Optics of cone photoreceptors in the chicken (Gallus gallus domesticus)

Abstract

Vision is the primary sensory modality of birds, and its importance is evident in the sophistication of their visual systems. Coloured oil droplets in the cone photoreceptors represent an adaptation in the avian retina, acting as long-pass colour filters. However, we currently lack understanding of how the optical properties and morphology of component structures (e.g. oil droplet, mitochondrial ellipsoid and outer segment) of the cone photoreceptor influence the transmission of light into the outer segment and the ultimate effect they have on receptor sensitivity. In this study, we use data from microspectrophotometry, digital holographic microscopy and electron microscopy to inform electromagnetic models of avian cone photoreceptors to quantitatively investigate the integrated optical function of the cell. We find that pigmented oil droplets primarily function as spectral filters, not light collection devices, although the mitochondrial ellipsoid improves optical coupling between the inner segment and oil droplet. In contrast, unpigmented droplets found in violet-sensitive cones double sensitivity at its peak relative to other cone types. Oil droplets and ellipsoids both narrow the angular sensitivity of single cone photoreceptors, but not as strongly as those in human cones.

Coevolution of coloration and colour vision?

“…Even if avian visual photopigments are rather invariant, the relative numbers of the different cone types in the retina and the composition and density of oil droplet pigmentation might co-evolve with colour signals [37]. The oil droplets are pigmented by carotenoids that act as long-pass filters, thereby narrowing and red-shifting the cones' spectral sensitivities at the expense of the total light absorption [6]. Each cone type has a specific oil droplet: transparent (T, no pigment) in the UV/V (SWS1 opsin) cone, clear (C) in the blue (SWS2 opsin) cone, yellow (Y) in the green (RH2 opsin) cone and red (R) in the red (LWS opsin) cone [42,45].…”

Mechanisms of Photoreceptor Patterning in Vertebrates and Invertebrates

“…1C2)(40, 41). These cone types have been identified chiefly by differently colored oil droplets located between the inner and outer segments, which may act as a filter for specific wavelengths of light, as well as focusing photons onto the outer segment(42-45) (Fig. 1C2).…”

“…1C1). Further from the foveal center, cone packing becomes less dense(43, 45, 51, 52). In addition to the area centralis , rod numbers are reduced in a lateral stripe through the center of the retina(40) and in the dorsal retina ( central meridian and dorsal rod free zone , Fig.…”

Optical influence of oil droplets on cone photoreceptor sensitivity

“…Moreover, the enhancement factors do not reach the ideal predicted using receptor geometry, D G . In cylindrical outer segments, similar to chicken cones ( d OD =3 μm; d OS =1.5 μm; l OS =30 μm; Wilby et al, 2015) D G is 4, but calculated enhancement factors vary between 0.6 and 1.7, with the lowest values occurring for higher n OD and longer wavelength (Fig. 2A).…”

“…Dimensions and refractive indices were taken from the literature and are summarised in . For simplicity, a wavelength-invariant value of refractive index of 1.45 was used for the outer segment, as measured previously (Wilby et al, 2015). The refractive index change of the lipid membrane across the visible spectrum is <0.01 (Roberts et al, 2009) and the visual pigment has minimal influence on the refractive index (Stavenga and van Barneveld, 1975).…”