In Vivo Imaging of Human Cone Photoreceptor Inner Segments

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 7, 2014, Pages 4244-4251

  Scoles, Drew ^a   Sulai, Yusufu N ^b   Langlo, Christopher S ^c   Fishman, Gerald A ^d,e   Curcio, Christine A ^f   Carroll, Joseph ^c,g   Dubra, Alfredo ^c,g  

^a University of Rochester   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

^d Pangere Center for Inherited Retinal Diseases   (United States)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^f UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^g Marquette University   (United States)

Author keywords

AOSLO; Gene therapy; Photoreceptor

Indexed keywords

CYCLIC NUCLEOTIDE GATED CHANNEL;

ACCOMMODATION PARALYSIS; ARTICLE; COLOR BLINDNESS; CONTROLLED STUDY; EYE AXIS LENGTH; GENE THERAPY; GENETIC SCREENING; HUMAN; HUMAN TISSUE; LIGHT EXPOSURE; PHASE CONTRAST MICROSCOPY; PHOTORECEPTOR INNER SEGMENT; PRIORITY JOURNAL; REFRACTION INDEX; RETINA DEGENERATION; RETINA FOVEA; RETINA IMAGE; SCANNING LASER OPHTHALMOSCOPY; SIGNAL NOISE RATIO; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; VISUAL ACUITY;

AOSLO; GENE THERAPY; PHOTORECEPTOR;

ADULT; AGED; AGED, 80 AND OVER; COLOR VISION DEFECTS; FEMALE; GENETIC TESTING; HUMANS; MALE; OPHTHALMOSCOPY; REPRODUCIBILITY OF RESULTS; RETINAL DEGENERATION; RETINAL PHOTORECEPTOR CELL INNER SEGMENT; RETINITIS PIGMENTOSA; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 84904210421     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.14-14542     Document Type: Article

References (49)

1. Alexander JJ, Umino Y, Everhart D, et al. Restoration of cone vision in a mouse model of achromatopsia. Nat Med. 2007;13: 685-687.
2. Pang JJ, Deng WT, Dai X, et al. AAV-mediated cone rescue in a naturally occurring mouse model of CNGA3-achromatopsia. PLoS One. 2012;7:e35250.
3. Mancuso K, Hauswirth WW, Li Q, et al. Gene therapy for redgreen colour blindness in adult primates. Nature. 2009;461: 784-787.
4. Komaromy AM, Alexander JJ, Rowlan JS, et al. Gene therapy rescues cone function in congenital achromatopsia. Hum Mol Genet. 2010;19:2581-2593.
5. Pearson RA, Barber AC, Rizzi M, et al. Restoration of vision after transplantation of photoreceptors. Nature. 2012;485:99-103.
6. MacLaren RE, Pearson RA, MacNeil A, et al. Retinal repair by transplantation of photoreceptor precursors. Nature. 2006; 444:203-207.
7. Maclaren RE, Groppe M, Barnard AR, et al. Retinal gene therapy in patients with choroideremia: initial findings from a phase 1/2 clinical trial. Lancet. 2014;383:1129-1137.
8. Jacobson SG, Aleman TS, Cideciyan AV, et al. Identifying photoreceptors in blind eyes caused by RPE65 mutations: prerequisite for human gene therapy success. Proc Natl Acad Sci U S A. 2005;102:6177-6182.
9. Liang J, Williams DR. Aberrations and retinal image quality of the normal human eye. J Opt Soc Am A. 1997;14:2873-2883.
10. Dubra A, Sulai Y, Norris JL, et al. Noninvasive imaging of the human rod photoreceptor mosaic using a confocal adaptive optics scanning ophthalmoscope. Biomed Opt Express. 2011; 2:1864-1876.
11. Miller DT, Williams DR, Morris GM, Liang J. Images of cone photoreceptors in the living human eye. Vision Res. 1996;36: 1067-1079.
12. 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.
13. Hamilton DK, Sheppard CJR. Differential phase-contrast in scanning optical microscopy. J Microsc. 1984;133:27-39.
14. Wilson T, Hamilton D. Differential amplitude contrast imaging in the scanning optical microscope. Appl Phys B. 1983;32: 187-191.
15. Amos WB, Reichelt S, Cattermole DM, Laufer J. Re-evaluation of differential phase contrast (DPC) in a scanning laser microscope using a split detector as an alternative to differential interference contrast (DIC) optics. J Microsc. 2003;210:166-175.
16. Dubra A, Sulai Y. Reflective afocal broadband adaptive optics scanning ophthalmoscope. Biomed Opt Express. 2011;2: 1757-1768.
17. Roorda A, Romero-Borja F, Donnelly WJ, Queener H, Hebert TJ, Campbell MCW. Adaptive optics scanning laser ophthalmoscopy. Opt Express. 2002;10:405-412.
18. Calver R, Radhakrishnan H, Osuobeni E, O'Leary D. Peripheral refraction for distance and near vision in emmetropes and myopes. Ophthalmic Physiol Opt. 2007;27:584-593.
19. Mallen EAH, Kashyap P. Technical note: measurement of retinal contour and supine axial length using the Zeiss IOLMaster. Ophthalmic Physiol Opt. 2007;27:404-411.
20. Sundaram V, Wilde C, Aboshiha J, et al. Retinal structure and function in achromatopsia: implications for gene therapy. Ophthalmology. 2014;121:234-245.
21. Webb RH, Hughes GW, Delori FC. Confocal scanning laser ophthalmoscope. Appl Optics. 1987;26:1492-1499.
22. Ford TN, Chu KK, Mertz J. Phase-gradient microscopy in thick tissue with oblique back-illumination. Nat Methods. 2012;9: 1195-1197.
23. Sulai YN, Scoles D, Harvey Z, Dubra A. Visualization of retinal vascular structure and perfusion with a nonconfocal adaptive optics scanning light ophthalmoscope. J Opt Soc Am A. 2014; 31:569-579.
24. ANSI. American National Standard for Safe Use of Lasers in Research, Development, or Testing. Orlando, FL: Laser Institute of America; 2007.
25. Delori FC, Webb RH, Sliney DH. Maximum permissible exposures for ocular safety (ANSI 2000), with emphasis on ophthalmic devices. J Opt Soc Am A. 2007;24:1250-1265.
26. Dubra A, Harvey Z. Registration of 2D Images from Fast Scanning Ophthalmic Instruments. The 4th International Workshop on Biomedical Image Registration. Lübeck: Springer-Verlag; 2010.
27. Hirsch J, Curcio CA. The spatial resolution capacity of human foveal retina. Vision Res. 1989;29:1095-1101.
28. Rossi EA, Roorda A. The relationship between visual resolution and cone spacing in the human fovea. Nat Neurosci. 2010;13:156-157.
29. Curcio CA, Packer O, Kalina RE. A whole mount method for sequential analysis of photoreceptor and ganglion cell topography in a single retina. Vision Res. 1987;27:9-15.
30. Curcio CA, Sloan KR, Kalina RE, Hendrickson AE. Human photoreceptor topography. J Comp Neurol. 1990;292:497-523.
31. Curcio CA, Millican CL, Allen KA, Kalina RE. Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina. Invest Ophthalmol Vis Sci. 1993;34:3278-3296.
32. Weibel ER. Stereological Methods. New York: Academic Press; 1979.
33. Packer O, Hendrickson AE, Curcio CA. Photoreceptor topography of the retina in the adult pigtail macaque (Macaca nemestrina). J Comp Neurol. 1989;288:165-183.
34. Drasdo N, Millican CL, Katholi CR, Curcio CA. The length of Henle fibers in the human retina and a model of ganglion receptive field density in the visual field. Vision Res. 2007;47: 2901-2911.
35. Kolb H, Gouras P. Electron microscopic observations of human retinitis pigmentosa, dominantly inherited. Invest Ophthalmol. 1974;13:487-498.
36. Szamier RB, Berson EL. Retinal ultrastructure in advanced retinitis pigmentosa. Invest Ophthalmol Vis Sci. 1977;16:947-962.
37. Gao J, Cheon K, Nusinowitz S, et al. Progressive photoreceptor degeneration, outer segment dysplasia, and rhodopsin mislocalization in mice with targeted disruption of the retinitis pigmentosa-1 (Rp1) gene. Proc Natl Acad Sci U S A. 2002;99: 5698-5703.
38. Johnson PT, Lewis GP, Talaga KC, et al. Drusen-associated degeneration in the retina. Invest Ophthalmol Vis Sci. 2003; 44:4481-4488.
39. Curcio CA, Medeiros NE, Millican CL. Photoreceptor loss in age-related macular degeneration. Invest Ophthalmol Vis Sci. 1996;37:1236-1249.
40. Syed N, Smith JE, John SK, Seabra MC, Aguirre GD, Milam AH. Evaluation of retinal photoreceptors and pigment epithelium in a female carrier of choroideremia. Ophthalmology. 2001; 108:711-720.
41. Joeres S, Jones SM, Chen DC, et al. Retinal imaging with adaptive optics scanning laser ophthalmoscopy in unexplained central ring scotoma. Arch Ophthalmol. 2008;126: 543-547.
42. Carroll J, Kay DB, Scoles D, Dubra A, Lombardo M. Adaptive optics retinal imaging-clinical opportunities and challenges. Curr Eye Res. 2013;38:709-721.
43. Makiyama Y, Ooto S, Hangai M, et al. Macular cone abnormalities in retinitis pigmentosa with preserved central vision using adaptive optics scanning laser ophthalmoscopy. PLoS One. 2013;8:e79447.
44. Yokota S, Ooto S, Hangai M, et al. Objective assessment of foveal cone loss ratio in surgically closed macular holes using adaptive optics scanning laser ophthalmoscopy. PLoS One. 2013;8:e63786.
45. Hood DC, Zhang X, Ramachandran R, et al. The inner segment/outer segment border seen on optical coherence tomography is less intense in patients with diminished cone function. Invest Ophthalmol Vis Sci. 2011;52:9703-9709.
46. Thomas MG, McLean RJ, Kohl S, Sheth V, Gottlob I. Early signs of longitudinal progressive cone photoreceptor degeneration in achromatopsia. Br J Ophthalmol. 2012;96:1232-1236.
47. Genead MA, Fishman GA, Rha J, et al. Photoreceptor structure and function in patients with congenital achromatopsia. Invest Ophthalmol Vis Sci. 2011;52:7298-7308.
48. Cideciyan AV, Hufnagel RB, Carroll J, et al. Human cone visual pigment deletions spare sufficient photoreceptors to warrant gene therapy. Hum Gene Ther. 2013;24:993-1006.
49. Roorda A, Zhang Y, Duncan JL. High-resolution in vivo imaging of the RPE mosaic in eyes with retinal disease. Invest Ophthalmol Vis Sci. 2007;48:2297-2303.