Abstract

Oblique scanning laser ophthalmoscopy (oSLO) is a recently developed technique to provide three-dimensional volumetric fluorescence imaging in retinas over a large field of view, without the need for depth sectioning. In this study, we present volumetric fluorescein angiography (vFA) at 200 B-scans per second in mouse retina in vivo by oSLO. By using a low-cost industrial CMOS camera, imaging speed was improved to 2 volumes per second, ∼10 times more than our previous results. Enabled by the volumetric imaging, we visualized hemodynamics at single capillary level in a depth-dependent manner, and provided methods to quantify capillary hematocrit, absolute capillary blood flow speed, and detection of capillary flow stagnancy and stalling at different vascular layers. The quantitative metrics for capillary hemodynamics enhanced by volumetric imaging can offer valuable insight into vision science and retinal pathologies.

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

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References

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    [Crossref]

2019 (1)

A. Joseph, A. Guevara-Torres, and J. Schallek, “Imaging single-cell blood flow in the smallest to largest vessels in the living retina,” eLife 8, e45077 (2019).
[Crossref]

2018 (3)

2017 (2)

L. Zhang, A. Capilla, W. Y. Song, G. Mostoslavsky, and J. Yi, “Oblique scanning laser microscopy for simultaneously volumetric structural and molecular imaging using only one raster scan,” Sci. Rep. 7(1), 8591 (2017).
[Crossref]

J. Lu, B. Y. Gu, X. L. Wang, and Y. H. Zhang, “High-speed adaptive optics line scan confocal retinal imaging for human eye,” PLoS One 12(3), e0169358 (2017).
[Crossref]

2016 (3)

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. P. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Visual Sci. 57(9), OCT130 (2016).
[Crossref]

A. de Castro, G. Huang, L. Sawides, T. Luo, and S. A. Burns, “Rapid high resolution imaging with a dual-channel scanning technique,” Opt. Lett. 41(8), 1881–1884 (2016).
[Crossref]

A. Guevara-Torres, A. Joseph, and J. B. Schallek, “Label free measurement of retinal blood cell flux, velocity, hematocrit and capillary width in the living mouse eye,” Biomed. Opt. Express 7(10), 4228–4249 (2016).
[Crossref]

2015 (4)

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

X. F. Dai, H. Zhang, Y. He, Y. Qi, B. Chang, and J. J. Pang, “The Frequency-Response Electroretinogram Distinguishes Cone and Abnormal Rod Function in rd12 Mice,” PLoS One 10(2), e0117570 (2015).
[Crossref]

2014 (2)

Z. W. Zhi, J. R. Chao, T. Wietecha, K. L. Hudkins, C. E. Alpers, and R. K. K. Wang, “Noninvasive Imaging of Retinal Morphology and Microvasculature in Obese Mice Using Optical Coherence Tomography and Optical Microangiography,” Invest. Ophthalmol. Visual Sci. 55(2), 1024–1030 (2014).
[Crossref]

T. Y. P. Chui, M. Dubow, A. Pinhas, N. Shah, A. Gan, R. Weitz, Y. N. Sulai, A. Dubra, and R. B. Rosen, “Comparison of adaptive optics scanning light ophthalmoscopic fluorescein angiography and offset pinhole imaging,” Biomed. Opt. Express 5(4), 1173–1189 (2014).
[Crossref]

2012 (1)

2011 (2)

J. Tam, P. Tiruveedhula, and A. Roorda, “Characterization of single-file flow through human retinal parafoveal capillaries using an adaptive optics scanning laser ophthalmoscope,” Biomed. Opt. Express 2(4), 781–793 (2011).
[Crossref]

Z. Y. Zhong, H. X. Song, T. Y. P. Chui, B. L. Petrig, and S. A. Burns, “Noninvasive Measurements and Analysis of Blood Velocity Profiles in Human Retinal Vessels,” Invest. Ophthalmol. Visual Sci. 52(7), 4151–4157 (2011).
[Crossref]

2008 (3)

2002 (1)

1997 (1)

1987 (1)

1961 (1)

H. R. Novotny and D. L. Alvis, “A method of photographing fluorescence in circulating blood in the human retina,” Circulation 24(1), 82–86 (1961).
[Crossref]

Alexander, K. R.

K. R. Alexander, A. Raghuram, and J. J. McAnany, “Comparison of spectral measures of period doubling in the cone flicker electroretinogram,” Doc. Ophthalmol. 117(3), 197–203 (2008).
[Crossref]

Alpers, C. E.

Z. W. Zhi, J. R. Chao, T. Wietecha, K. L. Hudkins, C. E. Alpers, and R. K. K. Wang, “Noninvasive Imaging of Retinal Morphology and Microvasculature in Obese Mice Using Optical Coherence Tomography and Optical Microangiography,” Invest. Ophthalmol. Visual Sci. 55(2), 1024–1030 (2014).
[Crossref]

Alvis, D. L.

H. R. Novotny and D. L. Alvis, “A method of photographing fluorescence in circulating blood in the human retina,” Circulation 24(1), 82–86 (1961).
[Crossref]

Bedggood, P.

Bouchard, M. B.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

Bruno, R. M.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

Burns, M. E.

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Burns, S. A.

Camino, A.

Campbell, M. C. W.

Capilla, A.

L. Zhang, A. Capilla, W. Y. Song, G. Mostoslavsky, and J. Yi, “Oblique scanning laser microscopy for simultaneously volumetric structural and molecular imaging using only one raster scan,” Sci. Rep. 7(1), 8591 (2017).
[Crossref]

Carroll, J.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. P. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Visual Sci. 57(9), OCT130 (2016).
[Crossref]

Cepurna, W.

Chang, B.

X. F. Dai, H. Zhang, Y. He, Y. Qi, B. Chang, and J. J. Pang, “The Frequency-Response Electroretinogram Distinguishes Cone and Abnormal Rod Function in rd12 Mice,” PLoS One 10(2), e0117570 (2015).
[Crossref]

Chao, J. R.

Z. W. Zhi, J. R. Chao, T. Wietecha, K. L. Hudkins, C. E. Alpers, and R. K. K. Wang, “Noninvasive Imaging of Retinal Morphology and Microvasculature in Obese Mice Using Optical Coherence Tomography and Optical Microangiography,” Invest. Ophthalmol. Visual Sci. 55(2), 1024–1030 (2014).
[Crossref]

Chui, T. Y. P.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. P. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Visual Sci. 57(9), OCT130 (2016).
[Crossref]

T. Y. P. Chui, M. Dubow, A. Pinhas, N. Shah, A. Gan, R. Weitz, Y. N. Sulai, A. Dubra, and R. B. Rosen, “Comparison of adaptive optics scanning light ophthalmoscopic fluorescein angiography and offset pinhole imaging,” Biomed. Opt. Express 5(4), 1173–1189 (2014).
[Crossref]

Z. Y. Zhong, H. X. Song, T. Y. P. Chui, B. L. Petrig, and S. A. Burns, “Noninvasive Measurements and Analysis of Blood Velocity Profiles in Human Retinal Vessels,” Invest. Ophthalmol. Visual Sci. 52(7), 4151–4157 (2011).
[Crossref]

Dai, X. F.

X. F. Dai, H. Zhang, Y. He, Y. Qi, B. Chang, and J. J. Pang, “The Frequency-Response Electroretinogram Distinguishes Cone and Abnormal Rod Function in rd12 Mice,” PLoS One 10(2), e0117570 (2015).
[Crossref]

de Castro, A.

Delori, F. C.

Desai, M.

Donnelly, W. J.

Dubow, M.

Dubra, A.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. P. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Visual Sci. 57(9), OCT130 (2016).
[Crossref]

T. Y. P. Chui, M. Dubow, A. Pinhas, N. Shah, A. Gan, R. Weitz, Y. N. Sulai, A. Dubra, and R. B. Rosen, “Comparison of adaptive optics scanning light ophthalmoscopic fluorescein angiography and offset pinhole imaging,” Biomed. Opt. Express 5(4), 1173–1189 (2014).
[Crossref]

Dunsby, C.

Efstathiadis, E.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. P. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Visual Sci. 57(9), OCT130 (2016).
[Crossref]

Gan, A.

Geyman, L.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. P. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Visual Sci. 57(9), OCT130 (2016).
[Crossref]

Grueber, W. B.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

Gu, B. Y.

J. Lu, B. Y. Gu, X. L. Wang, and Y. H. Zhang, “High-speed adaptive optics line scan confocal retinal imaging for human eye,” PLoS One 12(3), e0169358 (2017).
[Crossref]

Guevara-Torres, A.

A. Joseph, A. Guevara-Torres, and J. Schallek, “Imaging single-cell blood flow in the smallest to largest vessels in the living retina,” eLife 8, e45077 (2019).
[Crossref]

A. Guevara-Torres, A. Joseph, and J. B. Schallek, “Label free measurement of retinal blood cell flux, velocity, hematocrit and capillary width in the living mouse eye,” Biomed. Opt. Express 7(10), 4228–4249 (2016).
[Crossref]

He, Y.

X. F. Dai, H. Zhang, Y. He, Y. Qi, B. Chang, and J. J. Pang, “The Frequency-Response Electroretinogram Distinguishes Cone and Abnormal Rod Function in rd12 Mice,” PLoS One 10(2), e0117570 (2015).
[Crossref]

Hebert, T. J.

Hillman, E. M. C.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

Huang, D.

Huang, G.

Hudkins, K. L.

Z. W. Zhi, J. R. Chao, T. Wietecha, K. L. Hudkins, C. E. Alpers, and R. K. K. Wang, “Noninvasive Imaging of Retinal Morphology and Microvasculature in Obese Mice Using Optical Coherence Tomography and Optical Microangiography,” Invest. Ophthalmol. Visual Sci. 55(2), 1024–1030 (2014).
[Crossref]

Hughes, G. W.

Jia, Y. L.

Jian, Y.

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Jian, Y. F.

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Joseph, A.

A. Joseph, A. Guevara-Torres, and J. Schallek, “Imaging single-cell blood flow in the smallest to largest vessels in the living retina,” eLife 8, e45077 (2019).
[Crossref]

A. Guevara-Torres, A. Joseph, and J. B. Schallek, “Label free measurement of retinal blood cell flux, velocity, hematocrit and capillary width in the living mouse eye,” Biomed. Opt. Express 7(10), 4228–4249 (2016).
[Crossref]

Krawitz, B.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. P. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Visual Sci. 57(9), OCT130 (2016).
[Crossref]

Lacefield, C.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

Lam, K. S.

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Li, Y.

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Li, Y. P.

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Liang, J.

Lu, J.

J. Lu, B. Y. Gu, X. L. Wang, and Y. H. Zhang, “High-speed adaptive optics line scan confocal retinal imaging for human eye,” PLoS One 12(3), e0169358 (2017).
[Crossref]

Luo, T.

Mann, R. S.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

McAnany, J. J.

K. R. Alexander, A. Raghuram, and J. J. McAnany, “Comparison of spectral measures of period doubling in the cone flicker electroretinogram,” Doc. Ophthalmol. 117(3), 197–203 (2008).
[Crossref]

Mendes, C. S.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

Metha, A.

Miller, D. T.

Mo, S.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. P. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Visual Sci. 57(9), OCT130 (2016).
[Crossref]

Morrison, J. C.

Mostoslavsky, G.

L. Zhang, A. Capilla, W. Y. Song, G. Mostoslavsky, and J. Yi, “Oblique scanning laser microscopy for simultaneously volumetric structural and molecular imaging using only one raster scan,” Sci. Rep. 7(1), 8591 (2017).
[Crossref]

Ness, S.

Novotny, H. R.

H. R. Novotny and D. L. Alvis, “A method of photographing fluorescence in circulating blood in the human retina,” Circulation 24(1), 82–86 (1961).
[Crossref]

Pang, J. J.

X. F. Dai, H. Zhang, Y. He, Y. Qi, B. Chang, and J. J. Pang, “The Frequency-Response Electroretinogram Distinguishes Cone and Abnormal Rod Function in rd12 Mice,” PLoS One 10(2), e0117570 (2015).
[Crossref]

Petrig, B. L.

Z. Y. Zhong, H. X. Song, T. Y. P. Chui, B. L. Petrig, and S. A. Burns, “Noninvasive Measurements and Analysis of Blood Velocity Profiles in Human Retinal Vessels,” Invest. Ophthalmol. Visual Sci. 52(7), 4151–4157 (2011).
[Crossref]

Z. Y. Zhong, B. L. Petrig, X. F. Qi, and S. A. Burns, “In vivo measurement of erythrocyte velocity and retinal blood flow using adaptive optics scanning laser ophthalmoscopy,” Opt. Express 16(17), 12746–12756 (2008).
[Crossref]

Pi, S. H.

Pinhas, A.

Pugh, E. N.

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Qi, X. F.

Qi, Y.

X. F. Dai, H. Zhang, Y. He, Y. Qi, B. Chang, and J. J. Pang, “The Frequency-Response Electroretinogram Distinguishes Cone and Abnormal Rod Function in rd12 Mice,” PLoS One 10(2), e0117570 (2015).
[Crossref]

Queener, H.

Raghuram, A.

K. R. Alexander, A. Raghuram, and J. J. McAnany, “Comparison of spectral measures of period doubling in the cone flicker electroretinogram,” Doc. Ophthalmol. 117(3), 197–203 (2008).
[Crossref]

Romero-Borja, F.

Roorda, A.

Rosen, R. B.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. P. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Visual Sci. 57(9), OCT130 (2016).
[Crossref]

T. Y. P. Chui, M. Dubow, A. Pinhas, N. Shah, A. Gan, R. Weitz, Y. N. Sulai, A. Dubra, and R. B. Rosen, “Comparison of adaptive optics scanning light ophthalmoscopic fluorescein angiography and offset pinhole imaging,” Biomed. Opt. Express 5(4), 1173–1189 (2014).
[Crossref]

Roy, S.

Sarunic, M. V.

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Sawides, L.

Schallek, J.

A. Joseph, A. Guevara-Torres, and J. Schallek, “Imaging single-cell blood flow in the smallest to largest vessels in the living retina,” eLife 8, e45077 (2019).
[Crossref]

Schallek, J. B.

Shah, N.

Shao, D.

Simonett, J.

Song, H. X.

Z. Y. Zhong, H. X. Song, T. Y. P. Chui, B. L. Petrig, and S. A. Burns, “Noninvasive Measurements and Analysis of Blood Velocity Profiles in Human Retinal Vessels,” Invest. Ophthalmol. Visual Sci. 52(7), 4151–4157 (2011).
[Crossref]

Song, W. Y.

W. Y. Song, L. B. Zhou, and J. Yi, “Multimodal Volumetric Retinal Imaging by Oblique Scanning Laser Ophthalmoscopy (OSLO) and Optical Coherence Tomography (OCT),” J. Visualized Exp. 138, e57814 (2018).
[Crossref]

L. Zhang, W. Y. Song, D. Shao, S. Zhang, M. Desai, S. Ness, S. Roy, and J. Yi, “Volumetric fluorescence retinal imaging in vivo over a 30-degree field of view by oblique scanning laser ophthalmoscopy (oSLO),” Biomed. Opt. Express 9(1), 25–40 (2018).
[Crossref]

L. Zhang, A. Capilla, W. Y. Song, G. Mostoslavsky, and J. Yi, “Oblique scanning laser microscopy for simultaneously volumetric structural and molecular imaging using only one raster scan,” Sci. Rep. 7(1), 8591 (2017).
[Crossref]

Sulai, Y. N.

Tam, J.

Tiruveedhula, P.

Voleti, V.

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

Wang, R. K. K.

Z. W. Zhi, J. R. Chao, T. Wietecha, K. L. Hudkins, C. E. Alpers, and R. K. K. Wang, “Noninvasive Imaging of Retinal Morphology and Microvasculature in Obese Mice Using Optical Coherence Tomography and Optical Microangiography,” Invest. Ophthalmol. Visual Sci. 55(2), 1024–1030 (2014).
[Crossref]

Wang, X.

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Wang, X. L.

J. Lu, B. Y. Gu, X. L. Wang, and Y. H. Zhang, “High-speed adaptive optics line scan confocal retinal imaging for human eye,” PLoS One 12(3), e0169358 (2017).
[Crossref]

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Webb, R. H.

Wei, X.

Weitz, R.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. P. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Visual Sci. 57(9), OCT130 (2016).
[Crossref]

T. Y. P. Chui, M. Dubow, A. Pinhas, N. Shah, A. Gan, R. Weitz, Y. N. Sulai, A. Dubra, and R. B. Rosen, “Comparison of adaptive optics scanning light ophthalmoscopic fluorescein angiography and offset pinhole imaging,” Biomed. Opt. Express 5(4), 1173–1189 (2014).
[Crossref]

Wietecha, T.

Z. W. Zhi, J. R. Chao, T. Wietecha, K. L. Hudkins, C. E. Alpers, and R. K. K. Wang, “Noninvasive Imaging of Retinal Morphology and Microvasculature in Obese Mice Using Optical Coherence Tomography and Optical Microangiography,” Invest. Ophthalmol. Visual Sci. 55(2), 1024–1030 (2014).
[Crossref]

Williams, D. R.

Yi, J.

L. Zhang, W. Y. Song, D. Shao, S. Zhang, M. Desai, S. Ness, S. Roy, and J. Yi, “Volumetric fluorescence retinal imaging in vivo over a 30-degree field of view by oblique scanning laser ophthalmoscopy (oSLO),” Biomed. Opt. Express 9(1), 25–40 (2018).
[Crossref]

W. Y. Song, L. B. Zhou, and J. Yi, “Multimodal Volumetric Retinal Imaging by Oblique Scanning Laser Ophthalmoscopy (OSLO) and Optical Coherence Tomography (OCT),” J. Visualized Exp. 138, e57814 (2018).
[Crossref]

L. Zhang, A. Capilla, W. Y. Song, G. Mostoslavsky, and J. Yi, “Oblique scanning laser microscopy for simultaneously volumetric structural and molecular imaging using only one raster scan,” Sci. Rep. 7(1), 8591 (2017).
[Crossref]

Zam, A.

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Zawadzki, R. J.

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Zhang, H.

X. F. Dai, H. Zhang, Y. He, Y. Qi, B. Chang, and J. J. Pang, “The Frequency-Response Electroretinogram Distinguishes Cone and Abnormal Rod Function in rd12 Mice,” PLoS One 10(2), e0117570 (2015).
[Crossref]

Zhang, L.

L. Zhang, W. Y. Song, D. Shao, S. Zhang, M. Desai, S. Ness, S. Roy, and J. Yi, “Volumetric fluorescence retinal imaging in vivo over a 30-degree field of view by oblique scanning laser ophthalmoscopy (oSLO),” Biomed. Opt. Express 9(1), 25–40 (2018).
[Crossref]

L. Zhang, A. Capilla, W. Y. Song, G. Mostoslavsky, and J. Yi, “Oblique scanning laser microscopy for simultaneously volumetric structural and molecular imaging using only one raster scan,” Sci. Rep. 7(1), 8591 (2017).
[Crossref]

Zhang, P.

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Zhang, P. F.

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

Zhang, S.

Zhang, Y. H.

J. Lu, B. Y. Gu, X. L. Wang, and Y. H. Zhang, “High-speed adaptive optics line scan confocal retinal imaging for human eye,” PLoS One 12(3), e0169358 (2017).
[Crossref]

Zhi, Z. W.

Z. W. Zhi, J. R. Chao, T. Wietecha, K. L. Hudkins, C. E. Alpers, and R. K. K. Wang, “Noninvasive Imaging of Retinal Morphology and Microvasculature in Obese Mice Using Optical Coherence Tomography and Optical Microangiography,” Invest. Ophthalmol. Visual Sci. 55(2), 1024–1030 (2014).
[Crossref]

Zhong, Z. Y.

Z. Y. Zhong, H. X. Song, T. Y. P. Chui, B. L. Petrig, and S. A. Burns, “Noninvasive Measurements and Analysis of Blood Velocity Profiles in Human Retinal Vessels,” Invest. Ophthalmol. Visual Sci. 52(7), 4151–4157 (2011).
[Crossref]

Z. Y. Zhong, B. L. Petrig, X. F. Qi, and S. A. Burns, “In vivo measurement of erythrocyte velocity and retinal blood flow using adaptive optics scanning laser ophthalmoscopy,” Opt. Express 16(17), 12746–12756 (2008).
[Crossref]

Zhou, L. B.

W. Y. Song, L. B. Zhou, and J. Yi, “Multimodal Volumetric Retinal Imaging by Oblique Scanning Laser Ophthalmoscopy (OSLO) and Optical Coherence Tomography (OCT),” J. Visualized Exp. 138, e57814 (2018).
[Crossref]

Appl. Opt. (1)

Biomed. Opt. Express (6)

Circulation (1)

H. R. Novotny and D. L. Alvis, “A method of photographing fluorescence in circulating blood in the human retina,” Circulation 24(1), 82–86 (1961).
[Crossref]

Doc. Ophthalmol. (1)

K. R. Alexander, A. Raghuram, and J. J. McAnany, “Comparison of spectral measures of period doubling in the cone flicker electroretinogram,” Doc. Ophthalmol. 117(3), 197–203 (2008).
[Crossref]

eLife (1)

A. Joseph, A. Guevara-Torres, and J. Schallek, “Imaging single-cell blood flow in the smallest to largest vessels in the living retina,” eLife 8, e45077 (2019).
[Crossref]

Invest. Ophthalmol. Visual Sci. (3)

Z. W. Zhi, J. R. Chao, T. Wietecha, K. L. Hudkins, C. E. Alpers, and R. K. K. Wang, “Noninvasive Imaging of Retinal Morphology and Microvasculature in Obese Mice Using Optical Coherence Tomography and Optical Microangiography,” Invest. Ophthalmol. Visual Sci. 55(2), 1024–1030 (2014).
[Crossref]

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. P. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Visual Sci. 57(9), OCT130 (2016).
[Crossref]

Z. Y. Zhong, H. X. Song, T. Y. P. Chui, B. L. Petrig, and S. A. Burns, “Noninvasive Measurements and Analysis of Blood Velocity Profiles in Human Retinal Vessels,” Invest. Ophthalmol. Visual Sci. 52(7), 4151–4157 (2011).
[Crossref]

J. Biomed. Opt. (2)

P. F. Zhang, A. Zam, Y. F. Jian, X. L. Wang, Y. P. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy–optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref]

J. Opt. Soc. Am. A (1)

J. Visualized Exp. (1)

W. Y. Song, L. B. Zhou, and J. Yi, “Multimodal Volumetric Retinal Imaging by Oblique Scanning Laser Ophthalmoscopy (OSLO) and Optical Coherence Tomography (OCT),” J. Visualized Exp. 138, e57814 (2018).
[Crossref]

Nat. Photonics (1)

M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9(2), 113–119 (2015).
[Crossref]

Opt. Express (3)

Opt. Lett. (1)

PLoS One (2)

X. F. Dai, H. Zhang, Y. He, Y. Qi, B. Chang, and J. J. Pang, “The Frequency-Response Electroretinogram Distinguishes Cone and Abnormal Rod Function in rd12 Mice,” PLoS One 10(2), e0117570 (2015).
[Crossref]

J. Lu, B. Y. Gu, X. L. Wang, and Y. H. Zhang, “High-speed adaptive optics line scan confocal retinal imaging for human eye,” PLoS One 12(3), e0169358 (2017).
[Crossref]

Sci. Rep. (1)

L. Zhang, A. Capilla, W. Y. Song, G. Mostoslavsky, and J. Yi, “Oblique scanning laser microscopy for simultaneously volumetric structural and molecular imaging using only one raster scan,” Sci. Rep. 7(1), 8591 (2017).
[Crossref]

Supplementary Material (1)

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» Visualization 1       Quantitative metrics for retinal capillary hemodynamics in 3D

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Figures (6)

Fig. 1.
Fig. 1. Schematic of the oblique scanning laser ophthalmoscopy (oSLO). The components within the shaded area are mounted on a 2-axis translational stage.
Fig. 2.
Fig. 2. Volumetric fluorescein angiography (vFA) in mouse retina in vivo. (a) A depth-encoded vFA image from a mouse retina over a 27° field-of-view. The pseudo-color is in HSV space. The depth coordinate of the maximum intensity denotes the hue, and the image intensity denotes the saturation and value. Two cross-sectional images are exemplified along the white dash lines. (b) The depth distribution of the vFA signal within the yellow region of interest in panel (a). NFL: nerve fiber layer; IPL: inner plexiform layer; OPL: outer plexiform layer. (c-f) The averaged vFA from NFL, IPL, OPL, and choroid, respectively. The contrast was adjusted separately for each layer. Scale bar = 200 µm.
Fig. 3.
Fig. 3. Capillary hematocrit calculation via temporal averaging. (a) Illustration of the fluorescence signal generation with repeated B-scans at a single capillary. T is short for time. (b-c) An example of an en face and cross-sectional vFA image from a mouse retina in vivo. (d) The temporal vFA signal from three cross point between scanning line and blood vessel (C3 to C5) in OPL from panel (b). The green and yellow regions exemplified the region-of-interests (ROIs) for calculating vFA at 0% hematocrit in plasma, and virtually 100% hematocrit in a non-vascular area. (e) The quantitative hematocrit calculation based on the vFA signal intensity with temporal averaging every 0.5s over a total period of 2.5s. For C1 to C5, five measurements were averaged over a total 2.5s data (n = 5). Error bar = SEM (standard error of the mean). Scale bar = 50 µm.
Fig. 4.
Fig. 4. Measurements of absolute blood speed at individual capillary level. (a) vFA image at deep capillary plexus at outer plexiform layer (OPL). Two alternating B-scan locations are labeled with two white lines. Bar = 0.2 mm. (b) The temporal vFA signal at two capillaries, C1 and C2, as pointed out in panel (a). (c) The temporal correlation of two temporal vFA signals between C1 and C2. The peak of the correlation measures the time delay. (d) Examples of vFA temporal signal from five capillaries, with various blood speed. (e) The capillary flow speed measured longitudinally from the same retina after anesthesia (n = 5). Error bar = SEM. The vertical axis of (b) and (d) is 10 µm.
Fig. 5.
Fig. 5. Capillary flow dynamics in high-speed vFA at 2 volume per second segmented at the inner plexiform layer, IPL (a-d) and outer plexiform layer, OPL (e-h). Yellow arrows point to one capillary segment showing a transient ischemia, and the red arrows point to a capillary having stalled blood flow. Scale bar = 100 µm.
Fig. 6.
Fig. 6. (a-b) vFA segmented at inner plexiform (IPL) and outer plexiform layer (OPL) with denoted capillary segments. (c)The heat map showing longitudinal hematocrit change at each capillary segment over a total period of 15s with 0.5s interval. (d) The averaged hematocrit over 15s for each capillary segment labeled in panel (a-b) (n = 15). (e) The heat map showing the temporal image correlation between two vFA collected 0.5s apart within each capillary segment. (f) The averaged image correlation averaged over a total period of 15s (n = 14). Error bar = SEM. Scale bar = 100 µm.

Tables (1)

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Table 1. Summary of different vFA imaging protocols

Equations (2)

Equations on this page are rendered with MathJax. Learn more.

H c t = I I 0 % H c t I 100 % H c t I 0 % H c t × 100 % .
v = L Δ T + T c ,