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Development of the primate area of high acuity, 3: Temporal relationships between pit formation, retinal elongation and cone packing
- A.D. SPRINGER, A.E. HENDRICKSON
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- Journal:
- Visual Neuroscience / Volume 22 / Issue 2 / March 2005
- Published online by Cambridge University Press:
- 02 June 2005, pp. 171-185
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By establishing an avascular, highly elastic, region within the fetal area of high acuity (AHA), the developing primate eye has created a unique substrate on which the mechanical forces of intraocular pressure (IOP) and growth-induced retinal stretch (stretch) can act. We proposed (Springer & Hendrickson, 2004b) that these forces generate both the pit and high cone density found in the adult AHA. In this paper, we use quantitative measures to determine the temporal relationships between nasal and temporal retinal elongation, changes in pit depth, cone packing, and cone morphology over M. nemestrina retinal development. Retinal length increased rapidly to about 105 days postconception (dpc; Phase 1) and then elongation virtually ceased (Phase 2) until just after birth (180 dpc). Retinal elongation due to stretch resumed during Phase 3 until approximately 315 dpc (4–5 months), after which time the retina appeared mature (Phase 4). The pit appeared during the quiescent Phase 2, suggesting that IOP acts, in conjunction with molecular changes in the inner retina, on the highly elastic, avascular, AHA to generate a deep, narrow pit and causes inner retinal cellular displacements. Subsequently (Phase 3), the pit widened, became 50% shallower and central inner retinal lamina thinned slightly due to a small amount of retinal stretch occurring in the AHA. Centripetal movement of cones was minimal until just after birth when the pit reached 88% of its maximal depth. Accelerated cone packing during Phase 3 was temporally correlated with increased stretch. A slight stretching of the central inner retina generates “lift” forces that cause the pit to become shallower and wider. In turn, these “lift” forces draw cones toward the center of the AHA (Springer, 1999). Localized changes in cone morphology associated with packing, included smaller cell body size, a change from a monolayer to a multilayered mound of cell bodies, elongation of inner segments and tilting of the apical portion toward the AHA. These changes began in cones overlying the edges of the pit, not its center. Henle cone axons formed initially in association with centrifugal displacement of the inner retina during pit formation, with an additional subsequent elongation due to cones moving centripetally. An integrated, two-factor model of AHA formation is presented. Initially, during the second half of gestation (Phase 2), IOP acts on the hyperelastic avascular zone of the AHA to generate a deep pit in the inner retina. In the first 4 months after birth (Phase 3), central retinal stretch generates tensile “lift” forces that remodel the pit and pack cones by drawing them toward the AHA center.
Development of the primate area of high acuity. 2. Quantitative morphological changes associated with retinal and pars plana growth
- A.D. SPRINGER, A.E. HENDRICKSON
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- Journal:
- Visual Neuroscience / Volume 21 / Issue 5 / September 2004
- Published online by Cambridge University Press:
- 01 September 2004, pp. 775-790
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Mechanisms underlying the development of the primate area of high acuity (AHA) remain poorly understood. Finite-element models have identified retinal stretch and intraocular pressure (IOP) as possible mechanical forces that can form a pit (Springer & Hendrickson, 2004). A series of Macaca nemestrina monkey retinas between 68 days postconception (dpc) and adult were used to quantify growth and morphological changes. Retinal and pars plana length, optic disc diameter, disc-pit distance, and inner and outer retinal laminar thickness were measured over development to identify when and where IOP or stretch might operate. Horizontal optic disc diameter increased 500 μm between 115 dpc and 2 months after birth when it reached adult diameter. Disc growth mainly influences the immediate surrounding retina, presumably displacing retinal tissue centrifugally. Pars plana elongation also began at 115 dpc and continued steadily to 3–4 years postnatal, so its influence would be relatively constant over retinal development. Unexpectedly, horizontal retinal length showed nonlinear growth, divided into distinct phases. Retinal length increased rapidly until 115 dpc and then remained unchanged (quiescent phase) between 115–180 dpc. After birth, the retina grew rapidly for 3 months and then very slowly into adulthood. The onset of pit development overlapped the late fetal quiescent phase, suggesting that the major mechanical factor initiating pit formation is IOP, not retinal growth-induced stretch. Developmental changes in the thickness of retinal layers were different for inner and outer retina at many, but not all, of the ten eccentricities examined. Peripheral inner and outer retinal layers thinned appreciably with age, consistent with retinal stretch having a larger effect on the retinal periphery. Central inner retina around the area of high acuity (AHA) changed tri-phasically. It increased in thickness prenatally, thinned transiently after birth, and then resumed thickening. Transient postnatal inner retinal thinning around the pit coincided with the resumption of retinal growth and with cone packing providing evidence that a small amount of growth-induced central retinal stretch may account for cone packing as previously hypothesized (Springer, 1999). Central outer retina around the AHA progressively thickened over the fetal period. It reached asymptotic thickness at birth and continued to thicken into adulthood at some temporal, but not nasal, central eccentricities. These data indicate that peripheral outer and inner retina progressively thin with age because of eye growth-induced stretch, while central retina is minimally affected by stretch. Outer and inner retinal laminar thickness at the same locus can change in different directions, suggesting that they shear with respect to one another. This shearing induces the elongation of Henle axons, while their angle reflects the direction of shear.
Development of the primate area of high acuity. 1. Use of finite element analysis models to identify mechanical variables affecting pit formation
- A.D. SPRINGER, A.E. HENDRICKSON
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- Journal:
- Visual Neuroscience / Volume 21 / Issue 1 / January 2004
- Published online by Cambridge University Press:
- 03 May 2004, pp. 53-62
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Most primate retinas have an area dedicated for high visual acuity called the fovea centralis. Little is known about specific mechanisms that drive development of this complex central retinal specialization. The primate area of high acuity (AHA) is characterized by the presence of a pit that displaces the inner retinal layers. Virtual engineering models were analyzed with finite element analysis (FEA) to identify mechanical mechanisms potentially critical for pit formation. Our hypothesis is that the pit emerges within the AHA because it contains an avascular zone (AZ). The absence of blood vessels makes the tissue within the AZ more elastic and malleable than the surrounding vascularized retina. Models evaluated the contribution to pit formation of varying elasticity ratios between the AZ and surrounding retina, AZ shape, and width. The separate and interactive effects of two mechanical variables, intraocular pressure (IOP) and ocular growth-induced retinal stretch, on pit formation were also evaluated. Either stretch or IOP alone produced a pit when applied to a FEA model having a highly elastic AZ surrounded by a less elastic region. Pit depth and width increased when the elasticity ratio increased, but a pit could not be generated in models lacking differential elasticity. IOP alone produced a deeper pit than did stretch alone and the deepest pit resulted from the combined effects of IOP and stretch. These models predict that the pit in the AHA is formed because an absence of vasculature makes the inner retinal tissue of the AZ very deformable. Once a differential elasticity gradient is established, pit formation can be driven by either IOP or ocular growth-induced retinal stretch.