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Development of the primate area of high acuity. 2. Quantitative morphological changes associated with retinal and pars plana growth

Published online by Cambridge University Press:  01 September 2004

A.D. SPRINGER  and
A.E. HENDRICKSON
A.D. SPRINGER
Affiliation:
Deptartment of Cell Biology and Anatomy, New York Medical College, Valhalla
A.E. HENDRICKSON
Affiliation:
Biological Structure and Ophthalmology, University of Washington, Seattle
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Abstract

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.

Keywords

MonkeyMechanicalLaminarThicknessPars planaOptic discFoveaMorphology
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 5 , September 2004 , pp. 775 - 790
Copyright
2004 Cambridge University Press

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References

REFERENCES

Abramov, I., Gordon, J., Hendrickson, A., Hainline, L., Dobson, V., & LaBossiere, E. (1982). The retina of the newborn human infant. Science 217, 265–267.Google 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.Google Scholar
Chievitz, J.H. (1887). Die area und fovea centrales retinae beim menschlichen fetus. Internationale Monatsschrift für Anatomie und Physiologie 4, 201.Google Scholar
Chievitz, J.H. (1888). Entwicklung der fovea centralis retinae. Anatomischer Anzeiger 3, 579.Google Scholar
Cornish, E.E., Hendrickson, A.E., & Provis, J.M. (2004). Distribution of short-wavelength-sensitive cones in human fetal and postnatal retina: Early development of spatial order and density profiles. Vision Research 44, 2019–2026.Google Scholar
Curtin, B.J. (1985). The Myopias. Philadelphia, Pennsylvania: Harper & Row.
Dacey, D.M. (1999). Primate retina: Cell types, circuits and color opponency. Progress in Retina and Eye Research 18, 737–763.Google Scholar
Diaz-Araya, C. & Provis, J.M. (1992). Evidence of photoreceptor migration during early foveal development: A quantitative analysis of human fetal retinae. Visual Neuroscience 8, 505–514.Google Scholar
Fischer, A.J., Hendrickson, A., & Reh, T.A. (2001). Immunocytochemical characterization of cysts in the peripheral retina and pars plana of the adult primate. Investigative Ophthalmology and Visual Science 42, 3256–3263.Google Scholar
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
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.Google Scholar
Grunert, U., Greferath, U., Boycott, B.B., & Wassle, H. (1993). Parasol (P alpha) ganglion-cells of the primate fovea: Immunocytochemical staining with antibodies against GABAA-receptors. Vision Research 33, 1–14.Google Scholar
Henderson, Z., Finlay, B.L., & Wikler, K.C. (1988). Development of ganglion cell topography in ferret retina. Journal of Neuroscience 8, 1194–1205.Google Scholar
Hendrickson, A. (1992). A morphological comparison of foveal development in man and monkey. Eye 6, 136–144.Google 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.Google Scholar
LaVail, M.M., Rapaport, D.H., & Rakic, P. (1991). Cytogenesis in the monkey retina. Journal of Comparative Neurology 309, 86–114.Google Scholar
Leventhal, A.G. (1996). Evidence that retinal ganglion cell density affects foveal development. Perspectives on Developmental Neurobiology 3, 203–11.Google Scholar
Lia, B., Williams, R.W., & Chalupa, L.M. (1987). Formation of retinal ganglion cell topography during prenatal development. Science 236, 848–851.Google Scholar
Mann, I. (1964). The Development of the Human Eye. New York: Grune & Stratton.
Mastronarde, D.N., Thibeault, M.A., & Dubin, M.W. (1984). Non-uniform postnatal growth of the cat retina. Journal of Comparative Neurology 228, 598–608.Google Scholar
Milleret, C., Buisseret, P., & Gary Bobo, E. (1988). Area centralis position relative to the optic disc projection in kittens as a function of age. Investigative Ophthalmology and Visual Science 29, 1299–1305.Google 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.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.Google Scholar
Provis, J.M., Leech, J., Diaz, C.M., Penfold, P.L., Stone, J., & Keshet, E. (1997). Development of the human retinal vasculature: Cellular relations and VEGF expression. Experimental Eye Research 65, 555–568.Google 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.Google 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
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.Google Scholar
Rapaport, D.H. & Stone, J. (1984). The area centralis of the retina in the cat and other mammals: Focal point for function and development of the visual system. Neuroscience 11, 289–301.Google Scholar
Rimmer, S., Keating, C., Chou, T., Farb, M.D., Christenson, P.D., Foos, R.Y., & Bateman, J.B. (1993). Growth of the human optic disk and nerve during gestation, childhood, and early adulthood. American Journal of Ophthalmology 116, 748–753.Google Scholar
Robinson, S.R. (1987). Ontogeny of the area centralis in the cat. Journal of Comparative Neurology 255, 50–67.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., Dreher, B., & McCall, M.J. (1989). Nonuniform retinal expansion during the formation of the rabbit's visual streak: Implications for the ontogeny of mammalian retinal topography. Visual Neuroscience 2, 201–219.Google Scholar
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.Google Scholar
Rohrenbeck, J., Wassle, H., & Boycott, B.B. (1989). Horizontal cells in the monkey retina: Immunocytochemical staining with antibodies against calcium binding proteins. European Journal of Neuroscience 1, 407–420.Google Scholar
Roonwal, M.L. & Mohnot, S.M. (1977). Primates of South Asia Ecology, Sociobiology, and Behavior. Cambridge, Massachusetts.: Harvard University Press.
Schepens, C.L. (1983). Retinal detachment and allied diseases. In The Standard Peripheral Fundus and Its Variations, ed. Anonymous. Philadelphia, Pennsylvania: W.B. Saunders.
Springer, A.D. (1999). New role for the primate fovea: A retinal excavation determines photoreceptor deployment and shape. Visual Neuroscience 16, 629–636.Google Scholar
Springer, A.D. & Diener, H. (1994). Determinants of retinal specializations: A new approach using finite element analysis. Neuroscience Abstracts 20, 1322.Google Scholar
Springer, A.D. & Kauffmann-Jokl, D.H. (2000). A finite element analysis (FEA) simulation of the effects of eye growth and ridge elasticity on retinal detachment in ROP. Investigative Ophthalmology and Visual Science 41, 5335.Google Scholar
Springer, A.D. & Hendrickson, A.E. (2004). Development of the primate area of high acuity. 1. Use of finite element analysis models to identify mechanical variables affecting pit formation. Visual Neuroscience 21, 53–62.Google Scholar
Steineke, T.C. & Kirby, M.A. (1993). Early axon outgrowth of retinal ganglion cells in the fetal rhesus macaque. Developmental Brain Research 74, 151–162.Google 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.Google Scholar
Yuodelis, C. & Hendrickson, A. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research 26, 847–855.Google Scholar