Changes in Astroglial K<sup>+</sup> upon Brief Periods of Energy Deprivation in the Mouse Neocortex
2022
Sara Eitelmann | Jonathan Stephan | Katharina Everaerts | Simone Durry | Nils Pape | Niklas J. Gerkau | Christine R. Rose
Malfunction of astrocytic K<sup>+</sup> regulation contributes to the breakdown of extracellular K<sup>+</sup> homeostasis during ischemia and spreading depolarization events. Studying astroglial K<sup>+</sup> changes is, however, hampered by a lack of suitable techniques. Here, we combined results from fluorescence imaging, ion-selective microelectrodes, and patch-clamp recordings in murine neocortical slices with the calculation of astrocytic [K<sup>+</sup>]. Brief chemical ischemia caused a reversible ATP reduction and a transient depolarization of astrocytes. Moreover, astrocytic [Na<sup>+</sup>] increased by 24 mM and extracellular [Na<sup>+</sup>] decreased. Extracellular [K<sup>+</sup>] increased, followed by an undershoot during recovery. Feeding these data into the Goldman–Hodgkin–Katz equation revealed a baseline astroglial [K<sup>+</sup>] of 146 mM, an initial K<sup>+</sup> loss by 43 mM upon chemical ischemia, and a transient K<sup>+</sup> overshoot of 16 mM during recovery. It also disclosed a biphasic mismatch in astrocytic Na<sup>+</sup>/K<sup>+</sup> balance, which was initially ameliorated, but later aggravated by accompanying changes in pH and bicarbonate, respectively. Altogether, our study predicts a loss of K<sup>+</sup> from astrocytes upon chemical ischemia followed by a net gain. The overshooting K<sup>+</sup> uptake will promote low extracellular K<sup>+</sup> during recovery, likely exerting a neuroprotective effect. The resulting late cation/anion imbalance requires additional efflux of cations and/or influx of anions, the latter eventually driving delayed astrocyte swelling.
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