Spatial and temporal patterns of growth and differentiation of cone oil droplets in the chick retina

Abstract

Avian cone photoreceptors have an oil droplet in the outer portion of their inner segment that acts as a long-pass cut-off filter between incident light and visual pigment. Chick cone droplets are mainly red, orange, yellow, green, and colorless, and the colors are due to three carotenoid pigments with characteristic absorption spectra. Little is known of the differentiation of this organelle, the natural marker of cones, and the little that is known is largely controversial. We used flat whole-mounts of fresh retinas to study the time and place of the appearance of droplets, their growth rates, the sequence of droplet color differentiation, and the spatial distribution of these colors. We show that droplet differentiation starts on embryonic Day 10 (E10) in a relatively small area above the optic nerve head. The differentiation spreads to the rest of the retina in a manner similar to that of photoreceptor neurogenesis, with three decreasing gradients of droplet size and color between E13-E20: from central to peripheral, dorsal to ventral, and temporal to nasal. The rate of growth of the droplets was not constant, but showed a maximum between E17 and postnatal Day 1 (P1) in most of the retinal zones. Color differentiation started at E16-E17, 5-6 days after their appearance, when the droplets were already of considerable size. Initially, all droplets were colorless, and then turned pale green or yellow to acquire progressively the mature colors. Differentiation ended in the whole retina by P15, with ventral droplets of larger diameter than dorsal ones, the peripheral ones generally larger than the central ones, and with the color distribution varying with the retinal area. Our results show that growth and color differentiation of the droplets is regulated temporally and spatially, and the cones complete differentiation at P15 rather than at prenatal stages, as is thought generally.

Avian Cone Photoreceptors Tile the Retina as Five Independent, Self-Organizing Mosaics

“…We found that at all timepoints examined, the data fall on the same curve as the data from P15 (inset in Figure 6A). Since oil droplet pigmentation first becomes apparent in the peripheral retina around E16–17 and full pigmentation of all the red cones first appears somewhat later [53], E18 was the earliest point at which we could reliably distinguish all cones of this type. We therefore conclude that, at least for red cones, the adult pattern of spatial organization is already achieved at the earliest point at which oil droplets can be distinguished.…”

Immunohistochemical characterization of the chick marginal retina

“…Other lines of evidence support this possibility. For instance, photoreceptor oil droplets appear first in the center and later in the periphery (22), and the developmental timing and distribution of wavelength-specific cone opsin expression also differs from center to periphery (1).…”

Developmental regulation of muscleblind‐like (MBNL) gene expression in the chicken embryo retina

“…8). The isolated photoreceptors were readily identified in the dissociates as rods, double cones, and single cones based on their structure and the shape of their outer segments; single cone subtypes were distinguished based on their characteristic oil droplets (López et al, 2005). These identification criteria have been verified by PCR of individual cells (Wahlin et al, 2004;Huang and Adler, 2005;Wahlin et al, 2007).…”