Relationship between the foveal avascular zone and foveal pit morphology

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 3, 2012, Pages 1628-1636

  Dubis, Adam M ^a   Hansen, Benjamin R ^b,c   Cooper, Robert F ^c   Beringer, Joseph ^d   Dubra, Alfredo ^c,d,e   Carroll, Joseph ^a,c,d,e  

^a Departments of Cell Biology Neurobiology and Anatomy   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c Marquette University   (United States)

^d Departments of Ophthalmology   (United States)

^e Departments of Biophysics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; EYE AXIS LENGTH; FEMALE; FOVEAL AVASCULAR ZONE; HUMAN; INTERFEROMETER; MALE; MORPHOLOGY; PRIORITY JOURNAL; RETINA BLOOD VESSEL; RETINA FOVEA; RETINA MACULA LUTEA; SCANNING LASER OPHTHALMOSCOPY; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; THICKNESS; ADOLESCENT; CAPILLARY; HISTOLOGY; MIDDLE AGED; OPTICAL COHERENCE TOMOGRAPHY; VASCULARIZATION;

ADOLESCENT; ADULT; AGED; CAPILLARIES; FEMALE; FOVEA CENTRALIS; HUMANS; MALE; MIDDLE AGED; TOMOGRAPHY, OPTICAL COHERENCE; YOUNG ADULT;

EID: 84860594263     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.11-8488     Document Type: Article

References (80)

1. Hendrickson A. Organization of the adult primate fovea. In: Penfold PL, Provis JM, eds. Macular Degeneration. Heidelberg: Springer-Verlag; 2005:1-20.
2. Provis JM, Penfold PL, Cornish EE, Sandercoe TM, Madigan MC. Anatomy and development of the macula: specialisation and the volunerability to macular degeneration. Clin Exp Optom. 2005;88: 269-281.
3. Isenberg SJ. Macular development in the premature infant. Am J Ophthalmol. 1986;101:74-80.
4. Mintz-Hittner HA, Knight-Nanan DM, Satriano DR, Kretzer FL. A small foveal avascular zone may be an historic mark of prematurity. Ophthalmology. 1999;106:1409-1413.
5. Hammer DX, Iftimia NV, Ferguson RD, et al. Foveal fine structure in retinopathy of prematurity: an adaptive optics Fourier domain optical coherence tomography study. Invest Ophthalmol Vis Sci.2008;49:2061-2070.
6. Vinekar A, Avadhani K, Sivakumar M, et al. Understanding clinically undetected macular changes in early retinopathy of prematurity on spectral domain optical coherence tomography. Invest Ophthalmol Vis Sci. 2011;52:5183-5188.
7. Gregor Z. The perifoveal vasculature in albinism. Br J Ophthalmol.1978;62:554-557.
8. Abadi RV, Pascal D. The recognition and management of albinism. Ophthalmic Physiol Opt. 1989;9:3-15.
9. Kinnear PE, Jay B, Witkop CJJ. Albinism. Surv Ophthalmol. 1985; 30:75-101.
10. Oetting WS, Summers CG, King RA. Albinism and the associated ocular defects. Metab Pediatr Syst Ophthalmol. 1994;17:5-9.
11. 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.
12. McAllister JT, Dubis AM, Tait DM, et al. Arrested development: high-resolution imaging of foveal morphology in albinism. Vision Res. 2010;50:810-817.
13. Bresnick GH, Condit R, Syrjala S, Palta M, Groo A, Korth K. Abnormalities of the foveal avascular zone in diabetic retinopathy. Arch Ophthalmol. 1984;102:1286-1293.
14. Conrath J, Giorgi R, Raccah D, Ridings B. Foveal avascular zone in diabetic retinopathy: quantitative vs qualitative assessment. Eye (Lond). 2005;19:322-326.
15. Tam J, Dhamdhere KP, Tiruveedhula P, et al. Disruption of the retinal parafoveal capillary network in type 2 diabetes before the onset of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2011;52: 9257-9266.
16. Elsner AE, Weber A, Cheney MC, VanNasdale DA, Miura M. Imaging polarimetry in patients with neovascular age-related macular degeneration. J Opt Soc Am A. 2007;24:1468-1480.
17. Springer AD. New role for the primate fovea: a retinal excavation determines photoreceptor deployment and shape. Vis Neurosci.1999;16:629-636.
18. Bone RA, Landrum JT, Fernandez L, Tarsis S. Analysis of the macular pigment by HPLC: retinal distribution and age study. Invest Ophthalmol Vis Sci. 1988;29:843-849.
19. Berendschot TTJM, Willemse-Assink JJM, Bastiaanse M, de Jong PTVM, van Norren D. Macular pigment and melanin in age related maculopathy in a general population. Invest Ophthalmol Vis Sci.2002;43:1928-1932.
20. Kirby ML, Beatty S, Loane E, et al. A central dip in the macular pigment spatial profile is associated with age and smoking. Invest Ophthalmol Vis Sci. 2010;51:6722-6728.
21. Hammond BR, Caruso-Avery M. Macular pigment optical density in a Southwestern sample. Invest Ophthalmol Vis Sci. 2000;41:1492-1497.
22. Whitehead AJ, Mares JA, Danis RP. Macular pigment: a review of current knowledge. Arch Ophthalmol. 2006;124:1038-1045.
23. Kimble TDH, Williams RW. Structure of the cone photoreceptor mosaic in the retinal periphery of adult humans: analysis as a function of age, sex, and hemifield. Anat Embryol. 2000;201:305-316.
24. Song H, Chui TYP, Zhong Z, Elsner AE, Burns SA. Variation in cone photoreceptor packing density with retinal eccentricity and age. Invest Ophthalmol Vis Sci. 2011;52:7376-7384.
25. 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.
26. Curcio CA, Medeiros NE, Millican CL. Photoreceptor loss in agerelated macular degeneration. Invest Ophthalmol Vis Sci. 1996; 37:1236-1249.
27. Gorrand JM, Delori FC. Reflectance and curvature of the inner limiting membrane at the foveola. J Opt Soc Am A. 1999;16:1229-1237.
28. Tick S, Rossant F, Ghorbel I, et al. Foveal shape and structure in a normal population. Invest Ophthalmol Vis Sci. 2011;52:5105-5110.
29. Laatikainen L, Larinkari J. Capillary-free area of the fovea with advancing age. Invest Ophthalmol Vis Sci. 1977;16:1154-1157.
30. Sanders RJ, Brown GC, Rosenstein RB, Magargal L. Foveal avascular zone diameter and sickle cell disease. Arch Ophthalmol. 1991;109: 812-815.
31. Curcio CA, Messinger JD, Sloan KR, Mitra A, McGwin G, Spaide RF. Human chorioretinal layer thicknesses measured in macula-wide, high-resolution histologic sections. Invest Ophthalmol Vis Sci.2011;52:3943-3954.
32. Nolan JM, Stringham JM, Beatty S, Snodderly DM. Spatial profile of macular pigment and its relationship to foveal architecture. Invest Ophthalmol Vis Sci. 2008;49:2134-2142.
33. Dubis AM, McAllister JT, Carroll J. Reconstructing foveal pit morphology from optical coherence tomography imaging. Br J Ophthalmol.2009;93:1223-1227.
34. Kirby ML, Galea M, Loane E, Stack J, Beatty S, Nolan JM. Foveal anatomic associations with the secondary peak and the slope of the macular pigment spatial profile. Invest Ophthalmol Vis Sci.2009;50:1383-1391.
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. Levi DM, Klein SA, Yap YL. Positional uncertainty in peripheral and amblyopic vision. Vision Res. 1987;27:581-598.
37. Zeffren BS, Applegate RA, Bradley A, van Heuven WAJ. Retinal fixation point location in the foveal avascular zone. Invest Ophthalmol Vis Sci. 1990;31:2099-2105.
38. Bradley A, Applegate RA, Zeffren BS, van Heuven WA. Psychophysical measurement of the size and shape of the human foveal avascular zone. Ophthalmic Physiol Opt. 1992;12:18-23.
39. Zheng Y, Gandhi JS, Stangos AN, Campa C, Broadbent DM, Harding SP. Automated segmentation of foveal avascular zone in fundus fluorescein angiography. Invest Ophthalmol Vis Sci. 2010;51: 3653-3659.
40. Provis JM, Hendrickson AE. The foveal avascular region of developing human retina. Arch Ophthalmol. 2008;126:507-511.
41. Wang Q, Kocaoglu OP, Cense B, et al. Imaging retinal capillaries using ultrahigh-resolution optical coherence tomography and adaptive optics. Invest Ophthalmol Vis Sci. 2011;52:6292-6299.
42. Kim DY, Fingler J, Zawadzki RJ, et al. Noninvasive imaging of the foveal avascular zone with high-speed phase-variance optical coherence tomography. Invest Ophthalmol Vis Sci. 2012;53:85-92.
43. Tam J, Martin JA, Roorda A. Non-invasive visualization and analysis of parafoveal capillaries in humans. Invest Ophthalmol Vis Sci.2010;51:1691-1698.
44. Popovic Z, Knutsson P, Thaung J, Owner-Peterson M, Sjöstrand J. Noninvasive imaging of human foveal capillary network using dual-conjugate adaptive optics. Invest Ophthalmol Vis Sci. 2011; 52:2649-2655.
45. 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.
46. 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.
47. Merino D, Duncan JL, Tiruveedhula P, Roorda A. Observation of cone and rod photoreceptors in normal subjects and patients using a new generation adaptive optics scanning laser ophthalmoscope. Biomed Opt Express. 2011;2:2189-2201.
48. Izhaky D, Nelson DA, Burgansky-Eliash Z, Grinvald A. Functional imaging using the retinal function imager: direct imaging of blood velocity, achieving fluorescein angiography-like images without any contrast agent, qualitative oximetry, and functional metabolic signals. Jpn J Ophthalmol. 2009;53:345-351.
49. Dubra A, Sulai Y. Reflective afocal broadband adaptive optics scanning ophthalmoscope. Biomed Opt Express. 2011;2:1757-1768.
50. Dubra A, Harvey Z. Registration of 2D images from fast scanning ophthalmic instruments. Proceedings of the 4th International Conference on Biomedical Image Registration. Heidelberg: Springer-Verlag; 2010:60-71.
51. Abramoff MD, Magelhaes PJ, Ram SJ. Image processing with ImageJ. Biophotonics Int. 2004;11:36-42.
52. Polyak SL. The Retina. Chicago: The University of Chicago Press; 1941.
53. Yamada E. Some structural features of the fovea centralis in the human retina. Arch Ophthalmol. 1969;82:151-159.
54. Hendrickson AE, Yuodelis C. The morphological development of the human fovea. Ophthalmology. 1984;91:603-612.
55. 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.
56. Gupta A, Laxmi G, Nittala MG, Raman R. Structural and functional correlates in color vision deficiency. Eye (Lond). 2011;25:909-917.
57. 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.
58. Walls GL. Significance of the foveal depression. Arch Ophthalmol.1937;18:912-919.
59. Mohammad S, Gottlob I, Kumar A, et al. The functional significance of foveal abnormalities in albinism measured using spectraldomain optical coherence tomography. Ophthalmology. 2011; 118:1645-1652.
60. 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.
61. Rossi EA, Weiser P, Tarrant J, Roorda A. Visual performance in emmetropia and low myopia after correction of high-order aberrations. J Vis. 2007;7:1-14.
62. Rossi EA, Roorda A. The relationship between visual resolution and cone spacing in the human fovea. Nat Neurosci. 2010;13:156-157.
63. Arend O, Wolf S, Jung F, et al. Retinal microcirculation in patients with diabetes mellitus: dynamic and morphological analysis of perifoveal capillary network. Br J Ophthalmol. 1991;75:514-518.
64. John D, Kuriakose T, Devasahayam S, Braganza A. Dimensions of the foveal avascular zone using the Heidelberg retinal angiogram-2 in normal eyes. Indian J Ophthalmol. 2011;59:9-11.
65. Curcio CA, Sloan KR, Kalina RE, Hendrickson AE. Human photoreceptor topography. J Comp Neurol. 1990;292:497-523.
66. Duncan JL, Zhang Y, Gandhi J, et al. High-resolution imaging with adaptive optics in patients with inherited retinal degeneration. Invest Ophthalmol Vis Sci. 2007;48:3283-3291.
67. 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.
68. Chui TY, Song H, Burns SA. Adaptive-optics imaging of human cone photoreceptor distribution. J Opt Soc Am A. 2008;25:3021-3029.
69. 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.
70. Duncan JL, Talcott KE, Ratnam K, et al. Cone structure in retinal degeneration associated with mutations in the peripherin/RDS gene. Invest Ophthalmol Vis Sci. 2011;52:1557-1566.
71. Stensaas SS, Eddington DK, Dobelle WH. The topography and variability of the primary visual cortex in man. J Neurosurg. 1974; 40:747-755.
72. Andrews TJ, Halpern SD, Purves D. Correlated size variations in human visual cortex, lateral geniculate nucleus, and optic tract. J Neurosci. 1997;17:2859-2868.
73. Dougherty RF, Koch VM, Brewer AA, Fischer B, Modersitzki J, Wandell BA. Visual field representations and locations of visual areas V1/2/3 in human visual cortex. J Vis. 2003;3:586-598.
74. Wandell BA, Brewer AA, Dougherty RF. Visual field map clusters in human cortex. Philos Trans R Soc Lond B Biol Sci. 2005;360:639-707.
75. Provis JM, Diaz CM, Dreher B. Ontogeny of the primate fovea: a central issue in retinal development. Prog Neurobiol. 1998;54: 549-581.
76. Hendrickson A, Provis J. Comparison of development of the primate fovea centralis with peripheral retina. In: Sernagor E, Eglen S, Harris B, Wong R, eds. Retinal Development. Cambridge: Cambridge University Press; 2006.
77. Maldonado RS, O'Connell RV, Sarin N, et al. Dynamics of human foveal development after premature birth. Ophthalmology. 2011; 118:2315-2325.
78. Kozulin P, Natoli R, Bumsted O'Brien KM, Madigan MC, Provis JM. Differential expression of anti-angiogenic factors and guidance genes in the developing macula. Mol Vis. 2009;15:49-59.
79. Kozulin P, Natoli R, Bumsted O'Brien KM, Madigan MC, Provis J. The cellular expression of antiangiogenic factors in fetal primate macula. Invest Ophthalmol Vis Sci. 2010;51:4298-4306.
80. Putnam N, Hammer D, Zhang Y, Merino D, Roorda A. Modeling the foveal cone mosaic imaged with adaptive optics scanning laser ophthalmoscopy. Opt Express. 2010;18:24902-24916.