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Foveal cone density shows a rapid postnatal maturation in the marmoset monkey

Published online by Cambridge University Press:  22 December 2011

ALAN D. SPRINGER ,
DAVID TROILO ,
DANIEL POSSIN  and
ANITA E. HENDRICKSON
ALAN D. SPRINGER*
Affiliation:
Department of Cell Biology and Anatomy, New York Medical College, Valhalla, New York Department of Ophthalmology, New York Medical College, Valhalla, New York
DAVID TROILO
Affiliation:
Department of Biological and Vision Sciences, State University of New York College of Optometry, New York, New York
DANIEL POSSIN
Affiliation:
Department of Ophthalmology, University of Washington, Seattle, Washington
ANITA E. HENDRICKSON
Affiliation:
Department of Ophthalmology, University of Washington, Seattle, Washington Department of Biological Structure, University of Washington, Seattle, Washington
*
*Address correspondence and reprint requests to: Alan D. Springer, Department of Cell Biology and Anatomy, New York Medical College, Valhalla, NY 10595. E-mail: [email protected]
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Abstract

The spatial and temporal pattern of cone packing during marmoset foveal development was explored to understand the variables involved in creating a high acuity area. Retinal ages were between fetal day (Fd) 125 and 6 years. Cone density was determined in wholemounts using a new hexagonal quantification method. Wholemounts were labeled immunocytochemically with rod markers to identify reliably the foveal center. Cones were counted in small windows and density was expressed as cones × 103/mm2 (K). Two weeks before birth (Fd 125–130), cone density had a flat distribution of 20–30 K across the central retina encompassing the fovea. Density began to rise at postnatal day 1 (Pd 1) around, but not in, the foveal center and reached a parafoveal peak of 45–55 K by Pd 10. Between Pd 10 and 33, there was an inversion such that cone density at the foveal center rose rapidly, reaching 283 K by 3 months and 600 K by 5.4 months. Peak foveal density then diminished to 440 K at 6 months and older. Counts done in sections showed the same pattern of low foveal density up to Pd 1, a rapid rise from Pd 30 to 90, followed by a small decrease into adulthood. Increasing foveal cone density was accompanied by 1) a reduction in the amount of Müller cell cytoplasm surrounding each cone, 2) increased stacking of foveal cone nuclei into a mound 6–10 deep, and 3) a progressive narrowing of the rod-free zone surrounding the fovea. Retaining foveal cones in a monolayer precludes final foveal cone densities above 60 K. However, high foveal adult cone density (300 K) can be achieved by having cone nuclei stack into columns and without reducing their nuclear diameter. Marmosets reach adult peak cone density by 3–6 months postnatal, while macaques and humans take much longer. Early weaning and an arboreal environment may require rapid postnatal maturation of the marmoset fovea.

Keywords

RetinaFoveaPrimatePackingStacking
Type
Research Articles
Information
Visual Neuroscience , Volume 28 , Issue 6 , November 2011 , pp. 473 - 484
Copyright
Copyright © Cambridge University Press 2011

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References

Abercrombie, M. (1946). Estimation of nuclear population from microtome sections. The Anatomical Record 94, 239–247.CrossRefGoogle ScholarPubMed
Carroll, J., Baraas, R.C., Wagner-Schuman, M., Rha, J., Siebe, C.A., Sloan, C., Tait, D.M., Thompson, S., Morgan, J.I., Neitz, J., Williams, D.R., Foster, D.H. & Neitz, M. (2009). Cone photoreceptor mosaic disruption associated with Cys203Arg mutation in the M-cone opsin. Proceedings of the National Academy of Sciences of the United States of America 106, 20948–20953.CrossRefGoogle ScholarPubMed
Carroll, J., Rossi, E.A., Porter, J., Neitz, J., Roorda, A., Williams, D.R. & Neitz, M. (2010). Deletion of the X-linked opsin gene array locus control region (LCR) results in disruption of the cone mosaic. Vision Research 50, 1989–1999.CrossRefGoogle ScholarPubMed
Cornish, E.E., Natoli, R.C., Hendrickson, A. & Provis, J.M. (2004). Differential distribution of fibroblast growth factor receptors (FGFRs) on foveal cones: FGFR-4 is an early marker of cone photoreceptors. Molecular Vision 10, 1–14.Google ScholarPubMed
Curcio, C.A., Sloan, K.R., Kalina, R.E. & Hendrickson, A.E. (1990). Human photoreceptor topography. The Journal of Comparative Neurology 292, 497–523.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Dorn, E.M., Hendrickson, L. & Hendrickson, A.E. (1995). The appearance of rod opsin during monkey retinal development. Investigative Ophthalmology and Visual Science 36, 2634–2651.Google ScholarPubMed
Hammer, D.X., Iftimia, N.V., Ferguson, R.D., Bigelow, C.E., Ustun, T.E., Barnaby, A.M. & Fulton, A.B. (2008). Foveal fine structure in retinopathy of prematurity: An adaptive optics Fourier domain optical coherence tomography study. Investigative Ophthalmology and Visual Science 49, 2061–2070.CrossRefGoogle ScholarPubMed
Hearn, J.P. (1987). Marmosets and tamarins. In The UFAW Handbook of the Care and Management of Laboratory Animals, ed. Poole, T.B., pp. 568–581. London: Longman Scientific & Technical.Google Scholar
Hendrickson, A. (1992). A morphological comparison of foveal development in man and monkey. Eye 6, 136–144.CrossRefGoogle ScholarPubMed
Hendrickson, A., Djajadi, H., Erickson, A. & Possin, D. (2006 a). Development of the human retina in the absence of ganglion cells. Experimental Eye Research 83, 920–931.CrossRefGoogle ScholarPubMed
Hendrickson, A. & Kupfer, C. (1976). The histogenesis of the fovea in the macaque monkey. Investigative Ophthalmology and Visual Science 15, 746–756.Google ScholarPubMed
Hendrickson, A., Troilo, D., Djajadi, H., Possin, D. & Springer, A. (2009). Expression of synaptic and phototransduction markers during photoreceptor development in the marmoset monkey Callithrix jacchus. The Journal of Comparative Neurology 512, 218–231.CrossRefGoogle ScholarPubMed
Hendrickson, A., Troilo, D., Possin, D. & Springer, A. (2006 b). Development of the neural retina and its vasculature in the marmoset Callithrix jacchus. The Journal of Comparative Neurology 497, 270–286.CrossRefGoogle ScholarPubMed
Hendrickson, A.E. & Yuodelis, C. (1984). The morphological development of the human fovea. Ophthalmology 91, 603–612.CrossRefGoogle ScholarPubMed
Kozulin, P., Natoli, R., O’Brien, K.M., Madigan, M.C. & Provis, J.M. (2009). Differential expression of anti-angiogenic factors and guidance genes in the developing macula. Molecular Vision 15, 45–59.Google ScholarPubMed
Kozulin, P., Natoli, R.C., Bumsted O’Brien, K.M., Madigan, M.C. & Provis, J.M. (2010). The cellular expression of anti-angiogenic factors in fetal primate macula. Investigative Ophthalmology and Visual Science 51, 4298–4306.CrossRefGoogle Scholar
Marmor, M.F., Choi, S.S., Zawadzki, R.J. & Werner, J.S. (2008). Visual insignificance of the foveal pit: Reassessment of foveal hypoplasia as fovea plana. Archives of Ophthalmology 126, 907–913.CrossRefGoogle ScholarPubMed
McAllister, J.T., Dubis, A.M., Tait, D.M., Ostler, S., Rha, J., Stepien, K.E., Summers, C.G. & Carroll, J. (2010). Arrested development: High-resolution imaging of foveal morphology in albinism. Vision Research 50, 810–817.CrossRefGoogle ScholarPubMed
Packer, O., Hendrickson, A.E. & Curcio, C.A. (1989). Photoreceptor topography of the retina in the adult pigtail macaque (Macaca nemestrina). The Journal of Comparative Neurology 288, 165–183.CrossRefGoogle ScholarPubMed
Packer, O., Hendrickson, A.E. & Curcio, C.A. (1990). Developmental redistribution of photoreceptors across the Macaca nemestrina (pigtail macaque) retina. The Journal of Comparative Neurology 298, 472–493.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 ScholarPubMed
Springer, A.D. (1999). New role for the primate fovea: A retinal excavation determines photoreceptor deployment and shape. Visual Neuroscience 16, 629–636.CrossRefGoogle ScholarPubMed
Springer, A.D. & Hendrickson, A.E. (2004 a). 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.CrossRefGoogle ScholarPubMed
Springer, A.D. & Hendrickson, A.E. (2004 b). Development of the primate area of high acuity. 2. Quantitative morphological changes associated with retina and pars plana growth. Visual Neuroscience 21, 775–790.CrossRefGoogle ScholarPubMed
Springer, A.D. & Hendrickson, A.E. (2005). Development of the primate area of high acuity. 3. Temporal relationships between pit formation, retinal elongation and cone packing. Visual Neuroscience 22, 171–185.CrossRefGoogle ScholarPubMed
Springer, A.D. & Hendrickson, A.E. (2006). The role of intraocular pressure in formation of the primate foveal pit and vascular retinal impressions. ARVO Meeting Abstracts 47, 2772.Google Scholar
Springer, A.D. & Hendrickson, A.E. (2009). The human fovea lacks a single center. ARVO Meeting Abstracts 50, 2138.Google Scholar
Troilo, D. (1998). Changes in retinal morphology following experimentally induced myopia. OSA Technical Digest 1, 206–209.Google Scholar
Troilo, D., Howland, H.C. & Judge, S.J. (1993). Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus). Vision Research 33, 1301–1310.CrossRefGoogle ScholarPubMed
Wagner-Schuman, M., Neitz, J., Rha, J., Williams, D.R., Neitz, M. & Carroll, J. (2010). Color-deficient cone mosaics associated with Xq28 opsin mutations: A stop codon versus gene deletions. Vision Research 50, 2396–2402.CrossRefGoogle ScholarPubMed
Wilder, H.D., Grünert, U., Lee, B.B. & Martin, P.R. (1996). Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus. Visual Neuroscience 13, 335–352.CrossRefGoogle ScholarPubMed
Williams, R.W. & Rakic, P. (1988). Three-dimensional counting: An accurate and direct method to estimate numbers of cells in sectioned material. The Journal of Comparative Neurology 278, 344–352.CrossRefGoogle ScholarPubMed
Xiao, M. & Hendrickson, A. (2000). Spatial and temporal expression of short, long/medium, or both opsins in human fetal cones. The Journal of Comparative Neurology 425, 545–559.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Yuodelis, C. & Hendrickson, A. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research 26, 847–855.CrossRefGoogle ScholarPubMed