Vertebrate vision: About physical determinants of photoreceptor sensitivity and kinetics

Rod and cone photoreceptors transform information about incoming light into neural signals with broadly similar molecular mechanisms. Yet their sensitivity, response kinetics and adaptation properties are quite different as rods mediate dim-light vision and cones function mainly under daylight. This thesis 1. addresses the functional differences between rods and cones as well as mammalian and non-mammalian photoreceptors and 2. provides novel findings regarding the existence and regulation of rod-cone interactions at the photoreceptor level. Rod and cone photoresponses to brief flashes of light were recorded with electroretinogram (ERG) from isolated rodent and amphibian retinas. Various phototransduction models were used to compare their relevant parameters over a range of adapting conditions. The study focused on how the following physical factors shape and limit photoreceptor function: operating temperature, thermal stability of the amphibian long wavelength sensitive (A1-)visual pigment, outer segment dimensions, morphology and electrical connections between adjacent rods and cones. Mammalian rod photoreceptors generate faster photoresponses but light-adapt less efficiently than amphibian rods. In the rodent and anuran rods studied in this thesis, the main differences could be accounted for by the higher operating temperature and smaller outer segment size of the rodent photoreceptors. Additionally, the slender outer segments of the mammalian rods enabled sufficient quantal responses and high quantum catch despite the observed desensitizing effect of warming. Long wavelength -sensitive cone photoreceptors have been hypothesized to be desensitized by thermal excitation of their visual pigment molecules. However, it has been shown experimentally only in amphibian cones that utilize the A2-chromophore. The relative stability of the A1-based cone pigments - used by all terrestrial vertebrates - has remained unclear, as well as its role in limiting cone function. In this study, thermal isomerization rate of the long wavelength sensitive (A1-)visual pigment was estimated to play at most a minor role in regulating cone sensitivity of the frog Rana temporaria. Finally, ERG light responses originating in mouse cone photoreceptors were found to be suppressed in the dark-adapted retina, apparently through direct electrical coupling between rods and cones. The results indicated this coupling is weakened by moderate background light, explaining a long known phenomenon of unknown origin: light-induced growth of cone flash responses in mammalian ERG. This is indicative of a previously unknown mechanism of retinal adaptation.