Development and postnatal neurogenesis in the retina: a comparison between altricial and precocial bird species

Abstract

The visual system is affected by neurodegenerative diseases caused by the degeneration of specific retinal neurons, the leading cause of irreversible blindness in humans. Throughout vertebrate phylogeny, the retina has two kinds of specialized niches of constitutive neurogenesis: the retinal progenitors located in the circumferential marginal zone and Müller glia. The proliferative activity in the retinal progenitors located in the circumferential marginal zone in precocial birds such as the chicken, the commonest bird model used in developmental and regenerative studies, is very low. This region adds only a few retinal cells to the peripheral edge of the retina during several months after hatching, but does not seem to be involved in retinal regeneration. Müller cells in the chicken retina are not proliferative under physiological conditions, but after acute damage some of them undergo a reprogramming event, dedifferentiating into retinal stem cells and generating new retinal neurons. Therefore, regenerative response after injury occurs with low efficiency in the precocial avian retina. In contrast, it has recently been shown that neurogenesis is intense in the retina of altricial birds at hatching. In particular, abundant proliferative activity is detected both in the circumferential marginal zone and in the outer half of the inner nuclear layer. Therefore, stem cell niches are very active in the retina of altricial birds. Although more extensive research is needed to assess the potential of proliferating cells in the adult retina of altricial birds, it emerges as an attractive model for studying different aspects of neurogenesis and neural regeneration in vertebrates.

Retinal Development in a Precocial Bird Species, the Quail (Coturnix coturnix, Linnaeus 1758)

“…Therefore, there are only minimal differences between developmental features in quail and chick embryos during the early stages of development, in agreement with results previously reported [35,76] [19,20,32,79]. PCNAand pHisH3-immunoreactivity is absent from the entire retina in this bird species (present study; [27]), and visinin-immunoreactive photoreceptors are morphologically mature with a well-developed outer segment.…”

“…In the case of an avian embryo, most of the studies on retinal development have been conducted on chickens ( Gallus gallus , Linnaeus 1758) [ 9 , 10 , 11 , 12 ], a precocial bird species. Currently, the chicken retina is being recognized as one of the most suitable tools to study molecular mechanisms that govern neural development and connectivity [ 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 ], but also a wide range of ocular diseases and conditions [ 24 ]. In contrast, relatively little is known of how the basic events of retinal differentiation, such as neurogenesis, axon outgrowth, histogenesis, and cell death, fit into the varying developmental durations during the embryonic period in other bird species.…”

“…In this sense, important differences are found in the timing of the development of various visual system morphogenesis features, and the differentiation between precocial and altricial birds. The morphogenesis of the optic vesicle and optic cup, the onset of differentiation of ganglion cells, photoreceptors, and horizontal cells, and the emergence of the plexiform layers occur at earlier stages in G. gallus than in altricial bird embryos [ 19 , 25 , 26 , 27 ]. Furthermore, the different waves of programmed cell death during visual system morphogenesis and retinogenesis is completely restricted to the embryonic period in precocial birds [ 28 , 29 ], while the highest incidence of programmed cell death in the retina of altricial bird species occurs in the post-hatching period [ 30 ].…”

“…Furthermore, the different waves of programmed cell death during visual system morphogenesis and retinogenesis is completely restricted to the embryonic period in precocial birds [ 28 , 29 ], while the highest incidence of programmed cell death in the retina of altricial bird species occurs in the post-hatching period [ 30 ]. At hatching, the precocial retina presents the multi-layered organization, is devoid of proliferative activity, and shows morphologically differentiated cells [ 1 , 19 , 20 , 27 , 31 , 32 ]. However, abundant features of immaturity are found in the retina of altricial hatchlings, with poorly developed plexiform layers, abundant proliferative activity, and the presence of morphological immature cell types [ 19 , 25 , 26 , 27 , 32 ].…”

“…At hatching, the precocial retina presents the multi-layered organization, is devoid of proliferative activity, and shows morphologically differentiated cells [ 1 , 19 , 20 , 27 , 31 , 32 ]. However, abundant features of immaturity are found in the retina of altricial hatchlings, with poorly developed plexiform layers, abundant proliferative activity, and the presence of morphological immature cell types [ 19 , 25 , 26 , 27 , 32 ].…”