Extracellular K⁺ reflects light-evoked changes in retinal energy metabolism

Retinal neurons spend most of their energy to support the transmembrane movement of ions. Light-induced electrical activity is associated with a redistribution of ions, which affects the energy demand and results in a change in metabolism. Light-induced metabolic changes are expected to be different in distal and proximal retina due to differences in the light responses of different retinal cells. Extracellular K⁺ concentration ([K⁺]_o) is a reliable indicator of local electrophysiological activity, and the purpose of this work was to compare [K⁺]_o changes evoked by steady and flickering light in distal and proximal retina. Data were obtained from isolated mouse (C57Bl/6J) retinae. Double-barreled K⁺-selective microelectrodes were used to simultaneously record [K⁺]_o and local ERGs. In the distal retina, photoreceptor hyperpolarization led to suppression of ion transfer, a decrease in [K⁺]_o by 0.3-0.5 mM, reduced energy demand, and, as previously shown in vivo, decreased metabolism. Flickering light had the same effect on [K⁺]_o in the distal retina as steady light of equivalent illumination. The conductance and voltage changes in postreceptor neurons are cell-specific, but the overall effect of steady light in the proximal retina is excitation, which is reflected in a [K⁺]_o increase there (by a maximum of 0.2 mM). In steady light the [K⁺]_o increase lasts only 1-2 s, but a sustained [K⁺]_o increase is evoked by flickering light. A squarewave low frequency (1 Hz) flicker of photopic intensity produced the largest increases in [K⁺]_o. Judging by measurements of [K⁺]_o, steady illumination decreases energy metabolism in the distal retina, but not in the proximal retina (except for the first few seconds). Flickering light evokes the same decrease in the distal retina, but also evokes a sustained [K⁺]_o increase in the proximal retina, suggesting an increase of metabolic demand there, especially at 1 Hz, when neurons of both on- and off-pathways appear to contribute maximally. This proximal retinal metabolic response to flicker correlates to the increase in blood flow during flicker that constitutes neurovascular coupling.