrocytes by crossing conditional connexin43-deficient mice with connexin30–/– mice. Similar to wild-type astrocytes, genetically uncoupled hippocampal astrocytes displayed negative resting membrane potentials, time- and voltage-independent whole-cell currents, and typical astrocyte morphologies. Astrocyte densities were also unchanged. Using potassium-selective microelectrodes, we assessed changes in potassium buffering in hippocampal slices of mice with coupling-deficient astrocytes. We demonstrate that astrocytic gap junctions accelerate potassium clearance, limit potassium accumulation during synchronized neuronal firing, and aid in radial potassium relocation in the stratum lacunosum moleculare. Furthermore, slices of mice with coupling-deficient astrocytes displayed a reduced threshold for the generation of epileptiform events. However, it was evident that radial relocation of potassium in the stratum radiatum was not dependent on gap junctional coupling. We suggest that the perpendicular array of individual astrocytes in the stratum radiatum makes these cells ideally suited for spatial buffering of potassium released by pyramidal cells, independent of gap junctions. In general, a surprisingly large capacity for K+ clearance was conserved in mice with coupling-deficient astrocytes, indicating that gap junction-dependent processes only partially account for K+ buffering in the hippocampus.
Key words: Cx43; Cx30; epileptiform events; potassium buffering; hippocampus; astrocyte
Received Jan. 5, 2006; revised April 12, 2006; accepted April 12, 2006.
Correspondence should be addressed to Dr. Christian Steinhäuser, Department of Experimental Neurobiology, Neurosurgery, University of Bonn, Sigmund-Freud-Strasse 25, D-53125 Bonn, Germany. Email: christian.steinhaeuser{at}ukb.uni-bonn.de
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