Calcium gradients and light-evoked calcium changes outside rods in the intact cat retina

We have studied light-evoked changes in extracellular Ca2+ concentration ([Ca2+]o) in the intact cat eye using ion-sensitive double-barreled microelectrodes. Two prominent changes in Ca2+ concentration were observed that differed in retinal location. There was a light-evoked increase in [Ca2+]o, accompanied by brief ON and OFF transients, which was maximal in the inner plexiform layer and was not further studied. There was an unexpected sustained light-evoked decrease in [Ca2+]o, of relatively rapid onset and offset, which was maximal in the distalmost region of the subretinal space (SRS). [Ca2+]o in the SRS was 1.0 mM higher than in the vitreous humor during dark adaptation and this transretinal gradient disappeared during rod-saturating illumination. After correcting for the light-evoked increase in the volume of the SRS, an increase in the total Ca2+ content of the SRS during illumination was revealed, which presumably represents the Ca2+ released by rods. To explain the light-evoked [Ca2+]o changes, we used the diffusion model described in the accompanying paper (Li et al., 1994b), with the addition of light-dependent sources of Ca2+ at the retina/retinal pigment epithelium (RPE) border and rod outer segments. We conclude that a drop in [Ca2+]o around photoreceptors, which persists during illumination and reduces a transretinal Ca2+ gradient, is the combined effect of the light-evoked SRS volume increase, Ca2+ release from photoreceptors, and an unidentified mechanism(s), which is presumably Ca2+ transport by the RPE. The relatively rapid onset and offset of the [Ca2+]o decrease remains unexplained. These steady-state shifts in [Ca2+]o should have significant effects on photoreceptor function, especially adaptation.