Abstract

We present SPIM-μPIV as a flow imaging system, capable of measuring in vivo flow information with 3D micron-scale resolution. Our system was validated using a phantom experiment consisting of a flow of beads in a 50 μm diameter FEP tube. Then, with the help of optical gating techniques, we obtained 3D + time flow fields throughout the full heartbeat in a ∼3 day old zebrafish larva using fluorescent red blood cells as tracer particles. From this we were able to recover 3D flow fields at 31 separate phases in the heartbeat. From our measurements of this specimen, we found the net pumped blood volume through the atrium to be 0.239 nL per beat. SPIM-μPIV enables high quality in vivo measurements of flow fields that will be valuable for studies of heart function and fluid-structure interaction in a range of small-animal models.

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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    [Crossref]
  2. F. Boselli and J. Vermot, “Live imaging and modeling for shear stress quantification in the embryonic zebrafish heart,” Methods 94, 129–134 (2016).
    [Crossref]
  3. F. Boselli, J.B. Freund, and J. Vermot, “Blood flow mechanics in cardiovascular development,” Cellular and Molecular Life Sciences 72, 2545–2559 (2015).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  5. Y. Wang and G. Yao, “Optical tractography of the mouse heart using polarization-sensitive optical coherence tomography,” Biomed. Opt. Express 4, 2540–2545 (2013).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref]
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    [Crossref] [PubMed]
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    [Crossref]
  15. R. Adrian, “Particle-imaging techniques for experimental fluid mechanics,” Annual Review of Fluid Mechanics 23, 261–304 (1991).
    [Crossref]
  16. R. J. Adrian and J. Westerweel, Particle Image Velocimetry (Cambridge University Press, 2011).
  17. M. Raffel, C. E. Willert, S. T. Wereley, and J. Kompenhans, Particle Image Velocimetry: A Practical Guide (Springer, 2007).
  18. C. Poelma, A. Kloosterman, B. P. B. Hierck, and J. Westerweel, “Accurate blood flow measurements: are artificial tracers necessary?” PloS one 7, e45247 (2012).
    [Crossref] [PubMed]
  19. J. M. Taylor, J. M. Girkin, and G. D. Love, “High-resolution 3d optical microscopy inside the beating zebrafish heart using prospective optical gating,” Biomed. Opt. Express 3, 3043–3053 (2012).
    [Crossref] [PubMed]
  20. M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  23. K. Greger, J. Swoger, and E. H. K. Stelzer, “Basic building units and properties of a fluorescence single plane illumination microscope,” Review of Scientific Instruments 78, 1–7 (2007).
    [Crossref]
  24. J. Westerweel, P. Geelhoed, and R. Lindken, “Single-pixel resolution ensemble correlation for micro-PIV applications,” Experiments in Fluids 37, 375–384 (2004).
    [Crossref]
  25. Z. J. Taylor, R. Gurka, G. A. Kopp, and A. Liberzon, “Long-duration time-resolved piv to study unsteady aerodynamics,” IEEE Transactions on Instrumentation and Measurement 59, 3262–3269 (2010).
    [Crossref]
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  27. 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]
  28. R. Kopp, T. Schwerte, and B. Pelster, “Cardiac performance in the zebrafish breakdance mutant,” The Journal of Experimental Biology 208, 2123–2134 (2005).
    [Crossref] [PubMed]
  29. J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
    [Crossref] [PubMed]
  30. A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
    [Crossref] [PubMed]
  31. C. A. Schneider, W.S. Rasband, and K.W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis”, Nature Methods 9, 671–675 (2012).
    [Crossref] [PubMed]
  32. P. Ramachandran and G. Varoquaux, “Mayavi: 3D Visualization of Scientific Data”, IEEE Computing in Science & Engineering 13, 40–51 (2011)
    [Crossref]
  33. S. J. Williams, C. Park, and S. T. Wereley, “Advances and applications on microfluidic velocimetry techniques,” Microfluid. Nanofluid. 8, 709–726 (2010)
    [Crossref]

2016 (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]

2015 (3)

F. Boselli, J.B. Freund, and J. Vermot, “Blood flow mechanics in cardiovascular development,” Cellular and Molecular Life Sciences 72, 2545–2559 (2015).
[Crossref] [PubMed]

B. Wieneke, “PIV uncertainty quantification from correlation statistics,” Measurement Science and Technology 26, 074002 (2015).
[Crossref]

A. Lopez-Perez, R. Sebastian, and J. M. Ferrero, “Three-dimensional cardiac computational modelling: methods, features and applications,” BioMedical Engineering OnLine 14, 35 (2015).
[Crossref] [PubMed]

2014 (2)

J. M. Taylor, “Optically gated beating-heart imaging,” Frontiers in Physiology 5, 481 (2014).
[Crossref]

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

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]

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Y. Wang and G. Yao, “Optical tractography of the mouse heart using polarization-sensitive optical coherence tomography,” Biomed. Opt. Express 4, 2540–2545 (2013).
[Crossref] [PubMed]

2012 (4)

R. A. Jamison, A. Fouras, and R. J. Bryson-Richardson, “Cardiac-phase filtering in intracardiac particle image velocimetry,” J. Biomed. Opt. 17, 036007 (2012).
[Crossref] [PubMed]

C. Poelma, A. Kloosterman, B. P. B. Hierck, and J. Westerweel, “Accurate blood flow measurements: are artificial tracers necessary?” PloS one 7, e45247 (2012).
[Crossref] [PubMed]

J. M. Taylor, J. M. Girkin, and G. D. Love, “High-resolution 3d optical microscopy inside the beating zebrafish heart using prospective optical gating,” Biomed. Opt. Express 3, 3043–3053 (2012).
[Crossref] [PubMed]

C. A. Schneider, W.S. Rasband, and K.W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis”, Nature Methods 9, 671–675 (2012).
[Crossref] [PubMed]

2011 (1)

P. Ramachandran and G. Varoquaux, “Mayavi: 3D Visualization of Scientific Data”, IEEE Computing in Science & Engineering 13, 40–51 (2011)
[Crossref]

2010 (2)

S. J. Williams, C. Park, and S. T. Wereley, “Advances and applications on microfluidic velocimetry techniques,” Microfluid. Nanofluid. 8, 709–726 (2010)
[Crossref]

Z. J. Taylor, R. Gurka, G. A. Kopp, and A. Liberzon, “Long-duration time-resolved piv to study unsteady aerodynamics,” IEEE Transactions on Instrumentation and Measurement 59, 3262–3269 (2010).
[Crossref]

2009 (2)

B. M. W. Tsui and D. L. Kraitchman, “Recent advances in small-animal cardiovascular imaging,” Journal of Nuclear Medicine 50, 667–670 (2009).
[Crossref] [PubMed]

J. Ohn, H.-J. Tsai, and M. Liebling, “Joint dynamic imaging of morphogenesis and function in the developing heart,” Organogenesis 5, 248–255 (2009).
[Crossref]

2008 (1)

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]

2007 (2)

J. Huisken and D. Y. R. Stainier, “Even fluorescence excitation by multidirectional selective plane illumination microscopy (mSPIM),” Opt. Lett. 32, 2608–2610 (2007).
[Crossref] [PubMed]

K. Greger, J. Swoger, and E. H. K. Stelzer, “Basic building units and properties of a fluorescence single plane illumination microscope,” Review of Scientific Instruments 78, 1–7 (2007).
[Crossref]

2005 (2)

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[Crossref] [PubMed]

R. Kopp, T. Schwerte, and B. Pelster, “Cardiac performance in the zebrafish breakdance mutant,” The Journal of Experimental Biology 208, 2123–2134 (2005).
[Crossref] [PubMed]

2004 (1)

J. Westerweel, P. Geelhoed, and R. Lindken, “Single-pixel resolution ensemble correlation for micro-PIV applications,” Experiments in Fluids 37, 375–384 (2004).
[Crossref]

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]

2000 (2)

C. D. Meinhart, S. T. Wereley, and J. G. Santiago, “A PIV Algorithm for Estimating Time-Averaged Velocity Fields,” Journal of Fluids Engineering 122, 285–289 (2000).
[Crossref]

M. G. Olsen and R. J. Adrian, “Out-of-focus effects on particle image visibility and correlation in microscopic particle image velocimetry,” Experiments in Fluids 29, S166–S174 (2000).
[Crossref]

1991 (1)

R. Adrian, “Particle-imaging techniques for experimental fluid mechanics,” Annual Review of Fluid Mechanics 23, 261–304 (1991).
[Crossref]

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]

Adrian, R.

R. Adrian, “Particle-imaging techniques for experimental fluid mechanics,” Annual Review of Fluid Mechanics 23, 261–304 (1991).
[Crossref]

Adrian, R. J.

M. G. Olsen and R. J. Adrian, “Out-of-focus effects on particle image visibility and correlation in microscopic particle image velocimetry,” Experiments in Fluids 29, S166–S174 (2000).
[Crossref]

R. J. Adrian and J. Westerweel, Particle Image Velocimetry (Cambridge University Press, 2011).

Bao, Z.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

Beebe, T.

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Bokinsky, A.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

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]

F. Boselli, J.B. Freund, and J. Vermot, “Blood flow mechanics in cardiovascular development,” Cellular and Molecular Life Sciences 72, 2545–2559 (2015).
[Crossref] [PubMed]

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]

R. A. Jamison, A. Fouras, and R. J. Bryson-Richardson, “Cardiac-phase filtering in intracardiac particle image velocimetry,” J. Biomed. Opt. 17, 036007 (2012).
[Crossref] [PubMed]

Cao, H.

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Chan, K. G.

K. G. Chan and M. Liebling, “Estimation of Divergence-Free 3D Cardiac Blood Flow in a Zebrafish Larva Using Multi-View Microscopy,” in “IEEE 12th International Symposium on Biomedical Imaging,” (IEEE, 2015).

Chandris, P.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

Chi, N. C.

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Christensen, R.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

Colón-Ramos, D. A.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

Craig, M. P.

J. R. Hove and M. P. Craig, “High-speed confocal imaging of zebrafish heart development,” in “Methods in Molecular Biology,” 843X. Peng and M. Antonyak, eds. (Humana Press, 2012), pp. 309–328.
[Crossref] [PubMed]

Dickinson, M. E.

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[Crossref] [PubMed]

Eliceiri, K.W.

C. A. Schneider, W.S. Rasband, and K.W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis”, Nature Methods 9, 671–675 (2012).
[Crossref] [PubMed]

Ferrero, J. M.

A. Lopez-Perez, R. Sebastian, and J. M. Ferrero, “Three-dimensional cardiac computational modelling: methods, features and applications,” BioMedical Engineering OnLine 14, 35 (2015).
[Crossref] [PubMed]

Forouhar, A. S.

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[Crossref] [PubMed]

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]

Fouras, A.

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]

R. A. Jamison, A. Fouras, and R. J. Bryson-Richardson, “Cardiac-phase filtering in intracardiac particle image velocimetry,” J. Biomed. Opt. 17, 036007 (2012).
[Crossref] [PubMed]

Fraser, S. E.

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]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[Crossref] [PubMed]

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]

Freund, J.B.

F. Boselli, J.B. Freund, and J. Vermot, “Blood flow mechanics in cardiovascular development,” Cellular and Molecular Life Sciences 72, 2545–2559 (2015).
[Crossref] [PubMed]

Gandler, W.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

Geelhoed, P.

J. Westerweel, P. Geelhoed, and R. Lindken, “Single-pixel resolution ensemble correlation for micro-PIV applications,” Experiments in Fluids 37, 375–384 (2004).
[Crossref]

Gharib, M.

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]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[Crossref] [PubMed]

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]

Girkin, J. M.

Greger, K.

K. Greger, J. Swoger, and E. H. K. Stelzer, “Basic building units and properties of a fluorescence single plane illumination microscope,” Review of Scientific Instruments 78, 1–7 (2007).
[Crossref]

Gurka, R.

Z. J. Taylor, R. Gurka, G. A. Kopp, and A. Liberzon, “Long-duration time-resolved piv to study unsteady aerodynamics,” IEEE Transactions on Instrumentation and Measurement 59, 3262–3269 (2010).
[Crossref]

Hierck, B. P. B.

C. Poelma, A. Kloosterman, B. P. B. Hierck, and J. Westerweel, “Accurate blood flow measurements: are artificial tracers necessary?” PloS one 7, e45247 (2012).
[Crossref] [PubMed]

Hove, J. R.

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]

J. R. Hove and M. P. Craig, “High-speed confocal imaging of zebrafish heart development,” in “Methods in Molecular Biology,” 843X. Peng and M. Antonyak, eds. (Humana Press, 2012), pp. 309–328.
[Crossref] [PubMed]

Hsiai, T. K.

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Huisken, J.

Jamison, R. A.

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]

R. A. Jamison, A. Fouras, and R. J. Bryson-Richardson, “Cardiac-phase filtering in intracardiac particle image velocimetry,” J. Biomed. Opt. 17, 036007 (2012).
[Crossref] [PubMed]

Kloosterman, A.

C. Poelma, A. Kloosterman, B. P. B. Hierck, and J. Westerweel, “Accurate blood flow measurements: are artificial tracers necessary?” PloS one 7, e45247 (2012).
[Crossref] [PubMed]

Kompenhans, J.

M. Raffel, C. E. Willert, S. T. Wereley, and J. Kompenhans, Particle Image Velocimetry: A Practical Guide (Springer, 2007).

Kopp, G. A.

Z. J. Taylor, R. Gurka, G. A. Kopp, and A. Liberzon, “Long-duration time-resolved piv to study unsteady aerodynamics,” IEEE Transactions on Instrumentation and Measurement 59, 3262–3269 (2010).
[Crossref]

Kopp, R.

R. Kopp, T. Schwerte, and B. Pelster, “Cardiac performance in the zebrafish breakdance mutant,” The Journal of Experimental Biology 208, 2123–2134 (2005).
[Crossref] [PubMed]

Köster, R. W.

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]

Kraitchman, D. L.

B. M. W. Tsui and D. L. Kraitchman, “Recent advances in small-animal cardiovascular imaging,” Journal of Nuclear Medicine 50, 667–670 (2009).
[Crossref] [PubMed]

Kumar, A.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

Kung, E.

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Lee, J.

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Liberzon, A.

Z. J. Taylor, R. Gurka, G. A. Kopp, and A. Liberzon, “Long-duration time-resolved piv to study unsteady aerodynamics,” IEEE Transactions on Instrumentation and Measurement 59, 3262–3269 (2010).
[Crossref]

Liebling, M.

J. Ohn, H.-J. Tsai, and M. Liebling, “Joint dynamic imaging of morphogenesis and function in the developing heart,” Organogenesis 5, 248–255 (2009).
[Crossref]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[Crossref] [PubMed]

K. G. Chan and M. Liebling, “Estimation of Divergence-Free 3D Cardiac Blood Flow in a Zebrafish Larva Using Multi-View Microscopy,” in “IEEE 12th International Symposium on Biomedical Imaging,” (IEEE, 2015).

Lien, C.-L.

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Lindken, R.

J. Westerweel, P. Geelhoed, and R. Lindken, “Single-pixel resolution ensemble correlation for micro-PIV applications,” Experiments in Fluids 37, 375–384 (2004).
[Crossref]

Lopez-Perez, A.

A. Lopez-Perez, R. Sebastian, and J. M. Ferrero, “Three-dimensional cardiac computational modelling: methods, features and applications,” BioMedical Engineering OnLine 14, 35 (2015).
[Crossref] [PubMed]

Love, G. D.

Lu, J.

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]

Marsden, A. L.

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

McAuliffe, M.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

McCreedy, E.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

Meinhart, C. D.

C. D. Meinhart, S. T. Wereley, and J. G. Santiago, “A PIV Algorithm for Estimating Time-Averaged Velocity Fields,” Journal of Fluids Engineering 122, 285–289 (2000).
[Crossref]

Miller, Y.

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Moghadam, M. E.

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Ohn, J.

J. Ohn, H.-J. Tsai, and M. Liebling, “Joint dynamic imaging of morphogenesis and function in the developing heart,” Organogenesis 5, 248–255 (2009).
[Crossref]

Olsen, M. G.

M. G. Olsen and R. J. Adrian, “Out-of-focus effects on particle image visibility and correlation in microscopic particle image velocimetry,” Experiments in Fluids 29, S166–S174 (2000).
[Crossref]

Park, C.

S. J. Williams, C. Park, and S. T. Wereley, “Advances and applications on microfluidic velocimetry techniques,” Microfluid. Nanofluid. 8, 709–726 (2010)
[Crossref]

Pelster, B.

R. Kopp, T. Schwerte, and B. Pelster, “Cardiac performance in the zebrafish breakdance mutant,” The Journal of Experimental Biology 208, 2123–2134 (2005).
[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. Biomed. Opt. 13, 014006 (2008).
[Crossref] [PubMed]

Poelma, C.

C. Poelma, A. Kloosterman, B. P. B. Hierck, and J. Westerweel, “Accurate blood flow measurements: are artificial tracers necessary?” PloS one 7, e45247 (2012).
[Crossref] [PubMed]

Raffel, M.

M. Raffel, C. E. Willert, S. T. Wereley, and J. Kompenhans, Particle Image Velocimetry: A Practical Guide (Springer, 2007).

Ramachandran, P.

P. Ramachandran and G. Varoquaux, “Mayavi: 3D Visualization of Scientific Data”, IEEE Computing in Science & Engineering 13, 40–51 (2011)
[Crossref]

Rasband, W.S.

C. A. Schneider, W.S. Rasband, and K.W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis”, Nature Methods 9, 671–675 (2012).
[Crossref] [PubMed]

Roman, B. L.

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Rondeau, G.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[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]

Santiago, J. G.

C. D. Meinhart, S. T. Wereley, and J. G. Santiago, “A PIV Algorithm for Estimating Time-Averaged Velocity Fields,” Journal of Fluids Engineering 122, 285–289 (2000).
[Crossref]

Schneider, C. A.

C. A. Schneider, W.S. Rasband, and K.W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis”, Nature Methods 9, 671–675 (2012).
[Crossref] [PubMed]

Schwerte, T.

R. Kopp, T. Schwerte, and B. Pelster, “Cardiac performance in the zebrafish breakdance mutant,” The Journal of Experimental Biology 208, 2123–2134 (2005).
[Crossref] [PubMed]

Sebastian, R.

A. Lopez-Perez, R. Sebastian, and J. M. Ferrero, “Three-dimensional cardiac computational modelling: methods, features and applications,” BioMedical Engineering OnLine 14, 35 (2015).
[Crossref] [PubMed]

Shroff, H.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

Stainier, D. Y. R.

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,” Review of Scientific Instruments 78, 1–7 (2007).
[Crossref]

Swoger, J.

K. Greger, J. Swoger, and E. H. K. Stelzer, “Basic building units and properties of a fluorescence single plane illumination microscope,” Review of Scientific Instruments 78, 1–7 (2007).
[Crossref]

Taylor, J. M.

J. M. Taylor, “Optically gated beating-heart imaging,” Frontiers in Physiology 5, 481 (2014).
[Crossref]

J. M. Taylor, J. M. Girkin, and G. D. Love, “High-resolution 3d optical microscopy inside the beating zebrafish heart using prospective optical gating,” Biomed. Opt. Express 3, 3043–3053 (2012).
[Crossref] [PubMed]

V. Zickus and J. M. Taylor, “Spim micro-piv measurements http://dx.doi.org/10.5525/gla.researchdata.275,” (2017).

Taylor, Z. J.

Z. J. Taylor, R. Gurka, G. A. Kopp, and A. Liberzon, “Long-duration time-resolved piv to study unsteady aerodynamics,” IEEE Transactions on Instrumentation and Measurement 59, 3262–3269 (2010).
[Crossref]

Tsai, H.-J.

J. Ohn, H.-J. Tsai, and M. Liebling, “Joint dynamic imaging of morphogenesis and function in the developing heart,” Organogenesis 5, 248–255 (2009).
[Crossref]

Tsui, B. M. W.

B. M. W. Tsui and D. L. Kraitchman, “Recent advances in small-animal cardiovascular imaging,” Journal of Nuclear Medicine 50, 667–670 (2009).
[Crossref] [PubMed]

Varoquaux, G.

P. Ramachandran and G. Varoquaux, “Mayavi: 3D Visualization of Scientific Data”, IEEE Computing in Science & Engineering 13, 40–51 (2011)
[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]

F. Boselli, J.B. Freund, and J. Vermot, “Blood flow mechanics in cardiovascular development,” Cellular and Molecular Life Sciences 72, 2545–2559 (2015).
[Crossref] [PubMed]

Wang, Y.

Wereley, S. T.

S. J. Williams, C. Park, and S. T. Wereley, “Advances and applications on microfluidic velocimetry techniques,” Microfluid. Nanofluid. 8, 709–726 (2010)
[Crossref]

C. D. Meinhart, S. T. Wereley, and J. G. Santiago, “A PIV Algorithm for Estimating Time-Averaged Velocity Fields,” Journal of Fluids Engineering 122, 285–289 (2000).
[Crossref]

M. Raffel, C. E. Willert, S. T. Wereley, and J. Kompenhans, Particle Image Velocimetry: A Practical Guide (Springer, 2007).

Westerweel, J.

C. Poelma, A. Kloosterman, B. P. B. Hierck, and J. Westerweel, “Accurate blood flow measurements: are artificial tracers necessary?” PloS one 7, e45247 (2012).
[Crossref] [PubMed]

J. Westerweel, P. Geelhoed, and R. Lindken, “Single-pixel resolution ensemble correlation for micro-PIV applications,” Experiments in Fluids 37, 375–384 (2004).
[Crossref]

R. J. Adrian and J. Westerweel, Particle Image Velocimetry (Cambridge University Press, 2011).

Wieneke, B.

B. Wieneke, “PIV uncertainty quantification from correlation statistics,” Measurement Science and Technology 26, 074002 (2015).
[Crossref]

Willert, C. E.

M. Raffel, C. E. Willert, S. T. Wereley, and J. Kompenhans, Particle Image Velocimetry: A Practical Guide (Springer, 2007).

Williams, S. J.

S. J. Williams, C. Park, and S. T. Wereley, “Advances and applications on microfluidic velocimetry techniques,” Microfluid. Nanofluid. 8, 709–726 (2010)
[Crossref]

Wu, Y.

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

Yao, G.

Zickus, V.

V. Zickus and J. M. Taylor, “Spim micro-piv measurements http://dx.doi.org/10.5525/gla.researchdata.275,” (2017).

Annual Review of Fluid Mechanics (1)

R. Adrian, “Particle-imaging techniques for experimental fluid mechanics,” Annual Review of Fluid Mechanics 23, 261–304 (1991).
[Crossref]

Biomed. Opt. Express (2)

BioMedical Engineering OnLine (1)

A. Lopez-Perez, R. Sebastian, and J. M. Ferrero, “Three-dimensional cardiac computational modelling: methods, features and applications,” BioMedical Engineering OnLine 14, 35 (2015).
[Crossref] [PubMed]

Cellular and Molecular Life Sciences (1)

F. Boselli, J.B. Freund, and J. Vermot, “Blood flow mechanics in cardiovascular development,” Cellular and Molecular Life Sciences 72, 2545–2559 (2015).
[Crossref] [PubMed]

Experiments in Fluids (2)

M. G. Olsen and R. J. Adrian, “Out-of-focus effects on particle image visibility and correlation in microscopic particle image velocimetry,” Experiments in Fluids 29, S166–S174 (2000).
[Crossref]

J. Westerweel, P. Geelhoed, and R. Lindken, “Single-pixel resolution ensemble correlation for micro-PIV applications,” Experiments in Fluids 37, 375–384 (2004).
[Crossref]

Frontiers in Physiology (1)

J. M. Taylor, “Optically gated beating-heart imaging,” Frontiers in Physiology 5, 481 (2014).
[Crossref]

IEEE Computing in Science & Engineering (1)

P. Ramachandran and G. Varoquaux, “Mayavi: 3D Visualization of Scientific Data”, IEEE Computing in Science & Engineering 13, 40–51 (2011)
[Crossref]

IEEE Transactions on Instrumentation and Measurement (1)

Z. J. Taylor, R. Gurka, G. A. Kopp, and A. Liberzon, “Long-duration time-resolved piv to study unsteady aerodynamics,” IEEE Transactions on Instrumentation and Measurement 59, 3262–3269 (2010).
[Crossref]

J. Biomed. Opt. (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]

R. A. Jamison, A. Fouras, and R. J. Bryson-Richardson, “Cardiac-phase filtering in intracardiac particle image velocimetry,” J. Biomed. Opt. 17, 036007 (2012).
[Crossref] [PubMed]

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10, 054001 (2005).
[Crossref] [PubMed]

Journal of Fluids Engineering (1)

C. D. Meinhart, S. T. Wereley, and J. G. Santiago, “A PIV Algorithm for Estimating Time-Averaged Velocity Fields,” Journal of Fluids Engineering 122, 285–289 (2000).
[Crossref]

Journal of Nuclear Medicine (1)

B. M. W. Tsui and D. L. Kraitchman, “Recent advances in small-animal cardiovascular imaging,” Journal of Nuclear Medicine 50, 667–670 (2009).
[Crossref] [PubMed]

Measurement Science and Technology (1)

B. Wieneke, “PIV uncertainty quantification from correlation statistics,” Measurement Science and Technology 26, 074002 (2015).
[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]

Microfluid. Nanofluid. (1)

S. J. Williams, C. Park, and S. T. Wereley, “Advances and applications on microfluidic velocimetry techniques,” Microfluid. Nanofluid. 8, 709–726 (2010)
[Crossref]

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]

Nature Methods (1)

C. A. Schneider, W.S. Rasband, and K.W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis”, Nature Methods 9, 671–675 (2012).
[Crossref] [PubMed]

Nature Protocols (1)

A. Kumar, Y. Wu, R. Christensen, P. Chandris, W. Gandler, E. McCreedy, A. Bokinsky, D. A. Colón-Ramos, Z. Bao, M. McAuliffe, G. Rondeau, and H. Shroff, “Dual-view plane illumination microscopy for rapid and spatially isotropic imaging,” Nature Protocols 9, 2555–2573 (2014).
[Crossref] [PubMed]

Opt. Lett. (1)

Organogenesis (1)

J. Ohn, H.-J. Tsai, and M. Liebling, “Joint dynamic imaging of morphogenesis and function in the developing heart,” Organogenesis 5, 248–255 (2009).
[Crossref]

PloS one (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]

C. Poelma, A. Kloosterman, B. P. B. Hierck, and J. Westerweel, “Accurate blood flow measurements: are artificial tracers necessary?” PloS one 7, e45247 (2012).
[Crossref] [PubMed]

J. Lee, M. E. Moghadam, E. Kung, H. Cao, T. Beebe, Y. Miller, B. L. Roman, C.-L. Lien, N. C. Chi, A. L. Marsden, and T. K. Hsiai, “Moving domain computational fluid dynamics to interface with an embryonic model of cardiac morphogenesis,” PloS one 8, e72924 (2013).
[Crossref] [PubMed]

Review of Scientific Instruments (1)

K. Greger, J. Swoger, and E. H. K. Stelzer, “Basic building units and properties of a fluorescence single plane illumination microscope,” Review of Scientific Instruments 78, 1–7 (2007).
[Crossref]

The Journal of Experimental Biology (1)

R. Kopp, T. Schwerte, and B. Pelster, “Cardiac performance in the zebrafish breakdance mutant,” The Journal of Experimental Biology 208, 2123–2134 (2005).
[Crossref] [PubMed]

Other (5)

V. Zickus and J. M. Taylor, “Spim micro-piv measurements http://dx.doi.org/10.5525/gla.researchdata.275,” (2017).

R. J. Adrian and J. Westerweel, Particle Image Velocimetry (Cambridge University Press, 2011).

M. Raffel, C. E. Willert, S. T. Wereley, and J. Kompenhans, Particle Image Velocimetry: A Practical Guide (Springer, 2007).

K. G. Chan and M. Liebling, “Estimation of Divergence-Free 3D Cardiac Blood Flow in a Zebrafish Larva Using Multi-View Microscopy,” in “IEEE 12th International Symposium on Biomedical Imaging,” (IEEE, 2015).

J. R. Hove and M. P. Craig, “High-speed confocal imaging of zebrafish heart development,” in “Methods in Molecular Biology,” 843X. Peng and M. Antonyak, eds. (Humana Press, 2012), pp. 309–328.
[Crossref] [PubMed]

Supplementary Material (2)

NameDescription
» Visualization 1       3D-2C PIV measurements throughout the heartbeat of a ~3 day old zebrafish heart.
» Visualization 2       3D-2C PIV measurements throughout the heartbeat of a ~3 day old zebrafish heart.

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Figures (10)

Fig. 1
Fig. 1 Our SPIM microscope is based around a Nikon 10× 0.3NA air objective in the launch path and a Nikon 16× 0.8NA water dipping objective in the imaging path. A Coherent Obis 488 nm laser (15 mW) was used for the tube flow experiments, and an Omicron Versalase multiwavelength laser system was used at 561 nm wavelength (30 mW) for zebrafish RBC imaging. PIV frame pairs were recorded using QImaging QIClick CCD cameras (CCD1, CCD2), and brightfield images for heart synchronization were recorded using an Allied Vision GS650 CCD camera (CCD3). Chroma T495lpxr-UF2 and T550lpxr-UF2 dichroics were used for the green and red channels respectively. Further, Thorlabs MF525-39 and Semrock FF01-607/70-25 filters were used at CCD 1 and 2 respectively. Shadow effects on the illumination arm were minimized using a resonant mirror (RM) after [22], which is essential to prevent shadow artefacts that would bias the PIV analysis.
Fig. 2
Fig. 2 The PIV algorithm, and comparison between two shift estimation methods. (a) Sub-regions of the frame pairs are cross-correlated in time, yielding a matrix of the cross-correlation result, the peak of which then indicates the most likely motion of particle image between the two frames. Peak detection is then followed by subpixel interpolation of the peak and certain criteria tests probing the validity of the measurement, details in [25]. In case of correlation-averaging, each result IW pair matching from the same phase is averaged before peak fitting is executed. (b) shows the standard analysis based on direct cross correlation, while (c) illustrates our substitution of the sum of absolute differences metric in the cross-correlation stage of the analysis. Notice that the calculated flow in (b) is biased towards high intensities and produces vectors which appear to be pointing inwards, towards the center of the blood vessel. The same parameters were used in the PIV algorithm for both analyses.
Fig. 3
Fig. 3 Timing of fluorescence and brightfield camera (BF) exposures (grey boxes), and their associated pulsed illumination (blue and red boxes). By laser-illuminating the sample only for short intervals at the end and beginning of successive fluorescence camera exposures, we were able to sample the flow with better temporal resolution than that implied by the maximum framerate of the camera. Furthermore, the BF images used for heart synchronization may be contaminated by stray laser/fluorescence light leaking through the BF filters; this cross-talk can be avoided by sequencing the BF camera exposures to avoid the laser pulses, as shown here.
Fig. 4
Fig. 4 PIV analysis results of the FEP tube experiment data acquired using BF channel. Top row: 0.5 μl/min nominal flow rate beads; bottom row: 1 μl/min beads. Profiles are shown at the location of the peak flow. Shaded area represents tube walls. The profiles of the u-components of velocity in xy (a,d) have very similar shapes for both flow rate values (semi-minor axis ranges ≈25.0 – 25.6 μm). However, the xz plane (b, e) data reveal that the experimentally recovered flow profile stretches with increasing flow rate (semi-major axis increasing from ≈39.8 to 61.6 μm). The contours (c,f) of the x-velocity magnitudes in the yz plane illustrate the apparent elongation of the parabolic flow profile along the z-axis when measured using BF (f) which does not occur in fluorescence, see Figure 5. Dashes show a diameter of 50μm.
Fig. 5
Fig. 5 SPIM-μPIV analysis results of FEP tube experiments in locations of peak flow, from analysis of fluorescence imagery. Top row - 0.5 μl/min nominal flow rate beads, bottom row - 1 μl/min beads. Shaded area represents tube walls. The profiles of the u-components of velocity in xy (a,d) have very similar shapes for all experiments (semi-minor axis ranges ≈26.3 – 26.5 μm). Similarly, the xz planes (b,e) show similar profile shape (semi-major axis ranges ≈25.9 – 25.8 μm). This confirms that there is no significant anomalous bias to the flow profile recovered in the xz plane, thus validating our use of SPIM-μPIV for 3D flow mapping. (c,f) show colormaps of the velocity magnitude in the yz plane, confirming that to a good approximation the reconstructed flow is circularly symmetric and Poiseuille-like. Dashes show a diameter of 50μm.
Fig. 6
Fig. 6 Heatmap visualization of correlation matrices from a z stack (representing a single IW selected from our FEP tube data, Figs. 4 and 5), flow rates of 0.5 μl/min (a,b) and 1 μl/min (c,d). These plots give insight into the origin of strong biasing effects that compromise brightfield μPIV analysis. The images represent a cut parallel to the x axis through the peak of the correlation matrices (correlation amplitude represented as color), for each z plane in our dataset. In μPIV analysis, the flow velocity is determined from the location of the peak correlation matrix value in each plane (annotated with red squares). For the fluorescence data (b, d) it can be seen that the correlation matrices consist of a single well-defined peak at each z, with the location of that peak following the expected parabolic profile. However for the brightfield data (a, c) it can be seen that there is significant broadening and clutter present in the correlation matrices which compromises the velocity and leads to the incorrect flattened parabolic profiles shown in Fig. 4. Nevertheless, a “ghost” of the true underlying parabolic profile can be discerned in (c), although its weaker amplitude means it is not correctly identified as the calculated flow value.
Fig. 7
Fig. 7 PIV measurement error vs. out-of-plane motion. The 4 solid lines with dots represent individual correlation-averaged results from different volumes in the tube. The bold dashed line with squares indicates the simple mean of the 4 measurements. The finely dashed line marks the acceptable amount of error on the velocity measurement of 0.3 pixels (following [1]). FWHM of the light sheet used in this experiment ≈ 2.5μm.
Fig. 8
Fig. 8 3D flow reconstruction using 2D flow data in the zebrafish heart (walls expressing flk1:GFP and RBCs expressing gata:DsRed). (a) 3D cut-plane image of blood flow in a ∼3 dpf zebrafish heart. Peak flow vectors (corresponding to the high end of the colorbar) are plotted, but not visible in this orientation. For the most part of the heart the calculated flow field is smooth. The erroneous areas mostly correspond to positions where the flow is out-of-plane. The flow measurements are reliable as long as the plane of the flow is reasonably well-aligned with the imaging plane (in-plane motion dominates over out-of-plane motion). The sample mounting in SPIM allows many sample orientation options, however, the geometry of the heart often determines a preferred orientation for flow imaging. (b) Close up of the xy plane of (a). Visualization 1 in the supplementary material also shows the flow in the heart, over the full heartbeat. Visualization 2 further illustrates the depth-resolved flow results at a single phase. The square root of velocity magnitudes is displayed to better demonstrate the dynamic range. Visualized using Mayavi [32].
Fig. 9
Fig. 9 Flow through the atrium. (a) Several orientations of the flow in our chosen cross section through the middle of the atrium at phase bin 1.2 in a ∼3 days old zebrafish atrium. We note that we discarded data well outside the walls of the atrium. Visualized using Mayavi [32]. (b) Net flow rate integrated across this cross section in the atrium, as a function of heart phase. Positive flow (pumping, towards the ventricle) shaded in red; negative flow (regurgitation, out of the atrium and back into sinus venosus) shaded in blue. The area under the curve gives the pumped volume. The plotted error bars were obtained by splitting the data set in two halves (effectively reducing the seeding by half) and using the absolute difference between the flow rate results of two values as the measure of the spread within each phase bin. The least reliable phases correspond to near full contraction of the atrium. Here the flow is complex and bidirectional due to the fact that the valves are not yet fully developed – this, combined with the extremely high flows through the constriction of the partially-formed valve, make flow measurements at this exact location extremely challenging.
Fig. 10
Fig. 10 Comparison of correlation averaged (white line with squares) and single-pair (multi-colored dots) u-component measurements for 31 phases for interrogation window at (x = 239.5px, y = 107.5px), which is approximately at the 3/4 of the atrium length from the left edge of the atrium at the 7th z-plane (around the middle of the atrium depth-wise). The lack of spread phase-wise suggests that synchronization was sufficiently robust against any beat-to-beat variations in the heart. Note that this plot displays every raw datapoint, with no exclusion of outliers such as frame pairs containing no RBCs. The detailed features of this plot are interpreted further in the main text.

Tables (2)

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Table 1 Main experimental and PIV analysis parameters summarized for both the phantom validation experiment and the zebrafish heart. Effective single pixel size was 0.3225 μm (at 20x magnification). The number of frame pairs is approximate, as it varied slightly from one plane to another due to our acquisition code. The variation was greater for the heart data, however, phase bins had around 50 frame pairs.(*) days post fertilization.

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Table 2 Data fitting parameters summarized (see Figure 4 and Figure 5 for data points). The tube radius was measured from the images to be 26.450 ± 0.645 μm. Parameters a and b are the semi-minor and major axes of a parabolic flow profile. For a parabolic flow in a tube, which drops off to zero at the tube walls, a and b will match the radius of the tube. Note the dramatic and unphysical variation in the b parameter for brightfield datasets. The incorrect profile recovered with BF PIV analysis can be seen in Figure 4.

Equations (1)

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V ( x , y , z ) = V max ( 1 ( ( y y c ) 2 a 2 + ( z z c ) 2 b 2 ) ) ,

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