Functional significance of the taper of vertebrate cone photoreceptors

Abstract

Vertebrate photoreceptors are commonly distinguished based on the shape of their outer segments: those of cones taper, whereas the ones from rods do not. The functional advantages of cone taper, a common occurrence in vertebrate retinas, remain elusive. In this study, we investigate this topic using theoretical analyses aimed at revealing structure–function relationships in photoreceptors. Geometrical optics combined with spectrophotometric and morphological data are used to support the analyses and to test predictions. Three functions are considered for correlations between taper and functionality. The first function proposes that outer segment taper serves to compensate for self-screening of the visual pigment contained within. The second function links outer segment taper to compensation for a signal-to-noise ratio decline along the longitudinal dimension. Both functions are supported by the data: real cones taper more than required for these compensatory roles. The third function relates outer segment taper to the optical properties of the inner compartment whereby the primary determinant is the inner segment’s ability to concentrate light via its ellipsoid. In support of this idea, the rod/cone ratios of primarily diurnal animals are predicted based on a principle of equal light flux gathering between photoreceptors. In addition, ellipsoid concentration factor, a measure of ellipsoid ability to concentrate light onto the outer segment, correlates positively with outer segment taper expressed as a ratio of characteristic lengths, where critical taper is the yardstick. Depending on a light-funneling property and the presence of focusing organelles such as oil droplets, cone outer segments can be reduced in size to various degrees. We conclude that outer segment taper is but one component of a miniaturization process that reduces metabolic costs while improving signal detection. Compromise solutions in the various retinas and retinal regions occur between ellipsoid size and acuity, on the one hand, and faster response time and reduced light sensitivity, on the other.

Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors

“…In contrast, migrations to new environments do not induce changes in cone outer segment morphology (e.g. size, taper) in salmonid fishes, and we are not aware of reports to the contrary for other animals featured in the literature (Hárosi and Novales Flamarique, 2012). It thus seems that the reported phenotypic plasticity in opsin expression of fishes is probably based on changes in the relative numbers of spectral cone types.…”

“…At the ellipsoid level, single and double cones formed square mosaics in the ventral retina (Fig.5G) and mostly row mosaics in the rest of the retina (Fig.5D). As is the case for the majority of fish species that have been studied (see Hárosi and Novales Flamarique, 2012), the square mosaic unit of the threespine stickleback consisted of four double cones forming a square, or cruciform, arrangement and a variable number of single cones, from 1 to 5 (Fig.5A-C,G-I). Single cones were predominantly central in the mosaic unit, at the hypothetical intersection of neighbouring double cone partitions (Novales Flamarique, 2001;Cheng et al, 2006), but a few corner cones could also be found in the central and centro-dorsal areas of the retina (Fig.5A,B).…”

“…Microspectrophotometry, the other technique employed in these studies, can only be used to support correlative trends between cone types and opsin expression as sample size is extremely small, in comparison with photoreceptor numbers in the retina (Fein and Szuts, 1982), and most studied animals have topographical variation in both opsin expression and photoreceptor types across the retina (see Hárosi and Novales Flamarique, 2012). In the above studies (Fuller et al, 2005;Shand et al, 2008;Hofmann et al, 2010;Fuller and Claricoates, 2011), differences in opsin expression are assumed to reflect changes in the abundance of the various cone types or differences in the size and/or visual pigment density of cone outer segments (Fuller and Claricoates, 2011), the ciliary structures whose lamellae house the visual pigments (Fein and Szuts, 1982).…”

Evolutionary transformation of rod photoreceptors in the all-cone retina of a diurnal garter snake

“…Enlarged, rod-like outer segments are known to increase sensitivity by increasing cell volume and, as a result, the number of visual pigment molecules available to catch photons (3,34). Recent theoretical work has proposed that the small tapering outer segments of cones may help to reduce self-screening of the visual pigments, increase signal-to-noise ratios, and allow light to more efficiently be focused on the outer segment by the ellipsoid (35). Interestingly, recent work has also suggested that reduction of RH1 expression alone can result in a more cone-like morphology, decreasing the photosensitivity of the cell and increasing the kinetics of the phototransduction cascade (34,36,37).…”

Early development of the nervous system of the eutherian <i>Tupaia belangeri</i>

“…Addressing the optical properties of photoreceptor cells which, by geometry of the outer segment alone, "compensate for self-screening of the visual pigments" and/or for a "signal-to-noise ratio decline along the longitudinal dimension" (Hárosi and Novales Flamarique, 2012) will remain a fascinating research objective. Introducing megamitochondria into this field as a new mosaic piece has inspired the search for other organelles which are placed in the optic pathway and which may have an influence on the incoming light.…”