Video Abstract
Images of Rod Photoreceptors Inside the Living Human Eye

Abstract

The rod photoreceptors are implicated in a number of devastating retinal diseases. However, routine imaging of these cells has remained elusive, even with the advent of adaptive optics imaging. Here, we present the first in vivo images of the contiguous rod photoreceptor mosaic in nine healthy human subjects. The images were collected with three different confocal adaptive optics scanning ophthalmoscopes at two different institutions, using 680 and 775 nm superluminescent diodes for illumination. Estimates of photoreceptor density and rod:cone ratios in the 5°–15° retinal eccentricity range are consistent with histological findings, confirming our ability to resolve the rod mosaic by averaging multiple registered images, without the need for additional image processing. In one subject, we were able to identify the emergence of the first rods at approximately 190 μm from the foveal center, in agreement with previous histological studies. The rod and cone photoreceptor mosaics appear in focus at different retinal depths, with the rod mosaic best focus (i.e., brightest and sharpest) being at least 10 μm shallower than the cones at retinal eccentricities larger than 8°. This study represents an important step in bringing high-resolution imaging to bear on the study of rod disorders.

© 2011 OSA

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2011 (3)

2010 (4)

R. S. Jonnal, J. R. Besecker, J. C. Derby, O. P. Kocaoglu, B. Cense, W. Gao, Q. Wang, and D. T. Miller, “Imaging outer segment renewal in living human cone photoreceptors,” Opt. Express 18(5), 5257–5270 (2010).
[CrossRef] [PubMed]

J. Carroll, E. A. Rossi, J. Porter, J. Neitz, A. Roorda, D. R. Williams, and M. Neitz, “Deletion of the X-linked opsin gene array locus control region (LCR) results in disruption of the cone mosaic,” Vision Res. 50(19), 1989–1999 (2010).
[CrossRef] [PubMed]

J. T. McAllister, A. M. Dubis, D. M. Tait, S. Ostler, J. Rha, K. E. Stepien, C. G. Summers, and J. Carroll, “Arrested development: high-resolution imaging of foveal morphology in albinism,” Vision Res. 50(8), 810–817 (2010).
[CrossRef] [PubMed]

J. Carroll, E. Banin, D. M. Hunt, R. Martin, M. Michaelides, L. Mizrahi-Meissonnier, A. T. Moore, D. Sharon, D. R. Williams, and A. Dubra, “Evaluating the photoreceptor mosaic in blue cone monochromacy (BCM),” Invest. Ophthalmol. Vis. Sci. 51, E-Abstract 2935 (2010).

2009 (3)

M. K. Yoon, A. Roorda, Y. Zhang, C. Nakanishi, L. J. Wong, Q. Zhang, L. Gillum, A. Green, and J. L. Duncan, “Adaptive optics scanning laser ophthalmoscopy images in a family with the mitochondrial DNA T8993C mutation,” Invest. Ophthalmol. Vis. Sci. 50(4), 1838–1847 (2009).
[CrossRef] [PubMed]

J. Carroll, R. C. Baraas, M. Wagner-Schuman, J. Rha, C. A. Siebe, C. Sloan, D. M. Tait, S. Thompson, J. I. W. Morgan, J. Neitz, D. R. Williams, D. H. Foster, and M. Neitz, “Cone photoreceptor mosaic disruption associated with Cys203Arg mutation in the M-cone opsin,” Proc. Natl. Acad. Sci. U.S.A. 106(49), 20948–20953 (2009).
[CrossRef] [PubMed]

C. Torti, B. Považay, B. Hofer, A. Unterhuber, J. Carroll, P. K. Ahnelt, and W. Drexler, “Adaptive optics optical coherence tomography at 120,000 depth scans/s for non-invasive cellular phenotyping of the living human retina,” Opt. Express 17(22), 19382–19400 (2009).
[CrossRef] [PubMed]

2008 (4)

2007 (7)

2006 (3)

M. Michaelides, A. J. Hardcastle, D. M. Hunt, and A. T. Moore, “Progressive cone and cone-rod dystrophies: phenotypes and underlying molecular genetic basis,” Surv. Ophthalmol. 51(3), 232–258 (2006).
[CrossRef] [PubMed]

J. I. Wolfing, M. Chung, J. Carroll, A. Roorda, and D. R. Williams, “High-resolution retinal imaging of cone-rod dystrophy,” Ophthalmology 113(6), 1014–1019.e1 (2006).
[CrossRef] [PubMed]

S. S. Choi, N. Doble, J. L. Hardy, S. M. Jones, J. L. Keltner, S. S. Olivier, and J. S. Werner, “In vivo imaging of the photoreceptor mosaic in retinal dystrophies and correlations with visual function,” Invest. Ophthalmol. Vis. Sci. 47(5), 2080–2092 (2006).
[CrossRef] [PubMed]

2005 (1)

S. B. Stevenson and A. Roorda, “Correcting for miniature eye movements in high resolution scanning laser ophthalmoscopy,” Proc. SPIE 5688A, 145–151 (2005).
[CrossRef]

2004 (1)

J. Carroll, M. Neitz, H. Hofer, J. Neitz, and D. R. Williams, “Functional photoreceptor loss revealed with adaptive optics: an alternate cause of color blindness,” Proc. Natl. Acad. Sci. U.S.A. 101(22), 8461–8466 (2004).
[CrossRef] [PubMed]

2003 (1)

A. Pallikaris, D. R. Williams, and H. Hofer, “The reflectance of single cones in the living human eye,” Invest. Ophthalmol. Vis. Sci. 44(10), 4580–4592 (2003).
[CrossRef] [PubMed]

2002 (1)

A. Roorda and D. R. Williams, “Optical fiber properties of individual human cones,” J. Vis. 2(5), 4 (2002).
[CrossRef] [PubMed]

2001 (1)

A. Roorda, A. B. Metha, P. Lennie, and D. R. Williams, “Packing arrangement of the three cone classes in primate retina,” Vision Res. 41(10-11), 1291–1306 (2001).
[CrossRef] [PubMed]

2000 (2)

T. M. Nork, J. N. Ver Hoeve, G. L. Poulsen, R. W. Nickells, M. D. Davis, A. J. Weber, S. H. Vaegan, S. H. Sarks, H. L. Lemley, and L. L. Millecchia, “Swelling and loss of photoreceptors in chronic human and experimental glaucomas,” Arch. Ophthalmol. 118(2), 235–245 (2000).
[PubMed]

C. A. Curcio, C. Owsley, and G. R. Jackson, “Spare the rods, save the cones in aging and age-related maculopathy,” Invest. Ophthalmol. Vis. Sci. 41(8), 2015–2018 (2000).
[PubMed]

1999 (2)

R. Adler, C. Curcio, D. Hicks, D. Price, and F. Wong, “Cell death in age-related macular degeneration,” Mol. Vis. 5, 31 (1999).
[PubMed]

A. Roorda and D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397(6719), 520–522 (1999).
[CrossRef] [PubMed]

1997 (1)

1996 (2)

C. A. Curcio, N. E. Medeiros, and C. L. Millican, “Photoreceptor loss in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 37(7), 1236–1249 (1996).
[PubMed]

O. S. Packer, D. R. Williams, and D. G. Bensinger, “Photopigment transmittance imaging of the primate photoreceptor mosaic,” J. Neurosci. 16(7), 2251–2260 (1996).
[PubMed]

1995 (1)

K. R. Kendell, H. A. Quigley, L. A. Kerrigan, M. E. Pease, and E. N. Quigley, “Primary open-angle glaucoma is not associated with photoreceptor loss,” Invest. Ophthalmol. Vis. Sci. 36(1), 200–205 (1995).
[PubMed]

1993 (2)

E. L. Berson, “Retinitis pigmentosa. The Friedenwald Lecture,” Invest. Ophthalmol. Vis. Sci. 34(5), 1659–1676 (1993).
[PubMed]

C. A. Curcio, C. L. Millican, K. A. Allen, and R. E. Kalina, “Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina,” Invest. Ophthalmol. Vis. Sci. 34(12), 3278–3296 (1993).
[PubMed]

1992 (3)

H. Gao and J. G. Hollyfield, “Aging of the human retina. Differential loss of neurons and retinal pigment epithelial cells,” Invest. Ophthalmol. Vis. Sci. 33(1), 1–17 (1992).
[PubMed]

C. A. Curcio and K. R. Sloan, “Packing geometry of human cone photoreceptors: variation with eccentricity and evidence for local anisotropy,” Vis. Neurosci. 9(02), 169–180 (1992).
[CrossRef] [PubMed]

L. N. Thibos, M. Ye, X. Zhang, and A. Bradley, “The chromatic eye: a new reduced-eye model of ocular chromatic aberration in humans,” Appl. Opt. 31(19), 3594–3600 (1992).
[CrossRef] [PubMed]

1990 (2)

D. Pum, P. K. Ahnelt, and M. Grasl, “Iso-orientation areas in the foveal cone mosaic,” Vis. Neurosci. 5(06), 511–523 (1990).
[CrossRef] [PubMed]

C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
[CrossRef] [PubMed]

1988 (1)

D. R. Williams, “Topography of the foveal cone mosaic in the living human eye,” Vision Res. 28(3), 433–454 (1988).
[CrossRef] [PubMed]

1987 (1)

1986 (1)

Y. Miyake, K. Yagasaki, M. Horiguchi, Y. Kawase, and T. Kanda, “Congenital stationary night blindness with negative electroretinogram. A new classification,” Arch. Ophthalmol. 104(7), 1013–1020 (1986).
[PubMed]

1984 (1)

K. R. Alexander and G. A. Fishman, “Prolonged rod dark adaptation in retinitis pigmentosa,” Br. J. Ophthalmol. 68(8), 561–569 (1984).
[CrossRef] [PubMed]

1983 (1)

M. Alpern, C. C. Ching, and K. Kitahara, “The directional sensitivity of retinal rods,” J. Physiol. 343, 577–592 (1983).
[PubMed]

1975 (1)

J. A. Van Loo and J. M. Enoch, “The scotopic Stiles-Crawford effect,” Vision Res. 15(8-9), 1005–1009 (1975).
[CrossRef] [PubMed]

Adler, R.

R. Adler, C. Curcio, D. Hicks, D. Price, and F. Wong, “Cell death in age-related macular degeneration,” Mol. Vis. 5, 31 (1999).
[PubMed]

Ahnelt, P. K.

Alexander, K. R.

K. R. Alexander and G. A. Fishman, “Prolonged rod dark adaptation in retinitis pigmentosa,” Br. J. Ophthalmol. 68(8), 561–569 (1984).
[CrossRef] [PubMed]

Allen, K. A.

C. A. Curcio, C. L. Millican, K. A. Allen, and R. E. Kalina, “Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina,” Invest. Ophthalmol. Vis. Sci. 34(12), 3278–3296 (1993).
[PubMed]

Alpern, M.

M. Alpern, C. C. Ching, and K. Kitahara, “The directional sensitivity of retinal rods,” J. Physiol. 343, 577–592 (1983).
[PubMed]

Arathorn, D. W.

Banin, E.

J. Carroll, E. Banin, D. M. Hunt, R. Martin, M. Michaelides, L. Mizrahi-Meissonnier, A. T. Moore, D. Sharon, D. R. Williams, and A. Dubra, “Evaluating the photoreceptor mosaic in blue cone monochromacy (BCM),” Invest. Ophthalmol. Vis. Sci. 51, E-Abstract 2935 (2010).

Baraas, R. C.

J. Carroll, R. C. Baraas, M. Wagner-Schuman, J. Rha, C. A. Siebe, C. Sloan, D. M. Tait, S. Thompson, J. I. W. Morgan, J. Neitz, D. R. Williams, D. H. Foster, and M. Neitz, “Cone photoreceptor mosaic disruption associated with Cys203Arg mutation in the M-cone opsin,” Proc. Natl. Acad. Sci. U.S.A. 106(49), 20948–20953 (2009).
[CrossRef] [PubMed]

R. C. Baraas, J. Carroll, K. L. Gunther, M. Chung, D. R. Williams, D. H. Foster, and M. Neitz, “Adaptive optics retinal imaging reveals S-cone dystrophy in tritan color-vision deficiency,” J. Opt. Soc. Am. A 24(5), 1438–1447 (2007).
[CrossRef] [PubMed]

Bensinger, D. G.

O. S. Packer, D. R. Williams, and D. G. Bensinger, “Photopigment transmittance imaging of the primate photoreceptor mosaic,” J. Neurosci. 16(7), 2251–2260 (1996).
[PubMed]

Berson, E. L.

E. L. Berson, “Retinitis pigmentosa. The Friedenwald Lecture,” Invest. Ophthalmol. Vis. Sci. 34(5), 1659–1676 (1993).
[PubMed]

Besecker, J. R.

Bradley, A.

Branham, K. E. H.

J. L. Duncan, Y. Zhang, J. Gandhi, C. Nakanishi, M. Othman, K. E. H. Branham, A. Swaroop, and A. Roorda, “High-resolution imaging with adaptive optics in patients with inherited retinal degeneration,” Invest. Ophthalmol. Vis. Sci. 48(7), 3283–3291 (2007).
[CrossRef] [PubMed]

Burns, S. A.

Carlini, A. R.

Carroll, J.

J. Carroll, E. A. Rossi, J. Porter, J. Neitz, A. Roorda, D. R. Williams, and M. Neitz, “Deletion of the X-linked opsin gene array locus control region (LCR) results in disruption of the cone mosaic,” Vision Res. 50(19), 1989–1999 (2010).
[CrossRef] [PubMed]

J. T. McAllister, A. M. Dubis, D. M. Tait, S. Ostler, J. Rha, K. E. Stepien, C. G. Summers, and J. Carroll, “Arrested development: high-resolution imaging of foveal morphology in albinism,” Vision Res. 50(8), 810–817 (2010).
[CrossRef] [PubMed]

J. Carroll, E. Banin, D. M. Hunt, R. Martin, M. Michaelides, L. Mizrahi-Meissonnier, A. T. Moore, D. Sharon, D. R. Williams, and A. Dubra, “Evaluating the photoreceptor mosaic in blue cone monochromacy (BCM),” Invest. Ophthalmol. Vis. Sci. 51, E-Abstract 2935 (2010).

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S. S. Choi, N. Doble, J. L. Hardy, S. M. Jones, J. L. Keltner, S. S. Olivier, and J. S. Werner, “In vivo imaging of the photoreceptor mosaic in retinal dystrophies and correlations with visual function,” Invest. Ophthalmol. Vis. Sci. 47(5), 2080–2092 (2006).
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C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
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Herde, A. E.

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Hofer, H.

J. Carroll, M. Neitz, H. Hofer, J. Neitz, and D. R. Williams, “Functional photoreceptor loss revealed with adaptive optics: an alternate cause of color blindness,” Proc. Natl. Acad. Sci. U.S.A. 101(22), 8461–8466 (2004).
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J. Carroll, E. Banin, D. M. Hunt, R. Martin, M. Michaelides, L. Mizrahi-Meissonnier, A. T. Moore, D. Sharon, D. R. Williams, and A. Dubra, “Evaluating the photoreceptor mosaic in blue cone monochromacy (BCM),” Invest. Ophthalmol. Vis. Sci. 51, E-Abstract 2935 (2010).

M. Michaelides, A. J. Hardcastle, D. M. Hunt, and A. T. Moore, “Progressive cone and cone-rod dystrophies: phenotypes and underlying molecular genetic basis,” Surv. Ophthalmol. 51(3), 232–258 (2006).
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C. A. Curcio, C. Owsley, and G. R. Jackson, “Spare the rods, save the cones in aging and age-related maculopathy,” Invest. Ophthalmol. Vis. Sci. 41(8), 2015–2018 (2000).
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S. S. Choi, N. Doble, J. L. Hardy, S. M. Jones, J. L. Keltner, S. S. Olivier, and J. S. Werner, “In vivo imaging of the photoreceptor mosaic in retinal dystrophies and correlations with visual function,” Invest. Ophthalmol. Vis. Sci. 47(5), 2080–2092 (2006).
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Jonnal, R. S.

Kalina, R. E.

C. A. Curcio, C. L. Millican, K. A. Allen, and R. E. Kalina, “Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina,” Invest. Ophthalmol. Vis. Sci. 34(12), 3278–3296 (1993).
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Y. Miyake, K. Yagasaki, M. Horiguchi, Y. Kawase, and T. Kanda, “Congenital stationary night blindness with negative electroretinogram. A new classification,” Arch. Ophthalmol. 104(7), 1013–1020 (1986).
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Y. Miyake, K. Yagasaki, M. Horiguchi, Y. Kawase, and T. Kanda, “Congenital stationary night blindness with negative electroretinogram. A new classification,” Arch. Ophthalmol. 104(7), 1013–1020 (1986).
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S. S. Choi, N. Doble, J. L. Hardy, S. M. Jones, J. L. Keltner, S. S. Olivier, and J. S. Werner, “In vivo imaging of the photoreceptor mosaic in retinal dystrophies and correlations with visual function,” Invest. Ophthalmol. Vis. Sci. 47(5), 2080–2092 (2006).
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M. Alpern, C. C. Ching, and K. Kitahara, “The directional sensitivity of retinal rods,” J. Physiol. 343, 577–592 (1983).
[PubMed]

Kocaoglu, O. P.

Lee, S.

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T. M. Nork, J. N. Ver Hoeve, G. L. Poulsen, R. W. Nickells, M. D. Davis, A. J. Weber, S. H. Vaegan, S. H. Sarks, H. L. Lemley, and L. L. Millecchia, “Swelling and loss of photoreceptors in chronic human and experimental glaucomas,” Arch. Ophthalmol. 118(2), 235–245 (2000).
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Liang, J.

Martin, R.

J. Carroll, E. Banin, D. M. Hunt, R. Martin, M. Michaelides, L. Mizrahi-Meissonnier, A. T. Moore, D. Sharon, D. R. Williams, and A. Dubra, “Evaluating the photoreceptor mosaic in blue cone monochromacy (BCM),” Invest. Ophthalmol. Vis. Sci. 51, E-Abstract 2935 (2010).

McAllister, J. T.

J. T. McAllister, A. M. Dubis, D. M. Tait, S. Ostler, J. Rha, K. E. Stepien, C. G. Summers, and J. Carroll, “Arrested development: high-resolution imaging of foveal morphology in albinism,” Vision Res. 50(8), 810–817 (2010).
[CrossRef] [PubMed]

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C. A. Curcio, N. E. Medeiros, and C. L. Millican, “Photoreceptor loss in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 37(7), 1236–1249 (1996).
[PubMed]

Metha, A. B.

A. Roorda, A. B. Metha, P. Lennie, and D. R. Williams, “Packing arrangement of the three cone classes in primate retina,” Vision Res. 41(10-11), 1291–1306 (2001).
[CrossRef] [PubMed]

Michaelides, M.

J. Carroll, E. Banin, D. M. Hunt, R. Martin, M. Michaelides, L. Mizrahi-Meissonnier, A. T. Moore, D. Sharon, D. R. Williams, and A. Dubra, “Evaluating the photoreceptor mosaic in blue cone monochromacy (BCM),” Invest. Ophthalmol. Vis. Sci. 51, E-Abstract 2935 (2010).

M. Michaelides, A. J. Hardcastle, D. M. Hunt, and A. T. Moore, “Progressive cone and cone-rod dystrophies: phenotypes and underlying molecular genetic basis,” Surv. Ophthalmol. 51(3), 232–258 (2006).
[CrossRef] [PubMed]

Millecchia, L. L.

T. M. Nork, J. N. Ver Hoeve, G. L. Poulsen, R. W. Nickells, M. D. Davis, A. J. Weber, S. H. Vaegan, S. H. Sarks, H. L. Lemley, and L. L. Millecchia, “Swelling and loss of photoreceptors in chronic human and experimental glaucomas,” Arch. Ophthalmol. 118(2), 235–245 (2000).
[PubMed]

Miller, D. T.

Millican, C. L.

C. A. Curcio, N. E. Medeiros, and C. L. Millican, “Photoreceptor loss in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 37(7), 1236–1249 (1996).
[PubMed]

C. A. Curcio, C. L. Millican, K. A. Allen, and R. E. Kalina, “Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina,” Invest. Ophthalmol. Vis. Sci. 34(12), 3278–3296 (1993).
[PubMed]

Miyake, Y.

Y. Miyake, K. Yagasaki, M. Horiguchi, Y. Kawase, and T. Kanda, “Congenital stationary night blindness with negative electroretinogram. A new classification,” Arch. Ophthalmol. 104(7), 1013–1020 (1986).
[PubMed]

Mizrahi-Meissonnier, L.

J. Carroll, E. Banin, D. M. Hunt, R. Martin, M. Michaelides, L. Mizrahi-Meissonnier, A. T. Moore, D. Sharon, D. R. Williams, and A. Dubra, “Evaluating the photoreceptor mosaic in blue cone monochromacy (BCM),” Invest. Ophthalmol. Vis. Sci. 51, E-Abstract 2935 (2010).

Moore, A. T.

J. Carroll, E. Banin, D. M. Hunt, R. Martin, M. Michaelides, L. Mizrahi-Meissonnier, A. T. Moore, D. Sharon, D. R. Williams, and A. Dubra, “Evaluating the photoreceptor mosaic in blue cone monochromacy (BCM),” Invest. Ophthalmol. Vis. Sci. 51, E-Abstract 2935 (2010).

M. Michaelides, A. J. Hardcastle, D. M. Hunt, and A. T. Moore, “Progressive cone and cone-rod dystrophies: phenotypes and underlying molecular genetic basis,” Surv. Ophthalmol. 51(3), 232–258 (2006).
[CrossRef] [PubMed]

Morgan, J. I. W.

J. Carroll, R. C. Baraas, M. Wagner-Schuman, J. Rha, C. A. Siebe, C. Sloan, D. M. Tait, S. Thompson, J. I. W. Morgan, J. Neitz, D. R. Williams, D. H. Foster, and M. Neitz, “Cone photoreceptor mosaic disruption associated with Cys203Arg mutation in the M-cone opsin,” Proc. Natl. Acad. Sci. U.S.A. 106(49), 20948–20953 (2009).
[CrossRef] [PubMed]

Nakanishi, C.

M. K. Yoon, A. Roorda, Y. Zhang, C. Nakanishi, L. J. Wong, Q. Zhang, L. Gillum, A. Green, and J. L. Duncan, “Adaptive optics scanning laser ophthalmoscopy images in a family with the mitochondrial DNA T8993C mutation,” Invest. Ophthalmol. Vis. Sci. 50(4), 1838–1847 (2009).
[CrossRef] [PubMed]

J. L. Duncan, Y. Zhang, J. Gandhi, C. Nakanishi, M. Othman, K. E. H. Branham, A. Swaroop, and A. Roorda, “High-resolution imaging with adaptive optics in patients with inherited retinal degeneration,” Invest. Ophthalmol. Vis. Sci. 48(7), 3283–3291 (2007).
[CrossRef] [PubMed]

Neitz, J.

J. Carroll, E. A. Rossi, J. Porter, J. Neitz, A. Roorda, D. R. Williams, and M. Neitz, “Deletion of the X-linked opsin gene array locus control region (LCR) results in disruption of the cone mosaic,” Vision Res. 50(19), 1989–1999 (2010).
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J. Carroll, R. C. Baraas, M. Wagner-Schuman, J. Rha, C. A. Siebe, C. Sloan, D. M. Tait, S. Thompson, J. I. W. Morgan, J. Neitz, D. R. Williams, D. H. Foster, and M. Neitz, “Cone photoreceptor mosaic disruption associated with Cys203Arg mutation in the M-cone opsin,” Proc. Natl. Acad. Sci. U.S.A. 106(49), 20948–20953 (2009).
[CrossRef] [PubMed]

J. Carroll, M. Neitz, H. Hofer, J. Neitz, and D. R. Williams, “Functional photoreceptor loss revealed with adaptive optics: an alternate cause of color blindness,” Proc. Natl. Acad. Sci. U.S.A. 101(22), 8461–8466 (2004).
[CrossRef] [PubMed]

Neitz, M.

J. Carroll, E. A. Rossi, J. Porter, J. Neitz, A. Roorda, D. R. Williams, and M. Neitz, “Deletion of the X-linked opsin gene array locus control region (LCR) results in disruption of the cone mosaic,” Vision Res. 50(19), 1989–1999 (2010).
[CrossRef] [PubMed]

J. Carroll, R. C. Baraas, M. Wagner-Schuman, J. Rha, C. A. Siebe, C. Sloan, D. M. Tait, S. Thompson, J. I. W. Morgan, J. Neitz, D. R. Williams, D. H. Foster, and M. Neitz, “Cone photoreceptor mosaic disruption associated with Cys203Arg mutation in the M-cone opsin,” Proc. Natl. Acad. Sci. U.S.A. 106(49), 20948–20953 (2009).
[CrossRef] [PubMed]

R. C. Baraas, J. Carroll, K. L. Gunther, M. Chung, D. R. Williams, D. H. Foster, and M. Neitz, “Adaptive optics retinal imaging reveals S-cone dystrophy in tritan color-vision deficiency,” J. Opt. Soc. Am. A 24(5), 1438–1447 (2007).
[CrossRef] [PubMed]

J. Carroll, M. Neitz, H. Hofer, J. Neitz, and D. R. Williams, “Functional photoreceptor loss revealed with adaptive optics: an alternate cause of color blindness,” Proc. Natl. Acad. Sci. U.S.A. 101(22), 8461–8466 (2004).
[CrossRef] [PubMed]

Nickells, R. W.

T. M. Nork, J. N. Ver Hoeve, G. L. Poulsen, R. W. Nickells, M. D. Davis, A. J. Weber, S. H. Vaegan, S. H. Sarks, H. L. Lemley, and L. L. Millecchia, “Swelling and loss of photoreceptors in chronic human and experimental glaucomas,” Arch. Ophthalmol. 118(2), 235–245 (2000).
[PubMed]

Nork, T. M.

T. M. Nork, J. N. Ver Hoeve, G. L. Poulsen, R. W. Nickells, M. D. Davis, A. J. Weber, S. H. Vaegan, S. H. Sarks, H. L. Lemley, and L. L. Millecchia, “Swelling and loss of photoreceptors in chronic human and experimental glaucomas,” Arch. Ophthalmol. 118(2), 235–245 (2000).
[PubMed]

Olivier, S. S.

S. S. Choi, N. Doble, J. L. Hardy, S. M. Jones, J. L. Keltner, S. S. Olivier, and J. S. Werner, “In vivo imaging of the photoreceptor mosaic in retinal dystrophies and correlations with visual function,” Invest. Ophthalmol. Vis. Sci. 47(5), 2080–2092 (2006).
[CrossRef] [PubMed]

Ostler, S.

J. T. McAllister, A. M. Dubis, D. M. Tait, S. Ostler, J. Rha, K. E. Stepien, C. G. Summers, and J. Carroll, “Arrested development: high-resolution imaging of foveal morphology in albinism,” Vision Res. 50(8), 810–817 (2010).
[CrossRef] [PubMed]

Othman, M.

J. L. Duncan, Y. Zhang, J. Gandhi, C. Nakanishi, M. Othman, K. E. H. Branham, A. Swaroop, and A. Roorda, “High-resolution imaging with adaptive optics in patients with inherited retinal degeneration,” Invest. Ophthalmol. Vis. Sci. 48(7), 3283–3291 (2007).
[CrossRef] [PubMed]

Owsley, C.

C. A. Curcio, C. Owsley, and G. R. Jackson, “Spare the rods, save the cones in aging and age-related maculopathy,” Invest. Ophthalmol. Vis. Sci. 41(8), 2015–2018 (2000).
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K. R. Kendell, H. A. Quigley, L. A. Kerrigan, M. E. Pease, and E. N. Quigley, “Primary open-angle glaucoma is not associated with photoreceptor loss,” Invest. Ophthalmol. Vis. Sci. 36(1), 200–205 (1995).
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K. R. Kendell, H. A. Quigley, L. A. Kerrigan, M. E. Pease, and E. N. Quigley, “Primary open-angle glaucoma is not associated with photoreceptor loss,” Invest. Ophthalmol. Vis. Sci. 36(1), 200–205 (1995).
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J. Carroll, R. C. Baraas, M. Wagner-Schuman, J. Rha, C. A. Siebe, C. Sloan, D. M. Tait, S. Thompson, J. I. W. Morgan, J. Neitz, D. R. Williams, D. H. Foster, and M. Neitz, “Cone photoreceptor mosaic disruption associated with Cys203Arg mutation in the M-cone opsin,” Proc. Natl. Acad. Sci. U.S.A. 106(49), 20948–20953 (2009).
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J. Carroll, E. A. Rossi, J. Porter, J. Neitz, A. Roorda, D. R. Williams, and M. Neitz, “Deletion of the X-linked opsin gene array locus control region (LCR) results in disruption of the cone mosaic,” Vision Res. 50(19), 1989–1999 (2010).
[CrossRef] [PubMed]

M. K. Yoon, A. Roorda, Y. Zhang, C. Nakanishi, L. J. Wong, Q. Zhang, L. Gillum, A. Green, and J. L. Duncan, “Adaptive optics scanning laser ophthalmoscopy images in a family with the mitochondrial DNA T8993C mutation,” Invest. Ophthalmol. Vis. Sci. 50(4), 1838–1847 (2009).
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K. Grieve and A. Roorda, “Intrinsic signals from human cone photoreceptors,” Invest. Ophthalmol. Vis. Sci. 49(2), 713–719 (2008).
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J. L. Duncan, Y. Zhang, J. Gandhi, C. Nakanishi, M. Othman, K. E. H. Branham, A. Swaroop, and A. Roorda, “High-resolution imaging with adaptive optics in patients with inherited retinal degeneration,” Invest. Ophthalmol. Vis. Sci. 48(7), 3283–3291 (2007).
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A. Roorda, Y. Zhang, and J. L. Duncan, “High-resolution in vivo imaging of the RPE mosaic in eyes with retinal disease,” Invest. Ophthalmol. Vis. Sci. 48(5), 2297–2303 (2007).
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K. Y. Li and A. Roorda, “Automated identification of cone photoreceptors in adaptive optics retinal images,” J. Opt. Soc. Am. A 24(5), 1358–1363 (2007).
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J. I. Wolfing, M. Chung, J. Carroll, A. Roorda, and D. R. Williams, “High-resolution retinal imaging of cone-rod dystrophy,” Ophthalmology 113(6), 1014–1019.e1 (2006).
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S. B. Stevenson and A. Roorda, “Correcting for miniature eye movements in high resolution scanning laser ophthalmoscopy,” Proc. SPIE 5688A, 145–151 (2005).
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A. Roorda and D. R. Williams, “Optical fiber properties of individual human cones,” J. Vis. 2(5), 4 (2002).
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A. Roorda, A. B. Metha, P. Lennie, and D. R. Williams, “Packing arrangement of the three cone classes in primate retina,” Vision Res. 41(10-11), 1291–1306 (2001).
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A. Roorda and D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397(6719), 520–522 (1999).
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J. Carroll, E. A. Rossi, J. Porter, J. Neitz, A. Roorda, D. R. Williams, and M. Neitz, “Deletion of the X-linked opsin gene array locus control region (LCR) results in disruption of the cone mosaic,” Vision Res. 50(19), 1989–1999 (2010).
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T. M. Nork, J. N. Ver Hoeve, G. L. Poulsen, R. W. Nickells, M. D. Davis, A. J. Weber, S. H. Vaegan, S. H. Sarks, H. L. Lemley, and L. L. Millecchia, “Swelling and loss of photoreceptors in chronic human and experimental glaucomas,” Arch. Ophthalmol. 118(2), 235–245 (2000).
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J. Carroll, E. Banin, D. M. Hunt, R. Martin, M. Michaelides, L. Mizrahi-Meissonnier, A. T. Moore, D. Sharon, D. R. Williams, and A. Dubra, “Evaluating the photoreceptor mosaic in blue cone monochromacy (BCM),” Invest. Ophthalmol. Vis. Sci. 51, E-Abstract 2935 (2010).

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J. Carroll, R. C. Baraas, M. Wagner-Schuman, J. Rha, C. A. Siebe, C. Sloan, D. M. Tait, S. Thompson, J. I. W. Morgan, J. Neitz, D. R. Williams, D. H. Foster, and M. Neitz, “Cone photoreceptor mosaic disruption associated with Cys203Arg mutation in the M-cone opsin,” Proc. Natl. Acad. Sci. U.S.A. 106(49), 20948–20953 (2009).
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J. T. McAllister, A. M. Dubis, D. M. Tait, S. Ostler, J. Rha, K. E. Stepien, C. G. Summers, and J. Carroll, “Arrested development: high-resolution imaging of foveal morphology in albinism,” Vision Res. 50(8), 810–817 (2010).
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J. Carroll, R. C. Baraas, M. Wagner-Schuman, J. Rha, C. A. Siebe, C. Sloan, D. M. Tait, S. Thompson, J. I. W. Morgan, J. Neitz, D. R. Williams, D. H. Foster, and M. Neitz, “Cone photoreceptor mosaic disruption associated with Cys203Arg mutation in the M-cone opsin,” Proc. Natl. Acad. Sci. U.S.A. 106(49), 20948–20953 (2009).
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J. I. Wolfing, M. Chung, J. Carroll, A. Roorda, and D. R. Williams, “High-resolution retinal imaging of cone-rod dystrophy,” Ophthalmology 113(6), 1014–1019.e1 (2006).
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M. K. Yoon, A. Roorda, Y. Zhang, C. Nakanishi, L. J. Wong, Q. Zhang, L. Gillum, A. Green, and J. L. Duncan, “Adaptive optics scanning laser ophthalmoscopy images in a family with the mitochondrial DNA T8993C mutation,” Invest. Ophthalmol. Vis. Sci. 50(4), 1838–1847 (2009).
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M. K. Yoon, A. Roorda, Y. Zhang, C. Nakanishi, L. J. Wong, Q. Zhang, L. Gillum, A. Green, and J. L. Duncan, “Adaptive optics scanning laser ophthalmoscopy images in a family with the mitochondrial DNA T8993C mutation,” Invest. Ophthalmol. Vis. Sci. 50(4), 1838–1847 (2009).
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Zawadzki, R. J.

Zhang, Q.

M. K. Yoon, A. Roorda, Y. Zhang, C. Nakanishi, L. J. Wong, Q. Zhang, L. Gillum, A. Green, and J. L. Duncan, “Adaptive optics scanning laser ophthalmoscopy images in a family with the mitochondrial DNA T8993C mutation,” Invest. Ophthalmol. Vis. Sci. 50(4), 1838–1847 (2009).
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Zhang, Y.

M. K. Yoon, A. Roorda, Y. Zhang, C. Nakanishi, L. J. Wong, Q. Zhang, L. Gillum, A. Green, and J. L. Duncan, “Adaptive optics scanning laser ophthalmoscopy images in a family with the mitochondrial DNA T8993C mutation,” Invest. Ophthalmol. Vis. Sci. 50(4), 1838–1847 (2009).
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R. J. Zawadzki, B. Cense, Y. Zhang, S. S. Choi, D. T. Miller, and J. S. Werner, “Ultrahigh-resolution optical coherence tomography with monochromatic and chromatic aberration correction,” Opt. Express 16(11), 8126–8143 (2008).
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D. W. Arathorn, Q. Yang, C. R. Vogel, Y. Zhang, P. Tiruveedhula, and A. Roorda, “Retinally stabilized cone-targeted stimulus delivery,” Opt. Express 15(21), 13731–13744 (2007).
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A. Roorda, Y. Zhang, and J. L. Duncan, “High-resolution in vivo imaging of the RPE mosaic in eyes with retinal disease,” Invest. Ophthalmol. Vis. Sci. 48(5), 2297–2303 (2007).
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J. L. Duncan, Y. Zhang, J. Gandhi, C. Nakanishi, M. Othman, K. E. H. Branham, A. Swaroop, and A. Roorda, “High-resolution imaging with adaptive optics in patients with inherited retinal degeneration,” Invest. Ophthalmol. Vis. Sci. 48(7), 3283–3291 (2007).
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[CrossRef] [PubMed]

J. L. Duncan, Y. Zhang, J. Gandhi, C. Nakanishi, M. Othman, K. E. H. Branham, A. Swaroop, and A. Roorda, “High-resolution imaging with adaptive optics in patients with inherited retinal degeneration,” Invest. Ophthalmol. Vis. Sci. 48(7), 3283–3291 (2007).
[CrossRef] [PubMed]

A. Roorda, Y. Zhang, and J. L. Duncan, “High-resolution in vivo imaging of the RPE mosaic in eyes with retinal disease,” Invest. Ophthalmol. Vis. Sci. 48(5), 2297–2303 (2007).
[CrossRef] [PubMed]

K. Grieve and A. Roorda, “Intrinsic signals from human cone photoreceptors,” Invest. Ophthalmol. Vis. Sci. 49(2), 713–719 (2008).
[CrossRef] [PubMed]

M. K. Yoon, A. Roorda, Y. Zhang, C. Nakanishi, L. J. Wong, Q. Zhang, L. Gillum, A. Green, and J. L. Duncan, “Adaptive optics scanning laser ophthalmoscopy images in a family with the mitochondrial DNA T8993C mutation,” Invest. Ophthalmol. Vis. Sci. 50(4), 1838–1847 (2009).
[CrossRef] [PubMed]

J. Carroll, E. Banin, D. M. Hunt, R. Martin, M. Michaelides, L. Mizrahi-Meissonnier, A. T. Moore, D. Sharon, D. R. Williams, and A. Dubra, “Evaluating the photoreceptor mosaic in blue cone monochromacy (BCM),” Invest. Ophthalmol. Vis. Sci. 51, E-Abstract 2935 (2010).

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Figures (9)

Fig. 1
Fig. 1

Reflectance images of the human photoreceptor mosaic at three retinal locations along the temporal meridian for subject DLAB_0008, collected using 680 nm light and 0.4 Airy disk pinhole size. The same images are shown with linear (top row) and logarithmic (bottom row) grayscales, to facilitate visualization of the rod mosaic. The scale bars are 10 μm across.

Fig. 2
Fig. 2

The two images on the left and middle were collected in an excised primate retina, imaged in a bright field microscope in transmission [45]. These images, reproduced with permission from the Journal of Neuroscience, show the cone and rod outer segment tips, respectively, as bright spots. The image on the right shows an in vivo image from WLAB001 at similar eccentricity, collected using 775 nm light and 0.6 Airy disk pinhole size. The scale bar is 5 μm across.

Fig. 3
Fig. 3

Reflectance images of the human photoreceptor mosaic at 10° temporal to the fovea for subject JC_0138, collected using 680 nm light and 1.1 Airy disk pinhole size. From top to bottom the images are: a single frame, a registered average of 50 frames, and registered average of 6 batches of 50 frames, collected over a 6 hour period, 1 hour apart. The scale bars are 20 μm across.

Fig. 4
Fig. 4

Comparison of in vivo rod and cone metrics with those from Curcio et al. [1]. Shown on the left is a plot of the ratio of rods to cones as a function of retinal eccentricity. The solid line is the mean of Curcio’s measurements taken in the temporal meridian, and filled circles correspond to the data from this study. On the right is a plot of photoreceptor density as a function of retinal eccentricity. Density estimates for our subjects for rods and cones are shown as open squares and open circles, respectively. Also plotted is the mean rod (solid line) and cone (dashed line) density values reported by Curcio et al. [1] for the temporal meridian.

Fig. 5
Fig. 5

Analysis of the regularity of the peripheral photoreceptor mosaic. Shown in a is the 6-hour averaged image (logarithmic display) from subject JC_0138, taken at about 10° temporal to fixation, collected using 680 nm light and 1.1 Airy disk pinhole size. Color-coded Voronoi domains associated with each cell are shown in panel b), where the color indicates the number of sides on each Voronoi polygon (magenta = 4, cyan = 5, green = 6, yellow = 7, red = 8, dark blue = 9). Regions of six-sided polygons indicate a regular triangular lattice, while other color mark points of disruption of the mosaic. Panel c shows the color-coded Voronoi domains associated with just the cone photoreceptors in the image.

Fig. 6
Fig. 6

Reflectance image of the human photoreceptor mosaic from subject JC_0138, collected using 680 nm light and 1.1 Airy disk pinhole size and displayed with linear (left) and logarithmic (right) gray scale mappings. The image is a montage of two overlapping locations, stitched together using i2k Retina (Dual Align, LLC, Clifton Park, NY, USA). The arrows point to some of the rod photoreceptors closest to the foveal center (significantly smaller than surrounding cones), which is located at the bottom right corner. The scale bars are 50 μm across.

Fig. 7
Fig. 7

Reflectance images of the human photoreceptor mosaic from subject DLAB_007 at 10° temporal along the horizontal meridian at different retinal depths, shown with linear (top row) and logarithmic (bottom row) gray scales. The image series was collected by using 680 nm light and a 0.4 Airy disk pinhole size. The zero depth point indicates the innermost image of the stack, and, thus, increasing values indicate foci closer to the retinal pigment epithelium (RPE). The scale bars are 10 μm across.

Fig. 8
Fig. 8

Axial intensity profiles for the cone and rod photoreceptor mosaics shown in Fig. 7. The (very small) error bars correspond to the errors associated with identifying the boundary of the cones in the images

Fig. 9
Fig. 9

Reflectance images of the human photoreceptor mosaic collected using 680 and 775 nm light and 1.1 and 1.6 Airy disk pinhole sizes, respectively, shown with linear (left) and logarithmic (right) gray scales. Scale bars are 10 μm across.

Tables (1)

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Table 1 Axial Lengths and Retinal Locations Imaged in this Study for Cell Density Estimation

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