Abstract

We present a novel application of optical microangiography (OMAG) imaging technique for visualization of depth-resolved vascular network within retina and choroid as well as measurement of total retinal blood flow in mice. A fast speed spectral domain OCT imaging system at 820nm with a line scan rate of 140 kHz was developed to image the posterior segment of eyes in mice. By applying an OMAG algorithm to extract the moving blood flow signals out of the background tissue, we are able to provide true capillary level imaging of the retinal and choroidal vasculature. The microvascular patterns within different retinal layers are presented. An en face Doppler OCT approach [Srinivasan et al., Opt Express 18, 2477 (2010)] was adopted for retinal blood flow measurement. The flow is calculated by integrating the axial blood flow velocity over the vessel area measured in an en face plane without knowing the blood vessel angle. Total retinal blood flow can be measured from both retinal arteries and veins. The results indicate that OMAG has the potential for qualitative and quantitative evaluation of the microcirculation in posterior eye compartments in mouse models of retinopathy and neovascularization.

© 2012 OSA

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  4. R. Leitgeb, C. Hitzenberger, and A. Fercher, “Performance of fourier domain vs. time domain optical coherence tomography,” Opt. Express11(8), 889–894 (2003).
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    [CrossRef] [PubMed]
  22. S. Makita, T. Fabritius, and Y. Yasuno, “Quantitative retinal-blood flow measurement with three-dimensional vessel geometry determination using ultrahigh-resolution Doppler optical coherence angiography,” Opt. Lett.33(8), 836–838 (2008).
    [CrossRef] [PubMed]
  23. Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt.12(4), 041215 (2007).
    [CrossRef] [PubMed]
  24. Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “Retinal blood flow measurement by circumpapillary Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt.13(6), 064003 (2008).
    [CrossRef] [PubMed]
  25. V. J. Srinivasan, S. Sakadzić, I. Gorczynska, S. Ruvinskaya, W. Wu, J. G. Fujimoto, and D. A. Boas, “Quantitative cerebral blood flow with optical coherence tomography,” Opt. Express18(3), 2477–2494 (2010).
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    [CrossRef] [PubMed]
  27. W. Choi, B. Baumann, J. J. Liu, A. C. Clermont, E. P. Feener, J. S. Duker, and J. G. Fujimoto, “Measurement of pulsatile total blood flow in the human and rat retina with ultrahigh speed spectral/Fourier domain OCT,” Biomed. Opt. Express3(5), 1047–1061 (2012).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  30. R. T. Libby, R. S. Smith, O. V. Savinova, A. Zabaleta, J. E. Martin, F. J. Gonzalez, and S. W. M. John, “Modification of ocular defects in mouse developmental glaucoma models by tyrosinase,” Science299(5612), 1578–1581 (2003).
    [CrossRef] [PubMed]
  31. B. Chang, N. L. Hawes, R. E. Hurd, M. T. Davisson, S. Nusinowitz, and J. R. Heckenlively, “Retinal degeneration mutants in the mouse,” Vision Res.42(4), 517–525 (2002).
    [CrossRef] [PubMed]
  32. J. R. Heckenlively, N. L. Hawes, M. Friedlander, S. Nusinowitz, R. Hurd, M. Davisson, and B. Chang, “Mouse model of subretinal neovascularization with choroidal anastomosis,” Retina23(4), 518–522 (2003).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  34. V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S. E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.47(12), 5522–5528 (2006).
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    [CrossRef] [PubMed]
  36. K. H. Kim, M. Puoris’haag, G. N. Maguluri, Y. Umino, K. Cusato, R. B. Barlow, and J. F. de Boer, “Monitoring mouse retinal degeneration with high-resolution spectral-domain optical coherence tomography,” J. Vis.8(1), 17, 1–11 (2008).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  38. L. An, J. Qin, and R. K. Wang, “Ultrahigh sensitive optical microangiography for in vivo imaging of microcirculations within human skin tissue beds,” Opt. Express18(8), 8220–8228 (2010).
    [CrossRef] [PubMed]
  39. R. K. Wang, L. An, P. Francis, and D. J. Wilson, “Depth-resolved imaging of capillary networks in retina and choroid using ultrahigh sensitive optical microangiography,” Opt. Lett.35(9), 1467–1469 (2010).
    [CrossRef] [PubMed]
  40. Y. Jia, L. An, and R. K. Wang, “Label-free and highly sensitive optical imaging of detailed microcirculation within meninges and cortex in mice with the cranium left intact,” J. Biomed. Opt.15(3), 030510 (2010).
    [CrossRef] [PubMed]
  41. Z. Zhi, Y. Jung, Y. Jia, L. An, and R. K. Wang, “Highly sensitive imaging of renal microcirculation in vivo using ultrahigh sensitive optical microangiography,” Biomed. Opt. Express2(5), 1059–1068 (2011).
    [CrossRef] [PubMed]
  42. L. An, T. T. Shen, and R. K. K. Wang, “Using ultrahigh sensitive optical microangiography to achieve comprehensive depth resolved microvasculature mapping for human retina,” J. Biomed. Opt.16(10), 106013 (2011).
    [CrossRef] [PubMed]
  43. Z. Ma, A. Liu, X. Yin, A. Troyer, K. Thornburg, R. K. Wang, and S. Rugonyi, “Measurement of absolute blood flow velocity in outflow tract of HH18 chicken embryo based on 4D reconstruction using spectral domain optical coherence tomography,” Biomed. Opt. Express1(3), 798–811 (2010).
    [CrossRef] [PubMed]
  44. R. A. Cuthbertson and T. E. Mandel, “Anatomy of the mouse retina. Endothelial cell-pericyte ratio and capillary distribution,” Invest. Ophthalmol. Vis. Sci.27(11), 1659–1664 (1986).
    [PubMed]

2012

Y. Jia, O. Tan, J. Tokayer, B. Potsaid, Y. Wang, J. J. Liu, M. F. Kraus, H. Subhash, J. G. Fujimoto, J. Hornegger, and D. Huang, “Split-spectrum amplitude-decorrelation angiography with optical coherence tomography,” Opt. Express20(4), 4710–4725 (2012).
[CrossRef] [PubMed]

W. Choi, B. Baumann, J. J. Liu, A. C. Clermont, E. P. Feener, J. S. Duker, and J. G. Fujimoto, “Measurement of pulsatile total blood flow in the human and rat retina with ultrahigh speed spectral/Fourier domain OCT,” Biomed. Opt. Express3(5), 1047–1061 (2012).
[CrossRef] [PubMed]

2011

J. C. Morrison, W. O. Cepurna Ying Guo, and E. C. Johnson, “Pathophysiology of human glaucomatous optic nerve damage: insights from rodent models of glaucoma,” Exp. Eye Res.93(2), 156–164 (2011).
[CrossRef] [PubMed]

Z. Zhi, W. Cepurna, E. Johnson, T. Shen, J. Morrison, and R. K. Wang, “Volumetric and quantitative imaging of retinal blood flow in rats with optical microangiography,” Biomed. Opt. Express2(3), 579–591 (2011).
[CrossRef] [PubMed]

B. Baumann, B. Potsaid, M. F. Kraus, J. J. Liu, D. Huang, J. Hornegger, A. E. Cable, J. S. Duker, and J. G. Fujimoto, “Total retinal blood flow measurement with ultrahigh speed swept source/Fourier domain OCT,” Biomed. Opt. Express2(6), 1539–1552 (2011).
[CrossRef] [PubMed]

J. Enfield, E. Jonathan, and M. Leahy, “In vivo imaging of the microcirculation of the volar forearm using correlation mapping optical coherence tomography (cmOCT),” Biomed. Opt. Express2(5), 1184–1193 (2011).
[CrossRef] [PubMed]

G. Liu, L. Chou, W. Jia, W. Qi, B. Choi, and Z. Chen, “Intensity-based modified Doppler variance algorithm: application to phase instable and phase stable optical coherence tomography systems,” Opt. Express19(12), 11429–11440 (2011).
[CrossRef] [PubMed]

S. Zotter, M. Pircher, T. Torzicky, M. Bonesi, E. Götzinger, R. A. Leitgeb, and C. K. Hitzenberger, “Visualization of microvasculature by dual-beam phase-resolved Doppler optical coherence tomography,” Opt. Express19(2), 1217–1227 (2011).
[CrossRef] [PubMed]

D. Y. Kim, J. Fingler, J. S. Werner, D. M. Schwartz, S. E. Fraser, and R. J. Zawadzki, “In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography,” Biomed. Opt. Express2(6), 1504–1513 (2011).
[CrossRef] [PubMed]

Z. Zhi, Y. Jung, Y. Jia, L. An, and R. K. Wang, “Highly sensitive imaging of renal microcirculation in vivo using ultrahigh sensitive optical microangiography,” Biomed. Opt. Express2(5), 1059–1068 (2011).
[CrossRef] [PubMed]

L. An, T. T. Shen, and R. K. K. Wang, “Using ultrahigh sensitive optical microangiography to achieve comprehensive depth resolved microvasculature mapping for human retina,” J. Biomed. Opt.16(10), 106013 (2011).
[CrossRef] [PubMed]

2010

Z. Ma, A. Liu, X. Yin, A. Troyer, K. Thornburg, R. K. Wang, and S. Rugonyi, “Measurement of absolute blood flow velocity in outflow tract of HH18 chicken embryo based on 4D reconstruction using spectral domain optical coherence tomography,” Biomed. Opt. Express1(3), 798–811 (2010).
[CrossRef] [PubMed]

L. An, J. Qin, and R. K. Wang, “Ultrahigh sensitive optical microangiography for in vivo imaging of microcirculations within human skin tissue beds,” Opt. Express18(8), 8220–8228 (2010).
[CrossRef] [PubMed]

R. K. Wang, L. An, P. Francis, and D. J. Wilson, “Depth-resolved imaging of capillary networks in retina and choroid using ultrahigh sensitive optical microangiography,” Opt. Lett.35(9), 1467–1469 (2010).
[CrossRef] [PubMed]

Y. Jia, L. An, and R. K. Wang, “Label-free and highly sensitive optical imaging of detailed microcirculation within meninges and cortex in mice with the cranium left intact,” J. Biomed. Opt.15(3), 030510 (2010).
[CrossRef] [PubMed]

V. J. Srinivasan, S. Sakadzić, I. Gorczynska, S. Ruvinskaya, W. Wu, J. G. Fujimoto, and D. A. Boas, “Quantitative cerebral blood flow with optical coherence tomography,” Opt. Express18(3), 2477–2494 (2010).
[CrossRef] [PubMed]

V. J. Srinivasan, J. Y. Jiang, M. A. Yaseen, H. Radhakrishnan, W. Wu, S. Barry, A. E. Cable, and D. A. Boas, “Rapid volumetric angiography of cortical microvasculature with optical coherence tomography,” Opt. Lett.35(1), 43–45 (2010).
[CrossRef] [PubMed]

2009

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
[CrossRef] [PubMed]

T. Schmoll, C. Kolbitsch, and R. A. Leitgeb, “Ultra-high-speed volumetric tomography of human retinal blood flow,” Opt. Express17(5), 4166–4176 (2009).
[CrossRef] [PubMed]

G. Huber, S. C. Beck, C. Grimm, A. Sahaboglu-Tekgoz, F. Paquet-Durand, A. Wenzel, P. Humphries, T. M. Redmond, M. W. Seeliger, and M. D. Fischer, “Spectral domain optical coherence tomography in mouse models of retinal degeneration,” Invest. Ophthalmol. Vis. Sci.50(12), 5888–5895 (2009).
[CrossRef] [PubMed]

2008

K. H. Kim, M. Puoris’haag, G. N. Maguluri, Y. Umino, K. Cusato, R. B. Barlow, and J. F. de Boer, “Monitoring mouse retinal degeneration with high-resolution spectral-domain optical coherence tomography,” J. Vis.8(1), 17, 1–11 (2008).
[CrossRef] [PubMed]

A. Mariampillai, B. A. Standish, E. H. Moriyama, M. Khurana, N. R. Munce, M. K. Leung, J. Jiang, A. Cable, B. C. Wilson, I. A. Vitkin, and V. X. Yang, “Speckle variance detection of microvasculature using swept-source optical coherence tomography,” Opt. Lett.33(13), 1530–1532 (2008).
[CrossRef] [PubMed]

C. J. Pournaras, E. Rungger-Brändle, C. E. Riva, S. H. Hardarson, and E. Stefansson, “Regulation of retinal blood flow in health and disease,” Prog. Retin. Eye Res.27(3), 284–330 (2008).
[CrossRef] [PubMed]

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “Retinal blood flow measurement by circumpapillary Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt.13(6), 064003 (2008).
[CrossRef] [PubMed]

S. Makita, T. Fabritius, and Y. Yasuno, “Quantitative retinal-blood flow measurement with three-dimensional vessel geometry determination using ultrahigh-resolution Doppler optical coherence angiography,” Opt. Lett.33(8), 836–838 (2008).
[CrossRef] [PubMed]

M. Szkulmowski, A. Szkulmowska, T. Bajraszewski, A. Kowalczyk, and M. Wojtkowski, “Flow velocity estimation using joint Spectral and Time domain Optical Coherence Tomography,” Opt. Express16(9), 6008–6025 (2008).
[CrossRef] [PubMed]

Y. K. Tao, A. M. Davis, and J. A. Izatt, “Single-pass volumetric bidirectional blood flow imaging spectral domain optical coherence tomography using a modified Hilbert transform,” Opt. Express16(16), 12350–12361 (2008).
[CrossRef] [PubMed]

2007

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt.12(4), 041215 (2007).
[CrossRef] [PubMed]

I. H. Pang and A. F. Clark, “Rodent models for glaucoma retinopathy and optic neuropathy,” J. Glaucoma16(5), 483–505 (2007).
[CrossRef] [PubMed]

M. Ruggeri, H. Wehbe, S. Jiao, G. Gregori, M. E. Jockovich, A. Hackam, Y. Duan, and C. A. Puliafito, “In vivo three-dimensional high-resolution imaging of rodent retina with spectral-domain optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.48(4), 1808–1814 (2007).
[CrossRef] [PubMed]

O. P. Kocaoglu, S. R. Uhlhorn, E. Hernandez, R. A. Juarez, R. Will, J. M. Parel, and F. Manns, “Simultaneous fundus imaging and optical coherence tomography of the mouse retina,” Invest. Ophthalmol. Vis. Sci.48(3), 1283–1289 (2007).
[CrossRef] [PubMed]

J. Fingler, D. Schwartz, C. Yang, and S. E. Fraser, “Mobility and transverse flow visualization using phase variance contrast with spectral domain optical coherence tomography,” Opt. Express15(20), 12636–12653 (2007).
[CrossRef] [PubMed]

R. K. Wang, S. L. Jacques, Z. Ma, S. Hurst, S. R. Hanson, and A. Gruber, “Three dimensional optical angiography,” Opt. Express15(7), 4083–4097 (2007).
[CrossRef] [PubMed]

2006

S. Makita, Y. Hong, M. Yamanari, T. Yatagai, and Y. Yasuno, “Optical coherence angiography,” Opt. Express14(17), 7821–7840 (2006).
[CrossRef] [PubMed]

V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S. E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.47(12), 5522–5528 (2006).
[CrossRef] [PubMed]

2003

J. R. Heckenlively, N. L. Hawes, M. Friedlander, S. Nusinowitz, R. Hurd, M. Davisson, and B. Chang, “Mouse model of subretinal neovascularization with choroidal anastomosis,” Retina23(4), 518–522 (2003).
[CrossRef] [PubMed]

R. T. Libby, R. S. Smith, O. V. Savinova, A. Zabaleta, J. E. Martin, F. J. Gonzalez, and S. W. M. John, “Modification of ocular defects in mouse developmental glaucoma models by tyrosinase,” Science299(5612), 1578–1581 (2003).
[CrossRef] [PubMed]

R. Leitgeb, C. Hitzenberger, and A. Fercher, “Performance of fourier domain vs. time domain optical coherence tomography,” Opt. Express11(8), 889–894 (2003).
[CrossRef] [PubMed]

2002

J. Flammer, S. Orgül, V. P. Costa, N. Orzalesi, G. K. Krieglstein, L. M. Serra, J. P. Renard, and E. Stefánsson, “The impact of ocular blood flow in glaucoma,” Prog. Retin. Eye Res.21(4), 359–393 (2002).
[CrossRef] [PubMed]

Y. Zhao, Z. Chen, Z. Ding, H. Ren, and J. S. Nelson, “Real-time phase-resolved functional optical coherence tomography by use of optical Hilbert transformation,” Opt. Lett.27(2), 98–100 (2002).
[CrossRef] [PubMed]

B. Chang, N. L. Hawes, R. E. Hurd, M. T. Davisson, S. Nusinowitz, and J. R. Heckenlively, “Retinal degeneration mutants in the mouse,” Vision Res.42(4), 517–525 (2002).
[CrossRef] [PubMed]

1997

1992

V. Patel, S. Rassam, R. Newsom, J. Wiek, and E. Kohner, “Retinal blood flow in diabetic retinopathy,” BMJ305(6855), 678–683 (1992).
[CrossRef] [PubMed]

1986

R. A. Cuthbertson and T. E. Mandel, “Anatomy of the mouse retina. Endothelial cell-pericyte ratio and capillary distribution,” Invest. Ophthalmol. Vis. Sci.27(11), 1659–1664 (1986).
[PubMed]

An, L.

Z. Zhi, Y. Jung, Y. Jia, L. An, and R. K. Wang, “Highly sensitive imaging of renal microcirculation in vivo using ultrahigh sensitive optical microangiography,” Biomed. Opt. Express2(5), 1059–1068 (2011).
[CrossRef] [PubMed]

L. An, T. T. Shen, and R. K. K. Wang, “Using ultrahigh sensitive optical microangiography to achieve comprehensive depth resolved microvasculature mapping for human retina,” J. Biomed. Opt.16(10), 106013 (2011).
[CrossRef] [PubMed]

Y. Jia, L. An, and R. K. Wang, “Label-free and highly sensitive optical imaging of detailed microcirculation within meninges and cortex in mice with the cranium left intact,” J. Biomed. Opt.15(3), 030510 (2010).
[CrossRef] [PubMed]

L. An, J. Qin, and R. K. Wang, “Ultrahigh sensitive optical microangiography for in vivo imaging of microcirculations within human skin tissue beds,” Opt. Express18(8), 8220–8228 (2010).
[CrossRef] [PubMed]

R. K. Wang, L. An, P. Francis, and D. J. Wilson, “Depth-resolved imaging of capillary networks in retina and choroid using ultrahigh sensitive optical microangiography,” Opt. Lett.35(9), 1467–1469 (2010).
[CrossRef] [PubMed]

Bajraszewski, T.

Barlow, R. B.

K. H. Kim, M. Puoris’haag, G. N. Maguluri, Y. Umino, K. Cusato, R. B. Barlow, and J. F. de Boer, “Monitoring mouse retinal degeneration with high-resolution spectral-domain optical coherence tomography,” J. Vis.8(1), 17, 1–11 (2008).
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Bartlett, L. A.

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
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W. Choi, B. Baumann, J. J. Liu, A. C. Clermont, E. P. Feener, J. S. Duker, and J. G. Fujimoto, “Measurement of pulsatile total blood flow in the human and rat retina with ultrahigh speed spectral/Fourier domain OCT,” Biomed. Opt. Express3(5), 1047–1061 (2012).
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B. Baumann, B. Potsaid, M. F. Kraus, J. J. Liu, D. Huang, J. Hornegger, A. E. Cable, J. S. Duker, and J. G. Fujimoto, “Total retinal blood flow measurement with ultrahigh speed swept source/Fourier domain OCT,” Biomed. Opt. Express2(6), 1539–1552 (2011).
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G. Huber, S. C. Beck, C. Grimm, A. Sahaboglu-Tekgoz, F. Paquet-Durand, A. Wenzel, P. Humphries, T. M. Redmond, M. W. Seeliger, and M. D. Fischer, “Spectral domain optical coherence tomography in mouse models of retinal degeneration,” Invest. Ophthalmol. Vis. Sci.50(12), 5888–5895 (2009).
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Boas, D. A.

Bonesi, M.

S. Zotter, M. Pircher, T. Torzicky, M. Bonesi, E. Götzinger, R. A. Leitgeb, and C. K. Hitzenberger, “Visualization of microvasculature by dual-beam phase-resolved Doppler optical coherence tomography,” Opt. Express19(2), 1217–1227 (2011).
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Bouma, B. E.

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
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Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “Retinal blood flow measurement by circumpapillary Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt.13(6), 064003 (2008).
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Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt.12(4), 041215 (2007).
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V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S. E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.47(12), 5522–5528 (2006).
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Cable, A. E.

Carvalho, M.

V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S. E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.47(12), 5522–5528 (2006).
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Cepurna Ying Guo, W. O.

J. C. Morrison, W. O. Cepurna Ying Guo, and E. C. Johnson, “Pathophysiology of human glaucomatous optic nerve damage: insights from rodent models of glaucoma,” Exp. Eye Res.93(2), 156–164 (2011).
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J. R. Heckenlively, N. L. Hawes, M. Friedlander, S. Nusinowitz, R. Hurd, M. Davisson, and B. Chang, “Mouse model of subretinal neovascularization with choroidal anastomosis,” Retina23(4), 518–522 (2003).
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B. Chang, N. L. Hawes, R. E. Hurd, M. T. Davisson, S. Nusinowitz, and J. R. Heckenlively, “Retinal degeneration mutants in the mouse,” Vision Res.42(4), 517–525 (2002).
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Choi, B.

Choi, W.

W. Choi, B. Baumann, J. J. Liu, A. C. Clermont, E. P. Feener, J. S. Duker, and J. G. Fujimoto, “Measurement of pulsatile total blood flow in the human and rat retina with ultrahigh speed spectral/Fourier domain OCT,” Biomed. Opt. Express3(5), 1047–1061 (2012).
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Clark, A. F.

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V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S. E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.47(12), 5522–5528 (2006).
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W. Choi, B. Baumann, J. J. Liu, A. C. Clermont, E. P. Feener, J. S. Duker, and J. G. Fujimoto, “Measurement of pulsatile total blood flow in the human and rat retina with ultrahigh speed spectral/Fourier domain OCT,” Biomed. Opt. Express3(5), 1047–1061 (2012).
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K. H. Kim, M. Puoris’haag, G. N. Maguluri, Y. Umino, K. Cusato, R. B. Barlow, and J. F. de Boer, “Monitoring mouse retinal degeneration with high-resolution spectral-domain optical coherence tomography,” J. Vis.8(1), 17, 1–11 (2008).
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R. A. Cuthbertson and T. E. Mandel, “Anatomy of the mouse retina. Endothelial cell-pericyte ratio and capillary distribution,” Invest. Ophthalmol. Vis. Sci.27(11), 1659–1664 (1986).
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Davisson, M.

J. R. Heckenlively, N. L. Hawes, M. Friedlander, S. Nusinowitz, R. Hurd, M. Davisson, and B. Chang, “Mouse model of subretinal neovascularization with choroidal anastomosis,” Retina23(4), 518–522 (2003).
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Davisson, M. T.

B. Chang, N. L. Hawes, R. E. Hurd, M. T. Davisson, S. Nusinowitz, and J. R. Heckenlively, “Retinal degeneration mutants in the mouse,” Vision Res.42(4), 517–525 (2002).
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K. H. Kim, M. Puoris’haag, G. N. Maguluri, Y. Umino, K. Cusato, R. B. Barlow, and J. F. de Boer, “Monitoring mouse retinal degeneration with high-resolution spectral-domain optical coherence tomography,” J. Vis.8(1), 17, 1–11 (2008).
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Y. Zhao, Z. Chen, Z. Ding, H. Ren, and J. S. Nelson, “Real-time phase-resolved functional optical coherence tomography by use of optical Hilbert transformation,” Opt. Lett.27(2), 98–100 (2002).
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M. Ruggeri, H. Wehbe, S. Jiao, G. Gregori, M. E. Jockovich, A. Hackam, Y. Duan, and C. A. Puliafito, “In vivo three-dimensional high-resolution imaging of rodent retina with spectral-domain optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.48(4), 1808–1814 (2007).
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W. Choi, B. Baumann, J. J. Liu, A. C. Clermont, E. P. Feener, J. S. Duker, and J. G. Fujimoto, “Measurement of pulsatile total blood flow in the human and rat retina with ultrahigh speed spectral/Fourier domain OCT,” Biomed. Opt. Express3(5), 1047–1061 (2012).
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B. Baumann, B. Potsaid, M. F. Kraus, J. J. Liu, D. Huang, J. Hornegger, A. E. Cable, J. S. Duker, and J. G. Fujimoto, “Total retinal blood flow measurement with ultrahigh speed swept source/Fourier domain OCT,” Biomed. Opt. Express2(6), 1539–1552 (2011).
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V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S. E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.47(12), 5522–5528 (2006).
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Fabritius, T.

Feener, E. P.

W. Choi, B. Baumann, J. J. Liu, A. C. Clermont, E. P. Feener, J. S. Duker, and J. G. Fujimoto, “Measurement of pulsatile total blood flow in the human and rat retina with ultrahigh speed spectral/Fourier domain OCT,” Biomed. Opt. Express3(5), 1047–1061 (2012).
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Fingler, J.

D. Y. Kim, J. Fingler, J. S. Werner, D. M. Schwartz, S. E. Fraser, and R. J. Zawadzki, “In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography,” Biomed. Opt. Express2(6), 1504–1513 (2011).
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J. Fingler, D. Schwartz, C. Yang, and S. E. Fraser, “Mobility and transverse flow visualization using phase variance contrast with spectral domain optical coherence tomography,” Opt. Express15(20), 12636–12653 (2007).
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G. Huber, S. C. Beck, C. Grimm, A. Sahaboglu-Tekgoz, F. Paquet-Durand, A. Wenzel, P. Humphries, T. M. Redmond, M. W. Seeliger, and M. D. Fischer, “Spectral domain optical coherence tomography in mouse models of retinal degeneration,” Invest. Ophthalmol. Vis. Sci.50(12), 5888–5895 (2009).
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J. Flammer, S. Orgül, V. P. Costa, N. Orzalesi, G. K. Krieglstein, L. M. Serra, J. P. Renard, and E. Stefánsson, “The impact of ocular blood flow in glaucoma,” Prog. Retin. Eye Res.21(4), 359–393 (2002).
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R. K. Wang, L. An, P. Francis, and D. J. Wilson, “Depth-resolved imaging of capillary networks in retina and choroid using ultrahigh sensitive optical microangiography,” Opt. Lett.35(9), 1467–1469 (2010).
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D. Y. Kim, J. Fingler, J. S. Werner, D. M. Schwartz, S. E. Fraser, and R. J. Zawadzki, “In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography,” Biomed. Opt. Express2(6), 1504–1513 (2011).
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J. Fingler, D. Schwartz, C. Yang, and S. E. Fraser, “Mobility and transverse flow visualization using phase variance contrast with spectral domain optical coherence tomography,” Opt. Express15(20), 12636–12653 (2007).
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Friedlander, M.

J. R. Heckenlively, N. L. Hawes, M. Friedlander, S. Nusinowitz, R. Hurd, M. Davisson, and B. Chang, “Mouse model of subretinal neovascularization with choroidal anastomosis,” Retina23(4), 518–522 (2003).
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Fujimoto, J. G.

Y. Jia, O. Tan, J. Tokayer, B. Potsaid, Y. Wang, J. J. Liu, M. F. Kraus, H. Subhash, J. G. Fujimoto, J. Hornegger, and D. Huang, “Split-spectrum amplitude-decorrelation angiography with optical coherence tomography,” Opt. Express20(4), 4710–4725 (2012).
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W. Choi, B. Baumann, J. J. Liu, A. C. Clermont, E. P. Feener, J. S. Duker, and J. G. Fujimoto, “Measurement of pulsatile total blood flow in the human and rat retina with ultrahigh speed spectral/Fourier domain OCT,” Biomed. Opt. Express3(5), 1047–1061 (2012).
[CrossRef] [PubMed]

B. Baumann, B. Potsaid, M. F. Kraus, J. J. Liu, D. Huang, J. Hornegger, A. E. Cable, J. S. Duker, and J. G. Fujimoto, “Total retinal blood flow measurement with ultrahigh speed swept source/Fourier domain OCT,” Biomed. Opt. Express2(6), 1539–1552 (2011).
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V. J. Srinivasan, S. Sakadzić, I. Gorczynska, S. Ruvinskaya, W. Wu, J. G. Fujimoto, and D. A. Boas, “Quantitative cerebral blood flow with optical coherence tomography,” Opt. Express18(3), 2477–2494 (2010).
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V. J. Srinivasan, T. H. Ko, M. Wojtkowski, M. Carvalho, A. Clermont, S. E. Bursell, Q. H. Song, J. Lem, J. S. Duker, J. S. Schuman, and J. G. Fujimoto, “Noninvasive volumetric imaging and morphometry of the rodent retina with high-speed, ultrahigh-resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.47(12), 5522–5528 (2006).
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Fukumura, D.

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
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R. T. Libby, R. S. Smith, O. V. Savinova, A. Zabaleta, J. E. Martin, F. J. Gonzalez, and S. W. M. John, “Modification of ocular defects in mouse developmental glaucoma models by tyrosinase,” Science299(5612), 1578–1581 (2003).
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Gorczynska, I.

Götzinger, E.

S. Zotter, M. Pircher, T. Torzicky, M. Bonesi, E. Götzinger, R. A. Leitgeb, and C. K. Hitzenberger, “Visualization of microvasculature by dual-beam phase-resolved Doppler optical coherence tomography,” Opt. Express19(2), 1217–1227 (2011).
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M. Ruggeri, H. Wehbe, S. Jiao, G. Gregori, M. E. Jockovich, A. Hackam, Y. Duan, and C. A. Puliafito, “In vivo three-dimensional high-resolution imaging of rodent retina with spectral-domain optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.48(4), 1808–1814 (2007).
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G. Huber, S. C. Beck, C. Grimm, A. Sahaboglu-Tekgoz, F. Paquet-Durand, A. Wenzel, P. Humphries, T. M. Redmond, M. W. Seeliger, and M. D. Fischer, “Spectral domain optical coherence tomography in mouse models of retinal degeneration,” Invest. Ophthalmol. Vis. Sci.50(12), 5888–5895 (2009).
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Hackam, A.

M. Ruggeri, H. Wehbe, S. Jiao, G. Gregori, M. E. Jockovich, A. Hackam, Y. Duan, and C. A. Puliafito, “In vivo three-dimensional high-resolution imaging of rodent retina with spectral-domain optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.48(4), 1808–1814 (2007).
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Hardarson, S. H.

C. J. Pournaras, E. Rungger-Brändle, C. E. Riva, S. H. Hardarson, and E. Stefansson, “Regulation of retinal blood flow in health and disease,” Prog. Retin. Eye Res.27(3), 284–330 (2008).
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Hawes, N. L.

J. R. Heckenlively, N. L. Hawes, M. Friedlander, S. Nusinowitz, R. Hurd, M. Davisson, and B. Chang, “Mouse model of subretinal neovascularization with choroidal anastomosis,” Retina23(4), 518–522 (2003).
[CrossRef] [PubMed]

B. Chang, N. L. Hawes, R. E. Hurd, M. T. Davisson, S. Nusinowitz, and J. R. Heckenlively, “Retinal degeneration mutants in the mouse,” Vision Res.42(4), 517–525 (2002).
[CrossRef] [PubMed]

Heckenlively, J. R.

J. R. Heckenlively, N. L. Hawes, M. Friedlander, S. Nusinowitz, R. Hurd, M. Davisson, and B. Chang, “Mouse model of subretinal neovascularization with choroidal anastomosis,” Retina23(4), 518–522 (2003).
[CrossRef] [PubMed]

B. Chang, N. L. Hawes, R. E. Hurd, M. T. Davisson, S. Nusinowitz, and J. R. Heckenlively, “Retinal degeneration mutants in the mouse,” Vision Res.42(4), 517–525 (2002).
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Hernandez, E.

O. P. Kocaoglu, S. R. Uhlhorn, E. Hernandez, R. A. Juarez, R. Will, J. M. Parel, and F. Manns, “Simultaneous fundus imaging and optical coherence tomography of the mouse retina,” Invest. Ophthalmol. Vis. Sci.48(3), 1283–1289 (2007).
[CrossRef] [PubMed]

Hitzenberger, C.

Hitzenberger, C. K.

S. Zotter, M. Pircher, T. Torzicky, M. Bonesi, E. Götzinger, R. A. Leitgeb, and C. K. Hitzenberger, “Visualization of microvasculature by dual-beam phase-resolved Doppler optical coherence tomography,” Opt. Express19(2), 1217–1227 (2011).
[CrossRef] [PubMed]

Hong, Y.

Hornegger, J.

Huang, D.

Y. Jia, O. Tan, J. Tokayer, B. Potsaid, Y. Wang, J. J. Liu, M. F. Kraus, H. Subhash, J. G. Fujimoto, J. Hornegger, and D. Huang, “Split-spectrum amplitude-decorrelation angiography with optical coherence tomography,” Opt. Express20(4), 4710–4725 (2012).
[CrossRef] [PubMed]

B. Baumann, B. Potsaid, M. F. Kraus, J. J. Liu, D. Huang, J. Hornegger, A. E. Cable, J. S. Duker, and J. G. Fujimoto, “Total retinal blood flow measurement with ultrahigh speed swept source/Fourier domain OCT,” Biomed. Opt. Express2(6), 1539–1552 (2011).
[CrossRef] [PubMed]

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “Retinal blood flow measurement by circumpapillary Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt.13(6), 064003 (2008).
[CrossRef] [PubMed]

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt.12(4), 041215 (2007).
[CrossRef] [PubMed]

Huber, G.

G. Huber, S. C. Beck, C. Grimm, A. Sahaboglu-Tekgoz, F. Paquet-Durand, A. Wenzel, P. Humphries, T. M. Redmond, M. W. Seeliger, and M. D. Fischer, “Spectral domain optical coherence tomography in mouse models of retinal degeneration,” Invest. Ophthalmol. Vis. Sci.50(12), 5888–5895 (2009).
[CrossRef] [PubMed]

Humphries, P.

G. Huber, S. C. Beck, C. Grimm, A. Sahaboglu-Tekgoz, F. Paquet-Durand, A. Wenzel, P. Humphries, T. M. Redmond, M. W. Seeliger, and M. D. Fischer, “Spectral domain optical coherence tomography in mouse models of retinal degeneration,” Invest. Ophthalmol. Vis. Sci.50(12), 5888–5895 (2009).
[CrossRef] [PubMed]

Hurd, R.

J. R. Heckenlively, N. L. Hawes, M. Friedlander, S. Nusinowitz, R. Hurd, M. Davisson, and B. Chang, “Mouse model of subretinal neovascularization with choroidal anastomosis,” Retina23(4), 518–522 (2003).
[CrossRef] [PubMed]

Hurd, R. E.

B. Chang, N. L. Hawes, R. E. Hurd, M. T. Davisson, S. Nusinowitz, and J. R. Heckenlively, “Retinal degeneration mutants in the mouse,” Vision Res.42(4), 517–525 (2002).
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Hurst, S.

Izatt, J. A.

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “Retinal blood flow measurement by circumpapillary Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt.13(6), 064003 (2008).
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Y. K. Tao, A. M. Davis, and J. A. Izatt, “Single-pass volumetric bidirectional blood flow imaging spectral domain optical coherence tomography using a modified Hilbert transform,” Opt. Express16(16), 12350–12361 (2008).
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Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt.12(4), 041215 (2007).
[CrossRef] [PubMed]

Jacques, S. L.

Jain, R. K.

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
[CrossRef] [PubMed]

Jia, W.

Jia, Y.

Y. Jia, O. Tan, J. Tokayer, B. Potsaid, Y. Wang, J. J. Liu, M. F. Kraus, H. Subhash, J. G. Fujimoto, J. Hornegger, and D. Huang, “Split-spectrum amplitude-decorrelation angiography with optical coherence tomography,” Opt. Express20(4), 4710–4725 (2012).
[CrossRef] [PubMed]

Z. Zhi, Y. Jung, Y. Jia, L. An, and R. K. Wang, “Highly sensitive imaging of renal microcirculation in vivo using ultrahigh sensitive optical microangiography,” Biomed. Opt. Express2(5), 1059–1068 (2011).
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Y. Jia, L. An, and R. K. Wang, “Label-free and highly sensitive optical imaging of detailed microcirculation within meninges and cortex in mice with the cranium left intact,” J. Biomed. Opt.15(3), 030510 (2010).
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Jiang, J.

Jiang, J. Y.

Jiao, S.

M. Ruggeri, H. Wehbe, S. Jiao, G. Gregori, M. E. Jockovich, A. Hackam, Y. Duan, and C. A. Puliafito, “In vivo three-dimensional high-resolution imaging of rodent retina with spectral-domain optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.48(4), 1808–1814 (2007).
[CrossRef] [PubMed]

Jockovich, M. E.

M. Ruggeri, H. Wehbe, S. Jiao, G. Gregori, M. E. Jockovich, A. Hackam, Y. Duan, and C. A. Puliafito, “In vivo three-dimensional high-resolution imaging of rodent retina with spectral-domain optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.48(4), 1808–1814 (2007).
[CrossRef] [PubMed]

John, S. W. M.

R. T. Libby, R. S. Smith, O. V. Savinova, A. Zabaleta, J. E. Martin, F. J. Gonzalez, and S. W. M. John, “Modification of ocular defects in mouse developmental glaucoma models by tyrosinase,” Science299(5612), 1578–1581 (2003).
[CrossRef] [PubMed]

Johnson, E.

Johnson, E. C.

J. C. Morrison, W. O. Cepurna Ying Guo, and E. C. Johnson, “Pathophysiology of human glaucomatous optic nerve damage: insights from rodent models of glaucoma,” Exp. Eye Res.93(2), 156–164 (2011).
[CrossRef] [PubMed]

Jonathan, E.

Juarez, R. A.

O. P. Kocaoglu, S. R. Uhlhorn, E. Hernandez, R. A. Juarez, R. Will, J. M. Parel, and F. Manns, “Simultaneous fundus imaging and optical coherence tomography of the mouse retina,” Invest. Ophthalmol. Vis. Sci.48(3), 1283–1289 (2007).
[CrossRef] [PubMed]

Jung, Y.

Z. Zhi, Y. Jung, Y. Jia, L. An, and R. K. Wang, “Highly sensitive imaging of renal microcirculation in vivo using ultrahigh sensitive optical microangiography,” Biomed. Opt. Express2(5), 1059–1068 (2011).
[CrossRef] [PubMed]

Khurana, M.

Kim, D. Y.

D. Y. Kim, J. Fingler, J. S. Werner, D. M. Schwartz, S. E. Fraser, and R. J. Zawadzki, “In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography,” Biomed. Opt. Express2(6), 1504–1513 (2011).
[CrossRef] [PubMed]

Kim, K. H.

K. H. Kim, M. Puoris’haag, G. N. Maguluri, Y. Umino, K. Cusato, R. B. Barlow, and J. F. de Boer, “Monitoring mouse retinal degeneration with high-resolution spectral-domain optical coherence tomography,” J. Vis.8(1), 17, 1–11 (2008).
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Figures (6)

Fig. 1
Fig. 1

Schematic of the high speed spectral domain OCT/OMAG system. CMOS: line scan camera, PC: polarization controller, SLD: superluminescent diode.

Fig. 2
Fig. 2

Schematic of en face Doppler approach for flow measurement. (A) In conventional Doppler OCT methods, the blood vessel angle ϴ is required to compute absolute velocity values Vabs. Total blood flow is calculated by multiplying with Vabs the cross-sectional area of the vessel S'. (B) In En face Doppler method, total blood flow is computed by simply integrating the axial velocity components Vz over the en face cross-section S that intercepts the vessel.

Fig. 3
Fig. 3

OCT imaging of morphology in mouse posterior eye. A) OCT fundus image of mouse posterior eye, arrows point to optic nerve fiber bundles. B) Recognition of all the mouse retinal layers and choroid layer. NFL: nerve fiber layer, GCL: ganglion cell layer, IPL: inner plexiform layer, INL: inner nuclear layer, OPL: outer plexiform layer, ONL: outer nuclear layer, ELM: external limiting membrane, IS/OS: junction between the inner and outer segment of the photoreceptors, RPE: retinal pigment epithelium layer, CH: choroid. C) OCT section across the periphery retina. D) OCT section across the central retina (optic nerve head *) and E) corresponding blood flow image. Scale bar = 200 µm.

Fig. 4
Fig. 4

(A) Color coded depth projection map of the retinal vascular network, blue: superficial, green: deep. (B-D) Vascular perfusion maps within different retinal layers in mouse eye after segmentation, where (B) is microvasculature within NFL and GCL, A: artery, V: vein, (C) within IPL, and (D) within OPL. Image size: 2x2 mm2

Fig. 5
Fig. 5

Vascular perfusion map of choroid in mice eye. Arrows points to long posterior ciliary artery (LPCA) entering the choroid. ONH: optic nerve head.

Fig. 6
Fig. 6

Measurement of total retinal blood flow. (A) Angiography obtained with UHS-OMAG. (B) Maximum projection of bi-directional axial flow velocity obtained with Phase-resolved Doppler OCT analysis for region marked by yellow square in (A). Red: artery, green: vein. (C, D) En face plane view of the axial blood flow velocity at ~500 µm depth, where white squares denote the integration of arterial flow and yellow squares denote the integration of venous flow. Scale bar = 100 µm.

Tables (1)

Tables Icon

Table 1 Quantification of total retinal blood flow in mice

Equations (3)

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V Z = Δ φ λ 0 4 π n Δ t A
V Z max = ± λ 0 4 n Δ t A
F = x y p l a n e V Z ( x , y ) d x d y

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