Abstract

Retinal pigment epithelial (RPE) cells are well known to play a central role in the progression of numerous retinal diseases. Changes in the structure and function of these cells thus may serve as sensitive biomarkers of disease onset. While in vivo studies have focused on structural changes, functional ones may better capture cell health owing to their more direct connection to cell physiology. In this study, we developed a method based on adaptive optics optical coherence tomography (AO-OCT) and speckle field dynamics for characterizing organelle motility in individual RPE cells. We quantified the dynamics in terms of an exponential decay time constant, the time required for the speckle field to decorrelate. Using seven normal subjects, we found the RPE speckle field to decorrelate in about 5 s. This result has two fundamental implications for future clinical use. First, it establishes a path for generating a normative baseline to which motility of diseased RPE cells can be compared. Second, it predicts an AO-OCT image acquisition time that is 36 times faster than used in our earlier report for individuating RPE cells, thus a major improvement in clinical efficacy.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2019 (2)

S. A. Burns, A. E. Elsner, K. A. Sapoznik, R. L. Warner, and T. J. Gast, “Adaptive optics imaging of the human retina,” Prog. Retin. Eye Res. 68, 1–30 (2019).
[PubMed]

F. Zhang, K. Kurokawa, A. Lassoued, J. A. Crowell, and D. T. Miller, “Cone photoreceptor classification in the living human eye from photostimulation-induced phase dynamics,” Proc. Natl. Acad. Sci. U.S.A. 116(16), 7951–7956 (2019).
[Crossref] [PubMed]

2018 (5)

Z. Liu, J. Tam, O. Saeedi, and D. X. Hammer, “Trans-retinal cellular imaging with multimodal adaptive optics,” Biomed. Opt. Express 9(9), 4246–4262 (2018).
[Crossref] [PubMed]

K. Grieve, E. Gofas-Salas, R. D. Ferguson, J. A. Sahel, M. Paques, and E. A. Rossi, “In vivo near-infrared autofluorescence imaging of retinal pigment epithelial cells with 757 nm excitation,” Biomed. Opt. Express 9(12), 5946–5961 (2018).
[Crossref] [PubMed]

C. E. Granger, Q. Yang, H. Song, K. Saito, K. Nozato, L. R. Latchney, B. T. Leonard, M. M. Chung, D. R. Williams, and E. A. Rossi, “Human retinal pigment epithelium: In vivo cell morphometry, multispectral autofluorescence, and relationship to cone mosaic,” Invest. Ophthalmol. Vis. Sci. 59(15), 5705–5716 (2018).
[Crossref] [PubMed]

M. Azimipour, R. J. Zawadzki, I. Gorczynska, J. Migacz, J. S. Werner, and R. S. Jonnal, “Intraframe motion correction for raster-scanned adaptive optics images using strip-based cross-correlation lag biases,” PLoS One 13(10), e0206052 (2018).
[Crossref] [PubMed]

A. Pollreisz, J. D. Messinger, K. R. Sloan, T. J. Mittermueller, A. S. Weinhandl, E. K. Benson, G. J. Kidd, U. Schmidt-Erfurth, and C. A. Curcio, “Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy,” Exp. Eye Res. 166, 131–139 (2018).
[Crossref] [PubMed]

2017 (4)

T. Liu, H. Jung, J. Liu, M. Droettboom, and J. Tam, “Noninvasive near infrared autofluorescence imaging of retinal pigment epithelial cells in the human retina using adaptive optics,” Biomed. Opt. Express 8(10), 4348–4360 (2017).
[Crossref] [PubMed]

Z. Liu, K. Kurokawa, F. Zhang, J. J. Lee, and D. T. Miller, “Imaging and quantifying ganglion cells and other transparent neurons in the living human retina,” Proc. Natl. Acad. Sci. U.S.A. 114(48), 12803–12808 (2017).
[Crossref] [PubMed]

Z. Liu, K. Kurokawa, F. Zhang, and D. T. Miller, “Characterizing motility dynamics in human rpe cells,” Ophthalmic Technologies XXVII 10045, 1004515 (2017).
[Crossref]

M. A. Wilk, A. L. Huckenpahler, R. F. Collery, B. A. Link, and J. Carroll, “The effect of retinal melanin on optical coherence tomography images,” Transl. Vis. Sci. Technol. 6(2), 8 (2017).
[Crossref] [PubMed]

2016 (3)

Z. Liu, O. P. Kocaoglu, and D. T. Miller, “3D imaging of retinal pigment epithelial cells in the living human retina,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT533 (2016).
[Crossref] [PubMed]

J. Tam, J. Liu, A. Dubra, and R. Fariss, “In vivo imaging of the human retinal pigment epithelial mosaic using adaptive optics enhanced indocyanine green ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 57(10), 4376–4384 (2016).
[Crossref] [PubMed]

O. P. Kocaoglu, Z. Liu, F. Zhang, K. Kurokawa, R. S. Jonnal, and D. T. Miller, “Photoreceptor disc shedding in the living human eye,” Biomed. Opt. Express 7(11), 4554–4568 (2016).
[Crossref] [PubMed]

2015 (2)

K. Kurokawa, S. Makita, Y. J. Hong, and Y. Yasuno, “Two-dimensional micro-displacement measurement for laser coagulation using optical coherence tomography,” Biomed. Opt. Express 6(1), 170–190 (2015).
[Crossref] [PubMed]

M. Jiang, J. Esteve-Rudd, V. S. Lopes, T. Diemer, C. Lillo, A. Rump, and D. S. Williams, “Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis,” J. Cell Biol. 210(4), 595–611 (2015).
[Crossref] [PubMed]

2014 (5)

F. Felberer, J. S. Kroisamer, B. Baumann, S. Zotter, U. Schmidt-Erfurth, C. K. Hitzenberger, and M. Pircher, “Adaptive optics SLO/OCT for 3D imaging of human photoreceptors in vivo,” Biomed. Opt. Express 5(2), 439–456 (2014).
[Crossref] [PubMed]

T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
[Crossref] [PubMed]

R. S. Jonnal, O. P. Kocaoglu, R. J. Zawadzki, S. H. Lee, J. S. Werner, and D. T. Miller, “The cellular origins of the outer retinal bands in optical coherence tomography images,” Invest. Ophthalmol. Vis. Sci. 55(12), 7904–7918 (2014).
[Crossref] [PubMed]

O. P. Kocaoglu, R. D. Ferguson, R. S. Jonnal, Z. Liu, Q. Wang, D. X. Hammer, and D. T. Miller, “Adaptive optics optical coherence tomography with dynamic retinal tracking,” Biomed. Opt. Express 5(7), 2262–2284 (2014).
[Crossref] [PubMed]

O. P. Kocaoglu, T. L. Turner, Z. Liu, and D. T. Miller, “Adaptive optics optical coherence tomography at 1 MHz,” Biomed. Opt. Express 5(12), 4186–4200 (2014).
[Crossref] [PubMed]

2013 (5)

2012 (1)

J. M. Bruder, Z. A. Pfeiffer, J. M. Ciriello, D. M. Horrigan, N. L. Wicks, B. Flaherty, and E. Oancea, “Melanosomal dynamics assessed with a live-cell fluorescent melanosomal marker,” PLoS One 7(8), e43465 (2012).
[Crossref] [PubMed]

2011 (2)

2010 (1)

K. Jeong, J. J. Turek, and D. D. Nolte, “Speckle fluctuation spectroscopy of intracellular motion in living tissue using coherence-domain digital holography,” J. Biomed. Opt. 15(3), 030514 (2010).
[Crossref] [PubMed]

2009 (2)

J. I. 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 (2009).
[Crossref] [PubMed]

Z. Yuan, B. Chen, H. Ren, and Y. Pan, “On the possibility of time-lapse ultrahigh-resolution optical coherence tomography for bladder cancer grading,” J. Biomed. Opt. 14(5), 050502 (2009).
[Crossref] [PubMed]

2007 (2)

Y. T. Pan, Z. L. Wu, Z. J. Yuan, Z. G. Wang, and C. W. Du, “Subcellular imaging of epithelium with time-lapse optical coherence tomography,” J. Biomed. Opt. 12(5), 050504 (2007).
[Crossref] [PubMed]

R. S. Jonnal, J. Rha, Y. Zhang, B. Cense, W. Gao, and D. T. Miller, “In vivo functional imaging of human cone photoreceptors,” Opt. Express 15(24), 16141–16160 (2007).
[Crossref] [PubMed]

2006 (1)

C. E. Futter, “The molecular regulation of organelle transport in mammalian retinal pigment epithelial cells,” Pigment Cell Res. 19(2), 104–111 (2006).
[Crossref] [PubMed]

2005 (1)

O. Strauss, “The retinal pigment epithelium in visual function,” Physiol. Rev. 85(3), 845–881 (2005).
[Crossref] [PubMed]

2004 (2)

D. Gibbs, S. M. Azarian, C. Lillo, J. Kitamoto, A. E. Klomp, K. P. Steel, R. T. Libby, and D. S. Williams, “Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes,” J. Cell Sci. 117(26), 6473–6483 (2004).
[Crossref] [PubMed]

D. C. Barral and M. C. Seabra, “The melanosome as a model to study organelle motility in mammals,” Pigment Cell Res. 17(2), 111–118 (2004).
[Crossref] [PubMed]

2003 (2)

D. Gibbs, J. Kitamoto, and D. S. Williams, “Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein,” Proc. Natl. Acad. Sci. U.S.A. 100(11), 6481–6486 (2003).
[Crossref] [PubMed]

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]

2000 (1)

1997 (1)

A. K. Dunn, C. L. Smithpeter, A. J. Welch, and R. R. Richards-Kortum, “Finite-difference time-domain simulation of light scattering from single cells,” J. Biomed. Opt. 2(3), 262–266 (1997).
[Crossref] [PubMed]

1994 (1)

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]

1986 (1)

J. J. Weiter, F. C. Delori, G. L. Wing, and K. A. Fitch, “Retinal pigment epithelial lipofuscin and melanin and choroidal melanin in human eyes,” Invest. Ophthalmol. Vis. Sci. 27(2), 145–152 (1986).
[PubMed]

1973 (1)

A. W. Snyder and C. Pask, “The stiles-crawford effect-explanation and consequences,” Vision Res. 13(6), 1115–1137 (1973).
[Crossref] [PubMed]

Ablonczy, Z.

T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
[Crossref] [PubMed]

Ach, T.

T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
[Crossref] [PubMed]

Azarian, S. M.

D. Gibbs, S. M. Azarian, C. Lillo, J. Kitamoto, A. E. Klomp, K. P. Steel, R. T. Libby, and D. S. Williams, “Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes,” J. Cell Sci. 117(26), 6473–6483 (2004).
[Crossref] [PubMed]

Azimipour, M.

M. Azimipour, R. J. Zawadzki, I. Gorczynska, J. Migacz, J. S. Werner, and R. S. Jonnal, “Intraframe motion correction for raster-scanned adaptive optics images using strip-based cross-correlation lag biases,” PLoS One 13(10), e0206052 (2018).
[Crossref] [PubMed]

Barral, D. C.

D. C. Barral and M. C. Seabra, “The melanosome as a model to study organelle motility in mammals,” Pigment Cell Res. 17(2), 111–118 (2004).
[Crossref] [PubMed]

Bashkansky, M.

Baumann, B.

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).
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A. Pollreisz, J. D. Messinger, K. R. Sloan, T. J. Mittermueller, A. S. Weinhandl, E. K. Benson, G. J. Kidd, U. Schmidt-Erfurth, and C. A. Curcio, “Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy,” Exp. Eye Res. 166, 131–139 (2018).
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T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
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J. M. Bruder, Z. A. Pfeiffer, J. M. Ciriello, D. M. Horrigan, N. L. Wicks, B. Flaherty, and E. Oancea, “Melanosomal dynamics assessed with a live-cell fluorescent melanosomal marker,” PLoS One 7(8), e43465 (2012).
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S. A. Burns, A. E. Elsner, K. A. Sapoznik, R. L. Warner, and T. J. Gast, “Adaptive optics imaging of the human retina,” Prog. Retin. Eye Res. 68, 1–30 (2019).
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M. A. Wilk, A. L. Huckenpahler, R. F. Collery, B. A. Link, and J. Carroll, “The effect of retinal melanin on optical coherence tomography images,” Transl. Vis. Sci. Technol. 6(2), 8 (2017).
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R. F. Cooper, A. M. Dubis, A. Pavaskar, J. Rha, A. Dubra, and J. Carroll, “Spatial and temporal variation of rod photoreceptor reflectance in the human retina,” Biomed. Opt. Express 2(9), 2577–2589 (2011).
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Chen, B.

Z. Yuan, B. Chen, H. Ren, and Y. Pan, “On the possibility of time-lapse ultrahigh-resolution optical coherence tomography for bladder cancer grading,” J. Biomed. Opt. 14(5), 050502 (2009).
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C. E. Granger, Q. Yang, H. Song, K. Saito, K. Nozato, L. R. Latchney, B. T. Leonard, M. M. Chung, D. R. Williams, and E. A. Rossi, “Human retinal pigment epithelium: In vivo cell morphometry, multispectral autofluorescence, and relationship to cone mosaic,” Invest. Ophthalmol. Vis. Sci. 59(15), 5705–5716 (2018).
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E. A. Rossi, P. Rangel-Fonseca, K. Parkins, W. Fischer, L. R. Latchney, M. A. Folwell, D. R. Williams, A. Dubra, and M. M. Chung, “In vivo imaging of retinal pigment epithelium cells in age related macular degeneration,” Biomed. Opt. Express 4(11), 2527–2539 (2013).
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Ciriello, J. M.

J. M. Bruder, Z. A. Pfeiffer, J. M. Ciriello, D. M. Horrigan, N. L. Wicks, B. Flaherty, and E. Oancea, “Melanosomal dynamics assessed with a live-cell fluorescent melanosomal marker,” PLoS One 7(8), e43465 (2012).
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Collery, R. F.

M. A. Wilk, A. L. Huckenpahler, R. F. Collery, B. A. Link, and J. Carroll, “The effect of retinal melanin on optical coherence tomography images,” Transl. Vis. Sci. Technol. 6(2), 8 (2017).
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Cooper, R. F.

Crowell, J. A.

F. Zhang, K. Kurokawa, A. Lassoued, J. A. Crowell, and D. T. Miller, “Cone photoreceptor classification in the living human eye from photostimulation-induced phase dynamics,” Proc. Natl. Acad. Sci. U.S.A. 116(16), 7951–7956 (2019).
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Curcio, C. A.

A. Pollreisz, J. D. Messinger, K. R. Sloan, T. J. Mittermueller, A. S. Weinhandl, E. K. Benson, G. J. Kidd, U. Schmidt-Erfurth, and C. A. Curcio, “Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy,” Exp. Eye Res. 166, 131–139 (2018).
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T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
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Q. X. Zhang, R. W. Lu, J. D. Messinger, C. A. Curcio, V. Guarcello, and X. C. Yao, “In vivo optical coherence tomography of light-driven melanosome translocation in retinal pigment epithelium,” Sci. Rep. 3(1), 2644 (2013).
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Delori, F. C.

J. J. Weiter, F. C. Delori, G. L. Wing, and K. A. Fitch, “Retinal pigment epithelial lipofuscin and melanin and choroidal melanin in human eyes,” Invest. Ophthalmol. Vis. Sci. 27(2), 145–152 (1986).
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Diemer, T.

M. Jiang, J. Esteve-Rudd, V. S. Lopes, T. Diemer, C. Lillo, A. Rump, and D. S. Williams, “Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis,” J. Cell Biol. 210(4), 595–611 (2015).
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Droettboom, M.

Du, C. W.

Y. T. Pan, Z. L. Wu, Z. J. Yuan, Z. G. Wang, and C. W. Du, “Subcellular imaging of epithelium with time-lapse optical coherence tomography,” J. Biomed. Opt. 12(5), 050504 (2007).
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Dubra, A.

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A. K. Dunn, C. L. Smithpeter, A. J. Welch, and R. R. Richards-Kortum, “Finite-difference time-domain simulation of light scattering from single cells,” J. Biomed. Opt. 2(3), 262–266 (1997).
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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).
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Elsner, A. E.

S. A. Burns, A. E. Elsner, K. A. Sapoznik, R. L. Warner, and T. J. Gast, “Adaptive optics imaging of the human retina,” Prog. Retin. Eye Res. 68, 1–30 (2019).
[PubMed]

Esteve-Rudd, J.

M. Jiang, J. Esteve-Rudd, V. S. Lopes, T. Diemer, C. Lillo, A. Rump, and D. S. Williams, “Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis,” J. Cell Biol. 210(4), 595–611 (2015).
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Fariss, R.

J. Tam, J. Liu, A. Dubra, and R. Fariss, “In vivo imaging of the human retinal pigment epithelial mosaic using adaptive optics enhanced indocyanine green ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 57(10), 4376–4384 (2016).
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Felberer, F.

Ferguson, R. D.

Fischer, W.

Fitch, K. A.

J. J. Weiter, F. C. Delori, G. L. Wing, and K. A. Fitch, “Retinal pigment epithelial lipofuscin and melanin and choroidal melanin in human eyes,” Invest. Ophthalmol. Vis. Sci. 27(2), 145–152 (1986).
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Flaherty, B.

J. M. Bruder, Z. A. Pfeiffer, J. M. Ciriello, D. M. Horrigan, N. L. Wicks, B. Flaherty, and E. Oancea, “Melanosomal dynamics assessed with a live-cell fluorescent melanosomal marker,” PLoS One 7(8), e43465 (2012).
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Folwell, M. A.

Futter, C. E.

C. E. Futter, “The molecular regulation of organelle transport in mammalian retinal pigment epithelial cells,” Pigment Cell Res. 19(2), 104–111 (2006).
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Gast, T. J.

S. A. Burns, A. E. Elsner, K. A. Sapoznik, R. L. Warner, and T. J. Gast, “Adaptive optics imaging of the human retina,” Prog. Retin. Eye Res. 68, 1–30 (2019).
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Gibbs, D.

D. Gibbs, S. M. Azarian, C. Lillo, J. Kitamoto, A. E. Klomp, K. P. Steel, R. T. Libby, and D. S. Williams, “Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes,” J. Cell Sci. 117(26), 6473–6483 (2004).
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D. Gibbs, J. Kitamoto, and D. S. Williams, “Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein,” Proc. Natl. Acad. Sci. U.S.A. 100(11), 6481–6486 (2003).
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Gofas-Salas, E.

Gorczynska, I.

M. Azimipour, R. J. Zawadzki, I. Gorczynska, J. Migacz, J. S. Werner, and R. S. Jonnal, “Intraframe motion correction for raster-scanned adaptive optics images using strip-based cross-correlation lag biases,” PLoS One 13(10), e0206052 (2018).
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Götzinger, E.

Granger, C. E.

C. E. Granger, Q. Yang, H. Song, K. Saito, K. Nozato, L. R. Latchney, B. T. Leonard, M. M. Chung, D. R. Williams, and E. A. Rossi, “Human retinal pigment epithelium: In vivo cell morphometry, multispectral autofluorescence, and relationship to cone mosaic,” Invest. Ophthalmol. Vis. Sci. 59(15), 5705–5716 (2018).
[Crossref] [PubMed]

Grieve, K.

Guarcello, V.

Q. X. Zhang, R. W. Lu, J. D. Messinger, C. A. Curcio, V. Guarcello, and X. C. Yao, “In vivo optical coherence tomography of light-driven melanosome translocation in retinal pigment epithelium,” Sci. Rep. 3(1), 2644 (2013).
[Crossref] [PubMed]

Gutierrez, D. B.

T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
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Hammer, D. X.

Hitzenberger, C. K.

Hofer, H.

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).
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Hong, Y. J.

Horrigan, D. M.

J. M. Bruder, Z. A. Pfeiffer, J. M. Ciriello, D. M. Horrigan, N. L. Wicks, B. Flaherty, and E. Oancea, “Melanosomal dynamics assessed with a live-cell fluorescent melanosomal marker,” PLoS One 7(8), e43465 (2012).
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Huang, X. R.

X. R. Huang, R. W. Knighton, Y. Zhou, and X. P. Zhao, “Reflectance speckle of retinal nerve fiber layer reveals axonal activity,” Invest. Ophthalmol. Vis. Sci. 54(4), 2616–2623 (2013).
[Crossref] [PubMed]

Huckenpahler, A. L.

M. A. Wilk, A. L. Huckenpahler, R. F. Collery, B. A. Link, and J. Carroll, “The effect of retinal melanin on optical coherence tomography images,” Transl. Vis. Sci. Technol. 6(2), 8 (2017).
[Crossref] [PubMed]

Huisingh, C.

T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
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K. Jeong, J. J. Turek, and D. D. Nolte, “Speckle fluctuation spectroscopy of intracellular motion in living tissue using coherence-domain digital holography,” J. Biomed. Opt. 15(3), 030514 (2010).
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Jiang, M.

M. Jiang, J. Esteve-Rudd, V. S. Lopes, T. Diemer, C. Lillo, A. Rump, and D. S. Williams, “Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis,” J. Cell Biol. 210(4), 595–611 (2015).
[Crossref] [PubMed]

Jonnal, R. S.

M. Azimipour, R. J. Zawadzki, I. Gorczynska, J. Migacz, J. S. Werner, and R. S. Jonnal, “Intraframe motion correction for raster-scanned adaptive optics images using strip-based cross-correlation lag biases,” PLoS One 13(10), e0206052 (2018).
[Crossref] [PubMed]

O. P. Kocaoglu, Z. Liu, F. Zhang, K. Kurokawa, R. S. Jonnal, and D. T. Miller, “Photoreceptor disc shedding in the living human eye,” Biomed. Opt. Express 7(11), 4554–4568 (2016).
[Crossref] [PubMed]

O. P. Kocaoglu, R. D. Ferguson, R. S. Jonnal, Z. Liu, Q. Wang, D. X. Hammer, and D. T. Miller, “Adaptive optics optical coherence tomography with dynamic retinal tracking,” Biomed. Opt. Express 5(7), 2262–2284 (2014).
[Crossref] [PubMed]

R. S. Jonnal, O. P. Kocaoglu, R. J. Zawadzki, S. H. Lee, J. S. Werner, and D. T. Miller, “The cellular origins of the outer retinal bands in optical coherence tomography images,” Invest. Ophthalmol. Vis. Sci. 55(12), 7904–7918 (2014).
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R. S. Jonnal, J. Rha, Y. Zhang, B. Cense, W. Gao, and D. T. Miller, “In vivo functional imaging of human cone photoreceptors,” Opt. Express 15(24), 16141–16160 (2007).
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Jung, H.

Kidd, G. J.

A. Pollreisz, J. D. Messinger, K. R. Sloan, T. J. Mittermueller, A. S. Weinhandl, E. K. Benson, G. J. Kidd, U. Schmidt-Erfurth, and C. A. Curcio, “Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy,” Exp. Eye Res. 166, 131–139 (2018).
[Crossref] [PubMed]

Kitamoto, J.

D. Gibbs, S. M. Azarian, C. Lillo, J. Kitamoto, A. E. Klomp, K. P. Steel, R. T. Libby, and D. S. Williams, “Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes,” J. Cell Sci. 117(26), 6473–6483 (2004).
[Crossref] [PubMed]

D. Gibbs, J. Kitamoto, and D. S. Williams, “Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein,” Proc. Natl. Acad. Sci. U.S.A. 100(11), 6481–6486 (2003).
[Crossref] [PubMed]

Klomp, A. E.

D. Gibbs, S. M. Azarian, C. Lillo, J. Kitamoto, A. E. Klomp, K. P. Steel, R. T. Libby, and D. S. Williams, “Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes,” J. Cell Sci. 117(26), 6473–6483 (2004).
[Crossref] [PubMed]

Knighton, R. W.

X. R. Huang, R. W. Knighton, Y. Zhou, and X. P. Zhao, “Reflectance speckle of retinal nerve fiber layer reveals axonal activity,” Invest. Ophthalmol. Vis. Sci. 54(4), 2616–2623 (2013).
[Crossref] [PubMed]

Kocaoglu, O. P.

Kroisamer, J. S.

Kurokawa, K.

F. Zhang, K. Kurokawa, A. Lassoued, J. A. Crowell, and D. T. Miller, “Cone photoreceptor classification in the living human eye from photostimulation-induced phase dynamics,” Proc. Natl. Acad. Sci. U.S.A. 116(16), 7951–7956 (2019).
[Crossref] [PubMed]

Z. Liu, K. Kurokawa, F. Zhang, J. J. Lee, and D. T. Miller, “Imaging and quantifying ganglion cells and other transparent neurons in the living human retina,” Proc. Natl. Acad. Sci. U.S.A. 114(48), 12803–12808 (2017).
[Crossref] [PubMed]

Z. Liu, K. Kurokawa, F. Zhang, and D. T. Miller, “Characterizing motility dynamics in human rpe cells,” Ophthalmic Technologies XXVII 10045, 1004515 (2017).
[Crossref]

O. P. Kocaoglu, Z. Liu, F. Zhang, K. Kurokawa, R. S. Jonnal, and D. T. Miller, “Photoreceptor disc shedding in the living human eye,” Biomed. Opt. Express 7(11), 4554–4568 (2016).
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K. Kurokawa, S. Makita, Y. J. Hong, and Y. Yasuno, “Two-dimensional micro-displacement measurement for laser coagulation using optical coherence tomography,” Biomed. Opt. Express 6(1), 170–190 (2015).
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Lassoued, A.

F. Zhang, K. Kurokawa, A. Lassoued, J. A. Crowell, and D. T. Miller, “Cone photoreceptor classification in the living human eye from photostimulation-induced phase dynamics,” Proc. Natl. Acad. Sci. U.S.A. 116(16), 7951–7956 (2019).
[Crossref] [PubMed]

Latchney, L. R.

C. E. Granger, Q. Yang, H. Song, K. Saito, K. Nozato, L. R. Latchney, B. T. Leonard, M. M. Chung, D. R. Williams, and E. A. Rossi, “Human retinal pigment epithelium: In vivo cell morphometry, multispectral autofluorescence, and relationship to cone mosaic,” Invest. Ophthalmol. Vis. Sci. 59(15), 5705–5716 (2018).
[Crossref] [PubMed]

E. A. Rossi, P. Rangel-Fonseca, K. Parkins, W. Fischer, L. R. Latchney, M. A. Folwell, D. R. Williams, A. Dubra, and M. M. Chung, “In vivo imaging of retinal pigment epithelium cells in age related macular degeneration,” Biomed. Opt. Express 4(11), 2527–2539 (2013).
[Crossref] [PubMed]

Lee, J. J.

Z. Liu, K. Kurokawa, F. Zhang, J. J. Lee, and D. T. Miller, “Imaging and quantifying ganglion cells and other transparent neurons in the living human retina,” Proc. Natl. Acad. Sci. U.S.A. 114(48), 12803–12808 (2017).
[Crossref] [PubMed]

Lee, S. H.

R. S. Jonnal, O. P. Kocaoglu, R. J. Zawadzki, S. H. Lee, J. S. Werner, and D. T. Miller, “The cellular origins of the outer retinal bands in optical coherence tomography images,” Invest. Ophthalmol. Vis. Sci. 55(12), 7904–7918 (2014).
[Crossref] [PubMed]

Leonard, B. T.

C. E. Granger, Q. Yang, H. Song, K. Saito, K. Nozato, L. R. Latchney, B. T. Leonard, M. M. Chung, D. R. Williams, and E. A. Rossi, “Human retinal pigment epithelium: In vivo cell morphometry, multispectral autofluorescence, and relationship to cone mosaic,” Invest. Ophthalmol. Vis. Sci. 59(15), 5705–5716 (2018).
[Crossref] [PubMed]

Libby, R. T.

D. Gibbs, S. M. Azarian, C. Lillo, J. Kitamoto, A. E. Klomp, K. P. Steel, R. T. Libby, and D. S. Williams, “Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes,” J. Cell Sci. 117(26), 6473–6483 (2004).
[Crossref] [PubMed]

Lillo, C.

M. Jiang, J. Esteve-Rudd, V. S. Lopes, T. Diemer, C. Lillo, A. Rump, and D. S. Williams, “Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis,” J. Cell Biol. 210(4), 595–611 (2015).
[Crossref] [PubMed]

D. Gibbs, S. M. Azarian, C. Lillo, J. Kitamoto, A. E. Klomp, K. P. Steel, R. T. Libby, and D. S. Williams, “Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes,” J. Cell Sci. 117(26), 6473–6483 (2004).
[Crossref] [PubMed]

Link, B. A.

M. A. Wilk, A. L. Huckenpahler, R. F. Collery, B. A. Link, and J. Carroll, “The effect of retinal melanin on optical coherence tomography images,” Transl. Vis. Sci. Technol. 6(2), 8 (2017).
[Crossref] [PubMed]

Liu, J.

T. Liu, H. Jung, J. Liu, M. Droettboom, and J. Tam, “Noninvasive near infrared autofluorescence imaging of retinal pigment epithelial cells in the human retina using adaptive optics,” Biomed. Opt. Express 8(10), 4348–4360 (2017).
[Crossref] [PubMed]

J. Tam, J. Liu, A. Dubra, and R. Fariss, “In vivo imaging of the human retinal pigment epithelial mosaic using adaptive optics enhanced indocyanine green ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci. 57(10), 4376–4384 (2016).
[Crossref] [PubMed]

Liu, T.

Liu, Z.

Z. Liu, J. Tam, O. Saeedi, and D. X. Hammer, “Trans-retinal cellular imaging with multimodal adaptive optics,” Biomed. Opt. Express 9(9), 4246–4262 (2018).
[Crossref] [PubMed]

Z. Liu, K. Kurokawa, F. Zhang, and D. T. Miller, “Characterizing motility dynamics in human rpe cells,” Ophthalmic Technologies XXVII 10045, 1004515 (2017).
[Crossref]

Z. Liu, K. Kurokawa, F. Zhang, J. J. Lee, and D. T. Miller, “Imaging and quantifying ganglion cells and other transparent neurons in the living human retina,” Proc. Natl. Acad. Sci. U.S.A. 114(48), 12803–12808 (2017).
[Crossref] [PubMed]

Z. Liu, O. P. Kocaoglu, and D. T. Miller, “3D imaging of retinal pigment epithelial cells in the living human retina,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT533 (2016).
[Crossref] [PubMed]

O. P. Kocaoglu, Z. Liu, F. Zhang, K. Kurokawa, R. S. Jonnal, and D. T. Miller, “Photoreceptor disc shedding in the living human eye,” Biomed. Opt. Express 7(11), 4554–4568 (2016).
[Crossref] [PubMed]

O. P. Kocaoglu, T. L. Turner, Z. Liu, and D. T. Miller, “Adaptive optics optical coherence tomography at 1 MHz,” Biomed. Opt. Express 5(12), 4186–4200 (2014).
[Crossref] [PubMed]

O. P. Kocaoglu, R. D. Ferguson, R. S. Jonnal, Z. Liu, Q. Wang, D. X. Hammer, and D. T. Miller, “Adaptive optics optical coherence tomography with dynamic retinal tracking,” Biomed. Opt. Express 5(7), 2262–2284 (2014).
[Crossref] [PubMed]

Z. Liu, O. P. Kocaoglu, and D. T. Miller, “In-the-plane design of an off-axis ophthalmic adaptive optics system using toroidal mirrors,” Biomed. Opt. Express 4(12), 3007–3029 (2013).
[Crossref] [PubMed]

Lopes, V. S.

M. Jiang, J. Esteve-Rudd, V. S. Lopes, T. Diemer, C. Lillo, A. Rump, and D. S. Williams, “Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis,” J. Cell Biol. 210(4), 595–611 (2015).
[Crossref] [PubMed]

Lu, R. W.

Q. X. Zhang, R. W. Lu, J. D. Messinger, C. A. Curcio, V. Guarcello, and X. C. Yao, “In vivo optical coherence tomography of light-driven melanosome translocation in retinal pigment epithelium,” Sci. Rep. 3(1), 2644 (2013).
[Crossref] [PubMed]

Makita, S.

McGwin, G.

T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
[Crossref] [PubMed]

Merigan, W. H.

J. I. 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 (2009).
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Messinger, J. D.

A. Pollreisz, J. D. Messinger, K. R. Sloan, T. J. Mittermueller, A. S. Weinhandl, E. K. Benson, G. J. Kidd, U. Schmidt-Erfurth, and C. A. Curcio, “Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy,” Exp. Eye Res. 166, 131–139 (2018).
[Crossref] [PubMed]

T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
[Crossref] [PubMed]

Q. X. Zhang, R. W. Lu, J. D. Messinger, C. A. Curcio, V. Guarcello, and X. C. Yao, “In vivo optical coherence tomography of light-driven melanosome translocation in retinal pigment epithelium,” Sci. Rep. 3(1), 2644 (2013).
[Crossref] [PubMed]

Migacz, J.

M. Azimipour, R. J. Zawadzki, I. Gorczynska, J. Migacz, J. S. Werner, and R. S. Jonnal, “Intraframe motion correction for raster-scanned adaptive optics images using strip-based cross-correlation lag biases,” PLoS One 13(10), e0206052 (2018).
[Crossref] [PubMed]

Miller, D. T.

F. Zhang, K. Kurokawa, A. Lassoued, J. A. Crowell, and D. T. Miller, “Cone photoreceptor classification in the living human eye from photostimulation-induced phase dynamics,” Proc. Natl. Acad. Sci. U.S.A. 116(16), 7951–7956 (2019).
[Crossref] [PubMed]

Z. Liu, K. Kurokawa, F. Zhang, J. J. Lee, and D. T. Miller, “Imaging and quantifying ganglion cells and other transparent neurons in the living human retina,” Proc. Natl. Acad. Sci. U.S.A. 114(48), 12803–12808 (2017).
[Crossref] [PubMed]

Z. Liu, K. Kurokawa, F. Zhang, and D. T. Miller, “Characterizing motility dynamics in human rpe cells,” Ophthalmic Technologies XXVII 10045, 1004515 (2017).
[Crossref]

Z. Liu, O. P. Kocaoglu, and D. T. Miller, “3D imaging of retinal pigment epithelial cells in the living human retina,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT533 (2016).
[Crossref] [PubMed]

O. P. Kocaoglu, Z. Liu, F. Zhang, K. Kurokawa, R. S. Jonnal, and D. T. Miller, “Photoreceptor disc shedding in the living human eye,” Biomed. Opt. Express 7(11), 4554–4568 (2016).
[Crossref] [PubMed]

O. P. Kocaoglu, T. L. Turner, Z. Liu, and D. T. Miller, “Adaptive optics optical coherence tomography at 1 MHz,” Biomed. Opt. Express 5(12), 4186–4200 (2014).
[Crossref] [PubMed]

O. P. Kocaoglu, R. D. Ferguson, R. S. Jonnal, Z. Liu, Q. Wang, D. X. Hammer, and D. T. Miller, “Adaptive optics optical coherence tomography with dynamic retinal tracking,” Biomed. Opt. Express 5(7), 2262–2284 (2014).
[Crossref] [PubMed]

R. S. Jonnal, O. P. Kocaoglu, R. J. Zawadzki, S. H. Lee, J. S. Werner, and D. T. Miller, “The cellular origins of the outer retinal bands in optical coherence tomography images,” Invest. Ophthalmol. Vis. Sci. 55(12), 7904–7918 (2014).
[Crossref] [PubMed]

Z. Liu, O. P. Kocaoglu, and D. T. Miller, “In-the-plane design of an off-axis ophthalmic adaptive optics system using toroidal mirrors,” Biomed. Opt. Express 4(12), 3007–3029 (2013).
[Crossref] [PubMed]

R. S. Jonnal, J. Rha, Y. Zhang, B. Cense, W. Gao, and D. T. Miller, “In vivo functional imaging of human cone photoreceptors,” Opt. Express 15(24), 16141–16160 (2007).
[Crossref] [PubMed]

Mittermueller, T. J.

A. Pollreisz, J. D. Messinger, K. R. Sloan, T. J. Mittermueller, A. S. Weinhandl, E. K. Benson, G. J. Kidd, U. Schmidt-Erfurth, and C. A. Curcio, “Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy,” Exp. Eye Res. 166, 131–139 (2018).
[Crossref] [PubMed]

Morgan, J. I.

J. I. 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 (2009).
[Crossref] [PubMed]

Nolte, D. D.

K. Jeong, J. J. Turek, and D. D. Nolte, “Speckle fluctuation spectroscopy of intracellular motion in living tissue using coherence-domain digital holography,” J. Biomed. Opt. 15(3), 030514 (2010).
[Crossref] [PubMed]

Nozato, K.

C. E. Granger, Q. Yang, H. Song, K. Saito, K. Nozato, L. R. Latchney, B. T. Leonard, M. M. Chung, D. R. Williams, and E. A. Rossi, “Human retinal pigment epithelium: In vivo cell morphometry, multispectral autofluorescence, and relationship to cone mosaic,” Invest. Ophthalmol. Vis. Sci. 59(15), 5705–5716 (2018).
[Crossref] [PubMed]

Oancea, E.

J. M. Bruder, Z. A. Pfeiffer, J. M. Ciriello, D. M. Horrigan, N. L. Wicks, B. Flaherty, and E. Oancea, “Melanosomal dynamics assessed with a live-cell fluorescent melanosomal marker,” PLoS One 7(8), e43465 (2012).
[Crossref] [PubMed]

Pallikaris, A.

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]

Pan, Y.

Z. Yuan, B. Chen, H. Ren, and Y. Pan, “On the possibility of time-lapse ultrahigh-resolution optical coherence tomography for bladder cancer grading,” J. Biomed. Opt. 14(5), 050502 (2009).
[Crossref] [PubMed]

Pan, Y. T.

Y. T. Pan, Z. L. Wu, Z. J. Yuan, Z. G. Wang, and C. W. Du, “Subcellular imaging of epithelium with time-lapse optical coherence tomography,” J. Biomed. Opt. 12(5), 050504 (2007).
[Crossref] [PubMed]

Paques, M.

Parkins, K.

Pask, C.

A. W. Snyder and C. Pask, “The stiles-crawford effect-explanation and consequences,” Vision Res. 13(6), 1115–1137 (1973).
[Crossref] [PubMed]

Pavaskar, A.

Pfeiffer, Z. A.

J. M. Bruder, Z. A. Pfeiffer, J. M. Ciriello, D. M. Horrigan, N. L. Wicks, B. Flaherty, and E. Oancea, “Melanosomal dynamics assessed with a live-cell fluorescent melanosomal marker,” PLoS One 7(8), e43465 (2012).
[Crossref] [PubMed]

Pircher, M.

Pollreisz, A.

A. Pollreisz, J. D. Messinger, K. R. Sloan, T. J. Mittermueller, A. S. Weinhandl, E. K. Benson, G. J. Kidd, U. Schmidt-Erfurth, and C. A. Curcio, “Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy,” Exp. Eye Res. 166, 131–139 (2018).
[Crossref] [PubMed]

Rangel-Fonseca, P.

Reintjes, J.

Ren, H.

Z. Yuan, B. Chen, H. Ren, and Y. Pan, “On the possibility of time-lapse ultrahigh-resolution optical coherence tomography for bladder cancer grading,” J. Biomed. Opt. 14(5), 050502 (2009).
[Crossref] [PubMed]

Rha, J.

Richards-Kortum, R. R.

A. K. Dunn, C. L. Smithpeter, A. J. Welch, and R. R. Richards-Kortum, “Finite-difference time-domain simulation of light scattering from single cells,” J. Biomed. Opt. 2(3), 262–266 (1997).
[Crossref] [PubMed]

Rossi, E. A.

Rudnicka, A. R.

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).
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Rump, A.

M. Jiang, J. Esteve-Rudd, V. S. Lopes, T. Diemer, C. Lillo, A. Rump, and D. S. Williams, “Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis,” J. Cell Biol. 210(4), 595–611 (2015).
[Crossref] [PubMed]

Saeedi, O.

Sahel, J. A.

Saito, K.

C. E. Granger, Q. Yang, H. Song, K. Saito, K. Nozato, L. R. Latchney, B. T. Leonard, M. M. Chung, D. R. Williams, and E. A. Rossi, “Human retinal pigment epithelium: In vivo cell morphometry, multispectral autofluorescence, and relationship to cone mosaic,” Invest. Ophthalmol. Vis. Sci. 59(15), 5705–5716 (2018).
[Crossref] [PubMed]

Sapoznik, K. A.

S. A. Burns, A. E. Elsner, K. A. Sapoznik, R. L. Warner, and T. J. Gast, “Adaptive optics imaging of the human retina,” Prog. Retin. Eye Res. 68, 1–30 (2019).
[PubMed]

Sattmann, H.

Schmidt-Erfurth, U.

A. Pollreisz, J. D. Messinger, K. R. Sloan, T. J. Mittermueller, A. S. Weinhandl, E. K. Benson, G. J. Kidd, U. Schmidt-Erfurth, and C. A. Curcio, “Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy,” Exp. Eye Res. 166, 131–139 (2018).
[Crossref] [PubMed]

F. Felberer, J. S. Kroisamer, B. Baumann, S. Zotter, U. Schmidt-Erfurth, C. K. Hitzenberger, and M. Pircher, “Adaptive optics SLO/OCT for 3D imaging of human photoreceptors in vivo,” Biomed. Opt. Express 5(2), 439–456 (2014).
[Crossref] [PubMed]

Scoles, D.

Seabra, M. C.

D. C. Barral and M. C. Seabra, “The melanosome as a model to study organelle motility in mammals,” Pigment Cell Res. 17(2), 111–118 (2004).
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Sloan, K. R.

A. Pollreisz, J. D. Messinger, K. R. Sloan, T. J. Mittermueller, A. S. Weinhandl, E. K. Benson, G. J. Kidd, U. Schmidt-Erfurth, and C. A. Curcio, “Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy,” Exp. Eye Res. 166, 131–139 (2018).
[Crossref] [PubMed]

T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
[Crossref] [PubMed]

Smith, R. T.

T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
[Crossref] [PubMed]

Smithpeter, C. L.

A. K. Dunn, C. L. Smithpeter, A. J. Welch, and R. R. Richards-Kortum, “Finite-difference time-domain simulation of light scattering from single cells,” J. Biomed. Opt. 2(3), 262–266 (1997).
[Crossref] [PubMed]

Snyder, A. W.

A. W. Snyder and C. Pask, “The stiles-crawford effect-explanation and consequences,” Vision Res. 13(6), 1115–1137 (1973).
[Crossref] [PubMed]

Song, H.

C. E. Granger, Q. Yang, H. Song, K. Saito, K. Nozato, L. R. Latchney, B. T. Leonard, M. M. Chung, D. R. Williams, and E. A. Rossi, “Human retinal pigment epithelium: In vivo cell morphometry, multispectral autofluorescence, and relationship to cone mosaic,” Invest. Ophthalmol. Vis. Sci. 59(15), 5705–5716 (2018).
[Crossref] [PubMed]

Steel, K. P.

D. Gibbs, S. M. Azarian, C. Lillo, J. Kitamoto, A. E. Klomp, K. P. Steel, R. T. Libby, and D. S. Williams, “Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes,” J. Cell Sci. 117(26), 6473–6483 (2004).
[Crossref] [PubMed]

Strauss, O.

O. Strauss, “The retinal pigment epithelium in visual function,” Physiol. Rev. 85(3), 845–881 (2005).
[Crossref] [PubMed]

Sulai, Y. N.

Tam, J.

Turek, J. J.

K. Jeong, J. J. Turek, and D. D. Nolte, “Speckle fluctuation spectroscopy of intracellular motion in living tissue using coherence-domain digital holography,” J. Biomed. Opt. 15(3), 030514 (2010).
[Crossref] [PubMed]

Turner, T. L.

Wang, Q.

Wang, Z. G.

Y. T. Pan, Z. L. Wu, Z. J. Yuan, Z. G. Wang, and C. W. Du, “Subcellular imaging of epithelium with time-lapse optical coherence tomography,” J. Biomed. Opt. 12(5), 050504 (2007).
[Crossref] [PubMed]

Warner, R. L.

S. A. Burns, A. E. Elsner, K. A. Sapoznik, R. L. Warner, and T. J. Gast, “Adaptive optics imaging of the human retina,” Prog. Retin. Eye Res. 68, 1–30 (2019).
[PubMed]

Weinhandl, A. S.

A. Pollreisz, J. D. Messinger, K. R. Sloan, T. J. Mittermueller, A. S. Weinhandl, E. K. Benson, G. J. Kidd, U. Schmidt-Erfurth, and C. A. Curcio, “Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy,” Exp. Eye Res. 166, 131–139 (2018).
[Crossref] [PubMed]

Weiter, J. J.

J. J. Weiter, F. C. Delori, G. L. Wing, and K. A. Fitch, “Retinal pigment epithelial lipofuscin and melanin and choroidal melanin in human eyes,” Invest. Ophthalmol. Vis. Sci. 27(2), 145–152 (1986).
[PubMed]

Welch, A. J.

A. K. Dunn, C. L. Smithpeter, A. J. Welch, and R. R. Richards-Kortum, “Finite-difference time-domain simulation of light scattering from single cells,” J. Biomed. Opt. 2(3), 262–266 (1997).
[Crossref] [PubMed]

Werner, J. S.

M. Azimipour, R. J. Zawadzki, I. Gorczynska, J. Migacz, J. S. Werner, and R. S. Jonnal, “Intraframe motion correction for raster-scanned adaptive optics images using strip-based cross-correlation lag biases,” PLoS One 13(10), e0206052 (2018).
[Crossref] [PubMed]

R. S. Jonnal, O. P. Kocaoglu, R. J. Zawadzki, S. H. Lee, J. S. Werner, and D. T. Miller, “The cellular origins of the outer retinal bands in optical coherence tomography images,” Invest. Ophthalmol. Vis. Sci. 55(12), 7904–7918 (2014).
[Crossref] [PubMed]

Wicks, N. L.

J. M. Bruder, Z. A. Pfeiffer, J. M. Ciriello, D. M. Horrigan, N. L. Wicks, B. Flaherty, and E. Oancea, “Melanosomal dynamics assessed with a live-cell fluorescent melanosomal marker,” PLoS One 7(8), e43465 (2012).
[Crossref] [PubMed]

Wilk, M. A.

M. A. Wilk, A. L. Huckenpahler, R. F. Collery, B. A. Link, and J. Carroll, “The effect of retinal melanin on optical coherence tomography images,” Transl. Vis. Sci. Technol. 6(2), 8 (2017).
[Crossref] [PubMed]

Williams, D. R.

C. E. Granger, Q. Yang, H. Song, K. Saito, K. Nozato, L. R. Latchney, B. T. Leonard, M. M. Chung, D. R. Williams, and E. A. Rossi, “Human retinal pigment epithelium: In vivo cell morphometry, multispectral autofluorescence, and relationship to cone mosaic,” Invest. Ophthalmol. Vis. Sci. 59(15), 5705–5716 (2018).
[Crossref] [PubMed]

E. A. Rossi, P. Rangel-Fonseca, K. Parkins, W. Fischer, L. R. Latchney, M. A. Folwell, D. R. Williams, A. Dubra, and M. M. Chung, “In vivo imaging of retinal pigment epithelium cells in age related macular degeneration,” Biomed. Opt. Express 4(11), 2527–2539 (2013).
[Crossref] [PubMed]

J. I. 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 (2009).
[Crossref] [PubMed]

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]

Williams, D. S.

M. Jiang, J. Esteve-Rudd, V. S. Lopes, T. Diemer, C. Lillo, A. Rump, and D. S. Williams, “Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis,” J. Cell Biol. 210(4), 595–611 (2015).
[Crossref] [PubMed]

D. Gibbs, S. M. Azarian, C. Lillo, J. Kitamoto, A. E. Klomp, K. P. Steel, R. T. Libby, and D. S. Williams, “Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes,” J. Cell Sci. 117(26), 6473–6483 (2004).
[Crossref] [PubMed]

D. Gibbs, J. Kitamoto, and D. S. Williams, “Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein,” Proc. Natl. Acad. Sci. U.S.A. 100(11), 6481–6486 (2003).
[Crossref] [PubMed]

Wing, G. L.

J. J. Weiter, F. C. Delori, G. L. Wing, and K. A. Fitch, “Retinal pigment epithelial lipofuscin and melanin and choroidal melanin in human eyes,” Invest. Ophthalmol. Vis. Sci. 27(2), 145–152 (1986).
[PubMed]

Wolfe, R.

J. I. 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 (2009).
[Crossref] [PubMed]

Wu, Z. L.

Y. T. Pan, Z. L. Wu, Z. J. Yuan, Z. G. Wang, and C. W. Du, “Subcellular imaging of epithelium with time-lapse optical coherence tomography,” J. Biomed. Opt. 12(5), 050504 (2007).
[Crossref] [PubMed]

Yang, Q.

C. E. Granger, Q. Yang, H. Song, K. Saito, K. Nozato, L. R. Latchney, B. T. Leonard, M. M. Chung, D. R. Williams, and E. A. Rossi, “Human retinal pigment epithelium: In vivo cell morphometry, multispectral autofluorescence, and relationship to cone mosaic,” Invest. Ophthalmol. Vis. Sci. 59(15), 5705–5716 (2018).
[Crossref] [PubMed]

Yao, X. C.

Q. X. Zhang, R. W. Lu, J. D. Messinger, C. A. Curcio, V. Guarcello, and X. C. Yao, “In vivo optical coherence tomography of light-driven melanosome translocation in retinal pigment epithelium,” Sci. Rep. 3(1), 2644 (2013).
[Crossref] [PubMed]

Yasuno, Y.

Yuan, Z.

Z. Yuan, B. Chen, H. Ren, and Y. Pan, “On the possibility of time-lapse ultrahigh-resolution optical coherence tomography for bladder cancer grading,” J. Biomed. Opt. 14(5), 050502 (2009).
[Crossref] [PubMed]

Yuan, Z. J.

Y. T. Pan, Z. L. Wu, Z. J. Yuan, Z. G. Wang, and C. W. Du, “Subcellular imaging of epithelium with time-lapse optical coherence tomography,” J. Biomed. Opt. 12(5), 050504 (2007).
[Crossref] [PubMed]

Zawadzki, R. J.

M. Azimipour, R. J. Zawadzki, I. Gorczynska, J. Migacz, J. S. Werner, and R. S. Jonnal, “Intraframe motion correction for raster-scanned adaptive optics images using strip-based cross-correlation lag biases,” PLoS One 13(10), e0206052 (2018).
[Crossref] [PubMed]

R. S. Jonnal, O. P. Kocaoglu, R. J. Zawadzki, S. H. Lee, J. S. Werner, and D. T. Miller, “The cellular origins of the outer retinal bands in optical coherence tomography images,” Invest. Ophthalmol. Vis. Sci. 55(12), 7904–7918 (2014).
[Crossref] [PubMed]

Zhang, F.

F. Zhang, K. Kurokawa, A. Lassoued, J. A. Crowell, and D. T. Miller, “Cone photoreceptor classification in the living human eye from photostimulation-induced phase dynamics,” Proc. Natl. Acad. Sci. U.S.A. 116(16), 7951–7956 (2019).
[Crossref] [PubMed]

Z. Liu, K. Kurokawa, F. Zhang, J. J. Lee, and D. T. Miller, “Imaging and quantifying ganglion cells and other transparent neurons in the living human retina,” Proc. Natl. Acad. Sci. U.S.A. 114(48), 12803–12808 (2017).
[Crossref] [PubMed]

Z. Liu, K. Kurokawa, F. Zhang, and D. T. Miller, “Characterizing motility dynamics in human rpe cells,” Ophthalmic Technologies XXVII 10045, 1004515 (2017).
[Crossref]

O. P. Kocaoglu, Z. Liu, F. Zhang, K. Kurokawa, R. S. Jonnal, and D. T. Miller, “Photoreceptor disc shedding in the living human eye,” Biomed. Opt. Express 7(11), 4554–4568 (2016).
[Crossref] [PubMed]

Zhang, Q. X.

Q. X. Zhang, R. W. Lu, J. D. Messinger, C. A. Curcio, V. Guarcello, and X. C. Yao, “In vivo optical coherence tomography of light-driven melanosome translocation in retinal pigment epithelium,” Sci. Rep. 3(1), 2644 (2013).
[Crossref] [PubMed]

Zhang, T.

T. Ach, C. Huisingh, G. McGwin, J. D. Messinger, T. Zhang, M. J. Bentley, D. B. Gutierrez, Z. Ablonczy, R. T. Smith, K. R. Sloan, and C. A. Curcio, “Quantitative autofluorescence and cell density maps of the human retinal pigment epithelium,” Invest. Ophthalmol. Vis. Sci. 55(8), 4832–4841 (2014).
[Crossref] [PubMed]

Zhang, Y.

Zhao, X. P.

X. R. Huang, R. W. Knighton, Y. Zhou, and X. P. Zhao, “Reflectance speckle of retinal nerve fiber layer reveals axonal activity,” Invest. Ophthalmol. Vis. Sci. 54(4), 2616–2623 (2013).
[Crossref] [PubMed]

Zhou, Y.

X. R. Huang, R. W. Knighton, Y. Zhou, and X. P. Zhao, “Reflectance speckle of retinal nerve fiber layer reveals axonal activity,” Invest. Ophthalmol. Vis. Sci. 54(4), 2616–2623 (2013).
[Crossref] [PubMed]

Zotter, S.

Biomed. Opt. Express (13)

E. A. Rossi, P. Rangel-Fonseca, K. Parkins, W. Fischer, L. R. Latchney, M. A. Folwell, D. R. Williams, A. Dubra, and M. M. Chung, “In vivo imaging of retinal pigment epithelium cells in age related macular degeneration,” Biomed. Opt. Express 4(11), 2527–2539 (2013).
[Crossref] [PubMed]

D. Scoles, Y. N. Sulai, and A. Dubra, “In vivo dark-field imaging of the retinal pigment epithelium cell mosaic,” Biomed. Opt. Express 4(9), 1710–1723 (2013).
[Crossref] [PubMed]

F. Felberer, J. S. Kroisamer, B. Baumann, S. Zotter, U. Schmidt-Erfurth, C. K. Hitzenberger, and M. Pircher, “Adaptive optics SLO/OCT for 3D imaging of human photoreceptors in vivo,” Biomed. Opt. Express 5(2), 439–456 (2014).
[Crossref] [PubMed]

T. Liu, H. Jung, J. Liu, M. Droettboom, and J. Tam, “Noninvasive near infrared autofluorescence imaging of retinal pigment epithelial cells in the human retina using adaptive optics,” Biomed. Opt. Express 8(10), 4348–4360 (2017).
[Crossref] [PubMed]

K. Grieve, E. Gofas-Salas, R. D. Ferguson, J. A. Sahel, M. Paques, and E. A. Rossi, “In vivo near-infrared autofluorescence imaging of retinal pigment epithelial cells with 757 nm excitation,” Biomed. Opt. Express 9(12), 5946–5961 (2018).
[Crossref] [PubMed]

Z. Liu, J. Tam, O. Saeedi, and D. X. Hammer, “Trans-retinal cellular imaging with multimodal adaptive optics,” Biomed. Opt. Express 9(9), 4246–4262 (2018).
[Crossref] [PubMed]

Z. Liu, O. P. Kocaoglu, and D. T. Miller, “In-the-plane design of an off-axis ophthalmic adaptive optics system using toroidal mirrors,” Biomed. Opt. Express 4(12), 3007–3029 (2013).
[Crossref] [PubMed]

O. P. Kocaoglu, T. L. Turner, Z. Liu, and D. T. Miller, “Adaptive optics optical coherence tomography at 1 MHz,” Biomed. Opt. Express 5(12), 4186–4200 (2014).
[Crossref] [PubMed]

O. P. Kocaoglu, R. D. Ferguson, R. S. Jonnal, Z. Liu, Q. Wang, D. X. Hammer, and D. T. Miller, “Adaptive optics optical coherence tomography with dynamic retinal tracking,” Biomed. Opt. Express 5(7), 2262–2284 (2014).
[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. Express 2(1), 100–112 (2011).
[Crossref] [PubMed]

R. F. Cooper, A. M. Dubis, A. Pavaskar, J. Rha, A. Dubra, and J. Carroll, “Spatial and temporal variation of rod photoreceptor reflectance in the human retina,” Biomed. Opt. Express 2(9), 2577–2589 (2011).
[Crossref] [PubMed]

O. P. Kocaoglu, Z. Liu, F. Zhang, K. Kurokawa, R. S. Jonnal, and D. T. Miller, “Photoreceptor disc shedding in the living human eye,” Biomed. Opt. Express 7(11), 4554–4568 (2016).
[Crossref] [PubMed]

K. Kurokawa, S. Makita, Y. J. Hong, and Y. Yasuno, “Two-dimensional micro-displacement measurement for laser coagulation using optical coherence tomography,” Biomed. Opt. Express 6(1), 170–190 (2015).
[Crossref] [PubMed]

Exp. Eye Res. (1)

A. Pollreisz, J. D. Messinger, K. R. Sloan, T. J. Mittermueller, A. S. Weinhandl, E. K. Benson, G. J. Kidd, U. Schmidt-Erfurth, and C. A. Curcio, “Visualizing melanosomes, lipofuscin, and melanolipofuscin in human retinal pigment epithelium using serial block face scanning electron microscopy,” Exp. Eye Res. 166, 131–139 (2018).
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Graefes Arch. Clin. Exp. Ophthalmol. (1)

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Supplementary Material (1)

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» Visualization 1       Intensity comparison between cone and RPE

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Figures (7)

Fig. 1
Fig. 1 Assessing motility dynamics in RPE and cone cells in a 26-year-old subject (S2) at 7° temporal retina using AO-OCT imaging. (A) Schematic depicts the three layers analyzed: (1) ONL, (2) cone (IS/OS + COST), and (3) RPE. En face images were extracted from the same registered and averaged AO-OCT volume at depths of (B) ONL, (C) cone (projection of cone IS/OS and COST), and (D) RPE. Average was over 45 registered AO-OCT volumes. Each RPE cell in (D) is represented by a Voronoi cell in (E). (F) Shown is a magnified view of Voronoi cells in the blue box superimposed on the RPE map in (E). A motility function (CF) was calculated for each Voronoi cell—an example for one RPE cell is diagrammed at bottom of (F)—and then averaged across cells to increase SNR.
Fig. 2
Fig. 2 Averaged and registered RPE images for the seven subjects imaged at 7° temporal to the fovea. N is the total number of images averaged. TI denotes mean time intervals between RPE images, which were selected one per AO-OCT video. 2-D power spectra are superimposed at bottom right of each en face image.
Fig. 3
Fig. 3 Motility dynamics measured at three retinal layers in seven subjects. (A) Representative raw motility function from S2 (Experiment 3) before normalization to the cone layer. Error bars represent standard deviation across 475 RPE cells. Colors represent measurements taken at three retinal layers: ONL (blue), Cone (IS/OS + COST) (red), and RPE (green). Colors in (A) also apply in (B). (B) Motility function is normalized to cone layer to remove residual eye motion and system errors. (C) Normalized RPE motility measurements are shown for the seven subjects. Scatterplots with ♦ symbols were from Experiment 1 with short video durations of 1.8 s, and scatterplots with ● symbols were from Experiments 2 and 3 with long video durations of ~9 s (see Table 2 for acquisition parameters). The gap between ~10 s and ~100 s for this data set is due to the time interval between two consecutive videos. (see Section 2.2). Fitted time constants are given in the key for each subject in each experiment.
Fig. 4
Fig. 4 Clarity of the RPE cell mosaic depends on the time interval between acquired AO-OCT images. En face images are averages of 35 volumes with an average time interval of (A) 0.23 s, (B) 7.8 s, and (C) 64.6 s in subject S2. The corresponding histograms of time interval (TI), 2-D power spectra and magnified sub-images (50 μm × 50 μm) indicated by the blue box in (A-C) are shown below each image. Note: Images of (A) and (B) are from the same patch of the retina; (C) is from a slightly different patch.
Fig. 5
Fig. 5 (A) Signal-to-noise ratio (SNR) of RPE mosaic fundamental frequency as a function of AO-OCT images averaged from subject S2. The RPE mosaic fundamental frequency and noise were determined from the power spectrum of the registered, averaged images. Images were acquired at averaged TI of 0.23 s (blue), 7.8 s (black) and 64.6 s (red). RPE en face images of: (B) single volume (N = 1), (C) average of 35 volumes with averaged TI = 0.23 s, (D) average of 35 volumes with TI = 7.8 s, and average of 5 volumes with averaged (E) TI = 0.18 s, and (G) TI = 6.16 s. The number of effective volumes that generate each image pixel in (E) and (G) varies between 0 and 5 depending on eye motion as shown in (F) and (H), respectively. The fast B-scan direction of the AO-OCT system is horizontal.
Fig. 6
Fig. 6 Motion-evoked speckle changes with depth in the RPE-BM complex. (A) Averaged AO-OCT B-scan of S2 shows distinct hyper- and hypo-reflective bands in the outer retina. Four depths are marked on the superimposed averaged A-line profile that represent apical, middle, and basal sub-layers of the RPE and the BM layer. The color-coded CFs at the four corresponding depths are shown in (B). The average time constants of four subjects (S2, S5-S7) are shown in (C). Error bars denote standard deviation. Also shown are the corresponding en face images of the averaged volume (D-G) and single frame from the reference volume (H-K) of S2.
Fig. 7
Fig. 7 Representative eye motion measured in two series of 35 AO-OCT images in three dimensions (3-D) from S2 with different time intervals (magenta: TI = 0.23 s, and blue: TI = 7.8 s). To better visualize the individual components, the 3-D motion is projected into the x-y, x-z, and y-z planes. Green point denotes the reference image coordinate: (x, y, z) = (0, 0, 0).

Tables (2)

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Table 1 AO-OCT system technical parameters for RPE motility imaging

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Table 2 Image acquisition parameters

Equations (3)

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CC( t n-1 )= r c ( R rc - R ¯ )( I rc ( t n-1 )- I( t n-1 ) ¯ ) r c [ ( R rc - R ¯ ) 2 ][ ( I rc ( t n-1 )- I( t n-1 ) ¯ ) 2 ] ,
CF=A(t)×exp( t τ ).
C F norm =A×exp( t τ )+B,

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