Highlights d RGR opsin and Rdh10 convert atROL to 11cROL upon exposure to visible light d Normal mouse retinas maintain cone sensitivity during exposure to background light d RgrÀ/À mouse retinas progressively lose cone sensitivity during light exposure d Treatment of normal mouse retinas with a M€ uller cell toxin replicates the RgrÀ/À phenotype
The brilliantly coloured cone oil droplets of the avian retina function as long-pass cut-off filters that tune the spectral sensitivity of the photoreceptors and are hypothesized to enhance colour discrimination and improve colour constancy. Although it has long been known that these droplets are pigmented with carotenoids, their precise composition has remained uncertain owing to the technical challenges of measuring these very small, dense and highly refractile optical organelles. In this study, we integrated results from high-performance liquid chromatography, hyperspectral microscopy and microspectrophotometry to obtain a comprehensive understanding of oil droplet carotenoid pigmentation in the chicken (Gallus gallus). We find that each of the four carotenoid-containing droplet types consists of a complex mixture of carotenoids, with a single predominant carotenoid determining the wavelength of the spectral filtering cut-off. Consistent with previous reports, we find that the predominant carotenoid type in the oil droplets of long-wavelength-sensitive, medium-wavelength-sensitive and short-wavelength-sensitive type 2 cones are astaxanthin, zeaxanthin and galloxanthin, respectively. In addition, the oil droplet of the principal member of the double cone contains a mixture of galloxanthin and two hydroxycarotenoids (lutein and zeaxanthin). Short-wavelength-absorbing apocarotenoids are present in all of the droplet types, providing filtering of light in a region of the spectrum where filtering by hydroxy-and ketocarotenoids may be incomplete. Thus, birds rely on a complex palette of carotenoid pigments within their cone oil droplets to achieve finely tuned spectral filtering.
Key points• When photoreceptors in vertebrate retina are exposed to bright light, a significant proportion of the photopigment in the rods can be bleached.• Bleaching produces a desensitization of the visual system that recovers slowly as pigment is slowly regenerated, by a process known as dark adaptation.• Experiments on isolated amphibian rods have revealed some of the features of bleach-induced desensitization, but such experiments have not so far been possible on mammals.• We now describe an improved method that makes possible the first direct measurements of pigment concentration and rod photoreceptor responses over a wide range of bleaching exposures from isolated cells or pieces of intact mammalian retina.• Our experiments reveal important features of mammalian bleaching adaptation and will now make possible future studies from mouse animal lines containing genetically altered photoreceptor proteins.Abstract When a substantial fraction of rhodopsin in a rod photoreceptor is exposed to bright light, the rod is desensitized by a process known as bleaching adaptation. Experiments on isolated photoreceptors in amphibians have revealed many of the features of bleaching adaptation, but such experiments have not so far been possible in mammals. We now describe a method for making microspectrophotometric measurements of pigment concentration and suction-electrode recording of electrical responses over a wide range of bleaching exposures from isolated mouse rods or pieces of mouse retina. We show that if pigment is bleached at a low rate in the presence of bovine serum albumin (BSA), and intermediate photoproducts are allowed to decay, mouse rods are stably desensitized; subsequent treatment with exogenous 11-cis retinal results in pigment regeneration and substantial recovery of sensitivity to the dark-adapted value. Stably bleached wild-type (WT) rods show a decrease in circulating current and acceleration of the time course of decay, much as in steady background light; similar effects are seen in guanylyl cyclase-activating protein knockout (GCAPs −/− ) rods, indicating that regulation of guanylyl cyclase is not necessary for at least a part of the adaptation produced by bleaching. Our experiments demonstrate that in mammalian rods, as in amphibian rods, steady-state desensitization after bleaching is produced by two components: (1) a reduction in the probability of photon absorption produced by a decrease in rhodopsin concentration; and (2) an equivalent background light whose intensity is proportional to the fraction of bleached pigment, and which adapts the rod like real background light. These two mechanisms together fully account for the 'log-linear' relationship in mammalian retina between sensitivity and per cent bleach, which can be measured in the steady state following exposure to S. Nymark and R. Frederiksen contributed equally to the work. bright light. Our methods will now make possible an examination of bleaching adaptation and pigment regeneration in mouse animal lines with mutations or other al...
Nocturnal animals relying on vision typically have eyes that are optically and morphologically adapted for both increased sensitivity and greater information capacity in dim light. Here, we investigate whether adaptations for increased sensitivity also are found in their photoreceptors by using closely related and fast-flying nocturnal and diurnal bees as model animals. The nocturnal bee Megalopta genalis is capable of foraging and homing by using visually discriminated landmarks at starlight intensities. Megalopta's near relative, Lasioglossum leucozonium, performs these tasks only in bright sunshine. By recording intracellular responses to Gaussian white-noise stimuli, we show that photoreceptors in Megalopta actually code less information at most light levels than those in Lasioglossum. However, as in several other nocturnal arthropods, Megalopta's photoreceptors possess a much greater gain of transduction, indicating that nocturnal photoreceptors trade information capacity for sensitivity. By sacrificing photoreceptor signal-to-noise ratio and information capacity in dim light for an increased gain and, thus, an increased sensitivity, this strategy can benefit nocturnal insects that use neural summation to improve visual reliability at night.
Visual pigments can be spontaneously activated by internal thermal energy, generating noise that interferes with real-light detection. Recently, we developed a physicochemical theory that successfully predicts the rate of spontaneous activity of representative rod and cone pigments from their peak-absorption wavelength (l max ), with pigments having longer l max being noisier. Interestingly, cone pigments may generally be~25 fold noisier than rod pigments of the same l max , possibly ascribed to an 'open' chromophore-binding pocket in cone pigments defined by the capability of chromophore-exchange in darkness. Here, we show in mice that the l max -dependence of pigment noise could be extended even to a mutant pigment, E122Q-rhodopsin. Moreover, although E122Q-rhodopsin shows some cone-pigment-like characteristics, its noise remained quantitatively predictable by the 'non-open' nature of its chromophore-binding pocket as in wildtype rhodopsin. The openness/closedness of the chromophore-binding pocket is potentially a useful indicator of whether a pigment is intended for detecting dim or bright light.
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