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A.D. Springer, A.E. Hendrickson; Complex Relationships Between Retinal Growth, Intraocular Pressure, Pit Formation and Cone Packing in the Formation of a Primate Fovea . Invest. Ophthalmol. Vis. Sci. 2005;46(13):593.
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Purpose: To understand the mechanisms underlying primate fovea formation, several retinal features were quantified over the course of development in monkeys. Retinal elongation, pit depth, laminar thickness and cone density were measured in the same sections to determine which inner and outer retinal changes were attributable to intraocular pressure (IOP) and which were attributable to retinal stretch. Methods: Measurements were made in paraffin sections through macaque retinas varying in age from fetal day 73 to 11 years. Results: Temporal retina elongates in 4 distinct phases. Phase 1 is marked by rapid retinal elongation. The retina stops elongating during Phase 2, which spans 2.5 months before birth. A shallow pit appears at the start of Phase 2 and reaches maximum depth by its end. Thus, the pit forms in the absence of retinal elongation. While the pit forms in Phase 2, cones remain in a monolayer. Phase 3, beginning just after birth, lasts for 4.5 months, during which the retina elongates rapidly by stretching. The pit becomes 50% shallower while the retina is elongating in Phase 3, suggesting that stretch causes the pit to become shallower. Abrupt changes in cone density occur first in Phase 3. Cone packing in Phase 3 is associated with the retina resuming elongation, pit depth becoming shallower and the parafoveal inner retinal laminae becoming thinner. All of these changes, occurring concurrently in Phase 3, are consistent with the central, parafoveal, retina being stretched. Finite element analysis indicated that about 300 µm of central retinal stretch could account for the various morphological changes occurring in Phase 3, resulting in a mature foveal morphology. Retinal length and pit depth change little in Phase 4 and the retina seems mature. Conclusions: Outward movement of inner retinal cells occurs while retinal growth is in a quiescent phase. These displacements are not caused by stretch. Instead, they probably occur in response to molecular changes within the foveal inner retinal tissue, making it deformable by IOP. Retinal elongation resumes after the pit reaches maximal depth. Resumed elongation coincides with laminar thinning around the fovea suggesting that the central retinal is being stretched. This finding supports the hypothesis that retinal stretch creates bending moments around the pit, causing the tissue at the pit to lift, thereby pulling and packing the cones centripetally. Stretch also causes both a flattened pit floor and a shallower pit. The data suggest that significant cone packing may depend on the formation of a deep pit.
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