Functional role of the potassium‐induced stimulation of oxygen uptake in brain slices studied with cesium as a probe

Abstract

The potassium-induced stimulation of oxygen consumption in brain slices has a threshold value of 15-20 mM potassium, and it reaches its maximum at 35-50 mM. Although this phenomenon now has been known for almost 50 years, its physiological role remains undetermined. One reason for this may be that the high concentrations of potassium that are required for this response also have many other consequences, e.g., a depolarization of the cells, and that the different effects to some extent may mask each other. For this reason this investigation studied the effects of cesium, which evokes a maximal stimulation of oxygen consumption already at 15 mM. Like potassium, concentrations of cesium that stimulate oxygen consumption also lead to an enhanced swelling. Unlike potassium, the sodium content is affected very little by these concentrations of cesium, whereas cesium and chloride contents are increased. On this basis it is concluded that the cesium-induced stimulation of oxygen uptake is a metabolic manifestation of an active uptake of cesium and chloride, which secondarily leads to an uptake of water, i.e., the cesium-induced swelling. Analogously, it is suggested that the potassium-induced stimulation of oxygen uptake represents an active accumulation of potassium and chloride.

Energy Metabolism in Astrocytes: High Rate of Oxidative Metabolism and Spatiotemporal Dependence on Glycolysis/Glycogenolysis

“…The stimulation of oxygen uptake in brain slices by elevated [K + ] e is also accompanied by astrocytic cell swelling (Hertz and Kjeldsen, 1985). This finding further supports a correlation between K + -mediated stimulation of oxygen consumption and activation of the Na + , K + , 2Cl − cotransporter with its subsequent stimulation of Na + , K + -ATPase activity, because the cotransporter and the Na + ,K + -ATPase together mediate net uptake of 2K + plus 2Cl − into the cells (Figure 3), and the ion uptake, for osmotic reasons, is accompanied by entry of water and cell swelling.…”

Ions, water, and energy in brain cells: A synopsis of interrelations

“…1). The proposed sequence of events between stimulation of oxidative metabolism, increase in intracellular C 0 2 tension, intracellular alkalinization, and accumulation of Na+, together with either HC0: or C1-, in astrocytes might account for an apparently close correlation between stimulation s f oxygen consumption and swelling in brain slices during exposure to elevated concentrations of either potassium or cesium (Hertz and Kjeldsen 1985). Alternatively, glial swelling in brain slices might be due mainly to extracellular accumulation of neuronally released compounds like glutamate (see below).…”

A tribute to Leif Hertz: The historical context of his pioneering studies of the roles of astrocytes in brain energy metabolism, neurotransmission, cognitive functions, and pharmacology identifies important, unresolved topics for future studies

“…Early studies in Leif Hertz' career demonstrated that high levels of K + enhanced respiration in cultured astrocytes and acute brain slices, indicating a primary metabolic effect on respiration in astrocytes, not neurons, in living brain tissue (Hertz et al, 1973; Hertz & Kjeldsen, 1985). Peng, Hertz, and colleagues (Peng et al, 1994; Peng & Hertz, 1993) subsequently reported that increased extracellular [K + ] stimulated oxidative metabolism of glucose in glutamatergic neuronal cultures and astrocytic cultures and enhanced glucose utilization (measured as [ 14 C]DG phosphorylation) in cultured astrocytes.…”