Abstract

We present a new instrument that is capable of imaging human photoreceptors in three dimensions. To achieve high lateral resolution, the system incorporates an adaptive optics system. The high axial resolution is achieved through the implementation of optical coherence tomography (OCT). The instrument records simultaneously both, scanning laser ophthalmoscope (SLO) and OCT en-face images, with a pixel to pixel correspondence. The information provided by the SLO is used to correct for transverse eye motion in post-processing. In order to correct for axial eye motion, the instrument is equipped with a high speed axial eye tracker. In vivo images of foveal cones as well as images recorded at an eccentricity from the fovea showing cones and rods are presented.

© 2014 Optical Society of America

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2013 (3)

2012 (2)

2011 (8)

O. P. Kocaoglu, S. Lee, R. S. Jonnal, Q. Wang, A. E. Herde, J. C. Derby, W. H. Gao, and D. T. Miller, “Imaging cone photoreceptors in three dimensions and in time using ultrahigh resolution optical coherence tomography with adaptive optics,” Biomed. Opt. Express2(4), 748–763 (2011).
[CrossRef] [PubMed]

W. Geitzenauer, C. K. Hitzenberger, and U. M. Schmidt-Erfurth, “Retinal optical coherence tomography: past, present and future perspectives,” Br. J. Ophthalmol.95(2), 171–177 (2011).
[CrossRef] [PubMed]

A. Dubra and Y. Sulai, “Reflective afocal broadband adaptive optics scanning ophthalmoscope,” Biomed. Opt. Express2(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, “Noninvasive imaging of the human rod photoreceptor mosaic using a confocal adaptive optics scanning ophthalmoscope,” Biomed. Opt. Express2(7), 1864–1876 (2011).
[CrossRef] [PubMed]

D. T. Miller, O. P. Kocaoglu, Q. Wang, and S. Lee, “Adaptive optics and the eye (super resolution OCT),” Eye (Lond.)25(3), 321–330 (2011).
[CrossRef] [PubMed]

D. R. Williams, “Imaging single cells in the living retina,” Vision Res.51(13), 1379–1396 (2011).
[CrossRef] [PubMed]

R. F. Spaide and C. A. Curcio, “Anatomical Correlates to the Bands Seen in the Outer Retina by Optical Coherence Tomography: Literature Review and Model,” Retina31(8), 1609–1619 (2011).
[CrossRef] [PubMed]

M. Pircher, J. S. Kroisamer, F. Felberer, H. Sattmann, E. Götzinger, and C. K. Hitzenberger, “Temporal changes of human cone photoreceptors observed in vivo with SLO/OCT,” Biomed. Opt. Express2(1), 100–112 (2011).
[CrossRef] [PubMed]

2010 (8)

M. Pircher, E. Götzinger, H. Sattmann, R. A. Leitgeb, and C. K. Hitzenberger, “In vivo investigation of human cone photoreceptors with SLO/OCT in combination with 3D motion correction on a cellular level,” Opt. Express18(13), 13935–13944 (2010).
[CrossRef] [PubMed]

R. G. Cucu, M. W. Hathaway, A. G. Podoleanu, and R. B. Rosen, “Variable lateral size imaging of the human retina in vivo by combined confocal/en face optical coherence tomography with closed loop OPD-locked low coherence interferometry based active axial eye motion,” Proc. SPIE7554, 75540J (2010).
[CrossRef]

N. M. Putnam, D. X. Hammer, Y. H. Zhang, D. Merino, and A. Roorda, “Modeling the foveal cone mosaic imaged with adaptive optics scanning laser ophthalmoscopy,” Opt. Express18(24), 24902–24916 (2010).
[CrossRef] [PubMed]

X. Zhu, A. Schülzgen, H. Li, H. Wei, J. V. Moloney, and N. Peyghambarian, “Coherent beam transformations using multimode waveguides,” Opt. Express18(7), 7506–7520 (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]

A. Roorda, “Applications of Adaptive Optics Scanning Laser Ophthalmoscopy,” Optom. Vis. Sci.87(4), 260–268 (2010).
[PubMed]

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,” Ophthalmology117(9), 1800–1809 (2010).
[CrossRef] [PubMed]

K. Kurokawa, K. Sasaki, S. Makita, M. Yamanari, B. Cense, and Y. Yasuno, “Simultaneous high-resolution retinal imaging and high-penetration choroidal imaging by one-micrometer adaptive optics optical coherence tomography,” Opt. Express18(8), 8515–8527 (2010).
[CrossRef] [PubMed]

2009 (1)

2008 (7)

V. J. Srinivasan, B. K. Monson, M. Wojtkowski, R. A. Bilonick, I. Gorczynska, R. Chen, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Characterization of outer retinal morphology with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.49(4), 1571–1579 (2008).
[CrossRef] [PubMed]

J. I. W. Morgan, A. Dubra, R. Wolfe, W. H. Merigan, and D. R. Williams, “In Vivo Autofluorescence Imaging of the Human and Macaque Retinal Pigment Epithelial Cell Mosaic,” Invest. Ophthalmol. Vis. Sci.50(3), 1350–1359 (2008).
[CrossRef] [PubMed]

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. Express16(11), 8126–8143 (2008).
[CrossRef] [PubMed]

G. H. Shi, Y. Dai, L. Wang, Z. H. Ding, X. J. Rao, and Y. D. Zhang, “Adaptive optics optical coherence tomography for retina imaging,” Chin. Opt. Lett.6, 424–425 (2008).
[CrossRef]

M. Pircher, R. J. Zawadzki, J. W. Evans, J. S. Werner, and C. K. Hitzenberger, “Simultaneous imaging of human cone mosaic with adaptive optics enhanced scanning laser ophthalmoscopy and high-speed transversal scanning optical coherence tomography,” Opt. Lett.33(1), 22–24 (2008).
[CrossRef] [PubMed]

W. Drexler and J. G. Fujimoto, “State-of-the-art retinal optical coherence tomography,” Prog. Retin. Eye Res.27(1), 45–88 (2008).
[CrossRef] [PubMed]

A. G. Podoleanu and R. B. Rosen, “Combinations of techniques in imaging the retina with high resolution,” Prog. Retin. Eye Res.27(4), 464–499 (2008).
[CrossRef] [PubMed]

2007 (5)

2006 (6)

2005 (5)

2004 (2)

M. Pircher, E. Goetzinger, R. Leitgeb, and C. K. Hitzenberger, “Transversal phase resolved polarization sensitive optical coherence tomography,” Phys. Med. Biol.49(7), 1257–1263 (2004).
[CrossRef] [PubMed]

B. Hermann, E. J. Fernández, A. Unterhuber, H. Sattmann, A. F. Fercher, W. Drexler, P. M. Prieto, and P. Artal, “Adaptive-optics ultrahigh-resolution optical coherence tomography,” Opt. Lett.29(18), 2142–2144 (2004).
[CrossRef] [PubMed]

2003 (4)

2002 (1)

1999 (1)

A. Roorda and D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature397(6719), 520–522 (1999).
[CrossRef] [PubMed]

1997 (2)

1996 (1)

1992 (1)

1991 (1)

C. K. Hitzenberger, “Optical Measurement of the Axial Eye Length by Laser Doppler Interferometry,” Invest. Ophthalmol. Vis. Sci.32(3), 616–624 (1991).
[PubMed]

1990 (1)

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 (1)

J. I. Yellott., “Spectral Analysis of Spatial Sampling by Photoreceptors: Topological Disorder Prevents Aliasing,” Vision Res.22(9), 1205–1210 (1982).
[CrossRef] [PubMed]

1961 (1)

J. M. Enoch, “Wave-Guide Modes in Retinal Receptors,” Science133, 1353–1354 (1961).

Ahnelt, P. K.

Ahrens, G.

Artal, P.

Bachmann, A. H.

Bauer, S.

Baumann, B.

Bigelow, C. E.

Bilonick, R. A.

V. J. Srinivasan, B. K. Monson, M. Wojtkowski, R. A. Bilonick, I. Gorczynska, R. Chen, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Characterization of outer retinal morphology with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.49(4), 1571–1579 (2008).
[CrossRef] [PubMed]

Bloom, B.

Bouma, B. E.

Bower, B. A.

Bradu, A.

Burns, S. A.

Campbell, M. C. W.

Carroll, J.

Cense, B.

Chen, R.

V. J. Srinivasan, B. K. Monson, M. Wojtkowski, R. A. Bilonick, I. Gorczynska, R. Chen, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Characterization of outer retinal morphology with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.49(4), 1571–1579 (2008).
[CrossRef] [PubMed]

Choi, S.

Choi, S. S.

Cooper, R. F.

Cucu, R. G.

R. G. Cucu, M. W. Hathaway, A. G. Podoleanu, and R. B. Rosen, “Variable lateral size imaging of the human retina in vivo by combined confocal/en face optical coherence tomography with closed loop OPD-locked low coherence interferometry based active axial eye motion,” Proc. SPIE7554, 75540J (2010).
[CrossRef]

Curcio, C. A.

R. F. Spaide and C. A. Curcio, “Anatomical Correlates to the Bands Seen in the Outer Retina by Optical Coherence Tomography: Literature Review and Model,” Retina31(8), 1609–1619 (2011).
[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]

Dai, Y.

Dainty, C.

de Boer, J. F.

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Biomed. Opt. Express (7)

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Opt. Express (18)

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R. J. Zawadzki, S. M. Jones, S. S. Olivier, M. T. Zhao, B. A. Bower, J. A. Izatt, S. Choi, S. Laut, and J. S. Werner, “Adaptive-optics optical coherence tomography for high-resolution and high-speed 3D retinal in vivo imaging,” Opt. Express13(21), 8532–8546 (2005).
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F. Felberer, J. S. Kroisamer, C. K. Hitzenberger, and M. Pircher, “Lens based adaptive optics scanning laser ophthalmoscope,” Opt. Express20(16), 17297–17310 (2012).
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M. Pircher, E. Götzinger, H. Sattmann, R. A. Leitgeb, and C. K. Hitzenberger, “In vivo investigation of human cone photoreceptors with SLO/OCT in combination with 3D motion correction on a cellular level,” Opt. Express18(13), 13935–13944 (2010).
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M. Pircher, B. Baumann, E. Götzinger, H. Sattmann, and C. K. Hitzenberger, “Simultaneous SLO/OCT imaging of the human retina with axial eye motion correction,” Opt. Express15(25), 16922–16932 (2007).
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Y. Zhang, J. T. Rha, R. S. Jonnal, and D. T. Miller, “Adaptive optics parallel spectral domain optical coherence tomography for imaging the living retina,” Opt. Express13(12), 4792–4811 (2005).
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D. Merino, C. Dainty, A. Bradu, and A. G. Podoleanu, “Adaptive optics enhanced simultaneous en-face optical coherence tomography and scanning laser ophthalmoscopy,” Opt. Express14(8), 3345–3353 (2006).
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K. Kurokawa, K. Sasaki, S. Makita, M. Yamanari, B. Cense, and Y. Yasuno, “Simultaneous high-resolution retinal imaging and high-penetration choroidal imaging by one-micrometer adaptive optics optical coherence tomography,” Opt. Express18(8), 8515–8527 (2010).
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R. Leitgeb, C. K. Hitzenberger, and A. F. Fercher, “Performance of fourier domain vs. time domain optical coherence tomography,” Opt. Express11(8), 889–894 (2003).
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K. Wiesauer, M. Pircher, E. Goetzinger, C. K. Hitzenberger, R. Engelke, G. Ahrens, G. Gruetzner, and D. Stifter, “Transversal ultrahigh-resolution polarization-sensitive optical coherence tomography for strain mapping in materials,” Opt. Express14(13), 5945–5953 (2006).
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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. Express16(11), 8126–8143 (2008).
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F. Felberer, G. Aschinger, J.-S. Kroisamer, C. K. Hitzenberger, and M. Pircher, “En-face adaptive optics optical coherence tomography with 3D-motion correction,” SPIE Photonics West, San Francisco, CA (2013).

Supplementary Material (5)

» Media 1: MOV (1546 KB)     
» Media 2: MOV (4034 KB)     
» Media 3: MOV (1314 KB)     
» Media 4: MOV (3782 KB)     
» Media 5: MOV (699 KB)     

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Figures (14)

Fig. 1
Fig. 1

Scheme of the sample arm of the AO-SLO/OCT system. SLD super luminescent diode, FOC fiber optic coupler, FPC fiber polarization controller, Col collimator, Pol polarizer, Disp. comp. dispersion compensation, PBS polarizing beam splitter, L1-L4 lenses with 200mm focal length, L5 lens (f = 75mm), L6 lens (f = 250mm), L7 lens (f = 300mm), L8 lens (f = 180mm), RS resonant scanner, GS galvanometer scanner, DM deformable mirror, Pel. Pellicle, QWP quarter wave plate, SHS Shack Hartmann wavefront sensor, APD avalanche photodiode, FT fixation target, I variable aperture stop, Dich. Mirr. dichroic mirror.

Fig. 2
Fig. 2

Scheme of the AO-SLO/OCT reference arm. LS light source, Col collimator, Pol polarizer, AOM accousto optic modulator, M mirror, PBS polarizing beam splitter, QWP quarter wave plate, Disp. Comp. dispersion compensation, L1 lens (80 mm), GS galvanometer scanner, FPC fiber polarization controller, FOC fiber optic coupler

Fig. 3
Fig. 3

Scheme of the axial eye tracking system. LS light source, Col Collimator, L1 lens, Dich. Mirr. dichroic mirror.

Fig. 4
Fig. 4

Averaged en-face SLO image (a) and depth integrated and squared OCT image (b) of the fovea of subject 1. (Both image channels are acquired simultaneously). The position of the center of the fovea (peak cone density) lies within the white square. (c) and (d) show an enlarged view of this central region (indicated with the white square in (a) and (b)). (e) and (f) show Yellott’s ring after FFT’s of (c) and (d). The scale bar is 30µm.

Fig. 5
Fig. 5

Radial average of Fig. 4(e) indicating the frequency of Yellott’s ring (marked with an arrow).

Fig. 6
Fig. 6

Depth averaged en-face images of the center of the fovea (subject 1) retrieved from the volume scan (Media 1) of the external limiting membrane (ELM, 26µm depth averaged) (a), the junction between inner and outer segments of photoreceptors (IS/OS, 22µm depth averaged) (b), the outer segments (OS, 17µm depth averaged) (c), the end tips of the cones photoreceptors (ETP, 20µm depth averaged) (d), and retinal pigment epithelium (RPE, 15µm depth averaged showing a regular structure) (e). (f) Enlarged section indicated by the white square in (e). The borders of the regular structure are emphasized with the blue lines. The scale bar in the images is 30 µm.

Fig. 7
Fig. 7

Center frame of a B-scan fly through movie (Media 2) of the recorded volume from the fovea region of subject 1 (image size: ~0.8°x200µm).

Fig. 8
Fig. 8

Selected regions of interest of the data set shown in Media 2 (subject 1). (a) cones showing distinct signals from three layers: ELM, IS/OS and ETP, (b) cone showing a signal throughout the outer segment, (c) Bright reflection spot (encircled) within the outer segment, (d) cone with signal from the IS/OS junction anterior to the IS/OS junction of neighboring cones.

Fig. 9
Fig. 9

SLO/OCT images recorded at ~8° eccentricity from the fovea of subject 2. Averaged SLO image (120 frames) (a), depth averaged en-face images of the external limiting membrane (b), junction between inner and outer segments of photoreceptors (c), end tips of the cones (d), layer between ET cones and RPE (e), and of the retinal pigment epithelium (f). The scale bar in all images is 30 µm. Media 3 shows the entire volume scan.

Fig. 10
Fig. 10

Representative B-Scan taken from the volume scan (Media 4) recorded in subject 2 at ~8 degree temporal to the fovea (top). Average over all B-scans (bottom). (Images are displayed on a linear grey scale, image size: 0.8° (x) x 200µm (z)). The light grey part on the left part of the image is caused by missing data due to eye motion.

Fig. 11
Fig. 11

Averaged (40 frames) en-face SLO image (a) and averaged OCT image (b) (recorded at an imaging depth corresponding to the layer between RPE and end tips of cones) retrieved from the volume scan shown in Media 5 of the retina (subject 2) recorded approximately 8 degree temporal from the fovea. The scale bar is 30 µm (Media 5 is best viewed in loop mode).

Fig. 12
Fig. 12

Composite false color image of different retinal layers of subject 2. End tips of cones (red), and layer located between end tips of cones and RPE (green) and) (scale bar: 30µm).

Fig. 13
Fig. 13

FFT’s over the entire field of view of the individual retinal layers displayed in Fig. 6. (a) external limiting membrane (ELM), (b) the junction between inner and outer segments of photoreceptors (IS/OS), (c) the outer segments (OS), (d) the end tips of the cone photoreceptors (ETP), and (e) retinal pigment epithelium (RPE) (Yellott’s rings are indicated with white arrows).

Fig. 14
Fig. 14

Radial average of the images displayed in Fig. 13 indicating the frequency of Yellott’s rings (The location of the ring from the RPE and IS/OS are marked with an arrow and the corresponding frequency value that was determined manually is displayed)

Metrics