High extracellular potassium concentrations stimulate oxidative metabolism in a glutamatergic neuronal culture and glycolysis in cultured astrocytes but have no stimulatory effect in a GABAergic neuronal culture

Abstract

Rates of deoxyglucose accumulation and of CO 2 production from [U- 14C]glucose, or from [U- 14C]lactate or [2- 14C]pyruvate (as a determination of tricarboxylic acid (TCA) cycle activity) were determined in primary cultures of either astrocytes, cerebellar granule cell neurons (utilizing glutamate as their transmitter) or cerebral cortical interneurons (utilizing GABA as their transmitter) during control (‘resting’) conditions and during exposure to an elevated extracellular potassium concentration, mimicking functional activity. The elevation of the extracellular potassium concentration increased the rate of deoxyglucose accumulation, but not of TCA cycle activity in astrocytes and both deoxyglucose accumulation and TCA cycle activity in cerebellar granule cells, but had no stimulatory effect in cerebral cortical neurons. Based on these observations it is suggested that the increase in energy metabolism in the CNS in vivo during functional activity mainly reflects increased active accumulation of potassium ions and extrusion of sodium ions in neurons receiving excitatory input and in adjacent astrocytes in order to re-establish pre-stimulus ion distribution across cell membranes.