Abstract
BackgroundNervous system development is dependent on early regional specification to create functionally distinct tissues within an initially undifferentiated zone. Within the retina, photoreceptors are topographically organized with rod free area centrales faithfully generated at the centre of gaze. How does the developing eye regulate this placement? Conventional wisdom indicates that the distal tip of the growing optic vesicle (OV) gives rise to the area centralis/fovea. Ectopic expression and ablation studies do not fully support this view, creating a controversy as to the origin of this region. In this study, the lineage of cells in the chicken OV was traced using DiI. The location of labelled cells was mapped onto the retina in relation to the rod-free zone at embryonic (E) 7 and E17.5. The ability to regenerate a rod free area after OV ablation was determined in conjunction with lineage tracing.ResultsAnterior OV gave rise to cells in nasal retina and posterior OV became temporal retina. The OV distal tip gave rise to cells above the optic nerve head. A dorsal and anterior region of the OV correlated with cells in the developing rod free area centralis. Only ablations including the dorsal anterior region gave rise to a retina lacking a rod free zone. DiI application after ablation indicated that cells movements were greater along the anterior/posterior axis compared with the dorsal/ventral axis.ConclusionOur data support the idea that the chicken rod free area centralis originates from cells located near, but not at the distal tip of the developing OV. Therefore, the hypothesis that the area centralis is derived from cells at the distal tip of the OV is not supported; rather, a region anterior and dorsal to the distal tip gives rise to the rod free region. When compared with other studies of retinal development, our results are supported on molecular, morphological and functional levels. Our data will lead to a better understanding of the mechanisms underlying the topographic organization of the retina, the origin of the rod free zone, and the general issue of compartmentalization of neural tissue before any indication of morphological differentiation.
Highlights
Nervous system development is dependent on early regional specification to create functionally distinct tissues within an initially undifferentiated zone
At E7, when the location of the visinin free spot (Figure 1C; open circle) was added to the map of the DiI labelled cells (Figure 1C, outlined area above optic disc), fate-mapped cells from the distal tip of the optic vesicles (OV) were always absent in the visinin free spot (n = 3; Figure 1C)
Placement of DiI into the anterior dorsal OV resulted in labelled cells localized to the visinin free spot at E7 (n = 4; Figure 2E, E') and the rod free area centralis at E17.5 (n = 4; Figure 2F, F')
Summary
Nervous system development is dependent on early regional specification to create functionally distinct tissues within an initially undifferentiated zone. The ability to regenerate a rod free area after OV ablation was determined in conjunction with lineage tracing. A hallmark of nervous system development is the early fate determination of tissues followed by progressive morphological differentiation of initially featureless regions into cyto-architecturally and functionally distinct organs and systems. The optic grooves (sulci) form when cells in the eye fields invaginate into the internal surface of the neural tube. Even though there are no obvious morphological specializations in the developing eye at the OV stage, it is at this point that the basic anterior/posterior and dorsal/ventral axes of the eye are established and positional coordinates forming a basic retinal map are assigned [3,4,5,6]
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