Abstract

Experimental characterization of blood flow in living organisms is crucial for understanding the development and function of cardiovascular systems, but there has been no technique reported for snapshot imaging of thick samples in large volumes with high precision. We have combined computational microscopy and the diffraction-free, self-bending property of Airy-beams to track fluorescent beads with sub-micron precision through an extended axial range (up to 600 \textmu m) within the flowing blood of 3 days post-fertilization (dpf) zebrafish embryos. The spatial trajectories of the tracer beads within flowing blood were recorded during transit through both cardinal and intersegmental vessels, and the trajectories were found to be consistent with the segmentation of the vasculature recorded using selective-plane illumination microscopy (SPIM). This method provides sufficiently precise spatial and temporal measurement of 3D blood flow that has the potential for directly probing key biomechanical quantities such as wall shear stress, as well as exploring the fluidic repercussions of cardiovascular diseases. Although we demonstrate the technique for blood flow, the ten-fold better enhancement in the depth range offers improvements in a wide range of applications of high-speed precision measurement of fluid flow, from microfluidics through measurement of cell dynamics to macroscopic aerosol characterizations.

Published by The Optical Society under the terms of the Creative Commons Attribution 4.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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References

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2018 (2)

2016 (3)

F. Boselli and J. Vermot, “Live imaging and modeling for shear stress quantification in the embryonic zebrafish heart,” Methods 94, 129–134 (2016).
[Crossref]

S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
[Crossref]

J. Steinwachs, C. Metzner, K. Skodzek, N. Lang, I. Thievessen, C. Mark, S. Münster, K. E. Aifantis, and B. Fabry, “Three-dimensional force microscopy of cells in biopolymer networks,” Nat. Methods 13, 171–176 (2016).
[Crossref]

2015 (1)

L. Fieramonti, E. A. Foglia, S. Malavasi, C. D’Andrea, G. Valentini, F. Cotelli, and A. Bassi, “Quantitative measurement of blood velocity in zebrafish with optical vector field tomography,” J. Biophotonics 8, 52–59 (2015).
[Crossref]

2014 (3)

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

S. Jia, J. C. Vaughan, and X. Zhuang, “Isotropic three-dimensional super-resolution imaging with a self-bending point spread function,” Nat. Photonics 8, 302–306 (2014).
[Crossref]

P. Zammit, A. R. Harvey, and G. Carles, “Extended depth-of-field imaging and ranging in a snapshot,” Optica 1, 209–216 (2014).
[Crossref]

2013 (3)

R. A. Jamison, C. R. Samarage, R. J. Bryson-Richardson, and A. Fouras, “In Vivo Wall Shear Measurements within the Developing Zebrafish Heart,” PLoS ONE 8, e75722 (2013).
[Crossref] [PubMed]

E. J. Gualda, T. Vale, P. Almada, J. A. Feijó, G. G. Martins, and N. Moreno, “OpenSpinMicroscopy: An open-source integrated microscopy platform,” Nat. Methods 10, 599–600 (2013).
[Crossref] [PubMed]

W. Trasischker, R. M. Werkmeister, S. Zotter, B. Baumann, T. Torzicky, M. Pircher, and C. K. Hitzenberger, “In vitro and in vivo three-dimensional velocity vector measurement by three-beam spectral-domain Doppler optical coherence tomography,” J. Biomed. Opt. 18, 116010 (2013).
[Crossref] [PubMed]

2012 (2)

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. St Croix, “High Resolution Imaging of Vascular Function in Zebrafish,” PLoS ONE 7, e44018 (2012).
[Crossref] [PubMed]

M. P. Craig, S. D. Gilday, D. Dabiri, and J. R. Hove, “An Optimized Method for Delivering Flow Tracer Particles to Intravital Fluid Environments in the Developing Zebrafish,” Zebrafish 9, 108–119 (2012).
[Crossref] [PubMed]

2010 (3)

J. Lu, F. Pereira, S. E. Fraser, and M. Gharib, “Three-dimensional real-time imaging of cardiac cell motions in living embryos,” J. biomedical optics 13, 014006 (2010).
[Crossref]

W. R. Legant, J. S. Miller, B. L. Blakely, D. M. Cohen, G. M. Genin, and C. S. Chen, “Measurement of mechanical tractions exerted by cells in three-dimensional matrices,” Nat. Methods 7, 969–971 (2010).
[Crossref] [PubMed]

M. Demenikov and A. R. Harvey, “Parametric blind-deconvolution algorithm to remove image artifacts in hybrid imaging systems,” Opt. Express 18, 18035–18040 (2010).
[PubMed]

2009 (4)

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106, 2995–2999 (2009).
[Crossref] [PubMed]

X. Pan, X. Shi, V. Korzh, H. Yu, and T. Wohland, “Line scan fluorescence correlation spectroscopy for three-dimensional microfluidic flow velocity measurements,” J. Biomed. Opt. 14, 024049 (2009).
[Crossref] [PubMed]

X. Shi, L. S. Teo, X. Pan, S. W. Chong, R. Kraut, V. Korzh, and T. Wohland, “Probing events with single molecule sensitivity in zebrafish and Drosophila embryos by fluorescence correlation spectroscopy,” Dev. Dyn. 238, 3156–3167 (2009).
[Crossref] [PubMed]

H. Hajjoul, S. Kocanova, I. Lassadi, K. Bystricky, and A. Bancaud, “Lab-on-Chip for fast 3D particle tracking in living cells,” Lab on a Chip 9, 3054 (2009).
[Crossref] [PubMed]

2008 (3)

J. Lu, F. Pereira, S. E. Fraser, and M. Gharib, “Three-dimensional real-time imaging of cardiac cell motions in living embryos,” J. Biomed. Opt. 13, 014006 (2008).
[Crossref] [PubMed]

S. Korzh, X. Pan, M. Garcia-Lecea, C. L. Winata, X. Pan, T. Wohland, V. Korzh, and Z. Gong, “Requirement of vasculogenesis and blood circulation in late stages of liver growth in zebrafish,” BMC Dev. Biol. 8, 1–15 (2008).
[Crossref]

N. V. Iftimia, D. X. Hammer, R. D. Ferguson, M. Mujat, D. Vu, and A. A. Ferrante, “Dual-beam fourier domain optical doppler tomography of zebrafish,” Opt. Express 16, 13624–13636 (2008).
[Crossref] [PubMed]

2007 (5)

K. Greger, J. Swoger, and E. H. K. Stelzer, “Basic building units and properties of a fluorescence single plane illumination microscope,” Rev. Sci. Instruments 78, 023705 (2007).
[Crossref]

G. J. Lieschke and P. D. Currie, “Animal models of human disease: zebrafish swim into view,” Nat. Rev. Genet. 8, 353–367 (2007).
[Crossref] [PubMed]

G. Kari, U. Rodeck, and A. P. Dicker, “Zebrafish: An emerging model system for human disease and drug discovery,” Clin. Pharmacol. & Ther. 82, 70–80 (2007).
[Crossref]

X. Pan, H. Yu, X. Shi, V. Korzh, and T. Wohland, “Characterization of flow direction in microchannels and zebrafish blood vessels by scanning fluorescence correlation spectroscopy,” J. Biomed. Opt. 12, 014034 (2007).
[Crossref] [PubMed]

L. Holtzer, T. Meckel, and T. Schmidt, “Nanometric three-dimensional tracking of individual quantum dots in cells,” Appl. Phys. Lett. 90, 053902 (2007).
[Crossref]

2006 (2)

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (storm),” Nat. Methods 3, 793–796 (2006).
[Crossref] [PubMed]

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751–753 (2006).
[Crossref] [PubMed]

2004 (1)

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[Crossref] [PubMed]

2003 (1)

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172–177 (2003).
[Crossref] [PubMed]

2002 (1)

F. Pereira and M. Gharib, “Defocusing digital particle image velocimetry and the three-dimensional characterization of two-phase flows,” Meas. Sci. Technol. 13, 683 (2002).
[Crossref]

2001 (2)

M. A. Mintun, B. N. Lundstrom, A. Z. Snyder, A. G. Vlassenko, G. L. Shulman, and M. E. Raichle, “Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data,” Proc. Natl. Acad. Sci. 98, 6859–6864 (2001).
[Crossref] [PubMed]

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. cerebral blood flow metabolism 21, 195–201 (2001).
[Crossref]

1996 (1)

J. C. Crocker and D. G. Grier, “Methods of digital video microscopy for colloidal studies,” J. Colloid InterfaceSci. 179, 298–310 (1996).
[Crossref]

1995 (2)

E. R. Dowski and W. T. Cathey, “Extended depth of field through wave-front coding,” Appl. Opt. 34, 1859–1866 (1995).
[Crossref] [PubMed]

M. Fujishima, S. Ibayashi, K. Fujii, and S. Mori, “Cerebral blood flow and brain function in hypertension,” Hypertens. Res. 18, 111–117 (1995).
[Crossref] [PubMed]

Acevedo-Bolton, G.

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172–177 (2003).
[Crossref] [PubMed]

Adams, R. H.

S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
[Crossref]

Aifantis, K. E.

J. Steinwachs, C. Metzner, K. Skodzek, N. Lang, I. Thievessen, C. Mark, S. Münster, K. E. Aifantis, and B. Fabry, “Three-dimensional force microscopy of cells in biopolymer networks,” Nat. Methods 13, 171–176 (2016).
[Crossref]

Almada, P.

E. J. Gualda, T. Vale, P. Almada, J. A. Feijó, G. G. Martins, and N. Moreno, “OpenSpinMicroscopy: An open-source integrated microscopy platform,” Nat. Methods 10, 599–600 (2013).
[Crossref] [PubMed]

Bancaud, A.

H. Hajjoul, S. Kocanova, I. Lassadi, K. Bystricky, and A. Bancaud, “Lab-on-Chip for fast 3D particle tracking in living cells,” Lab on a Chip 9, 3054 (2009).
[Crossref] [PubMed]

Bassi, A.

L. Fieramonti, E. A. Foglia, S. Malavasi, C. D’Andrea, G. Valentini, F. Cotelli, and A. Bassi, “Quantitative measurement of blood velocity in zebrafish with optical vector field tomography,” J. Biophotonics 8, 52–59 (2015).
[Crossref]

Bates, M.

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (storm),” Nat. Methods 3, 793–796 (2006).
[Crossref] [PubMed]

Baumann, B.

W. Trasischker, R. M. Werkmeister, S. Zotter, B. Baumann, T. Torzicky, M. Pircher, and C. K. Hitzenberger, “In vitro and in vivo three-dimensional velocity vector measurement by three-beam spectral-domain Doppler optical coherence tomography,” J. Biomed. Opt. 18, 116010 (2013).
[Crossref] [PubMed]

Biteen, J. S.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106, 2995–2999 (2009).
[Crossref] [PubMed]

Bixel, M. G.

S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
[Crossref]

Blakely, B. L.

W. R. Legant, J. S. Miller, B. L. Blakely, D. M. Cohen, G. M. Genin, and C. S. Chen, “Measurement of mechanical tractions exerted by cells in three-dimensional matrices,” Nat. Methods 7, 969–971 (2010).
[Crossref] [PubMed]

Blatter, C.

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

Boas, D. A.

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. cerebral blood flow metabolism 21, 195–201 (2001).
[Crossref]

Bolay, H.

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. cerebral blood flow metabolism 21, 195–201 (2001).
[Crossref]

Boselli, F.

F. Boselli and J. Vermot, “Live imaging and modeling for shear stress quantification in the embryonic zebrafish heart,” Methods 94, 129–134 (2016).
[Crossref]

Bryson-Richardson, R. J.

R. A. Jamison, C. R. Samarage, R. J. Bryson-Richardson, and A. Fouras, “In Vivo Wall Shear Measurements within the Developing Zebrafish Heart,” PLoS ONE 8, e75722 (2013).
[Crossref] [PubMed]

Bystricky, K.

H. Hajjoul, S. Kocanova, I. Lassadi, K. Bystricky, and A. Bancaud, “Lab-on-Chip for fast 3D particle tracking in living cells,” Lab on a Chip 9, 3054 (2009).
[Crossref] [PubMed]

Carles, G.

Cathey, W. T.

Chen, C. S.

W. R. Legant, J. S. Miller, B. L. Blakely, D. M. Cohen, G. M. Genin, and C. S. Chen, “Measurement of mechanical tractions exerted by cells in three-dimensional matrices,” Nat. Methods 7, 969–971 (2010).
[Crossref] [PubMed]

Chong, S. W.

X. Shi, L. S. Teo, X. Pan, S. W. Chong, R. Kraut, V. Korzh, and T. Wohland, “Probing events with single molecule sensitivity in zebrafish and Drosophila embryos by fluorescence correlation spectroscopy,” Dev. Dyn. 238, 3156–3167 (2009).
[Crossref] [PubMed]

Cohen, D. M.

W. R. Legant, J. S. Miller, B. L. Blakely, D. M. Cohen, G. M. Genin, and C. S. Chen, “Measurement of mechanical tractions exerted by cells in three-dimensional matrices,” Nat. Methods 7, 969–971 (2010).
[Crossref] [PubMed]

Cotelli, F.

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J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172–177 (2003).
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J. Lu, F. Pereira, S. E. Fraser, and M. Gharib, “Three-dimensional real-time imaging of cardiac cell motions in living embryos,” J. biomedical optics 13, 014006 (2010).
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J. Lu, F. Pereira, S. E. Fraser, and M. Gharib, “Three-dimensional real-time imaging of cardiac cell motions in living embryos,” J. Biomed. Opt. 13, 014006 (2008).
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J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172–177 (2003).
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Harvey, A. R.

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M. P. Craig, S. D. Gilday, D. Dabiri, and J. R. Hove, “An Optimized Method for Delivering Flow Tracer Particles to Intravital Fluid Environments in the Developing Zebrafish,” Zebrafish 9, 108–119 (2012).
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A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751–753 (2006).
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J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172–177 (2003).
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J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
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M. Fujishima, S. Ibayashi, K. Fujii, and S. Mori, “Cerebral blood flow and brain function in hypertension,” Hypertens. Res. 18, 111–117 (1995).
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R. A. Jamison, C. R. Samarage, R. J. Bryson-Richardson, and A. Fouras, “In Vivo Wall Shear Measurements within the Developing Zebrafish Heart,” PLoS ONE 8, e75722 (2013).
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H. Hajjoul, S. Kocanova, I. Lassadi, K. Bystricky, and A. Bancaud, “Lab-on-Chip for fast 3D particle tracking in living cells,” Lab on a Chip 9, 3054 (2009).
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S. Korzh, X. Pan, M. Garcia-Lecea, C. L. Winata, X. Pan, T. Wohland, V. Korzh, and Z. Gong, “Requirement of vasculogenesis and blood circulation in late stages of liver growth in zebrafish,” BMC Dev. Biol. 8, 1–15 (2008).
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X. Pan, X. Shi, V. Korzh, H. Yu, and T. Wohland, “Line scan fluorescence correlation spectroscopy for three-dimensional microfluidic flow velocity measurements,” J. Biomed. Opt. 14, 024049 (2009).
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S. Korzh, X. Pan, M. Garcia-Lecea, C. L. Winata, X. Pan, T. Wohland, V. Korzh, and Z. Gong, “Requirement of vasculogenesis and blood circulation in late stages of liver growth in zebrafish,” BMC Dev. Biol. 8, 1–15 (2008).
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X. Pan, H. Yu, X. Shi, V. Korzh, and T. Wohland, “Characterization of flow direction in microchannels and zebrafish blood vessels by scanning fluorescence correlation spectroscopy,” J. Biomed. Opt. 12, 014034 (2007).
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X. Shi, L. S. Teo, X. Pan, S. W. Chong, R. Kraut, V. Korzh, and T. Wohland, “Probing events with single molecule sensitivity in zebrafish and Drosophila embryos by fluorescence correlation spectroscopy,” Dev. Dyn. 238, 3156–3167 (2009).
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S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
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J. Steinwachs, C. Metzner, K. Skodzek, N. Lang, I. Thievessen, C. Mark, S. Münster, K. E. Aifantis, and B. Fabry, “Three-dimensional force microscopy of cells in biopolymer networks,” Nat. Methods 13, 171–176 (2016).
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H. Hajjoul, S. Kocanova, I. Lassadi, K. Bystricky, and A. Bancaud, “Lab-on-Chip for fast 3D particle tracking in living cells,” Lab on a Chip 9, 3054 (2009).
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W. R. Legant, J. S. Miller, B. L. Blakely, D. M. Cohen, G. M. Genin, and C. S. Chen, “Measurement of mechanical tractions exerted by cells in three-dimensional matrices,” Nat. Methods 7, 969–971 (2010).
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G. J. Lieschke and P. D. Currie, “Animal models of human disease: zebrafish swim into view,” Nat. Rev. Genet. 8, 353–367 (2007).
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S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
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S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
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S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106, 2995–2999 (2009).
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J. Lu, F. Pereira, S. E. Fraser, and M. Gharib, “Three-dimensional real-time imaging of cardiac cell motions in living embryos,” J. biomedical optics 13, 014006 (2010).
[Crossref]

J. Lu, F. Pereira, S. E. Fraser, and M. Gharib, “Three-dimensional real-time imaging of cardiac cell motions in living embryos,” J. Biomed. Opt. 13, 014006 (2008).
[Crossref] [PubMed]

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M. A. Mintun, B. N. Lundstrom, A. Z. Snyder, A. G. Vlassenko, G. L. Shulman, and M. E. Raichle, “Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data,” Proc. Natl. Acad. Sci. 98, 6859–6864 (2001).
[Crossref] [PubMed]

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L. Fieramonti, E. A. Foglia, S. Malavasi, C. D’Andrea, G. Valentini, F. Cotelli, and A. Bassi, “Quantitative measurement of blood velocity in zebrafish with optical vector field tomography,” J. Biophotonics 8, 52–59 (2015).
[Crossref]

Maniar, S.

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. St Croix, “High Resolution Imaging of Vascular Function in Zebrafish,” PLoS ONE 7, e44018 (2012).
[Crossref] [PubMed]

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J. Steinwachs, C. Metzner, K. Skodzek, N. Lang, I. Thievessen, C. Mark, S. Münster, K. E. Aifantis, and B. Fabry, “Three-dimensional force microscopy of cells in biopolymer networks,” Nat. Methods 13, 171–176 (2016).
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E. J. Gualda, T. Vale, P. Almada, J. A. Feijó, G. G. Martins, and N. Moreno, “OpenSpinMicroscopy: An open-source integrated microscopy platform,” Nat. Methods 10, 599–600 (2013).
[Crossref] [PubMed]

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L. Holtzer, T. Meckel, and T. Schmidt, “Nanometric three-dimensional tracking of individual quantum dots in cells,” Appl. Phys. Lett. 90, 053902 (2007).
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S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
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J. Steinwachs, C. Metzner, K. Skodzek, N. Lang, I. Thievessen, C. Mark, S. Münster, K. E. Aifantis, and B. Fabry, “Three-dimensional force microscopy of cells in biopolymer networks,” Nat. Methods 13, 171–176 (2016).
[Crossref]

Milia, C.

S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
[Crossref]

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W. R. Legant, J. S. Miller, B. L. Blakely, D. M. Cohen, G. M. Genin, and C. S. Chen, “Measurement of mechanical tractions exerted by cells in three-dimensional matrices,” Nat. Methods 7, 969–971 (2010).
[Crossref] [PubMed]

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M. A. Mintun, B. N. Lundstrom, A. Z. Snyder, A. G. Vlassenko, G. L. Shulman, and M. E. Raichle, “Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data,” Proc. Natl. Acad. Sci. 98, 6859–6864 (2001).
[Crossref] [PubMed]

Moerner, W. E.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106, 2995–2999 (2009).
[Crossref] [PubMed]

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E. J. Gualda, T. Vale, P. Almada, J. A. Feijó, G. G. Martins, and N. Moreno, “OpenSpinMicroscopy: An open-source integrated microscopy platform,” Nat. Methods 10, 599–600 (2013).
[Crossref] [PubMed]

Mori, S.

M. Fujishima, S. Ibayashi, K. Fujii, and S. Mori, “Cerebral blood flow and brain function in hypertension,” Hypertens. Res. 18, 111–117 (1995).
[Crossref] [PubMed]

Mosher, M.

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. St Croix, “High Resolution Imaging of Vascular Function in Zebrafish,” PLoS ONE 7, e44018 (2012).
[Crossref] [PubMed]

Moskowitz, M. A.

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. cerebral blood flow metabolism 21, 195–201 (2001).
[Crossref]

Mujat, M.

Münster, S.

J. Steinwachs, C. Metzner, K. Skodzek, N. Lang, I. Thievessen, C. Mark, S. Münster, K. E. Aifantis, and B. Fabry, “Three-dimensional force microscopy of cells in biopolymer networks,” Nat. Methods 13, 171–176 (2016).
[Crossref]

Nasiraei-Moghaddam, A.

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751–753 (2006).
[Crossref] [PubMed]

Pan, X.

X. Pan, X. Shi, V. Korzh, H. Yu, and T. Wohland, “Line scan fluorescence correlation spectroscopy for three-dimensional microfluidic flow velocity measurements,” J. Biomed. Opt. 14, 024049 (2009).
[Crossref] [PubMed]

X. Shi, L. S. Teo, X. Pan, S. W. Chong, R. Kraut, V. Korzh, and T. Wohland, “Probing events with single molecule sensitivity in zebrafish and Drosophila embryos by fluorescence correlation spectroscopy,” Dev. Dyn. 238, 3156–3167 (2009).
[Crossref] [PubMed]

S. Korzh, X. Pan, M. Garcia-Lecea, C. L. Winata, X. Pan, T. Wohland, V. Korzh, and Z. Gong, “Requirement of vasculogenesis and blood circulation in late stages of liver growth in zebrafish,” BMC Dev. Biol. 8, 1–15 (2008).
[Crossref]

S. Korzh, X. Pan, M. Garcia-Lecea, C. L. Winata, X. Pan, T. Wohland, V. Korzh, and Z. Gong, “Requirement of vasculogenesis and blood circulation in late stages of liver growth in zebrafish,” BMC Dev. Biol. 8, 1–15 (2008).
[Crossref]

X. Pan, H. Yu, X. Shi, V. Korzh, and T. Wohland, “Characterization of flow direction in microchannels and zebrafish blood vessels by scanning fluorescence correlation spectroscopy,” J. Biomed. Opt. 12, 014034 (2007).
[Crossref] [PubMed]

Pavani, S. R. P.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106, 2995–2999 (2009).
[Crossref] [PubMed]

Pereira, F.

J. Lu, F. Pereira, S. E. Fraser, and M. Gharib, “Three-dimensional real-time imaging of cardiac cell motions in living embryos,” J. biomedical optics 13, 014006 (2010).
[Crossref]

J. Lu, F. Pereira, S. E. Fraser, and M. Gharib, “Three-dimensional real-time imaging of cardiac cell motions in living embryos,” J. Biomed. Opt. 13, 014006 (2008).
[Crossref] [PubMed]

F. Pereira and M. Gharib, “Defocusing digital particle image velocimetry and the three-dimensional characterization of two-phase flows,” Meas. Sci. Technol. 13, 683 (2002).
[Crossref]

Piestun, R.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106, 2995–2999 (2009).
[Crossref] [PubMed]

Pircher, M.

W. Trasischker, R. M. Werkmeister, S. Zotter, B. Baumann, T. Torzicky, M. Pircher, and C. K. Hitzenberger, “In vitro and in vivo three-dimensional velocity vector measurement by three-beam spectral-domain Doppler optical coherence tomography,” J. Biomed. Opt. 18, 116010 (2013).
[Crossref] [PubMed]

Raichle, M. E.

M. A. Mintun, B. N. Lundstrom, A. Z. Snyder, A. G. Vlassenko, G. L. Shulman, and M. E. Raichle, “Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data,” Proc. Natl. Acad. Sci. 98, 6859–6864 (2001).
[Crossref] [PubMed]

Ramasamy, S. K.

S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
[Crossref]

Rodeck, U.

G. Kari, U. Rodeck, and A. P. Dicker, “Zebrafish: An emerging model system for human disease and drug discovery,” Clin. Pharmacol. & Ther. 82, 70–80 (2007).
[Crossref]

Roman, B. L.

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. St Croix, “High Resolution Imaging of Vascular Function in Zebrafish,” PLoS ONE 7, e44018 (2012).
[Crossref] [PubMed]

Roshthkari, S. J.

S. J. Roshthkari, “Analysis of blood flow during vascular development in chicken embryos,” Ph.D. thesis, McGill University (2011).

Rust, M. J.

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (storm),” Nat. Methods 3, 793–796 (2006).
[Crossref] [PubMed]

Samarage, C. R.

R. A. Jamison, C. R. Samarage, R. J. Bryson-Richardson, and A. Fouras, “In Vivo Wall Shear Measurements within the Developing Zebrafish Heart,” PLoS ONE 8, e75722 (2013).
[Crossref] [PubMed]

Santoro, M. M.

S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
[Crossref]

Schiller, M.

S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
[Crossref]

Schmetterer, L.

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

Schmidt, T.

L. Holtzer, T. Meckel, and T. Schmidt, “Nanometric three-dimensional tracking of individual quantum dots in cells,” Appl. Phys. Lett. 90, 053902 (2007).
[Crossref]

Shi, X.

X. Shi, L. S. Teo, X. Pan, S. W. Chong, R. Kraut, V. Korzh, and T. Wohland, “Probing events with single molecule sensitivity in zebrafish and Drosophila embryos by fluorescence correlation spectroscopy,” Dev. Dyn. 238, 3156–3167 (2009).
[Crossref] [PubMed]

X. Pan, X. Shi, V. Korzh, H. Yu, and T. Wohland, “Line scan fluorescence correlation spectroscopy for three-dimensional microfluidic flow velocity measurements,” J. Biomed. Opt. 14, 024049 (2009).
[Crossref] [PubMed]

X. Pan, H. Yu, X. Shi, V. Korzh, and T. Wohland, “Characterization of flow direction in microchannels and zebrafish blood vessels by scanning fluorescence correlation spectroscopy,” J. Biomed. Opt. 12, 014034 (2007).
[Crossref] [PubMed]

Shulman, G. L.

M. A. Mintun, B. N. Lundstrom, A. Z. Snyder, A. G. Vlassenko, G. L. Shulman, and M. E. Raichle, “Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data,” Proc. Natl. Acad. Sci. 98, 6859–6864 (2001).
[Crossref] [PubMed]

Skodzek, K.

J. Steinwachs, C. Metzner, K. Skodzek, N. Lang, I. Thievessen, C. Mark, S. Münster, K. E. Aifantis, and B. Fabry, “Three-dimensional force microscopy of cells in biopolymer networks,” Nat. Methods 13, 171–176 (2016).
[Crossref]

Snyder, A. Z.

M. A. Mintun, B. N. Lundstrom, A. Z. Snyder, A. G. Vlassenko, G. L. Shulman, and M. E. Raichle, “Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data,” Proc. Natl. Acad. Sci. 98, 6859–6864 (2001).
[Crossref] [PubMed]

Steinwachs, J.

J. Steinwachs, C. Metzner, K. Skodzek, N. Lang, I. Thievessen, C. Mark, S. Münster, K. E. Aifantis, and B. Fabry, “Three-dimensional force microscopy of cells in biopolymer networks,” Nat. Methods 13, 171–176 (2016).
[Crossref]

Stelzer, E. H. K.

K. Greger, J. Swoger, and E. H. K. Stelzer, “Basic building units and properties of a fluorescence single plane illumination microscope,” Rev. Sci. Instruments 78, 023705 (2007).
[Crossref]

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[Crossref] [PubMed]

Swoger, J.

K. Greger, J. Swoger, and E. H. K. Stelzer, “Basic building units and properties of a fluorescence single plane illumination microscope,” Rev. Sci. Instruments 78, 023705 (2007).
[Crossref]

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[Crossref] [PubMed]

Taylor, J. M.

Teo, L. S.

X. Shi, L. S. Teo, X. Pan, S. W. Chong, R. Kraut, V. Korzh, and T. Wohland, “Probing events with single molecule sensitivity in zebrafish and Drosophila embryos by fluorescence correlation spectroscopy,” Dev. Dyn. 238, 3156–3167 (2009).
[Crossref] [PubMed]

Thievessen, I.

J. Steinwachs, C. Metzner, K. Skodzek, N. Lang, I. Thievessen, C. Mark, S. Münster, K. E. Aifantis, and B. Fabry, “Three-dimensional force microscopy of cells in biopolymer networks,” Nat. Methods 13, 171–176 (2016).
[Crossref]

Thompson, M. A.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106, 2995–2999 (2009).
[Crossref] [PubMed]

Torzicky, T.

W. Trasischker, R. M. Werkmeister, S. Zotter, B. Baumann, T. Torzicky, M. Pircher, and C. K. Hitzenberger, “In vitro and in vivo three-dimensional velocity vector measurement by three-beam spectral-domain Doppler optical coherence tomography,” J. Biomed. Opt. 18, 116010 (2013).
[Crossref] [PubMed]

Trasischker, W.

W. Trasischker, R. M. Werkmeister, S. Zotter, B. Baumann, T. Torzicky, M. Pircher, and C. K. Hitzenberger, “In vitro and in vivo three-dimensional velocity vector measurement by three-beam spectral-domain Doppler optical coherence tomography,” J. Biomed. Opt. 18, 116010 (2013).
[Crossref] [PubMed]

Tsai, H.-J.

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751–753 (2006).
[Crossref] [PubMed]

Tsang, M.

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. St Croix, “High Resolution Imaging of Vascular Function in Zebrafish,” PLoS ONE 7, e44018 (2012).
[Crossref] [PubMed]

Twieg, R. J.

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106, 2995–2999 (2009).
[Crossref] [PubMed]

Vale, T.

E. J. Gualda, T. Vale, P. Almada, J. A. Feijó, G. G. Martins, and N. Moreno, “OpenSpinMicroscopy: An open-source integrated microscopy platform,” Nat. Methods 10, 599–600 (2013).
[Crossref] [PubMed]

Valentini, G.

L. Fieramonti, E. A. Foglia, S. Malavasi, C. D’Andrea, G. Valentini, F. Cotelli, and A. Bassi, “Quantitative measurement of blood velocity in zebrafish with optical vector field tomography,” J. Biophotonics 8, 52–59 (2015).
[Crossref]

Vaughan, J. C.

S. Jia, J. C. Vaughan, and X. Zhuang, “Isotropic three-dimensional super-resolution imaging with a self-bending point spread function,” Nat. Photonics 8, 302–306 (2014).
[Crossref]

Vermot, J.

F. Boselli and J. Vermot, “Live imaging and modeling for shear stress quantification in the embryonic zebrafish heart,” Methods 94, 129–134 (2016).
[Crossref]

Vlassenko, A. G.

M. A. Mintun, B. N. Lundstrom, A. Z. Snyder, A. G. Vlassenko, G. L. Shulman, and M. E. Raichle, “Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data,” Proc. Natl. Acad. Sci. 98, 6859–6864 (2001).
[Crossref] [PubMed]

Vu, D.

Watkins, S. C.

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. St Croix, “High Resolution Imaging of Vascular Function in Zebrafish,” PLoS ONE 7, e44018 (2012).
[Crossref] [PubMed]

Werkmeister, R. M.

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

W. Trasischker, R. M. Werkmeister, S. Zotter, B. Baumann, T. Torzicky, M. Pircher, and C. K. Hitzenberger, “In vitro and in vivo three-dimensional velocity vector measurement by three-beam spectral-domain Doppler optical coherence tomography,” J. Biomed. Opt. 18, 116010 (2013).
[Crossref] [PubMed]

Winata, C. L.

S. Korzh, X. Pan, M. Garcia-Lecea, C. L. Winata, X. Pan, T. Wohland, V. Korzh, and Z. Gong, “Requirement of vasculogenesis and blood circulation in late stages of liver growth in zebrafish,” BMC Dev. Biol. 8, 1–15 (2008).
[Crossref]

Wittbrodt, J.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[Crossref] [PubMed]

Wohland, T.

X. Shi, L. S. Teo, X. Pan, S. W. Chong, R. Kraut, V. Korzh, and T. Wohland, “Probing events with single molecule sensitivity in zebrafish and Drosophila embryos by fluorescence correlation spectroscopy,” Dev. Dyn. 238, 3156–3167 (2009).
[Crossref] [PubMed]

X. Pan, X. Shi, V. Korzh, H. Yu, and T. Wohland, “Line scan fluorescence correlation spectroscopy for three-dimensional microfluidic flow velocity measurements,” J. Biomed. Opt. 14, 024049 (2009).
[Crossref] [PubMed]

S. Korzh, X. Pan, M. Garcia-Lecea, C. L. Winata, X. Pan, T. Wohland, V. Korzh, and Z. Gong, “Requirement of vasculogenesis and blood circulation in late stages of liver growth in zebrafish,” BMC Dev. Biol. 8, 1–15 (2008).
[Crossref]

X. Pan, H. Yu, X. Shi, V. Korzh, and T. Wohland, “Characterization of flow direction in microchannels and zebrafish blood vessels by scanning fluorescence correlation spectroscopy,” J. Biomed. Opt. 12, 014034 (2007).
[Crossref] [PubMed]

Yu, H.

X. Pan, X. Shi, V. Korzh, H. Yu, and T. Wohland, “Line scan fluorescence correlation spectroscopy for three-dimensional microfluidic flow velocity measurements,” J. Biomed. Opt. 14, 024049 (2009).
[Crossref] [PubMed]

X. Pan, H. Yu, X. Shi, V. Korzh, and T. Wohland, “Characterization of flow direction in microchannels and zebrafish blood vessels by scanning fluorescence correlation spectroscopy,” J. Biomed. Opt. 12, 014034 (2007).
[Crossref] [PubMed]

Zammit, P.

Zeuschner, D.

S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
[Crossref]

Zhou, Y.

Zhuang, X.

S. Jia, J. C. Vaughan, and X. Zhuang, “Isotropic three-dimensional super-resolution imaging with a self-bending point spread function,” Nat. Photonics 8, 302–306 (2014).
[Crossref]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (storm),” Nat. Methods 3, 793–796 (2006).
[Crossref] [PubMed]

Zickus, V.

Zotter, S.

W. Trasischker, R. M. Werkmeister, S. Zotter, B. Baumann, T. Torzicky, M. Pircher, and C. K. Hitzenberger, “In vitro and in vivo three-dimensional velocity vector measurement by three-beam spectral-domain Doppler optical coherence tomography,” J. Biomed. Opt. 18, 116010 (2013).
[Crossref] [PubMed]

Appl. Opt. (1)

Appl. Phys. Lett. (1)

L. Holtzer, T. Meckel, and T. Schmidt, “Nanometric three-dimensional tracking of individual quantum dots in cells,” Appl. Phys. Lett. 90, 053902 (2007).
[Crossref]

Biomed. Opt. Express (1)

BMC Dev. Biol. (1)

S. Korzh, X. Pan, M. Garcia-Lecea, C. L. Winata, X. Pan, T. Wohland, V. Korzh, and Z. Gong, “Requirement of vasculogenesis and blood circulation in late stages of liver growth in zebrafish,” BMC Dev. Biol. 8, 1–15 (2008).
[Crossref]

Clin. Pharmacol. & Ther. (1)

G. Kari, U. Rodeck, and A. P. Dicker, “Zebrafish: An emerging model system for human disease and drug discovery,” Clin. Pharmacol. & Ther. 82, 70–80 (2007).
[Crossref]

Dev. Dyn. (1)

X. Shi, L. S. Teo, X. Pan, S. W. Chong, R. Kraut, V. Korzh, and T. Wohland, “Probing events with single molecule sensitivity in zebrafish and Drosophila embryos by fluorescence correlation spectroscopy,” Dev. Dyn. 238, 3156–3167 (2009).
[Crossref] [PubMed]

Hypertens. Res. (1)

M. Fujishima, S. Ibayashi, K. Fujii, and S. Mori, “Cerebral blood flow and brain function in hypertension,” Hypertens. Res. 18, 111–117 (1995).
[Crossref] [PubMed]

J. Biomed. Opt. (4)

X. Pan, H. Yu, X. Shi, V. Korzh, and T. Wohland, “Characterization of flow direction in microchannels and zebrafish blood vessels by scanning fluorescence correlation spectroscopy,” J. Biomed. Opt. 12, 014034 (2007).
[Crossref] [PubMed]

X. Pan, X. Shi, V. Korzh, H. Yu, and T. Wohland, “Line scan fluorescence correlation spectroscopy for three-dimensional microfluidic flow velocity measurements,” J. Biomed. Opt. 14, 024049 (2009).
[Crossref] [PubMed]

W. Trasischker, R. M. Werkmeister, S. Zotter, B. Baumann, T. Torzicky, M. Pircher, and C. K. Hitzenberger, “In vitro and in vivo three-dimensional velocity vector measurement by three-beam spectral-domain Doppler optical coherence tomography,” J. Biomed. Opt. 18, 116010 (2013).
[Crossref] [PubMed]

J. Lu, F. Pereira, S. E. Fraser, and M. Gharib, “Three-dimensional real-time imaging of cardiac cell motions in living embryos,” J. Biomed. Opt. 13, 014006 (2008).
[Crossref] [PubMed]

J. biomedical optics (1)

J. Lu, F. Pereira, S. E. Fraser, and M. Gharib, “Three-dimensional real-time imaging of cardiac cell motions in living embryos,” J. biomedical optics 13, 014006 (2010).
[Crossref]

J. Biophotonics (1)

L. Fieramonti, E. A. Foglia, S. Malavasi, C. D’Andrea, G. Valentini, F. Cotelli, and A. Bassi, “Quantitative measurement of blood velocity in zebrafish with optical vector field tomography,” J. Biophotonics 8, 52–59 (2015).
[Crossref]

J. cerebral blood flow metabolism (1)

A. K. Dunn, H. Bolay, M. A. Moskowitz, and D. A. Boas, “Dynamic imaging of cerebral blood flow using laser speckle,” J. cerebral blood flow metabolism 21, 195–201 (2001).
[Crossref]

J. Colloid InterfaceSci. (1)

J. C. Crocker and D. G. Grier, “Methods of digital video microscopy for colloidal studies,” J. Colloid InterfaceSci. 179, 298–310 (1996).
[Crossref]

Lab on a Chip (1)

H. Hajjoul, S. Kocanova, I. Lassadi, K. Bystricky, and A. Bancaud, “Lab-on-Chip for fast 3D particle tracking in living cells,” Lab on a Chip 9, 3054 (2009).
[Crossref] [PubMed]

Meas. Sci. Technol. (1)

F. Pereira and M. Gharib, “Defocusing digital particle image velocimetry and the three-dimensional characterization of two-phase flows,” Meas. Sci. Technol. 13, 683 (2002).
[Crossref]

Methods (1)

F. Boselli and J. Vermot, “Live imaging and modeling for shear stress quantification in the embryonic zebrafish heart,” Methods 94, 129–134 (2016).
[Crossref]

Nat. Commun. (1)

S. K. Ramasamy, A. P. Kusumbe, M. Schiller, D. Zeuschner, M. G. Bixel, C. Milia, J. Gamrekelashvili, A. Limbourg, A. Medvinsky, M. M. Santoro, F. P. Limbourg, and R. H. Adams, “Blood flow controls bone vascular function and osteogenesis,” Nat. Commun. 7, 1–13 (2016).
[Crossref]

Nat. Methods (4)

E. J. Gualda, T. Vale, P. Almada, J. A. Feijó, G. G. Martins, and N. Moreno, “OpenSpinMicroscopy: An open-source integrated microscopy platform,” Nat. Methods 10, 599–600 (2013).
[Crossref] [PubMed]

W. R. Legant, J. S. Miller, B. L. Blakely, D. M. Cohen, G. M. Genin, and C. S. Chen, “Measurement of mechanical tractions exerted by cells in three-dimensional matrices,” Nat. Methods 7, 969–971 (2010).
[Crossref] [PubMed]

J. Steinwachs, C. Metzner, K. Skodzek, N. Lang, I. Thievessen, C. Mark, S. Münster, K. E. Aifantis, and B. Fabry, “Three-dimensional force microscopy of cells in biopolymer networks,” Nat. Methods 13, 171–176 (2016).
[Crossref]

M. J. Rust, M. Bates, and X. Zhuang, “Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (storm),” Nat. Methods 3, 793–796 (2006).
[Crossref] [PubMed]

Nat. Photonics (1)

S. Jia, J. C. Vaughan, and X. Zhuang, “Isotropic three-dimensional super-resolution imaging with a self-bending point spread function,” Nat. Photonics 8, 302–306 (2014).
[Crossref]

Nat. Rev. Genet. (1)

G. J. Lieschke and P. D. Currie, “Animal models of human disease: zebrafish swim into view,” Nat. Rev. Genet. 8, 353–367 (2007).
[Crossref] [PubMed]

Nature (1)

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421, 172–177 (2003).
[Crossref] [PubMed]

Opt. Express (3)

Optica (1)

PLoS ONE (2)

R. A. Jamison, C. R. Samarage, R. J. Bryson-Richardson, and A. Fouras, “In Vivo Wall Shear Measurements within the Developing Zebrafish Heart,” PLoS ONE 8, e75722 (2013).
[Crossref] [PubMed]

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. St Croix, “High Resolution Imaging of Vascular Function in Zebrafish,” PLoS ONE 7, e44018 (2012).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. (1)

M. A. Mintun, B. N. Lundstrom, A. Z. Snyder, A. G. Vlassenko, G. L. Shulman, and M. E. Raichle, “Blood flow and oxygen delivery to human brain during functional activity: Theoretical modeling and experimental data,” Proc. Natl. Acad. Sci. 98, 6859–6864 (2001).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (1)

S. R. P. Pavani, M. A. Thompson, J. S. Biteen, S. J. Lord, N. Liu, R. J. Twieg, R. Piestun, and W. E. Moerner, “Three-dimensional, single-molecule fluorescence imaging beyond the diffraction limit by using a double-helix point spread function,” Proc. Natl. Acad. Sci. U.S.A. 106, 2995–2999 (2009).
[Crossref] [PubMed]

Prog. Retin. Eye Res. (1)

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

Rev. Sci. Instruments (1)

K. Greger, J. Swoger, and E. H. K. Stelzer, “Basic building units and properties of a fluorescence single plane illumination microscope,” Rev. Sci. Instruments 78, 023705 (2007).
[Crossref]

Science (2)

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305, 1007–1009 (2004).
[Crossref] [PubMed]

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H.-J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312, 751–753 (2006).
[Crossref] [PubMed]

Zebrafish (1)

M. P. Craig, S. D. Gilday, D. Dabiri, and J. R. Hove, “An Optimized Method for Delivering Flow Tracer Particles to Intravital Fluid Environments in the Developing Zebrafish,” Zebrafish 9, 108–119 (2012).
[Crossref] [PubMed]

Other (2)

Y. Zhou, V. Zickus, P. Zammit, J. M. Taylor, and A. R. Harvey, “Blood flow measurements using airy-ckm,” http://dx.doi.org/10.5525/gla.researchdata.619 (2018).

S. J. Roshthkari, “Analysis of blood flow during vascular development in chicken embryos,” Ph.D. thesis, McGill University (2011).

Supplementary Material (4)

NameDescription
» Dataset 1       High-speed extended-volume blood flow measurement using engineered point-spread function
» Visualization 1       This video shows the PSF-encoded images of microinjected tracer beads in a 3dpf zebrafish (on the left) and corresponding 3D reconstructed tracer trajectories (on the right). The region of interest is near the cloaca of the zebrafish and the frame ra
» Visualization 2       Multiviews of a composite image showing detected tracer locations (green spheres) embedded within a surface rendering (red) of the 3D blood vessel structure obtained from quasi-simultaneous SPIM imaging.
» Visualization 3       Superimposition of bead locations (green) obtained using Airy-CKM technique and surface rendering of blood vessels (red) obtained using SPIM.

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Figures (6)

Fig. 1
Fig. 1 (a) Airy-beam PSFs generated with an α = 7 cubic phase mask over a depth range of 200 μm, with the red curve indicating the accelerating translation along the image diagonal. (b) Corresponding recovered PSFs using Wiener deconvolution with the in-focus PSF used as the deconvolution kernel. (c) Schematic of the experimental setup. The dashed orange box indicates the the particle tracking arm. A 0.5 NA, 20 × CFI Plan Fluor objective was used to image the tracer particles. A cubic phase mask was placed at the re-imaged pupil plane of a 4-f relay system. The lateral beam splitter then generates two images of the same scene on the same camera sensor (camera 1), but with two opposite defocus offsets. Epi illumination was used for the 3D particle tracking, with a 532 nm solid state laser as the light source. The dashed blue box shows the SPIM illumination arm used for validation imaging (acquired with camera 2). The light sheet was launched with a 10 ×, 0.3 NA CFI Plan Fluor objective and a 75 mm cylindrical lens. The sample was mounted in a square glass capillary on a piezo z stage. CPM: cubic phase mask; LBS: lateral beam splitter.
Fig. 2
Fig. 2 (a) Epifluorescence image of a flk1:GFP zebrafish embryo, showing the region of interest (ROI) used in our experiment. CV: cardinal vein, CA: cardinal artery, ISV: intersegmental vessel. (b) PSF encoded image showing 1 μm fluorescent tracer beads flowing within the ROI. (c) 3D trajectories of tracers within cardinal and intersegmental vessels of zebrafish, reconstructed from 2000 frames. Color-coding is used to distinguish the trajectories of each tracer particle. Supplementary Visualization 1 shows the tracers flowing with the blood in real-time, along with a 3D reconstruction of tracer trajectories.
Fig. 3
Fig. 3 Temporal and spatial variation of the tracer velocity. (a) Velocity of a tracer flowing within the cardinal artery. (b) Fourier spectrum of the velocity profile in (a). (c) Velocity of a tracer that enters an intersegmental vessel from the cardinal vessel. (d) 3D trajectory of the tracer in (c), color-coded for depth.
Fig. 4
Fig. 4 Composite images showing detected tracer locations (green spheres) embedded within a surface rendering (red) of the 3D blood vessel structure obtained from quasi-simultaneous SPIM imaging ( Dataset 1 [35]). (a) View of several tail segments; (b) detail of a vessel junction. The recovered bead coordinates lie within the blood vessels, demonstrating that the Airy-CKM method is correctly identifying the 3D coordinates of the beads. Supplementary Visualization 2& Visualization 3 show multi-view animations of the composite image and beads flowing within SPIM-reconstructed blood vessels.
Fig. 5
Fig. 5 (a) Trajectory of a bead flowing though the dorsal aorta. Errors in z indicate non-uniformity in the tissue refractive index. (b) Injection area. The micro-injection was performed using a stereo microscope at the common cardinal vein (CCV) indicated with the red curve. Calibration curves of the 20×, 0.5NA system with an α = 7 phase mask. (c) Lookup table relating the two-channel disparity to the z coordinate of the particle. (d) Image translations in x and y as a function of z, which are used to correct the image shifts once z is deduced.
Fig. 6
Fig. 6 Algorithm used for 3D particle localization using the Airy-CKM method. I C + and I C are the recorded images from both channels; *−1 refers to the Wiener deconvolution operator; PSF focus + and PSF focus are PSFs that have been pre-recorded for a fluorescent bead locating at the nominal object plane; I C + and I C are recovered images by Wiener deconvolution; Δx and Δy are the shifts in the x and y coordinates due to the PSF translations.

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