Relationship between foveal cone specialization and pit morphology in Albinism

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 7, 2014, Pages 4186-4198

  Wilk, Melissa A ^a   McAllister, John T ^a   Cooper, Robert F ^b   Dubis, Adam M ^c,d   Patitucci, Teresa N ^a   Summerfelt, Phyllis ^a   Anderson, Jennifer L ^e   Stepien, Kimberly E ^a   Costakos, Deborah M ^a   Jr, Thomas B Connor ^a   Wirostko, William J ^a   Chiang, Pei Wen ^f   Dubra, Alfredo ^a,b   Curcio, Christine A ^g   Brilliant, Murray H ^e   Gail Summers, C ^h   Carroll, Joseph ^a,b  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b Marquette University   (United States)

^c MOORFIELDS EYE HOSPITAL   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e MARSHFIELD CLINIC   (United States)

^f Casey Molecular Diagnostic Laboratory   (United States)

^g UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^h UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Adaptive optics; Albinism; Foveal development; Foveal morphology

Indexed keywords

ADAPTIVE OPTICS; ALBINISM; FOVEAL DEVELOPMENT; FOVEAL MORPHOLOGY;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ALBINISM, OCULOCUTANEOUS; CELL COUNT; CHILD; DNA; ELECTRORETINOGRAPHY; EYE PROTEINS; FEMALE; FOVEA CENTRALIS; GENETIC TESTING; HUMANS; MALE; MIDDLE AGED; MUTATION; OPHTHALMOSCOPY; RETINAL CONE PHOTORECEPTOR CELLS; TOMOGRAPHY, OPTICAL COHERENCE; VISUAL ACUITY; YOUNG ADULT;

EID: 84904346942     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-13217     Document Type: Article

References (69)

1. King RA, Pietsch J, Fryer JP, et al. Tyrosinase gene mutations in oculocutaneous albinism 1 (OCA1): definition of the phenotype. Hum Genet. 2003;113:502-513.
2. Oetting WS, King RA. Molecular basis of albinism: mutations and polymorphisms of pigmentation genes associated with albinism. Hum Mutat. 1999;13:99-115.
3. Newton JM, Cohen-Barak O, Hagiwara N, et al. Mutations in the human orthologue of the mouse underwhite gene (uw) underlie a new form of oculocutaneous albinism, OCA4. Am J Hum Genet. 2001;69:981-988.
4. Oetting WS, Summers CG, King RA. Albinism and the associated ocular defects. Metab Pediatr Syst Ophthalmol. 1994;17:5-9.
5. Summers CG. Vision in albinism. Trans Am Ophthalmol Soc. 1996;94:1095-1155.
6. Onojafe IF, Adams DR, Simeonov DR, et al. Nitisinone improves eye and skin pigmentation defects in a mouse model of oculocutaneous albinism. J Clin Invest. 2011;121: 3914-3923.
7. Struck MC. Vision response to dopamine replacement. NCT01663935. 2012. Available at http://clinicaltrials.gov/ show/NCT01663935.
8. Summers CG. Trial of L-DOPA as a treatment to improve vision in albinism. NCT01176435.2010. Available at http:// clinicaltrials.gov/ct2/show/NCT01176435.
9. McAllister JT, Dubis AM, Tait DM, et al. Arrested development: high-resolution imaging of foveal morphology in albinism. Vision Res. 2010;50:810-817.
10. Marmor MF, Choi SS, Zawadzki RJ, Werner JS. Visual insignificance of the foveal pit: reassessment of foveal hypoplasia as fovea plana. Arch Ophthalmol. 2008;126:907-913.
11. Thomas MG, Kumar A, Mohammad S, et al. Structural grading of foveal hypoplasia using spectral-domain optical coherence tomography a predictor of visual acuity? Ophthalmology. 2011;118:1653-1660.
12. Seo JH, Yu YS, Kim JH, Choung HK, Heo JW, Kim SJ. Correlation of visual acuity with foveal hypoplasia grading by optical coherence tomography in albinism. Ophthalmology. 2007;114:1547-1551.
13. Chong GT, Farsiu S, Freedman SF, et al. Abnormal foveal morphology in ocular albinism imaged with spectral-domain optical coherence tomography. Arch Ophthalmol. 2009;127: 37-44.
14. Provis JM, Dubis AM, Maddess T, Carroll J. Adaptation of the central retina for high acuity vision: cones, the fovea, and the avascular zone. Prog Retin Eye Res. 2013;35:63-81.
15. Lujan BJ, Roorda A, Knighton RW, Carroll J. Revealing Henle's fiber layer using spectral domain optical coherence tomography. Invest Ophthalmol Vis Sci. 2011;52:1486-1492.
16. Chui TYP, Song HX, Burns SA. Individual variations in human cone photoreceptor packing density: variations with refractive error. Invest Ophthalmol Vis Sci. 2008;49:4679-4687.
17. Rossi EA, Chung M, Dubra A, Hunter JJ, Merigan WH, Williams DR. Imaging retinal mosaics in the living eye. Eye. 2011;25: 301-308.
18. Dubra A, Sulai Y, Norris JL, et al. Non-invasive imaging of the human rod photoreceptor mosaic using a confocal adaptive optics scanning ophthalmoscope. Biomed Opt Express. 2011; 2:1864-1876.
19. Garrison NA, Yi Z, Cohen-Barak O, et al. P gene mutations in patients with oculocutaneous albinism and findings suggestive of Hermansky-Pudlak syndrome. J Med Genet. 2004;41:e86.
20. Giebel LB, Strunk KM, Spritz RA. Organization and nucleotide sequences of the human tyrosinase gene and a truncated tyrosinase-related segment. Genomics. 1991;9:435-445.
21. Lee ST, Nicholls RD, Jong MTC, Fukai K, Spritz RA. Organization and sequence of the human P gene and identification of a new family of transport proteins. Genomics. 1995;26:354-363.
22. Schiaffino MV, Bassi MT, Galli L, et al. Analysis of the OA1 gene reveals mutations in only one-third of patients with X-linked ocular albinism. Hum Mol Genet. 1995;4:2319-2325.
23. Manga P, Kromberg JG, Box NF, Sturm RA, Jenkins T, Ramsay M. Rufous oculocutaneous albinism in southern African Blacks is caused by mutations in the TYRP1 gene. Am J Hum Genet. 1997;61:1095-1101.
24. Durham-Pierre D, Gardner JM, Nakatsu Y, et al. African origin of an intragenic deletion of the human P gene in tyrosinase positive oculocutaneous albinism. Nat Genet. 1994;7:176-179.
25. Tanna H, Dubis AM, Ayub N, et al. Retinal imaging using commercial broadband optical coherence tomography. Br J Ophthalmol. 2010;94:372-376.
26. Dubis AM, McAllister JT, Carroll J. Reconstructing foveal pit morphology from optical coherence tomography imaging. Br J Ophthalmol. 2009;93:1223-1227.
27. Dubis AM, Hansen BR, Cooper RF, Beringer J, Dubra A, Carroll J. Relationship between the foveal avascular zone and foveal pit morphology. Invest Ophthalmol Vis Sci. 2012;53:1628-1636.
28. Cooper RF, Dubis AM, Pavaskar A, Rha J, Dubra A, Carroll J. Spatial and temporal variation of rod photoreceptor reflectance in the human retina. Biomed Opt Express. 2011;2:2577-2589.
29. Dubra A, Harvey Z. Registration of 2D images from fast scanning ophthalmic instruments. In: Fischer B, Dawant BM, Lorenz C, ed. The 4th International Workshop on Biomedical Image Registration. Lübeck, Germany: Springer-Verlag Berlin, Heidelberg; 2010:60-71.
30. Garrioch R, Langlo C, Dubis AM, Cooper RF, Dubra A, Carroll J. Repeatability of in vivo parafoveal cone density and spacing measurements. Optom Vis Sci. 2012;89:632-643.
31. Curcio CA, Sloan KR, Kalina RE, Hendrickson AE. Human photoreceptor topography. J Comp Neurol. 1990;292:497-523.
32. Hutton SM, Spritz RA. A comprehensive genetic study of autosomal recessive ocular albinism in Caucasian patients. Invest Ophthalmol Vis Sci. 2008;49:868-872.
33. Preising MN, Forster H, Gonser M, Lorenz B. Screening of TYR, OCA2, GPR143, and MC1R in patients with congenital nystagmus, macular hypoplasia, and fundus hypopigmentation indicating albinism. Mol Vis. 2011;17:939-948.
34. Sengupta M, Sarkar D, Mondal M, Samanta S, Sil A, Ray K. Analysis of MC1R variants in Indian oculocutaneous albinism patients: highlighting the risk of skin cancer among albinos. J Genet. 2013;92:305-308.
35. Wagner-Schuman M, Dubis AM, Nordgren RN, et al. Race-and sex-related differences in retinal thickness and foveal pit morphology. Invest Ophthalmol Vis Sci. 2010;52:625-634.
36. Li KY, Tiruveedhula P, Roorda A. Intersubject variability of foveal cone photoreceptor density in relation to eye length. Invest Ophthalmol Vis Sci. 2010;51:6858-6867.
37. Gao H, Hollyfield JG. Aging of the human retina: differential loss of neurons and retinal pigment epithelial cells. Invest Ophthalmol Vis Sci. 1992;33:1-17.
38. Spaide RF, Curcio CA. Anatomical correlates to the bands seen in the outer retina by optical coherence tomography: literature review and model. Retina. 2011;31:1609-1619.
39. Spaide RF. Questioning optical coherence tomography. Ophthalmology. 2012;119:2203-2204.
40. Springer AD. New role for the primate fovea: a retinal excavation determines photoreceptor deployment and shape. Vis Neurosci. 1999;16:629-636.
41. Springer AD, Hendrickson AE. Development of the primate area of high acuity. 1. Use of finite element analysis models to identify mechanical variables affecting pit formation. Vis Neurosci. 2004;21:53-62.
42. Springer AD, Hendrickson AE. Development of the primate area of high acuity. 2: quantitative morphological changes associated with retinal and pars plana growth. Vis Neurosci. 2004;21:775-790.
43. Springer AD, Hendrickson AE. Development of the primate area of high acuity. 3: temporal relationships between pit formation, retinal elongation and cone packing. Vis Neurosci. 2005;22:171-185.
44. Provis JM, Diaz CM, Dreher B. Ontogeny of the primate fovea: a central issue in retinal development. Prog Neurobiol. 1998; 54:549-581.
45. Diaz-Araya C, Provis JM. Evidence of photoreceptor migration during early foveal development: a quantitative analysis of human fetal retinae. Vis Neurosci. 1992;8:505-514.
46. Cornish EE, Hendrickson AE, Provis JM. Distribution of shortwavelength-sensitive cones in human fetal and postnatal retina: early development of spatial order and density profiles. Vision Res. 2004;44:2019-2026.
47. Rossi EA, Roorda A. The relationship between visual resolution and cone spacing in the human fovea. Nat Neurosci. 2010;13:156-157.
48. Zawadzki R, Cense B, Zhang Y, Choi S, Miller D, Werner JS. Ultrahigh-resolution optical coherence tomography with monochromatic and chromatic aberration correction. Opt Express. 2008;16:8126-8143.
49. Götzinger E, Pircher M, Geitzenauer W, et al. Retinal pigment epithelium segmentation by polarization sensitive optical coherence tomography. Opt Express. 2008;16: 16410-16422.
50. Srinivasan VJ, Monson BK, Wojtkowski M, et al. Characterization of outer retinal morphology with high-speed, ultrahighresolution optical coherence tomography. Invest Ophthalmol Vis Sci. 2008;49:1571-1579.
51. Weiter JJ, Delori FC, Wing GL, Fitch KA. Retinal pigment epithelial lipofuscin and melanin and choroidal melanin in human eyes. Invest Ophthalmol Vis Sci. 1986;27:145-152.
52. Schmidt SY, Peisch RD. Melanin concentration in normal human retinal pigment epithelium: regional variation and age-related reduction. Invest Ophthalmol Vis Sci. 1986;27:1063-1067.
53. Bloom SM, Singal IP. The outer Bruch membrane layer: a previously undescribed spectral-domain optical coherence tomography finding. Retina. 2011;31:316-323.
54. Heriot WJ, Orlin C, Henkind P. Basal infolding density in the normal pigmented rat. Ophthalmology. 1986;93:484-486.
55. Hogan MJ. Role of the retinal pigment epithelium in macular disease. Trans Am Acad Ophthalmol Otolaryngol. 1972;76: 64-80.
56. Hogan MJ, Alvarado J, Weddell J. Histology of the Human Eye. Philadelphia, PA: W.B. Saunders Company; 1971.
57. Krebs W, Krebs I. Primate Retina and Choroid: Atlas of Fine Structure in Man and Monkey. New York, NY: Springer-Verlag New York, Inc.; 1991.
58. Woodell A, Coughlin B, Kunchithapautham K, et al. Alternative complement pathway deficiency ameliorates chronic smokeinduced functional and morphological ocular injury. PloS One. 2013;8:e67894.
59. Hoang QV, Linsenmeier RA, Chung CK, Curcio CA. Photoreceptor inner segments in monkey and human retina: mitochondrial density, optics, and regional variation. Vis Neurosci. 2002;19:395-407.
60. Torti C, Považay B, Hofer B, et al. Adaptive optics optical coherence tomography at 120,000 depth scans/s for noninvasive cellular phenotyping of the living human retina. Opt Express. 2009;17:19382-19400.
61. Kocaoglu OP, Cense B, Jonnal RS, et al. Imaging retinal nerve fiber bundles using optical coherence tomography with adaptive optics. Vision Res. 2011;51:1835-1844.
62. Kocaoglu OP, Lee S, Jonnal RS, et al. Imaging cone photoreceptors in three dimensions and in time using ultrahigh resolution optical coherence tomography with adaptive optics. Biomed Opt Express. 2011;2:748-763.
63. Piling RF, Thompson JR, Gottlob I. Social and visual function in nystagmus. Br J Ophthalmol. 2005;89:1278-1281.
64. Abadi RV, Bjerre A. Motor and sensory characteristics of infantile nystagmus. Br J Ophthalmol. 2002;86:1152-1160.
65. Fu VLN, Bilonick RA, Felius J, Hertle RW, Birch EE. Visual acuity development of children with infantile nystagmus syndrome. Invest Ophthalmol Vis Sci. 2011;52:1404-1411.
66. von dem Hagen E, Hoffmann MB, Morland AB. Identifying human albinism: a comparison of VEP and fMRI. Invest Ophthalmol Vis Sci. 2008;49:238-249.
67. von dem Hagen EA, Houston GC, Hoffmann MB, Morland AB. Pigmentation predicts the shift in the line of decussation in humans with albinism. Eur J Neurosci. 2007;25:503-511.
68. von dem Hagen EAH, Houston GC, Hoffman MB, Jeffery G, Morland AB. Retinal abnormalities in human albinism translate into a reduction of grey matter in the occipital cortex. Eur J Neurosci. 2005;22:2475-2480.
69. Hoffmann MB, Tolhurst DJ, Moore AT, Morland AB. Organization of the visual cortex in human albinism. J Neurosci. 2003; 23:8921-8930.