Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-24T11:41:58.188Z Has data issue: false hasContentIssue false
  • English
  • Français

Development of the primate area of high acuity. 1. Use of finite element analysis models to identify mechanical variables affecting pit formation

Published online by Cambridge University Press:  03 May 2004

A.D. SPRINGER  and
A.E. HENDRICKSON
A.D. SPRINGER
Affiliation:
Department of Cell Biology and Anatomy, New York Medical College, Valhalla
A.E. HENDRICKSON
Affiliation:
Biological Structure and Ophthalmology, University of Washington, Seattle
Get access Rights & Permissions [Opens in a new window]

Abstract

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.

Keywords

Fovea centralisFinite element analysisIntraocular pressureRetinal stretchFoveal hypoplasiaFoveal avascular zoneEye growth
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 1 , January 2004 , pp. 53 - 62
Copyright
2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arciniegas, A., Amaya, L.E., & Cardenas, M.J. (1979). Mechanical behavior of the vitreous. Annals of Ophthalmology 11, 1809–1813.Google Scholar
Arciniegas, A., Amaya, L.E., & Ruiz, L.A. (1980). Myopia: A bioengineering approach. Annals of Ophthalmology 12, 805–810.Google Scholar
Barbosa-Carneiro, L., Peret, M., Bichara, A., Coscarelli, G., & Peret, P. (2000). Isolated foveal hypoplasia. Investigative Ophthalmology and Visual Science 41, S571Google Scholar
Barraquer, J.I. & Miguel, V.J., Jr. (1971). Annotations concerning the relation of forces and pressure in eyes during physical growth. Annals of Ophthalmology 3, 425–427.Google Scholar
Bradley, D.V., Fernandes, A., Lynn, M., Tigges, M., & Boothe, R.G. (1999). Emmetropization in the rhesus monkey (Macaca mulatta): Birth to young adulthood. Investigative Ophthalmology and Visual Science 40, 214–229.Google Scholar
Brodland, G.W. (1994). Finite element methods for developmental biology. International Review of Cytology 150, 95–118.CrossRefGoogle Scholar
Bumsted, K., Jasoni, C., Szel, A., & Hendrickson, A. (1997). Spatial and temporal expression of cone opsins during monkey retinal development. Journal of Comparative Neurology 378, 117–134.3.0.CO;2-7>CrossRefGoogle Scholar
Colton, T. & Ederer, F. (1980). The distribution of intraocular pressures in the general population. Survey of Ophthalmology 25, 123–129.CrossRefGoogle Scholar
Cornish, E.E., Hales, A.M., Hendrickson, A.E., & Provis, J.M. (2002). A gradient in Fgf-2 expression during formation of the foveal depression correlates with cone morphology. Investigative Ophthalmology and Visual Science 43, E-Abstract 2684.Google Scholar
Coulombre, A.J. (1956). The role of intraocular pressure in the development of the chick eye. I: Control of eye size. Journal of Experimental Zoology 133, 211–225.Google Scholar
Crooks, J., Okada, M., & Hendrickson, A.E. (1995). Quantitative analysis of synaptogenesis in the inner plexiform layer of macaque monkey fovea. Journal of Comparative Neurology 360, 349–362.CrossRefGoogle Scholar
Curcio, C.A. (2001). Photoreceptor topography in ageing and age-related maculopathy. Eye 15, 376–383.CrossRefGoogle Scholar
Curcio, C.A. & Hendrickson, A.E. (1991). Organization and development of the primate photoreceptor mosaic. In Progress in Retinal Research, ed. Osborne, N. & Chader, J., pp. 89–120. Oxford: Pergamon Press.CrossRef
Curcio, C.A., Sloan, K.R., Kalina, R.E., & Hendrickson, A.E. (1990). Human photoreceptor topography. Journal of Comparative Neurology 292, 497–523.CrossRefGoogle Scholar
Curran, R.E. & Robb, R.M. (1976). Isolated foveal hypoplasia. Archives of Ophthalmology 94, 48–50.CrossRefGoogle Scholar
De Rousseau, C.J. & Bito, L.Z. (1981). Intraocular pressure of rhesus monkeys (Macaca mulatta). II. Juvenile ocular hypertension and its apparent relationship to ocular growth. Experimental Eye Research 32, 407–417.Google Scholar
Distelhorst, J.S. & Hughes, G.M. (2003). Open-angle glaucoma. American Family Physician 67, 1937–1944.Google Scholar
Duckman, R.H. & Fitzgerald, D.E. (1992). Evaluation of intraocular pressure in a pediatric population. Optometry and Vision Science 69, 705–709.CrossRefGoogle Scholar
Duke-Elder, S. & Cook, C. (1963). Normal and abnormal development: Part 1—Embryology. In System of Ophthalmology, ed. Duke-Elder & S., Vol. 3, pp. 304–313. St. Louis, Missouri: Mosby.
Eisenberg, D.L., Sherman, B.G., McKeown, C.A., & Schuman, J.S. (1998). Tonometry in adults and children. A manometric evaluation of pneumatonometry, applanation, and TonoPen in vitro and in vivo. Ophthalmology 105, 1173–1181.CrossRefGoogle Scholar
Fledelius, H.C. & Christensen, A.C. (1996). Reappraisal of the human ocular growth curve in fetal life, infancy, and early childhood. British Journal of Ophthalmology 80, 918–921.CrossRefGoogle Scholar
Franco, E.C.S., Finlay, B.L., Silveira, L.C.L., Yamada, E.S., & Crowley, J.C. (2000). Conservation of absolute foveal area in New World monkeys. A constraint on eye size and conformation. Brain, Behavior, and Evolution 56, 276–286.CrossRefGoogle Scholar
Fulton, A.B., Albert, D.M., & Craft, J.L. (1978). Human albinism. Light and electron microscopy study. Archives of Ophthalmology 96, 305–310.CrossRefGoogle Scholar
Fung, Y.C. (1993). Biomechanics: Mechanical Properties of Living Tissues. New York: Springer-Verlag.
Gariano, R.F., Iruela-Arispe, M.L., & Hendrickson, A.E. (1994). Vascular development in primate retina: Comparison of laminar plexus formation in monkey and human. Investigative Ophthalmology and Visual Science 35, 3442–3455.Google Scholar
Gariano, R.F., Kalina, R.E., & Hendrickson, A.E. (1996). Normal and pathological mechanisms in retinal vascular development. Survey of Ophthalmology 40, 481–490.CrossRefGoogle Scholar
Gariano, R.F., Provis, J.M., & Hendrickson, A.E. (2000). Development of the foveal avascular zone. Ophthalmology 107, 1026CrossRefGoogle Scholar
Georges, P., Madigan, M.C., & Provis, J.M. (1999). Apoptosis during development of the human retina: Relationship to foveal development and retinal synaptogenesis. Journal of Comparative Neurology 413, 198–208.3.0.CO;2-J>CrossRefGoogle Scholar
Gottlieb, M.D., Fugate-Wentzek, L.A., & Wallman, J. (1987). Different visual deprivations produce different ametropias and different eye shapes. Investigative Ophthalmology and Visual Science 28, 1225–1235.Google Scholar
Hendrickson, A. (1992). A morphological comparison of foveal development in man and monkey. Eye 6, 136–144.CrossRefGoogle Scholar
Hendrickson, A. & Kupfer, C. (1976). The histogenesis of the fovea in the macaque monkey. Investigative Ophthalmology and Visual Science 15, 746–756.Google Scholar
Hendrickson, A.E. & Yuodelis, C. (1984). The morphological development of the human fovea. Ophthalmology 91, 603–612.CrossRefGoogle Scholar
Hendrickson, A.E., Troilo, D., & Springer, A.D. (2003). Foveal development in the marmoset monkey. Investigative Ophthalmology and Visual Science 44, E-Abstract 1607.Google Scholar
Ichihara, K., Taguchi, T., Shimada, Y., Sakuramoto, I., Kawano, S., & Kawai, S. (2001). Gray matter of the bovine cervical spinal cord is mechanically more rigid and fragile than the white matter. Journal of Neurotrauma 18, 361–367.CrossRefGoogle Scholar
Jones, I.L., Warner, M., & Stevens, J.D. (1992). Mathematical modelling of the elastic properties of retina: A determination of Young's modulus. Eye 6, 556–559.CrossRefGoogle Scholar
Kiely, P.M., Crewther, S.G., Nathan, J., Brennan, N.A., Efron, N., & Madigan, M. (1987). A comparison of ocular development of the cynomolgus monkey and man. Clinical Vision Sciences 1, 269–280.Google Scholar
Kornblueth, W., Aladjemmoff, L., Magora, F., & Dor, D.B. (1964). Intraocular pressure in children measured under general anesthesia. Archives of Ophthalmology 72, 489–490.CrossRefGoogle Scholar
La Vail, M.M., Rapaport, D.H., & Rakic, P. (1991). Cytogenesis in the monkey retina. Journal of Comparative Neurology 309, 86–114.CrossRefGoogle Scholar
Leventhal, A.G., Ault, S.J., Vitek, D.J., & Shou, T. (1989). Extrinsic determinants of retinal ganglion cell development in primates. Journal of Comparative Neurology 286, 170–189.CrossRefGoogle Scholar
Linberg, K.A. & Fisher, S.K. (1990). A burst of differentiation in the outer posterior retina of the eleven-week human fetus: An ultrastructural study. Visual Neuroscience 5, 43–60.CrossRefGoogle Scholar
Okada, M., Erickson, A., & Hendrickson, A. (1994). Light and electron microscopic analysis of synaptic development in Macaca monkey retina as detected by immunocytochemical labeling for the synaptic vesicle protein, SV2. Journal of Comparative Neurology 339, 535–558.CrossRefGoogle Scholar
Oliver, M.D., Dotan, S.A., Chemke, J., & Abraham, F.A. (1987). Isolated foveal hypoplasia. British Journal of Ophthalmology 71, 926–930.CrossRefGoogle Scholar
Østerberg, G.A. (1935). Topography of the layer of rods and cones in the human retina. Acta Ophthalmologica (Copenhagen) 6 (Suppl. 13), 1–102.Google Scholar
Packer, O., Hendrickson, A.E., & Curcio, C.A. (1990). Developmental redistribution of photoreceptors across the Macaca nemestrina (pigtail macaque) retina. Journal of Comparative Neurology 298, 472–493.CrossRefGoogle Scholar
Polyak, S.L. (1941). The Retina: The Anatomy and the Histology of the Retina in Man, Ape, and Monkey, Including the Consideration of Visual Functions, the History of Physiological Optics, and the Histological Laboratory Technique. Chicago, Illinois: University of Chicago Press.
Porter, M.A. (1996). FEA Step by Step with Algor. Leawood, Kansas: Dynamic Analysis.
Provis, J.M. & Van Driel, D. (1985). Retinal development in humans: The roles of differential growth rates, cell migration and naturally occurring cell death. Australian and New Zealand Journal of Ophthalmology 13, 125–133.CrossRefGoogle Scholar
Provis, J.M., Van Driel, D., Billson, F.A., & Russell, P. (1985). Development of the human retina: Patterns of cell distribution and redistribution in the ganglion cell layer. Journal of Comparative Neurology 233, 429–451.CrossRefGoogle Scholar
Provis, J.M., Diaz, C.M., & Dreher, B. (1998). Ontogeny of the primate fovea: A central issue in retinal development. Progress in Neurobiology 54, 549–580.CrossRefGoogle Scholar
Provis, J.M., Sandercoe, T., & Hendrickson, A.E. (2000). Astrocytes and blood vessels define the foveal rim during primate retinal development. Investigative Ophthalmology and Visual Science 41, 2827–2836.Google Scholar
Rapaport, D.H., Rakic, P., & LaVail, M.M. (1996). Spatiotemporal gradients of cell genesis in the primate retina. Perspectives on Developmental Neurobiology 3, 147–159.Google Scholar
Reichenbach, A., Eberhardt, W., Scheibe, R., Deich, C., Seifert, B., Reichelt, W., Dahnert, K., & Rodenbeck, M. (1991). Development of the rabbit retina. IV. Tissue tensility and elasticity in dependence on topographic specializations. Experimental Eye Research 53, 241–251.CrossRefGoogle Scholar
Robb, R.M. (1982). Increase in retinal surface area during infancy and childhood. Journal of Pediatric Ophthalmology and Strabismus 19, 16–20.Google Scholar
Robinson, S.R. (1991). Development of the mammalian retina. In Neuroanatomy of the Visual Pathways and their Development, ed. Dreher, B. & Robinson, S.R., pp. 69–128. Boca Raton, Florida: CRC Press.
Robinson, S.R. & Hendrickson, A. (1995). Shifting relationships between photoreceptors and pigment epithelial cells in monkey retina: Implications for the development of retinal topography. Visual Neuroscience 12, 767–778.CrossRefGoogle Scholar
Sandercoe, T.M., Madigan, M.C., Billson, F.A., Penfold, P.L., & Provis, J.M. (1999). Astrocyte proliferation during development of the human retinal vasculature. Experimental Eye Research 69, 511–523.CrossRefGoogle Scholar
Sandercoe, T.M., Geller, S.F., Hendrickson, A.E., Stone, J., & Provis, J.M. (2003). VEGF expression by ganglion cells in central retina before formation of the foveal depression in monkey retina: Evidence of developmental hypoxia. Journal of Comparative Neurology 462, 42–54.CrossRefGoogle Scholar
Scammon, R.E. & Armstrong, E.L. (1924). On the growth of the human eyeball and optic nerve. Journal of Comparative Neurology 38, 165–219.Google Scholar
Schnitzer, J. (1988). The development of astrocytes and blood vessels in the postnatal rabbit retina. Journal of Neurocytology 17, 433–449.CrossRefGoogle Scholar
Sears, S., Erickson, A., & Hendrickson, A. (2000). The spatial and temporal expression of outer segment proteins during development of Macaca monkey cones. Investigative Ophthalmology and Visual Science 41, 971–979.Google Scholar
Spedick, M.J. & Beauchamp, G.R. (1986). Retinal vascular and optic nerve abnormalities in albinism. Journal of Pediatric Ophthalmology and Strabismus 23, 58–63.Google Scholar
Springer, A.D. (1999). New role for the primate fovea: A retinal excavation determines photoreceptor deployment and shape. Visual Neuroscience 16, 629–636.CrossRefGoogle Scholar
Springer, A.D. & Diener, H. (1994). Determinants of retinal specializations: A new approach using finite element analysis. Neuroscience Abstracts 20, 1322Google Scholar
Springer, A.D. & Hendrickson, A.E. (2001). Foveal avascularity leads to the formation of the fovea: A virtual experiment. Investigative Ophthalmology and Visual Science 42, S379.Google Scholar
Springer, A.D. & Hendrickson, A.E. (2003). Role of pressure and stretch in forming the fovea. Investigative Ophthalmology and Visual Science 44, E-Abstract 1606.Google Scholar
Spyrakos, C.C. & Raftoyiannis, J. (1997). Linear and Nonlinear Finite Element Analysis in Engineering Practice. Pittsburgh, Pennsylvania: Algor Publishing Division.
Stevens, J.D., Jones, I.L., Warner, M., Lavin, M.J., & Leaver, P.K. (1992). Mathematical modelling of retinal tear formation: Implications for the use of heavy liquids. Eye 6, 69–74.CrossRefGoogle Scholar
Summers, C.G., Knobloch, W.H., Witkop, C.J., Jr., & King, R.A. (1988). Hermansky-Pudlak syndrome. Ophthalmic findings. Ophthalmology 95, 545–554.CrossRefGoogle Scholar
Troilo, D. (1998). Changes in retinal morphology following experimentally induced myopia. Optical Society of America Technical Digest 1, 206–209.Google Scholar
Troilo, D., Gottlieb, M.D., & Wallman, J. (1987). Visual deprivation causes myopia in chicks with optic nerve section. Current Eye Research 6, 993–999.CrossRefGoogle Scholar
Usher, C.H. (1920). Histological examination of an adult human albino's eyeball, with a note on mesoblastic pigmentation in foetal eyes. Biometrika 13, 46–56.CrossRefGoogle Scholar
Van Essen, D.C. (1997). A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385, 313–318.CrossRefGoogle Scholar
Wallman, J. & Adams, J.I. (1987). Developmental aspects of experimental myopia in chicks: Susceptibility, recovery and relation to emmetropization. Vision Research 27, 1139–1163.CrossRefGoogle Scholar
Walls, G.L. (1937). Significance of the foveal depression. Archives of Ophthalmology 18, 912–919.CrossRefGoogle Scholar
Wu, W., Peters, W.H.I., & Hammer, M.E. (1987). Basic mechanical properties of retina in simple elongation. Journal of Biomechanical Engineering 109, 65–67.CrossRefGoogle Scholar
Xiao, M. & Hendrickson, A. (2000). Spatial and temporal expression of short, long/medium, or both opsins in human fetal cones. Journal of Comparative Neurology 425, 545–559.3.0.CO;2-3>CrossRefGoogle Scholar
Yuodelis, C. & Hendrickson, A. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research 26, 847–855.CrossRefGoogle Scholar