Metabolic responses to light in monkey photoreceptors

Transient changes in intraretinal oxygen tension (PO(2)) in response to light stimuli were studied in order to understand the dynamics of light-evoked changes in photoreceptor oxidative metabolism.

PO(2) changes during illumination were recorded by double-barreled microelectrodes in the outer part of the perifoveal retina in five macaques (Rhesus and Cynomolgus) and were fitted to a single exponential equation to obtain the time constant (tau) and maximum PO(2) change.

At the onset of light, PO(2) increased at all illuminations in all animals. The magnitude of the light-evoked PO(2) change increased with increasing illumination over 3-4 log units but decreased in all animals at the maximum illumination. The median time constant of the PO(2) change (tau) was 26 sec and was not correlated with illumination. The time constant for the return to darkness was similar for illuminations below rod saturation. Since O(2) diffusion is fast over the short distance from the choroid to the inner segments, tau reflects the time course of the underlying change in oxidative metabolism.

Previous results suggested that two competing processes influence the change in photoreceptor oxidative metabolism with light, Na(+)/K(+) pumping and cyclic guanosine monophosphate (cGMP) turnover. Because a single exponential fitted the PO(2) data, it appears that these processes have time constants that differ by no more than a few seconds in primate. In monkeys, tau is longer than previously reported values for cat and rat. Longer time constants are related to larger photoreceptor volume, possibly because metabolic rate is controlled by intracellular Na(+), and a change in intracellular Na(+) after the onset of illumination occurs more slowly in larger photoreceptors. The "metabolic threshold" illumination that reduced oxygen consumption by about 10% is approximately the same as the illumination that closes 10% of the light-dependent cation channels that are open in the dark.