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V. J. Kefalov, J.-S. Wang; Functional Cone-Specific Visual Cycle Within the Primate Retina. Invest. Ophthalmol. Vis. Sci. 2009;50(13):3003.
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Biochemical studies from cone-dominant species have suggested the existence of a cone-specific visual cycle for recycling chromophore within the retina that is independent of the pigment epithelium. The presence of such a visual cycle is controversial in mice and unknown in primates. To test the existence of a visual cycle in primate retina and determine its possible role in cone function, we investigated whether the isolated monkey retina can promote cone pigment regeneration and dark-adaptation independently of the pigment epithelium.
Using trans-retinal electroretinogram recordings from isolated primate retina, we recorded rod and cone photoresponses (a-wave) after pharmacologically blocking synaptic transmission. The eyeballs of freshly euthanized macaques were removed in bright light. The eyes were hemisected and their retinas, isolated or still attached to the pigment epithelium in the eyecup, were bleached with 40 sec bright white light and then allowed to recover in darkness for 3 hours prior to recordings.
Rod and cone pigments were initially bleached by extracting the eyes in bright light. Following dark-adaptation of the isolated retina, rod responses were undetectable. However, dark-adaptation of the isolated retina promoted recovery of cone response amplitude and sensitivity. In contrast, dark-adapting the retina in eyecup with pigment epithelium restored both cone and rod responses. Using the dark-adapted in that way retina, we obtained similar results following a subsequent 40 sec bleach. Cone sensitivity following a bleach in the isolated retina recovered within 7 minutes to 1/3 of its pre-bleach dark-adapted value. The incomplete recovery was most likely due to loss of chromophore from cones to the solution and to Müller cell damage during the dissection. In the presence of the pigment epithelium in eyecup, pigment regeneration and dark adaptation took place in both cones and rods. Cone recovery was blocked when the isolated retina was pre-incubated in the Müller cell-specific glyotoxin L--amino adipic acid (L--AAA) so that cone sensitivity was decreased over 100-fold by the bleach. The persistent bleaching adaptation in rods from isolated retina and cones from L--AAA treated isolated retina could be reversed by exogenous 11-cis-retinal.
Our results demonstrate that the isolated primate retina is able to promote pigment regeneration in cones, and not in rods, without pigment epithelium by instead using Müller cells. We establish the existence of a cone-specific visual cycle within the primate neural retina.
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