Abstract

Blood flow changes are highly related to neural activities in the retina. It has been reported that neural activity increases when flickering light stimulation of the retina is used. It is known that blood flow changes with flickering light stimulation can be altered in patients with vascular disease and that measurement of flicker-induced vasodilatation is an easily applied tool for monitoring functional microvascular alterations. However, details of distortions in retinal neurovascular coupling associated with major eye diseases are not well understood due to the limitation of existing techniques. In this study, flickering light stimulation was applied to mouse retinas to investigate stimulus evoked hemodynamic responses in individual retinal layers. A spectral domain optical coherence tomography (OCT) angiography imaging system was developed to provide dynamic mapping of hemodynamic responses in the ganglion cell layer, inner plexiform layer, outer plexiform layer and choroid layer before, during and after flickering light stimulation. Experimental results showed hemodynamic responses with different magnitudes and time courses in individual retinal layers. We anticipate that the dynamic OCT angiography of stimulus evoked hemodynamic responses can greatly foster the study of neurovascular coupling mechanisms in the retina, promising new biomarkers for retinal disease detection and diagnosis.

© 2016 Optical Society of America

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2016 (3)

M. Adhi, E. Badaro, J. J. Liu, M. F. Kraus, C. R. Baumal, A. J. Witkin, J. Hornegger, J. G. Fujimoto, J. S. Duker, and N. K. Waheed, “Three-dimensional enhanced imaging of vitreoretinal interface in diabetic retinopathy using swept-source optical coherence tomography,” Am. J. Ophthalmol. 162, 140–149 (2016).

U. Baran and R. K. Wang, “Review of optical coherence tomography based angiography in neuroscience,” Neurophotonics 3(1), 010902 (2016).
[Crossref] [PubMed]

I. Gorczynska, J. V. Migacz, R. J. Zawadzki, A. G. Capps, and J. S. Werner, “Comparison of amplitude-decorrelation, speckle-variance and phase-variance OCT angiography methods for imaging the human retina and choroid,” Biomed. Opt. Express 7(3), 911–942 (2016).
[Crossref] [PubMed]

2015 (7)

J. Xu, S. Han, C. Balaratnasingam, Z. Mammo, K. S. Wong, S. Lee, M. Cua, M. Young, A. Kirker, D. Albiani, F. Forooghian, P. Mackenzie, A. Merkur, D. Y. Yu, and M. V. Sarunic, “Retinal angiography with real-time speckle variance optical coherence tomography,” Br. J. Ophthalmol. 99(10), 1315–1319 (2015).
[Crossref] [PubMed]

A. Zhang, Q. Zhang, C. L. Chen, and R. K. Wang, “Methods and algorithms for optical coherence tomography-based angiography: a review and comparison,” J. Biomed. Opt. 20(10), 100901 (2015).
[Crossref] [PubMed]

C. L. Shields, J. Manalac, C. Das, J. Saktanasate, and J. A. Shields, “Review of spectral domain-enhanced depth imaging optical coherence tomography of tumors of the retina and retinal pigment epithelium in children and adults,” Indian J. Ophthalmol. 63(2), 128–132 (2015).
[Crossref] [PubMed]

G. Liu, O. Tan, S. S. Gao, A. D. Pechauer, B. Lee, C. D. Lu, J. G. Fujimoto, and D. Huang, “Postprocessing algorithms to minimize fixed-pattern artifact and reduce trigger jitter in swept source optical coherence tomography,” Opt. Express 23(8), 9824–9834 (2015).
[Crossref] [PubMed]

S. Sugiyama, Y. J. Hong, D. Kasaragod, S. Makita, S. Uematsu, Y. Ikuno, M. Miura, and Y. Yasuno, “Birefringence imaging of posterior eye by multi-functional Jones matrix optical coherence tomography,” Biomed. Opt. Express 6(12), 4951–4974 (2015).
[Crossref] [PubMed]

Q. Zhang, R. Lu, B. Wang, J. D. Messinger, C. A. Curcio, and X. Yao, “Functional optical coherence tomography enables in vivo physiological assessment of retinal rod and cone photoreceptors,” Sci. Rep. 5, 9595 (2015).
[Crossref] [PubMed]

A. D. Pechauer, D. Huang, and Y. Jia, “Detecting blood flow response to stimulation of the human eye,” BioMed Res. Int. 2015, 121973 (2015).
[Crossref] [PubMed]

2014 (6)

H. Kanda, T. Mihashi, T. Miyoshi, Y. Hirohara, T. Morimoto, Y. Terasawa, and T. Fujikado, “Evaluation of electrochemically treated bulk electrodes for a retinal prosthesis by examination of retinal intrinsic signals in cats,” Jpn. J. Ophthalmol. 58(4), 309–319 (2014).
[Crossref] [PubMed]

R. M. Werkmeister, M. Vietauer, C. Knopf, C. Fürnsinn, R. A. Leitgeb, H. Reitsamer, M. Gröschl, G. Garhöfer, W. Vilser, and L. Schmetterer, “Measurement of retinal blood flow in the rat by combining Doppler Fourier-domain optical coherence tomography with fundus imaging,” J. Biomed. Opt. 19(10), 106008 (2014).
[Crossref] [PubMed]

R. Told, S. Palkovits, A. Boltz, D. Schmidl, K. J. Napora, R. M. Werkmeister, H. Haslacher, S. Frantal, A. Popa-Cherecheanu, L. Schmetterer, and G. Garhöfer, “Flicker-induced retinal vasodilatation is not dependent on complement factor H polymorphism in healthy young subjects,” Acta Ophthalmol. 92(7), e540–e545 (2014).
[Crossref] [PubMed]

B. Wang, Q. Zhang, R. Lu, Y. Zhi, and X. Yao, “Functional optical coherence tomography reveals transient phototropic change of photoreceptor outer segments,” Opt. Lett. 39(24), 6923–6926 (2014).
[Crossref] [PubMed]

X. Liu, M. Kirby, and F. Zhao, “Motion analysis and removal in intensity variation based OCT angiography,” Biomed. Opt. Express 5(11), 3833–3847 (2014).
[Crossref] [PubMed]

T. E. Kornfield and E. A. Newman, “Regulation of blood flow in the retinal trilaminar vascular network,” J. Neurosci. 34(34), 11504–11513 (2014).
[Crossref] [PubMed]

2013 (10)

M. S. Mahmud, D. W. Cadotte, B. Vuong, C. Sun, T. W. Luk, A. Mariampillai, and V. X. Yang, “Review of speckle and phase variance optical coherence tomography to visualize microvascular networks,” J. Biomed. Opt. 18(5), 050901 (2013).
[Crossref] [PubMed]

H. Radhakrishnan and V. J. Srinivasan, “Multiparametric optical coherence tomography imaging of the inner retinal hemodynamic response to visual stimulation,” J. Biomed. Opt. 18(8), 086010 (2013).
[Crossref] [PubMed]

E. Wei, Y. Jia, O. Tan, B. Potsaid, J. J. Liu, W. Choi, J. G. Fujimoto, and D. Huang, “Parafoveal retinal vascular response to pattern visual stimulation assessed with OCT angiography,” PLoS One 8(12), e81343 (2013).
[Crossref] [PubMed]

X. Liu, Y. Huang, J. C. Ramella-Roman, S. A. Mathews, and J. U. Kang, “Quantitative transverse flow measurement using optical coherence tomography speckle decorrelation analysis,” Opt. Lett. 38(5), 805–807 (2013).
[Crossref] [PubMed]

E. A. Newman, “Functional hyperemia and mechanisms of neurovascular coupling in the retinal vasculature,” J. Cereb. Blood Flow Metab. 33(11), 1685–1695 (2013).
[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, 2644 (2013).
[PubMed]

B. Wang, R. Lu, Q. Zhang, Y. Jiang, and X. Yao, “En face optical coherence tomography of transient light response at photoreceptor outer segments in living frog eyecup,” Opt. Lett. 38(22), 4526–4529 (2013).
[Crossref] [PubMed]

S. Mrejen and R. F. Spaide, “Optical coherence tomography: imaging of the choroid and beyond,” Surv. Ophthalmol. 58(5), 387–429 (2013).
[Crossref] [PubMed]

J. Tokayer, Y. Jia, A. H. Dhalla, and D. Huang, “Blood flow velocity quantification using split-spectrum amplitude-decorrelation angiography with optical coherence tomography,” Biomed. Opt. Express 4(10), 1909–1924 (2013).
[Crossref] [PubMed]

C. Blatter, S. Coquoz, B. Grajciar, A. S. Singh, M. Bonesi, R. M. Werkmeister, L. Schmetterer, and R. A. Leitgeb, “Dove prism based rotating dual beam bidirectional Doppler OCT,” Biomed. Opt. Express 4(7), 1188–1203 (2013).
[Crossref] [PubMed]

2012 (3)

G. Garhofer, R. Werkmeister, N. Dragostinoff, and L. Schmetterer, “Retinal blood flow in healthy young subjects,” Invest. Ophthalmol. Vis. Sci. 53(2), 698–703 (2012).
[Crossref] [PubMed]

J. Kur, E. A. Newman, and T. Chan-Ling, “Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease,” Prog. Retin. Eye Res. 31(5), 377–406 (2012).
[Crossref] [PubMed]

J. C. Lau and R. A. Linsenmeier, “Oxygen consumption and distribution in the Long-Evans rat retina,” Exp. Eye Res. 102, 50–58 (2012).
[Crossref] [PubMed]

2011 (3)

M. Hammer, W. Vilser, T. Riemer, F. Liemt, S. Jentsch, J. Dawczynski, and D. Schweitzer, “Retinal venous oxygen saturation increases by flicker light stimulation,” Invest. Ophthalmol. Vis. Sci. 52(1), 274–277 (2011).
[Crossref] [PubMed]

I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
[Crossref] [PubMed]

Y. Wang, A. A. Fawzi, O. Tan, X. Zhang, and D. Huang, “Flicker-induced changes in retinal blood flow assessed by Doppler optical coherence tomography,” Biomed. Opt. Express 2(7), 1852–1860 (2011).
[Crossref] [PubMed]

2010 (4)

D. Attwell, A. M. Buchan, S. Charpak, M. Lauritzen, B. A. Macvicar, and E. A. Newman, “Glial and neuronal control of brain blood flow,” Nature 468(7321), 232–243 (2010).
[Crossref] [PubMed]

C. E. Riva, M. Geiser, and B. L. Petrig, “Ocular blood flow assessment using continuous laser Doppler flowmetry,” Acta Ophthalmol. 88(6), 622–629 (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).
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A. Mariampillai, M. K. Leung, M. Jarvi, B. A. Standish, K. Lee, B. C. Wilson, A. Vitkin, and V. X. Yang, “Optimized speckle variance OCT imaging of microvasculature,” Opt. Lett. 35(8), 1257–1259 (2010).
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2009 (1)

2008 (1)

2007 (3)

R. K. Wang, “Three-dimensional optical micro-angiography maps directional blood perfusion deep within microcirculation tissue beds in vivo,” Phys. Med. Biol. 52(23), N531–N537 (2007).
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Y. Yasuno, Y. Hong, S. Makita, M. Yamanari, M. Akiba, M. Miura, and T. Yatagai, “In vivo high-contrast imaging of deep posterior eye by 1-microm swept source optical coherence tomography and scattering optical coherence angiography,” Opt. Express 15(10), 6121–6139 (2007).
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P. Jeppesen, J. Sanye-Hajari, and T. Bek, “Increased blood pressure induces a diameter response of retinal arterioles that increases with decreasing arteriolar diameter,” Invest. Ophthalmol. Vis. Sci. 48(1), 328–331 (2007).
[Crossref] [PubMed]

2006 (3)

V. J. Srinivasan, M. Wojtkowski, J. G. Fujimoto, and J. S. Duker, “In vivo measurement of retinal physiology with high-speed ultrahigh-resolution optical coherence tomography,” Opt. Lett. 31(15), 2308–2310 (2006).
[Crossref] [PubMed]

K. Bizheva, R. Pflug, B. Hermann, B. Povazay, H. Sattmann, P. Qiu, E. Anger, H. Reitsamer, S. Popov, J. R. Taylor, A. Unterhuber, P. Ahnelt, and W. Drexler, “Optophysiology: depth-resolved probing of retinal physiology with functional ultrahigh-resolution optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 103(13), 5066–5071 (2006).
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E. Nagel, W. Vilser, A. Fink, T. Riemer, and I. Lanzl, “Blood pressure effects on retinal vessel diameter and flicker response: a 1.5-year follow-up,” Eur. J. Ophthalmol. 16(4), 560–565 (2006).
[PubMed]

2005 (3)

2004 (2)

G. Garhöfer, C. Zawinka, H. Resch, K. H. Huemer, G. T. Dorner, and L. Schmetterer, “Diffuse luminance flicker increases blood flow in major retinal arteries and veins,” Vision Res. 44(8), 833–838 (2004).
[Crossref] [PubMed]

Y. Ido, K. Chang, and J. R. Williamson, “NADH augments blood flow in physiologically activated retina and visual cortex,” Proc. Natl. Acad. Sci. U.S.A. 101(2), 653–658 (2004).
[Crossref] [PubMed]

2003 (1)

K. Polak, B. Wimpissinger, F. Berisha, M. Georgopoulos, and L. Schmetterer, “Effects of sildenafil on retinal blood flow and flicker-induced retinal vasodilatation in healthy subjects,” Invest. Ophthalmol. Vis. Sci. 44(11), 4872–4876 (2003).
[Crossref] [PubMed]

2002 (2)

G. Michelson, A. Patzelt, and J. Harazny, “Flickering light increases retinal blood flow,” Retina 22(3), 336–343 (2002).
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G. Garhöfer, K. H. Huemer, C. Zawinka, L. Schmetterer, and G. T. Dorner, “Influence of diffuse luminance flicker on choroidal and optic nerve head blood flow,” Curr. Eye Res. 24(2), 109–113 (2002).
[Crossref] [PubMed]

2001 (1)

D. Attwell and S. B. Laughlin, “An energy budget for signaling in the grey matter of the brain,” J. Cereb. Blood Flow Metab. 21(10), 1133–1145 (2001).
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1998 (1)

W. E. Lieb, “Color Doppler imaging of the eye and orbit,” Radiol. Clin. North Am. 36(6), 1059–1071 (1998).
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1994 (1)

A. J. Scheiner, C. E. Riva, K. Kazahaya, and B. L. Petrig, “Effect of flicker on macular blood flow assessed by the blue field simulation technique,” Invest. Ophthalmol. Vis. Sci. 35(9), 3436–3441 (1994).
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1991 (1)

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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1980 (1)

1969 (1)

J. V. Hodge, J. C. Parr, and G. F. Spears, “Comparison of methods of measuring vessel widths on retinal photographs and the effect of fluorescein injection on apparent retinal vessel calibers,” Am. J. Ophthalmol. 68(6), 1060–1068 (1969).
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Adhi, M.

M. Adhi, E. Badaro, J. J. Liu, M. F. Kraus, C. R. Baumal, A. J. Witkin, J. Hornegger, J. G. Fujimoto, J. S. Duker, and N. K. Waheed, “Three-dimensional enhanced imaging of vitreoretinal interface in diabetic retinopathy using swept-source optical coherence tomography,” Am. J. Ophthalmol. 162, 140–149 (2016).

Ahnelt, P.

K. Bizheva, R. Pflug, B. Hermann, B. Povazay, H. Sattmann, P. Qiu, E. Anger, H. Reitsamer, S. Popov, J. R. Taylor, A. Unterhuber, P. Ahnelt, and W. Drexler, “Optophysiology: depth-resolved probing of retinal physiology with functional ultrahigh-resolution optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 103(13), 5066–5071 (2006).
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Akiba, M.

Albiani, D.

J. Xu, S. Han, C. Balaratnasingam, Z. Mammo, K. S. Wong, S. Lee, M. Cua, M. Young, A. Kirker, D. Albiani, F. Forooghian, P. Mackenzie, A. Merkur, D. Y. Yu, and M. V. Sarunic, “Retinal angiography with real-time speckle variance optical coherence tomography,” Br. J. Ophthalmol. 99(10), 1315–1319 (2015).
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An, L.

Anderson, D. R.

I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
[Crossref] [PubMed]

Anger, E.

K. Bizheva, R. Pflug, B. Hermann, B. Povazay, H. Sattmann, P. Qiu, E. Anger, H. Reitsamer, S. Popov, J. R. Taylor, A. Unterhuber, P. Ahnelt, and W. Drexler, “Optophysiology: depth-resolved probing of retinal physiology with functional ultrahigh-resolution optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 103(13), 5066–5071 (2006).
[Crossref] [PubMed]

Attwell, D.

D. Attwell, A. M. Buchan, S. Charpak, M. Lauritzen, B. A. Macvicar, and E. A. Newman, “Glial and neuronal control of brain blood flow,” Nature 468(7321), 232–243 (2010).
[Crossref] [PubMed]

D. Attwell and S. B. Laughlin, “An energy budget for signaling in the grey matter of the brain,” J. Cereb. Blood Flow Metab. 21(10), 1133–1145 (2001).
[Crossref] [PubMed]

Badaro, E.

M. Adhi, E. Badaro, J. J. Liu, M. F. Kraus, C. R. Baumal, A. J. Witkin, J. Hornegger, J. G. Fujimoto, J. S. Duker, and N. K. Waheed, “Three-dimensional enhanced imaging of vitreoretinal interface in diabetic retinopathy using swept-source optical coherence tomography,” Am. J. Ophthalmol. 162, 140–149 (2016).

Balaratnasingam, C.

J. Xu, S. Han, C. Balaratnasingam, Z. Mammo, K. S. Wong, S. Lee, M. Cua, M. Young, A. Kirker, D. Albiani, F. Forooghian, P. Mackenzie, A. Merkur, D. Y. Yu, and M. V. Sarunic, “Retinal angiography with real-time speckle variance optical coherence tomography,” Br. J. Ophthalmol. 99(10), 1315–1319 (2015).
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Baran, U.

U. Baran and R. K. Wang, “Review of optical coherence tomography based angiography in neuroscience,” Neurophotonics 3(1), 010902 (2016).
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Barton, J.

Baumal, C. R.

M. Adhi, E. Badaro, J. J. Liu, M. F. Kraus, C. R. Baumal, A. J. Witkin, J. Hornegger, J. G. Fujimoto, J. S. Duker, and N. K. Waheed, “Three-dimensional enhanced imaging of vitreoretinal interface in diabetic retinopathy using swept-source optical coherence tomography,” Am. J. Ophthalmol. 162, 140–149 (2016).

Bek, T.

P. Jeppesen, J. Sanye-Hajari, and T. Bek, “Increased blood pressure induces a diameter response of retinal arterioles that increases with decreasing arteriolar diameter,” Invest. Ophthalmol. Vis. Sci. 48(1), 328–331 (2007).
[Crossref] [PubMed]

Berisha, F.

K. Polak, B. Wimpissinger, F. Berisha, M. Georgopoulos, and L. Schmetterer, “Effects of sildenafil on retinal blood flow and flicker-induced retinal vasodilatation in healthy subjects,” Invest. Ophthalmol. Vis. Sci. 44(11), 4872–4876 (2003).
[Crossref] [PubMed]

Bizheva, K.

K. Bizheva, R. Pflug, B. Hermann, B. Povazay, H. Sattmann, P. Qiu, E. Anger, H. Reitsamer, S. Popov, J. R. Taylor, A. Unterhuber, P. Ahnelt, and W. Drexler, “Optophysiology: depth-resolved probing of retinal physiology with functional ultrahigh-resolution optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 103(13), 5066–5071 (2006).
[Crossref] [PubMed]

Blatter, C.

Boltz, A.

R. Told, S. Palkovits, A. Boltz, D. Schmidl, K. J. Napora, R. M. Werkmeister, H. Haslacher, S. Frantal, A. Popa-Cherecheanu, L. Schmetterer, and G. Garhöfer, “Flicker-induced retinal vasodilatation is not dependent on complement factor H polymorphism in healthy young subjects,” Acta Ophthalmol. 92(7), e540–e545 (2014).
[Crossref] [PubMed]

Bonesi, M.

Buchan, A. M.

D. Attwell, A. M. Buchan, S. Charpak, M. Lauritzen, B. A. Macvicar, and E. A. Newman, “Glial and neuronal control of brain blood flow,” Nature 468(7321), 232–243 (2010).
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Cadotte, D. W.

M. S. Mahmud, D. W. Cadotte, B. Vuong, C. Sun, T. W. Luk, A. Mariampillai, and V. X. Yang, “Review of speckle and phase variance optical coherence tomography to visualize microvascular networks,” J. Biomed. Opt. 18(5), 050901 (2013).
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Capps, A. G.

Chang, K.

Y. Ido, K. Chang, and J. R. Williamson, “NADH augments blood flow in physiologically activated retina and visual cortex,” Proc. Natl. Acad. Sci. U.S.A. 101(2), 653–658 (2004).
[Crossref] [PubMed]

Chang, W.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Chan-Ling, T.

J. Kur, E. A. Newman, and T. Chan-Ling, “Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease,” Prog. Retin. Eye Res. 31(5), 377–406 (2012).
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Charpak, S.

D. Attwell, A. M. Buchan, S. Charpak, M. Lauritzen, B. A. Macvicar, and E. A. Newman, “Glial and neuronal control of brain blood flow,” Nature 468(7321), 232–243 (2010).
[Crossref] [PubMed]

Chen, C. L.

A. Zhang, Q. Zhang, C. L. Chen, and R. K. Wang, “Methods and algorithms for optical coherence tomography-based angiography: a review and comparison,” J. Biomed. Opt. 20(10), 100901 (2015).
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Chen, Y.

Choi, W.

E. Wei, Y. Jia, O. Tan, B. Potsaid, J. J. Liu, W. Choi, J. G. Fujimoto, and D. Huang, “Parafoveal retinal vascular response to pattern visual stimulation assessed with OCT angiography,” PLoS One 8(12), e81343 (2013).
[Crossref] [PubMed]

Coquoz, S.

Costa, V. P.

I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
[Crossref] [PubMed]

Cua, M.

J. Xu, S. Han, C. Balaratnasingam, Z. Mammo, K. S. Wong, S. Lee, M. Cua, M. Young, A. Kirker, D. Albiani, F. Forooghian, P. Mackenzie, A. Merkur, D. Y. Yu, and M. V. Sarunic, “Retinal angiography with real-time speckle variance optical coherence tomography,” Br. J. Ophthalmol. 99(10), 1315–1319 (2015).
[Crossref] [PubMed]

Curcio, C. A.

Q. Zhang, R. Lu, B. Wang, J. D. Messinger, C. A. Curcio, and X. Yao, “Functional optical coherence tomography enables in vivo physiological assessment of retinal rod and cone photoreceptors,” Sci. Rep. 5, 9595 (2015).
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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, 2644 (2013).
[PubMed]

Das, C.

C. L. Shields, J. Manalac, C. Das, J. Saktanasate, and J. A. Shields, “Review of spectral domain-enhanced depth imaging optical coherence tomography of tumors of the retina and retinal pigment epithelium in children and adults,” Indian J. Ophthalmol. 63(2), 128–132 (2015).
[Crossref] [PubMed]

Dawczynski, J.

M. Hammer, W. Vilser, T. Riemer, F. Liemt, S. Jentsch, J. Dawczynski, and D. Schweitzer, “Retinal venous oxygen saturation increases by flicker light stimulation,” Invest. Ophthalmol. Vis. Sci. 52(1), 274–277 (2011).
[Crossref] [PubMed]

Dhalla, A. H.

Dorner, G. T.

G. Garhöfer, C. Zawinka, H. Resch, K. H. Huemer, G. T. Dorner, and L. Schmetterer, “Diffuse luminance flicker increases blood flow in major retinal arteries and veins,” Vision Res. 44(8), 833–838 (2004).
[Crossref] [PubMed]

G. Garhöfer, K. H. Huemer, C. Zawinka, L. Schmetterer, and G. T. Dorner, “Influence of diffuse luminance flicker on choroidal and optic nerve head blood flow,” Curr. Eye Res. 24(2), 109–113 (2002).
[Crossref] [PubMed]

Dragostinoff, N.

G. Garhofer, R. Werkmeister, N. Dragostinoff, and L. Schmetterer, “Retinal blood flow in healthy young subjects,” Invest. Ophthalmol. Vis. Sci. 53(2), 698–703 (2012).
[Crossref] [PubMed]

Drexler, W.

K. Bizheva, R. Pflug, B. Hermann, B. Povazay, H. Sattmann, P. Qiu, E. Anger, H. Reitsamer, S. Popov, J. R. Taylor, A. Unterhuber, P. Ahnelt, and W. Drexler, “Optophysiology: depth-resolved probing of retinal physiology with functional ultrahigh-resolution optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 103(13), 5066–5071 (2006).
[Crossref] [PubMed]

Duker, J. S.

Falsini, B.

C. E. Riva, E. Logean, and B. Falsini, “Visually evoked hemodynamical response and assessment of neurovascular coupling in the optic nerve and retina,” Prog. Retin. Eye Res. 24(2), 183–215 (2005).
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Fawzi, A. A.

Fink, A.

E. Nagel, W. Vilser, A. Fink, T. Riemer, and I. Lanzl, “Blood pressure effects on retinal vessel diameter and flicker response: a 1.5-year follow-up,” Eur. J. Ophthalmol. 16(4), 560–565 (2006).
[PubMed]

Flotte, T.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Forooghian, F.

J. Xu, S. Han, C. Balaratnasingam, Z. Mammo, K. S. Wong, S. Lee, M. Cua, M. Young, A. Kirker, D. Albiani, F. Forooghian, P. Mackenzie, A. Merkur, D. Y. Yu, and M. V. Sarunic, “Retinal angiography with real-time speckle variance optical coherence tomography,” Br. J. Ophthalmol. 99(10), 1315–1319 (2015).
[Crossref] [PubMed]

Francis, P.

Frantal, S.

R. Told, S. Palkovits, A. Boltz, D. Schmidl, K. J. Napora, R. M. Werkmeister, H. Haslacher, S. Frantal, A. Popa-Cherecheanu, L. Schmetterer, and G. Garhöfer, “Flicker-induced retinal vasodilatation is not dependent on complement factor H polymorphism in healthy young subjects,” Acta Ophthalmol. 92(7), e540–e545 (2014).
[Crossref] [PubMed]

Frenkel, R. E. P.

I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
[Crossref] [PubMed]

Fujikado, T.

H. Kanda, T. Mihashi, T. Miyoshi, Y. Hirohara, T. Morimoto, Y. Terasawa, and T. Fujikado, “Evaluation of electrochemically treated bulk electrodes for a retinal prosthesis by examination of retinal intrinsic signals in cats,” Jpn. J. Ophthalmol. 58(4), 309–319 (2014).
[Crossref] [PubMed]

Fujimoto, J. G.

M. Adhi, E. Badaro, J. J. Liu, M. F. Kraus, C. R. Baumal, A. J. Witkin, J. Hornegger, J. G. Fujimoto, J. S. Duker, and N. K. Waheed, “Three-dimensional enhanced imaging of vitreoretinal interface in diabetic retinopathy using swept-source optical coherence tomography,” Am. J. Ophthalmol. 162, 140–149 (2016).

G. Liu, O. Tan, S. S. Gao, A. D. Pechauer, B. Lee, C. D. Lu, J. G. Fujimoto, and D. Huang, “Postprocessing algorithms to minimize fixed-pattern artifact and reduce trigger jitter in swept source optical coherence tomography,” Opt. Express 23(8), 9824–9834 (2015).
[Crossref] [PubMed]

E. Wei, Y. Jia, O. Tan, B. Potsaid, J. J. Liu, W. Choi, J. G. Fujimoto, and D. Huang, “Parafoveal retinal vascular response to pattern visual stimulation assessed with OCT angiography,” PLoS One 8(12), e81343 (2013).
[Crossref] [PubMed]

V. J. Srinivasan, Y. Chen, J. S. Duker, and J. G. Fujimoto, “In vivo functional imaging of intrinsic scattering changes in the human retina with high-speed ultrahigh resolution OCT,” Opt. Express 17(5), 3861–3877 (2009).
[Crossref] [PubMed]

V. J. Srinivasan, M. Wojtkowski, J. G. Fujimoto, and J. S. Duker, “In vivo measurement of retinal physiology with high-speed ultrahigh-resolution optical coherence tomography,” Opt. Lett. 31(15), 2308–2310 (2006).
[Crossref] [PubMed]

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Fürnsinn, C.

R. M. Werkmeister, M. Vietauer, C. Knopf, C. Fürnsinn, R. A. Leitgeb, H. Reitsamer, M. Gröschl, G. Garhöfer, W. Vilser, and L. Schmetterer, “Measurement of retinal blood flow in the rat by combining Doppler Fourier-domain optical coherence tomography with fundus imaging,” J. Biomed. Opt. 19(10), 106008 (2014).
[Crossref] [PubMed]

Gao, S. S.

Garhofer, G.

G. Garhofer, R. Werkmeister, N. Dragostinoff, and L. Schmetterer, “Retinal blood flow in healthy young subjects,” Invest. Ophthalmol. Vis. Sci. 53(2), 698–703 (2012).
[Crossref] [PubMed]

I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
[Crossref] [PubMed]

Garhöfer, G.

R. Told, S. Palkovits, A. Boltz, D. Schmidl, K. J. Napora, R. M. Werkmeister, H. Haslacher, S. Frantal, A. Popa-Cherecheanu, L. Schmetterer, and G. Garhöfer, “Flicker-induced retinal vasodilatation is not dependent on complement factor H polymorphism in healthy young subjects,” Acta Ophthalmol. 92(7), e540–e545 (2014).
[Crossref] [PubMed]

R. M. Werkmeister, M. Vietauer, C. Knopf, C. Fürnsinn, R. A. Leitgeb, H. Reitsamer, M. Gröschl, G. Garhöfer, W. Vilser, and L. Schmetterer, “Measurement of retinal blood flow in the rat by combining Doppler Fourier-domain optical coherence tomography with fundus imaging,” J. Biomed. Opt. 19(10), 106008 (2014).
[Crossref] [PubMed]

G. Garhöfer, C. Zawinka, H. Resch, K. H. Huemer, G. T. Dorner, and L. Schmetterer, “Diffuse luminance flicker increases blood flow in major retinal arteries and veins,” Vision Res. 44(8), 833–838 (2004).
[Crossref] [PubMed]

G. Garhöfer, K. H. Huemer, C. Zawinka, L. Schmetterer, and G. T. Dorner, “Influence of diffuse luminance flicker on choroidal and optic nerve head blood flow,” Curr. Eye Res. 24(2), 109–113 (2002).
[Crossref] [PubMed]

Geiser, M.

C. E. Riva, M. Geiser, and B. L. Petrig, “Ocular blood flow assessment using continuous laser Doppler flowmetry,” Acta Ophthalmol. 88(6), 622–629 (2010).
[Crossref] [PubMed]

George, J. S.

Georgopoulos, M.

K. Polak, B. Wimpissinger, F. Berisha, M. Georgopoulos, and L. Schmetterer, “Effects of sildenafil on retinal blood flow and flicker-induced retinal vasodilatation in healthy subjects,” Invest. Ophthalmol. Vis. Sci. 44(11), 4872–4876 (2003).
[Crossref] [PubMed]

Gorczynska, I.

Grajciar, B.

Gregory, K.

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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, 2644 (2013).
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E. Wei, Y. Jia, O. Tan, B. Potsaid, J. J. Liu, W. Choi, J. G. Fujimoto, and D. Huang, “Parafoveal retinal vascular response to pattern visual stimulation assessed with OCT angiography,” PLoS One 8(12), e81343 (2013).
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G. Garhöfer, C. Zawinka, H. Resch, K. H. Huemer, G. T. Dorner, and L. Schmetterer, “Diffuse luminance flicker increases blood flow in major retinal arteries and veins,” Vision Res. 44(8), 833–838 (2004).
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E. Wei, Y. Jia, O. Tan, B. Potsaid, J. J. Liu, W. Choi, J. G. Fujimoto, and D. Huang, “Parafoveal retinal vascular response to pattern visual stimulation assessed with OCT angiography,” PLoS One 8(12), e81343 (2013).
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Lee, S.

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M. Hammer, W. Vilser, T. Riemer, F. Liemt, S. Jentsch, J. Dawczynski, and D. Schweitzer, “Retinal venous oxygen saturation increases by flicker light stimulation,” Invest. Ophthalmol. Vis. Sci. 52(1), 274–277 (2011).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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J. C. Lau and R. A. Linsenmeier, “Oxygen consumption and distribution in the Long-Evans rat retina,” Exp. Eye Res. 102, 50–58 (2012).
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E. Wei, Y. Jia, O. Tan, B. Potsaid, J. J. Liu, W. Choi, J. G. Fujimoto, and D. Huang, “Parafoveal retinal vascular response to pattern visual stimulation assessed with OCT angiography,” PLoS One 8(12), e81343 (2013).
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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, 2644 (2013).
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D. Attwell, A. M. Buchan, S. Charpak, M. Lauritzen, B. A. Macvicar, and E. A. Newman, “Glial and neuronal control of brain blood flow,” Nature 468(7321), 232–243 (2010).
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Mihashi, T.

H. Kanda, T. Mihashi, T. Miyoshi, Y. Hirohara, T. Morimoto, Y. Terasawa, and T. Fujikado, “Evaluation of electrochemically treated bulk electrodes for a retinal prosthesis by examination of retinal intrinsic signals in cats,” Jpn. J. Ophthalmol. 58(4), 309–319 (2014).
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[Crossref] [PubMed]

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M. Hammer, W. Vilser, T. Riemer, F. Liemt, S. Jentsch, J. Dawczynski, and D. Schweitzer, “Retinal venous oxygen saturation increases by flicker light stimulation,” Invest. Ophthalmol. Vis. Sci. 52(1), 274–277 (2011).
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C. L. Shields, J. Manalac, C. Das, J. Saktanasate, and J. A. Shields, “Review of spectral domain-enhanced depth imaging optical coherence tomography of tumors of the retina and retinal pigment epithelium in children and adults,” Indian J. Ophthalmol. 63(2), 128–132 (2015).
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Spaide, R. F.

S. Mrejen and R. F. Spaide, “Optical coherence tomography: imaging of the choroid and beyond,” Surv. Ophthalmol. 58(5), 387–429 (2013).
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J. V. Hodge, J. C. Parr, and G. F. Spears, “Comparison of methods of measuring vessel widths on retinal photographs and the effect of fluorescein injection on apparent retinal vessel calibers,” Am. J. Ophthalmol. 68(6), 1060–1068 (1969).
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Stalmans, I.

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Stinson, W. G.

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Taylor, J. R.

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Told, R.

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Unterhuber, A.

K. Bizheva, R. Pflug, B. Hermann, B. Povazay, H. Sattmann, P. Qiu, E. Anger, H. Reitsamer, S. Popov, J. R. Taylor, A. Unterhuber, P. Ahnelt, and W. Drexler, “Optophysiology: depth-resolved probing of retinal physiology with functional ultrahigh-resolution optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 103(13), 5066–5071 (2006).
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R. M. Werkmeister, M. Vietauer, C. Knopf, C. Fürnsinn, R. A. Leitgeb, H. Reitsamer, M. Gröschl, G. Garhöfer, W. Vilser, and L. Schmetterer, “Measurement of retinal blood flow in the rat by combining Doppler Fourier-domain optical coherence tomography with fundus imaging,” J. Biomed. Opt. 19(10), 106008 (2014).
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R. M. Werkmeister, M. Vietauer, C. Knopf, C. Fürnsinn, R. A. Leitgeb, H. Reitsamer, M. Gröschl, G. Garhöfer, W. Vilser, and L. Schmetterer, “Measurement of retinal blood flow in the rat by combining Doppler Fourier-domain optical coherence tomography with fundus imaging,” J. Biomed. Opt. 19(10), 106008 (2014).
[Crossref] [PubMed]

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E. Nagel, W. Vilser, A. Fink, T. Riemer, and I. Lanzl, “Blood pressure effects on retinal vessel diameter and flicker response: a 1.5-year follow-up,” Eur. J. Ophthalmol. 16(4), 560–565 (2006).
[PubMed]

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Vuong, B.

M. S. Mahmud, D. W. Cadotte, B. Vuong, C. Sun, T. W. Luk, A. Mariampillai, and V. X. Yang, “Review of speckle and phase variance optical coherence tomography to visualize microvascular networks,” J. Biomed. Opt. 18(5), 050901 (2013).
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Figures (7)

Fig. 1
Fig. 1 Optical diagram of spectral domain optical coherence tomography. BM: beam splitter; CL: collimation lens; L1, L2, L3: lens; PC: polarization controller; SLD: super luminescent diode. The retinal stimulator consists of a narrow-band LED light (λ = 505 nm).
Fig. 2
Fig. 2 The data processing flow chart for an M-scan tomogram.
Fig. 3
Fig. 3 Conventional (A) and consecutive (B) speckle variance calculation methods.
Fig. 4
Fig. 4 Representative OCT B-scan (A1), projection fundus (A2), and angiography (A3) images of a mouse retina across the optic nerve head (ONH). Representative OCT B-scan (B1), projection fundus (B2), and angiography (B3) images recorded from the retinal area at a 2 mm distance from the ONH. NFL/GC: nerve fiber layer/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: inner/outer segments; RPE: retinal pigment epithelium; CH: choroid; ONH: optic nerve head. OCT fundus scale bar indicates 200 µm.
Fig. 5
Fig. 5 (A) B-scan OCT sequence; (B) B-scan angiography sequence; (C) Dynamic angiography change with the pre-stimulus baseline subtracted; (D) Enlarged picture of image A0; (E) Enlarged picture of image B5; (F) Enlarged pictures of images C2 (F1), C5(F2). Scale bar indicates 200 µm.
Fig. 6
Fig. 6 Flattened images of Fig. 5(A7) (A), Fig. 5(B7) (B), and Fig. 5(C7) (C). (D) Differential M-scan tomogram of dynamic angiographic changes, corresponding to Fig. 5(C). (E) Averaged angiographic changes of individual functional layers. Red and blue arrowheads indicate the onset and time-to-peak, respectively.
Fig. 7
Fig. 7 Three representative depth-resolved angiography results (A1, B1 and C1), differential M-scan tomograms (A2, B2 and C2) and averaged changes (A3, B3 and C3) of individual functional layers.

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