Morphogenesis of the different types of photoreceptors of the chicken (Gallus domesticus) retina and the effect of amblyopia in neonatal chicken

Abstract

Despite the great variety in chicken photoreceptors, existing morphogenetic studies only deal with two types: rods and cones. We have therefore examined by scanning electron microscopy the first appearance and maturation of different retinal photoreceptors in 36 chicken embryos (Gallus domesticus), aged 5-19 days prehatching. On day 5 of incubation, chicken retinae were only composed of proliferating ventricular cells devoid of photoreceptors. On day 8, outer mitotic cells were separated from inner differentiating photoreceptors, by the transient layer of Chievitz. Ball-like protrusions appeared at the ventricular surface, representing the first signs of photoreceptor inner segment formation. From day 10 onward, double cones, single cones, and rods could be clearly distinguished, and occasional cilia were detected at their tip. On day 12, inner segments had increased in length and diameter, and frequently carried a cilium representing the beginning of outer segment formation. On day 14, most photoreceptors displayed a distinct outer segment. On day 19, photoreceptors had essentially assumed adult morphology. Based on the shape of their outer segments, two subtypes of cones and three subtypes of double cones could be distinguished. Throughout development, we observed microvilli close to maturing photoreceptors, either originating from their lateral sides, from their tip, or from Müller cells. Microvillus density peaked between day 12 and 14, indicating an important role in photoreceptor morphogenesis. Unilateral occlusion of the eyes of posthatching chicken reduced the proportion of double cones to single cones in the retina, indicating dependence of retinal morphogenesis upon functional activity of visual cells.

Mechanisms of Photoreceptor Patterning in Vertebrates and Invertebrates

“…Two morphologically different sets of double cones in chickens are sensitive to long wavelengths of light(46). In the more common double cone pair, both cones have an oil droplet(46, 47) (Fig. 1C2, Type B ).…”

“…In the other pair, only the larger (primary) cone contains an oil droplet (Fig. 1C2, Type A )(44, 46). These double cones may be specialized for motion detection rather than color vision, as they appear to contain the same photopigments and synapse on one another(3, 48, 49).…”

“…The chicken retina is similar to the zebrafish in that differentiation begins at a central patch, the area centralis(40, 46, 169). Sequential waves of transcription factor expression emanate from the center to the periphery to drive cell differentiation and retinal patterning (Fig.…”

“…Type B double cones both have oil droplets. Images adapted from Wai et al ., 2006 and Santiago Ramon y Cajal, 2000(46, 254). …”

Development and Aging of the Vertebrate Visual System

“…In addition to molecular and genetic control of the highly coordinated and precisely regulated cell proliferation in the germinative neuroepithelium, the mechanisms by which multipotent progenitor cells give rise to different neuronal and glial cell types in a characteristic order of birth have been analyzed in the retina as a model system [4][5][6][7][8][9][10] .…”