Metabolic Responses to Light in Monkey Photoreceptors

Abstract

Purpose: Transient changes in intraretinal oxygen tension (PO₂) in response to light stimuli were studied in order to understand the dynamics of light-evoked changes in photoreceptor oxidative metabolism.

Methods: PO₂ 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 (τ) and maximum PO₂ change.

Results: At the onset of light, PO₂ increased at all illuminations in all animals. The magnitude of the light-evoked PO₂ 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 PO₂ change (τ) 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 O₂ diffusion is fast over the short distance from the choroid to the inner segments, τ reflects the time course of the underlying change in oxidative metabolism.

Conclusions: 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 PO₂ data, it appears that these processes have time constants that differ by no more than a few seconds in primate. In monkeys, τ 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.

KEYWORDS::

• Non-human primate
• Monkey
• Retinal metabolism
• Photoreceptor
• Retina
• Oxygen
• Macaque

ACKNOWLEDGMENTS

This work was supported by NIH R01 EY05034. The authors thank Dr. Norbert D. Wangsa-Wirawan and Mrs. Yun Kim for their help during experiments and Mr. Kurt Qing for assistance with analysis.

Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.