Abstract

We demonstrate the capability of a new generation adaptive optics scanning laser ophthalmoscope (AOSLO) to resolve cones and rods in normal subjects, and confirm our findings by comparing cone and rod spacing with published histology measurements. Cone and rod spacing measurements are also performed on AOSLO images from two different diseased eyes, one affected by achromatopsia and the other by acute zonal occult outer retinopathy (AZOOR). The potential of AOSLO technology in the study of these and other retinal diseases is illustrated.

© 2011 OSA

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2011

J. L. Duncan, K. E. Talcott, K. Ratnam, S. M. Sundquist, A. S. Lucero, S. Day, Y. Zhang, and A. Roorda, “Cone structure in retinal degeneration associated with mutations in the peripherin/RDS gene,” Invest. Ophthalmol. Vis. Sci. 52(3), 1557–1566 (2011).
[CrossRef] [PubMed]

S. S. Choi, R. J. Zawadzki, M. C. Lim, J. D. Brandt, J. L. Keltner, N. Doble, and J. S. Werner, “Evidence of outer retinal changes in glaucoma patients as revealed by ultrahigh-resolution in vivo retinal imaging,” Br. J. Ophthalmol. 95(1), 131–141 (2011).
[CrossRef] [PubMed]

K. E. Talcott, K. Ratnam, S. M. Sundquist, A. S. Lucero, B. J. Lujan, W. Tao, T. C. Porco, A. Roorda, and J. L. Duncan, “Longitudinal study of cone photoreceptors during retinal degeneration and in response to ciliary neurotrophic factor treatment,” Invest. Ophthalmol. Vis. Sci. 52(5), 2219–2226 (2011).
[CrossRef] [PubMed]

A. Dubra and Y. Sulai, “Reflective afocal broadband adaptive optics scanning ophthalmoscope,” Biomed. Opt. Express 2(6), 1757–1768 (2011).
[CrossRef] [PubMed]

A. Dubra, Y. Sulai, J. L. Norris, R. F. Cooper, A. M. Dubis, D. R. Williams, and J. Carroll, “Non-invasive in vivo imaging of the human rod photoreceptor mosaic using a confocal adaptive optics scanning ophthalmoscope,” Biomed. Opt. Express 2(7), 1864–1876 (2011).
[CrossRef]

N. Doble, S. S. Choi, J. L. Codona, J. Christou, J. M. Enoch, and D. R. Williams, “In vivo imaging of the human rod photoreceptor mosaic,” Opt. Lett. 36(1), 31–33 (2011).
[CrossRef] [PubMed]

D. M. Monson and J. R. Smith, “Acute zonal occult outer retinopathy,” Surv. Ophthalmol. 56(1), 23–35 (2011).
[CrossRef] [PubMed]

2010

S. Ooto, M. Hangai, A. Sakamoto, A. Tsujikawa, K. Yamashiro, Y. Ojima, Y. Yamada, H. Mukai, S. Oshima, T. Inoue, and N. Yoshimura, “High-resolution imaging of resolved central serous chorioretinopathy using adaptive optics scanning laser ophthalmoscopy,” Ophthalmology 117(9), 1800–1809.e2 (2010).
[CrossRef] [PubMed]

P. Godara, A. M. Dubis, A. Roorda, J. L. Duncan, and J. Carroll, “Adaptive optics retinal imaging: emerging clinical applications,” Optom. Vis. Sci. 87(12), 930–941 (2010).
[CrossRef] [PubMed]

J. Rha, A. M. Dubis, M. Wagner-Schuman, D. M. Tait, P. Godara, B. Schroeder, K. Stepien, and J. Carroll, “Spectral domain optical coherence tomography and adaptive optics: imaging photoreceptor layer morphology to interpret preclinical phenotypes,” Adv. Exp. Med. Biol. 664, 309–316 (2010).
[CrossRef] [PubMed]

K. Y. Li, P. Tiruveedhula, and A. Roorda, “Intersubject variability of foveal cone photoreceptor density in relation to eye length,” Invest. Ophthalmol. Vis. Sci. 51(12), 6858–6867 (2010).
[CrossRef] [PubMed]

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]

2009

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]

M. K. Yoon, A. Roorda, Y. Zhang, C. Nakanishi, L.-J. C. 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]

A. Gómez-Vieyra, A. Dubra, D. Malacara-Hernández, and D. R. Williams, “First-order design of off-axis reflective ophthalmic adaptive optics systems using afocal telescopes,” Opt. Express 17(21), 18906–18919 (2009).
[CrossRef] [PubMed]

H. F. Fine, R. F. Spaide, E. H. Ryan, Y. Matsumoto, and L. A. Yannuzzi, “Acute zonal occult outer retinopathy in patients with multiple evanescent white dot syndrome,” Arch. Ophthalmol. 127(1), 66–70 (2009).
[CrossRef] [PubMed]

2008

N. Zibrandtsen, I. C. Munch, K. Klemp, T. M. Jørgensen, B. Sander, and M. Larsen, “Photoreceptor atrophy in acute zonal occult outer retinopathy,” Acta Ophthalmol. (Copenh.) 86(8), 913–916 (2008).
[CrossRef] [PubMed]

J. Carroll, S. S. Choi, and D. R. Williams, “In vivo imaging of the photoreceptor mosaic of a rod monochromat,” Vision Res. 48(26), 2564–2568 (2008).
[CrossRef] [PubMed]

T. Y. P. Chui, H. Song, and S. A. Burns, “Individual variations in human cone photoreceptor packing density: variations with refractive error,” Invest. Ophthalmol. Vis. Sci. 49(10), 4679–4687 (2008).
[CrossRef] [PubMed]

S. S. Choi, R. J. Zawadzki, J. L. Keltner, and J. S. Werner, “Changes in cellular structures revealed by ultra-high resolution retinal imaging in optic neuropathies,” Invest. Ophthalmol. Vis. Sci. 49(5), 2103–2119 (2008).
[CrossRef] [PubMed]

Y. Kitaguchi, T. Fujikado, K. Bessho, H. Sakaguchi, F. Gomi, T. Yamaguchi, N. Nakazawa, T. Mihashi, and Y. Tano, “Adaptive optics fundus camera to examine localized changes in the photoreceptor layer of the fovea,” Ophthalmology 115(10), 1771–1777 (2008).
[CrossRef] [PubMed]

T. Y. Chui, H. Song, and S. A. Burns, “Adaptive-optics imaging of human cone photoreceptor distribution,” J. Opt. Soc. Am. A 25(12), 3021–3029 (2008).
[CrossRef] [PubMed]

2007

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]

S. A. Burns, R. Tumbar, A. E. Elsner, D. Ferguson, and D. X. Hammer, “Large-field-of-view, modular, stabilized, adaptive-optics-based scanning laser ophthalmoscope,” J. Opt. Soc. Am. A 24(5), 1313–1326 (2007).
[CrossRef] [PubMed]

D. C. Chen, S. M. Jones, D. A. Silva, and S. S. Olivier, “High-resolution adaptive optics scanning laser ophthalmoscope with dual deformable mirrors,” J. Opt. Soc. Am. A 24(5), 1305–1312 (2007).
[CrossRef] [PubMed]

E. A. Rossi, P. Weiser, J. Tarrant, and A. Roorda, “Visual performance in emmetropia and low myopia after correction of high-order aberrations,” J. Vis. 7(8), 14 (2007).
[CrossRef] [PubMed]

D. Li and S. Kishi, “Loss of photoreceptor outer segment in acute zonal occult outer retinopathy,” Arch. Ophthalmol. 125(9), 1194–1200 (2007).
[CrossRef] [PubMed]

2006

Y. Zhang, S. Poonja, and A. Roorda, “MEMS-based adaptive optics scanning laser ophthalmoscopy,” Opt. Lett. 31(9), 1268–1270 (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]

D. Merino, C. Dainty, A. Bradu, and A. G. Podoleanu, “Adaptive optics enhanced simultaneous en-face optical coherence tomography and scanning laser ophthalmoscopy,” Opt. Express 14(8), 3345–3353 (2006).
[CrossRef] [PubMed]

2005

2004

2003

R. W. Rodieck, “The density recovery profile: a method for analysis of points in the plane applicable to retinal studies,” Vis. Neurosci. 20(3), 349 (2003).
[CrossRef] [PubMed]

2002

1999

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

1996

D. T. Miller, D. R. Williams, G. M. Morris, and J. Liang, “Images of cone photoreceptors in the living human eye,” Vision Res. 36(8), 1067–1079 (1996).
[CrossRef] [PubMed]

1994

A. G. Bennett, A. R. Rudnicka, and D. F. Edgar, “Improvements on Littmann’s method of determining the size of retinal features by fundus photography,” Graefes Arch. Clin. Exp. Ophthalmol. 232(6), 361–367 (1994).
[CrossRef] [PubMed]

1993

J. D. M. Gass, “Acute zonal occult outer retinopathy. Donders Lecture: The Netherlands Ophthalmological Society, Maastricht, Holland, June 19, 1992,” J. Clin. Neuroophthalmol. 13(2), 79–97 (1993).
[PubMed]

1992

C. A. Curcio and K. R. Sloan, “Packing geometry of human cone photoreceptors: variation with eccentricity and evidence for local anisotropy,” Vis. Neurosci. 9(2), 169–180 (1992).
[CrossRef] [PubMed]

1990

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]

1982

K. J. Bowman, “A method for quantitative scoring of the Farnsworth Panel D-15,” Acta Ophthalmol. (Copenh.) 60(6), 907–916 (1982).
[CrossRef] [PubMed]

1975

M. Glickstein and G. G. Heath, “Receptors in the monochromat eye,” Vision Res. 15(6), 633–636 (1975).
[CrossRef] [PubMed]

1965

H. F. Falls, J. R. Wolter, and M. Alpern, “Typical total monochromacy. A histological and psychophysical study,” Arch. Ophthalmol. 74(5), 610–616 (1965).
[PubMed]

1961

J. M. Enoch, “Wave-guide modes in retinal receptors,” Science 133(3461), 1353–1354 (1961).
[CrossRef] [PubMed]

1960

R. Harrison, D. Hoefnagel, and J. N. Hayward, “Congenital total color blindness: a clincopathological report,” Arch. Ophthalmol. 64, 685–692 (1960).
[PubMed]

Ahnelt, P. K.

Alpern, M.

H. F. Falls, J. R. Wolter, and M. Alpern, “Typical total monochromacy. A histological and psychophysical study,” Arch. Ophthalmol. 74(5), 610–616 (1965).
[PubMed]

Artal, P.

Bennett, A. G.

A. G. Bennett, A. R. Rudnicka, and D. F. Edgar, “Improvements on Littmann’s method of determining the size of retinal features by fundus photography,” Graefes Arch. Clin. Exp. Ophthalmol. 232(6), 361–367 (1994).
[CrossRef] [PubMed]

Besecker, J. R.

Bessho, K.

Y. Kitaguchi, T. Fujikado, K. Bessho, H. Sakaguchi, F. Gomi, T. Yamaguchi, N. Nakazawa, T. Mihashi, and Y. Tano, “Adaptive optics fundus camera to examine localized changes in the photoreceptor layer of the fovea,” Ophthalmology 115(10), 1771–1777 (2008).
[CrossRef] [PubMed]

Bower, B. A.

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Figures (9)

Fig. 1
Fig. 1

a) Optical design for a traditional AOSLO system with all the optical elements arranged along the same plane [28]. b) and c) show the optical design of the system presented in this paper from the light delivery beam and collection beam splitter (BS) to the eye. In b) and c) the beam reaches the different optical elements in the same order as in a), so the labels can help understand the light path. In b) and c) the optical elements are not arranged in just one plane, but they are placed at different heights. b) shows the projection of the system on the xy plane, and c) shows the same design projected on the yz plane.

Fig. 2
Fig. 2

Cone spacing vs eccentricity: 1. Cone spacing computed from AOSLO images of 3 different healthy subjects (◇ nasal direction, □◯ inferior direction); 2. Cone spacing computed from published histological images (black solid circles) by Curcio et al. [35]; 3. Cone spacing in the temporal (solid line) and nasal (dotted line) directions inferred from density data reported by Curcio et al. [35].

Fig. 3
Fig. 3

AOSLO retinal image at 7° eccentricity for one of the healthy subjects showing the cone photoreceptor mosaic and a finer structure filling in the space between these cone photoreceptors (scale bar is 20μm).

Fig. 4
Fig. 4

Rod spacing vs eccentricity. 1. Rod spacing computed from AOSLO images of 3 different healthy subjects (◇ nasal direction, □◯ inferior direction); 2. Rod spacing computed from published histological images (black circles) by Curcio et al. [35]; 3. Rod spacing in the temporal (solid line) and nasal (dotted line) directions inferred from rod density published data by Curcio et al. [35].

Fig. 5
Fig. 5

AOSLO retinal images at different eccentricities for a normal subject and a 39 year old patient with achromatopsia. The patient’s prescription on the eye imaged was −4.50sph, +0.50cyl, axis105 deg. Scale bar is 20 μm.

Fig. 6
Fig. 6

OCT image from a normal subject (left) and an achromatopsia patient (right). Due to nystagmus it was difficult to acquire an OCT image at the exact center of the anatomical fovea of the achromatopsia patient. The image presented is the closest to the anatomical fovea that could be acquired. The image shows ELM (bright), IS (dark) and OS (dark) layers visible throughout both images.

Fig. 7
Fig. 7

Cone (squares) and rod (circles) spacing calculated from AOLSO images for 3 different healthy subjects (open symbols), a patient with achromatopsia (black filled symbols) and a patient with AZOOR (grey filled symbols).

Fig. 8
Fig. 8

Visual field, infrared scanning laser ophthalmoscope image and OCT B-scan of an AZOOR patient. The two visual fields on the top panel show the deviation from normal (pattern deviation) over a 60 degree visual field. The numbers on the left field indicate the sensitivity difference from normal in decibels. The right field plots the probability that the visual sensitivity is part of a normal distribution. The relative scotoma starts between 4 and 6 degrees to the right of the fovea. The SLO fundus image (middle panel) spans 30 degrees and the location of the OCT B-scan (bottom panel) is indicated by the dashed white line. The arrow at 4.5 degrees corresponds to the point beyond which the regular mosaic of cones is no longer visible (Fig. 9). The OCT B-scan shows reflections, corresponding to an intact ELM and IS/OS junction, that persist into the relative scotoma, although the magnitude of the reflection is reduced.

Fig. 9
Fig. 9

AOSLO images from an eye of a 46 year old female patient affected by AZOOR. The top images correspond to 4 different eccentricities. Images at 1.5° and 2.5° eccentricity are outside the scotoma, while images at 6° and 7° eccentricity are within it. The bottom image, centered at 4.5° eccentricity, corresponds to the edge of the area where cones are not visible. The patient’s prescription was −1.50 sph, +1.25 cyl, axis 90 deg. Scale bar is 20μm.

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