Abstract

Motile cilia are cellular organelles that generate directional fluid flow across various epithelial surfaces including the embryonic node and respiratory mucosa. The proper functioning of cilia is necessary for normal embryo development and, for the respiratory system, the clearance of mucus and potentially harmful particulate matter. Here we show that optical coherence tomography (OCT) is well-suited for quantitatively characterizing the microfluidic-scale flow generated by motile cilia. Our imaging focuses on the ciliated epithelium of Xenopus tropicalis embryos, a genetically manipulable and experimentally tractable animal model of human disease. We show qualitative flow profile characterization using OCT-based particle pathline imaging. We show quantitative, two-dimensional, two-component flow velocity field characterization using OCT-based particle tracking velocimetry. Quantitative imaging and phenotyping of cilia-driven fluid flow using OCT will enable more detailed research in ciliary biology and in respiratory medicine.

© 2011 OSA

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2011 (1)

M. A. Choma, M. J. Suter, B. J. Vakoc, B. E. Bouma, and G. J. Tearney, “Physiological homology between Drosophila melanogaster and vertebrate cardiovascular systems,” Dis Model Mech 4(3), 411–420 (2011).
[CrossRef] [PubMed]

2010 (8)

Z. Ma, A. Liu, X. Yin, A. Troyer, K. Thornburg, R. K. Wang, and S. Rugonyi, “Measurement of absolute blood flow velocity in outflow tract of HH18 chicken embryo based on 4D reconstruction using spectral domain optical coherence tomography,” Biomed. Opt. Express 1(3), 798–811 (2010).
[CrossRef] [PubMed]

A. S. G. Singh, C. Kolbitsch, T. Schmoll, and R. A. Leitgeb, “Stable absolute flow estimation with Doppler OCT based on virtual circumpapillary scans,” Biomed. Opt. Express 1(4), 1047–1058 (2010).
[CrossRef] [PubMed]

F. Miskevich, “Imaging fluid flow and cilia beating pattern in Xenopus brain ventricles,” J. Neurosci. Methods 189(1), 1–4 (2010).
[CrossRef] [PubMed]

B. Guirao, A. Meunier, S. Mortaud, A. Aguilar, J. M. Corsi, L. Strehl, Y. Hirota, A. Desoeuvre, C. Boutin, Y. G. Han, Z. Mirzadeh, H. Cremer, M. Montcouquiol, K. Sawamoto, and N. Spassky, “Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia,” Nat. Cell Biol. 12(4), 341–350 (2010).
[CrossRef] [PubMed]

K. Ikegami, S. Sato, K. Nakamura, L. E. Ostrowski, and M. Setou, “Tubulin polyglutamylation is essential for airway ciliary function through the regulation of beating asymmetry,” Proc. Natl. Acad. Sci. U.S.A. 107(23), 10490–10495 (2010).
[CrossRef] [PubMed]

K. Oh, B. Smith, S. Devasia, J. J. Riley, and J. H. Chung, “Characterization of mixing performance for bio-mimetic silicone cilia,” Microfluidics Nanofluidics 9(4-5), 645–655 (2010).
[CrossRef]

M. W. Jenkins, L. Peterson, S. Gu, M. Gargesha, D. L. Wilson, M. Watanabe, and A. M. Rollins, “Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography,” J. Biomed. Opt. 15(6), 066022 (2010).
[CrossRef] [PubMed]

W. Wieser, B. R. Biedermann, T. Klein, C. M. Eigenwillig, and R. Huber, “Multi-megahertz OCT: high quality 3D imaging at 20 million A-scans and 4.5 GVoxels per second,” Opt. Express 18(14), 14685–14704 (2010).
[CrossRef] [PubMed]

2009 (8)

B. Mitchell, J. L. Stubbs, F. Huisman, P. Taborek, C. Yu, and C. Kintner, “The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin,” Curr. Biol. 19(11), 924–929 (2009).
[CrossRef] [PubMed]

R. J. Francis, B. Chatterjee, N. T. Loges, H. Zentgraf, H. Omran, and C. W. Lo, “Initiation and maturation of cilia-generated flow in newborn and postnatal mouse airway,” Am. J. Physiol. Lung Cell. Mol. Physiol. 296(6), L1067–L1075 (2009).
[CrossRef] [PubMed]

J. R. Colantonio, J. Vermot, D. Wu, A. D. Langenbacher, S. Fraser, J. N. Chen, and K. L. Hill, “The dynein regulatory complex is required for ciliary motility and otolith biogenesis in the inner ear,” Nature 457(7226), 205–209 (2009).
[CrossRef] [PubMed]

K. Baker and P. L. Beales, “Making sense of cilia in disease: the human ciliopathies,” Am. J. Med. Genet. C. Semin. Med. Genet. 151C(4), 281–295 (2009).
[CrossRef] [PubMed]

A. Davis, J. Izatt, and F. Rothenberg, “Quantitative measurement of blood flow dynamics in embryonic vasculature using spectral Doppler velocimetry,” Anat. Rec. (Hoboken) 292(3), 311–319 (2009).
[CrossRef] [PubMed]

S. J. Lee and S. Kim, “Advanced particle-based velocimetry techniques for microscale flows,” Microfluidics Nanofluidics 6(5), 577–588 (2009).
[CrossRef]

M. Baltussen, P. Anderson, F. Bos, and J. den Toonder, “Inertial flow effects in a micro-mixer based on artificial cilia,” Lab Chip 9(16), 2326–2331 (2009).
[CrossRef] [PubMed]

A. V. Bykov, A. V. Priezzhev, J. Lauri, and R. Myllylä, “Doppler OCT imaging of cytoplasm shuttle flow in Physarum polycephalum,” J Biophotonics 2(8-9), 540–547 (2009).
[CrossRef] [PubMed]

2008 (4)

2007 (5)

2006 (4)

K. Sawamoto, H. Wichterle, O. Gonzalez-Perez, J. A. Cholfin, M. Yamada, N. Spassky, N. S. Murcia, J. M. Garcia-Verdugo, O. Marin, J. L. R. Rubenstein, M. Tessier-Lavigne, H. Okano, and A. Alvarez-Buylla, “New neurons follow the flow of cerebrospinal fluid in the adult brain,” Science 311(5761), 629–632 (2006).
[CrossRef] [PubMed]

R. A. Lyons, E. Saridogan, and O. Djahanbakhch, “The reproductive significance of human Fallopian tube cilia,” Hum. Reprod. Update 12(4), 363–372 (2006).
[CrossRef] [PubMed]

M. A. Choma, A. K. Ellerbee, S. Yazdanfar, and J. A. Izatt, “Doppler flow imaging of cytoplasmic streaming using spectral domain phase microscopy,” J. Biomed. Opt. 11(2), 024014 (2006).
[CrossRef] [PubMed]

F. Pereira, H. Stuer, E. C. Graff, and M. Gharib, “Two-frame 3D particle tracking,” Meas. Sci. Technol. 17(7), 1680–1692 (2006).
[CrossRef]

2005 (2)

A. G. Kramer-Zucker, F. Olale, C. J. Haycraft, B. K. Yoder, A. F. Schier, and I. A. Drummond, “Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer’s vesicle is required for normal organogenesis,” Development 132(8), 1907–1921 (2005).
[CrossRef] [PubMed]

Y. Okada, S. Takeda, Y. Tanaka, J. C. I. Belmonte, and N. Hirokawa, “Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination,” Cell 121(4), 633–644 (2005).
[CrossRef] [PubMed]

2004 (2)

H. A. Stone, A. D. Stroock, and A. Ajdari, “Engineering flows in small devices: microfluidics toward a lab-on-a-chip,” Annu. Rev. Fluid Mech. 36(1), 381–411 (2004).
[CrossRef]

C. W. Xi, D. L. Marks, D. S. Parikh, L. Raskin, and S. A. Boppart, “Structural and functional imaging of 3D microfluidic mixers using optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 101(20), 7516–7521 (2004).
[CrossRef] [PubMed]

2003 (2)

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys. 66(2), 239–303 (2003).
[CrossRef]

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(6919), 172–177 (2003).
[CrossRef] [PubMed]

2002 (1)

M. K. Khokha, C. Chung, E. L. Bustamante, L. W. Gaw, K. A. Trott, J. Yeh, N. Lim, J. C. Lin, N. Taverner, E. Amaya, N. Papalopulu, J. C. Smith, A. M. Zorn, R. M. Harland, and T. C. Grammer, “Techniques and probes for the study of Xenopus tropicalis development,” Dev. Dyn. 225(4), 499–510 (2002).
[CrossRef] [PubMed]

2000 (1)

A. D. Stroock, M. Weck, D. T. Chiu, W. T. S. Huck, P. J. A. Kenis, R. F. Ismagilov, and G. M. Whitesides, “Patterning electro-osmotic flow with patterned surface charge,” Phys. Rev. Lett. 84(15), 3314–3317 (2000).
[CrossRef] [PubMed]

1998 (1)

1997 (1)

A. Patwardhan, “Subpixel position measurement using 1D, 2D and 3D centroid algorithms with emphasis on applications in confocal microscopy,” J. Microsc. (Oxford) 186(3), 246–257 (1997).
[CrossRef]

1996 (2)

R. H. Webb, “Confocal optical microscopy,” Rep. Prog. Phys. 59(3), 427–471 (1996).
[CrossRef]

J. A. Izatt, M. D. Kulkarni, H. W. Wang, K. Kobayashi, and M. V. Sivak, “Optical coherence tomography and microscopy in gastrointestinal tissues,” IEEE J. Sel. Top. Quantum Electron. 2(4), 1017–1028 (1996).
[CrossRef]

1991 (2)

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

R. J. Adrian, “Particle-imaging techniques for experimental fluid-mechanics,” Annu. Rev. Fluid Mech. 23(1), 261–304 (1991).
[CrossRef]

1971 (1)

F. S. Billett and R. P. Gould, “Fine structural changes in the differentiating epidermis of Xenopus laevis embryos,” J. Anat. 108(Pt 3), 465–480 (1971).
[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(6919), 172–177 (2003).
[CrossRef] [PubMed]

Adrian, R. J.

R. J. Adrian, “Particle-imaging techniques for experimental fluid-mechanics,” Annu. Rev. Fluid Mech. 23(1), 261–304 (1991).
[CrossRef]

Aguilar, A.

B. Guirao, A. Meunier, S. Mortaud, A. Aguilar, J. M. Corsi, L. Strehl, Y. Hirota, A. Desoeuvre, C. Boutin, Y. G. Han, Z. Mirzadeh, H. Cremer, M. Montcouquiol, K. Sawamoto, and N. Spassky, “Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia,” Nat. Cell Biol. 12(4), 341–350 (2010).
[CrossRef] [PubMed]

Ahn, Y. C.

Y. C. Ahn, W. G. Jung, and Z. P. Chen, “Optical sectioning for microfluidics: secondary flow and mixing in a meandering microchannel,” Lab Chip 8(1), 125–133 (2008).
[CrossRef] [PubMed]

Y. C. Ahn, W. Jung, and Z. P. Chen, “Quantification of a three-dimensional velocity vector using spectral-domain Doppler optical coherence tomography,” Opt. Lett. 32(11), 1587–1589 (2007).
[CrossRef] [PubMed]

Ajdari, A.

H. A. Stone, A. D. Stroock, and A. Ajdari, “Engineering flows in small devices: microfluidics toward a lab-on-a-chip,” Annu. Rev. Fluid Mech. 36(1), 381–411 (2004).
[CrossRef]

Alvarez-Buylla, A.

K. Sawamoto, H. Wichterle, O. Gonzalez-Perez, J. A. Cholfin, M. Yamada, N. Spassky, N. S. Murcia, J. M. Garcia-Verdugo, O. Marin, J. L. R. Rubenstein, M. Tessier-Lavigne, H. Okano, and A. Alvarez-Buylla, “New neurons follow the flow of cerebrospinal fluid in the adult brain,” Science 311(5761), 629–632 (2006).
[CrossRef] [PubMed]

Amaya, E.

M. K. Khokha, C. Chung, E. L. Bustamante, L. W. Gaw, K. A. Trott, J. Yeh, N. Lim, J. C. Lin, N. Taverner, E. Amaya, N. Papalopulu, J. C. Smith, A. M. Zorn, R. M. Harland, and T. C. Grammer, “Techniques and probes for the study of Xenopus tropicalis development,” Dev. Dyn. 225(4), 499–510 (2002).
[CrossRef] [PubMed]

Anderson, P.

M. Baltussen, P. Anderson, F. Bos, and J. den Toonder, “Inertial flow effects in a micro-mixer based on artificial cilia,” Lab Chip 9(16), 2326–2331 (2009).
[CrossRef] [PubMed]

Baker, K.

K. Baker and P. L. Beales, “Making sense of cilia in disease: the human ciliopathies,” Am. J. Med. Genet. C. Semin. Med. Genet. 151C(4), 281–295 (2009).
[CrossRef] [PubMed]

Baltussen, M.

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Y. Okada, S. Takeda, Y. Tanaka, J. C. I. Belmonte, and N. Hirokawa, “Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination,” Cell 121(4), 633–644 (2005).
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F. S. Billett and R. P. Gould, “Fine structural changes in the differentiating epidermis of Xenopus laevis embryos,” J. Anat. 108(Pt 3), 465–480 (1971).
[PubMed]

Bizheva, K. K.

Boas, D. A.

Boppart, S. A.

C. W. Xi, D. L. Marks, D. S. Parikh, L. Raskin, and S. A. Boppart, “Structural and functional imaging of 3D microfluidic mixers using optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 101(20), 7516–7521 (2004).
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Bos, F.

M. Baltussen, P. Anderson, F. Bos, and J. den Toonder, “Inertial flow effects in a micro-mixer based on artificial cilia,” Lab Chip 9(16), 2326–2331 (2009).
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Bouma, B. E.

M. A. Choma, M. J. Suter, B. J. Vakoc, B. E. Bouma, and G. J. Tearney, “Physiological homology between Drosophila melanogaster and vertebrate cardiovascular systems,” Dis Model Mech 4(3), 411–420 (2011).
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Boutin, C.

B. Guirao, A. Meunier, S. Mortaud, A. Aguilar, J. M. Corsi, L. Strehl, Y. Hirota, A. Desoeuvre, C. Boutin, Y. G. Han, Z. Mirzadeh, H. Cremer, M. Montcouquiol, K. Sawamoto, and N. Spassky, “Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia,” Nat. Cell Biol. 12(4), 341–350 (2010).
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M. K. Khokha, C. Chung, E. L. Bustamante, L. W. Gaw, K. A. Trott, J. Yeh, N. Lim, J. C. Lin, N. Taverner, E. Amaya, N. Papalopulu, J. C. Smith, A. M. Zorn, R. M. Harland, and T. C. Grammer, “Techniques and probes for the study of Xenopus tropicalis development,” Dev. Dyn. 225(4), 499–510 (2002).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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R. J. Francis, B. Chatterjee, N. T. Loges, H. Zentgraf, H. Omran, and C. W. Lo, “Initiation and maturation of cilia-generated flow in newborn and postnatal mouse airway,” Am. J. Physiol. Lung Cell. Mol. Physiol. 296(6), L1067–L1075 (2009).
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J. R. Colantonio, J. Vermot, D. Wu, A. D. Langenbacher, S. Fraser, J. N. Chen, and K. L. Hill, “The dynein regulatory complex is required for ciliary motility and otolith biogenesis in the inner ear,” Nature 457(7226), 205–209 (2009).
[CrossRef] [PubMed]

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Y. C. Ahn, W. G. Jung, and Z. P. Chen, “Optical sectioning for microfluidics: secondary flow and mixing in a meandering microchannel,” Lab Chip 8(1), 125–133 (2008).
[CrossRef] [PubMed]

Y. C. Ahn, W. Jung, and Z. P. Chen, “Quantification of a three-dimensional velocity vector using spectral-domain Doppler optical coherence tomography,” Opt. Lett. 32(11), 1587–1589 (2007).
[CrossRef] [PubMed]

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B. Mitchell, R. Jacobs, J. Li, S. Chien, and C. Kintner, “A positive feedback mechanism governs the polarity and motion of motile cilia,” Nature 447(7140), 97–101 (2007).
[CrossRef] [PubMed]

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A. D. Stroock, M. Weck, D. T. Chiu, W. T. S. Huck, P. J. A. Kenis, R. F. Ismagilov, and G. M. Whitesides, “Patterning electro-osmotic flow with patterned surface charge,” Phys. Rev. Lett. 84(15), 3314–3317 (2000).
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K. Sawamoto, H. Wichterle, O. Gonzalez-Perez, J. A. Cholfin, M. Yamada, N. Spassky, N. S. Murcia, J. M. Garcia-Verdugo, O. Marin, J. L. R. Rubenstein, M. Tessier-Lavigne, H. Okano, and A. Alvarez-Buylla, “New neurons follow the flow of cerebrospinal fluid in the adult brain,” Science 311(5761), 629–632 (2006).
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Choma, M. A.

M. A. Choma, M. J. Suter, B. J. Vakoc, B. E. Bouma, and G. J. Tearney, “Physiological homology between Drosophila melanogaster and vertebrate cardiovascular systems,” Dis Model Mech 4(3), 411–420 (2011).
[CrossRef] [PubMed]

M. A. Choma, A. K. Ellerbee, S. Yazdanfar, and J. A. Izatt, “Doppler flow imaging of cytoplasmic streaming using spectral domain phase microscopy,” J. Biomed. Opt. 11(2), 024014 (2006).
[CrossRef] [PubMed]

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M. K. Khokha, C. Chung, E. L. Bustamante, L. W. Gaw, K. A. Trott, J. Yeh, N. Lim, J. C. Lin, N. Taverner, E. Amaya, N. Papalopulu, J. C. Smith, A. M. Zorn, R. M. Harland, and T. C. Grammer, “Techniques and probes for the study of Xenopus tropicalis development,” Dev. Dyn. 225(4), 499–510 (2002).
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Chung, J. H.

K. Oh, B. Smith, S. Devasia, J. J. Riley, and J. H. Chung, “Characterization of mixing performance for bio-mimetic silicone cilia,” Microfluidics Nanofluidics 9(4-5), 645–655 (2010).
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J. R. Colantonio, J. Vermot, D. Wu, A. D. Langenbacher, S. Fraser, J. N. Chen, and K. L. Hill, “The dynein regulatory complex is required for ciliary motility and otolith biogenesis in the inner ear,” Nature 457(7226), 205–209 (2009).
[CrossRef] [PubMed]

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B. Guirao, A. Meunier, S. Mortaud, A. Aguilar, J. M. Corsi, L. Strehl, Y. Hirota, A. Desoeuvre, C. Boutin, Y. G. Han, Z. Mirzadeh, H. Cremer, M. Montcouquiol, K. Sawamoto, and N. Spassky, “Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia,” Nat. Cell Biol. 12(4), 341–350 (2010).
[CrossRef] [PubMed]

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B. Guirao, A. Meunier, S. Mortaud, A. Aguilar, J. M. Corsi, L. Strehl, Y. Hirota, A. Desoeuvre, C. Boutin, Y. G. Han, Z. Mirzadeh, H. Cremer, M. Montcouquiol, K. Sawamoto, and N. Spassky, “Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia,” Nat. Cell Biol. 12(4), 341–350 (2010).
[CrossRef] [PubMed]

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A. Davis, J. Izatt, and F. Rothenberg, “Quantitative measurement of blood flow dynamics in embryonic vasculature using spectral Doppler velocimetry,” Anat. Rec. (Hoboken) 292(3), 311–319 (2009).
[CrossRef] [PubMed]

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M. Baltussen, P. Anderson, F. Bos, and J. den Toonder, “Inertial flow effects in a micro-mixer based on artificial cilia,” Lab Chip 9(16), 2326–2331 (2009).
[CrossRef] [PubMed]

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B. Guirao, A. Meunier, S. Mortaud, A. Aguilar, J. M. Corsi, L. Strehl, Y. Hirota, A. Desoeuvre, C. Boutin, Y. G. Han, Z. Mirzadeh, H. Cremer, M. Montcouquiol, K. Sawamoto, and N. Spassky, “Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia,” Nat. Cell Biol. 12(4), 341–350 (2010).
[CrossRef] [PubMed]

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K. Oh, B. Smith, S. Devasia, J. J. Riley, and J. H. Chung, “Characterization of mixing performance for bio-mimetic silicone cilia,” Microfluidics Nanofluidics 9(4-5), 645–655 (2010).
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A. G. Kramer-Zucker, F. Olale, C. J. Haycraft, B. K. Yoder, A. F. Schier, and I. A. Drummond, “Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer’s vesicle is required for normal organogenesis,” Development 132(8), 1907–1921 (2005).
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Eigenwillig, C. M.

Ellerbee, A. K.

M. A. Choma, A. K. Ellerbee, S. Yazdanfar, and J. A. Izatt, “Doppler flow imaging of cytoplasmic streaming using spectral domain phase microscopy,” J. Biomed. Opt. 11(2), 024014 (2006).
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Fabritius, T.

Fercher, A. F.

A. F. Fercher, W. Drexler, C. K. Hitzenberger, and T. Lasser, “Optical coherence tomography - principles and applications,” Rep. Prog. Phys. 66(2), 239–303 (2003).
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Ferrante, A. A.

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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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J. 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(6919), 172–177 (2003).
[CrossRef] [PubMed]

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R. J. Francis, B. Chatterjee, N. T. Loges, H. Zentgraf, H. Omran, and C. W. Lo, “Initiation and maturation of cilia-generated flow in newborn and postnatal mouse airway,” Am. J. Physiol. Lung Cell. Mol. Physiol. 296(6), L1067–L1075 (2009).
[CrossRef] [PubMed]

Fraser, S.

J. R. Colantonio, J. Vermot, D. Wu, A. D. Langenbacher, S. Fraser, J. N. Chen, and K. L. Hill, “The dynein regulatory complex is required for ciliary motility and otolith biogenesis in the inner ear,” Nature 457(7226), 205–209 (2009).
[CrossRef] [PubMed]

Fraser, S. E.

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(6919), 172–177 (2003).
[CrossRef] [PubMed]

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

K. Sawamoto, H. Wichterle, O. Gonzalez-Perez, J. A. Cholfin, M. Yamada, N. Spassky, N. S. Murcia, J. M. Garcia-Verdugo, O. Marin, J. L. R. Rubenstein, M. Tessier-Lavigne, H. Okano, and A. Alvarez-Buylla, “New neurons follow the flow of cerebrospinal fluid in the adult brain,” Science 311(5761), 629–632 (2006).
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Gargesha, M.

M. W. Jenkins, L. Peterson, S. Gu, M. Gargesha, D. L. Wilson, M. Watanabe, and A. M. Rollins, “Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography,” J. Biomed. Opt. 15(6), 066022 (2010).
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M. K. Khokha, C. Chung, E. L. Bustamante, L. W. Gaw, K. A. Trott, J. Yeh, N. Lim, J. C. Lin, N. Taverner, E. Amaya, N. Papalopulu, J. C. Smith, A. M. Zorn, R. M. Harland, and T. C. Grammer, “Techniques and probes for the study of Xenopus tropicalis development,” Dev. Dyn. 225(4), 499–510 (2002).
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F. Pereira, H. Stuer, E. C. Graff, and M. Gharib, “Two-frame 3D particle tracking,” Meas. Sci. Technol. 17(7), 1680–1692 (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(6919), 172–177 (2003).
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Gonzalez-Perez, O.

K. Sawamoto, H. Wichterle, O. Gonzalez-Perez, J. A. Cholfin, M. Yamada, N. Spassky, N. S. Murcia, J. M. Garcia-Verdugo, O. Marin, J. L. R. Rubenstein, M. Tessier-Lavigne, H. Okano, and A. Alvarez-Buylla, “New neurons follow the flow of cerebrospinal fluid in the adult brain,” Science 311(5761), 629–632 (2006).
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Götzinger, E.

Gould, R. P.

F. S. Billett and R. P. Gould, “Fine structural changes in the differentiating epidermis of Xenopus laevis embryos,” J. Anat. 108(Pt 3), 465–480 (1971).
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Graff, E. C.

F. Pereira, H. Stuer, E. C. Graff, and M. Gharib, “Two-frame 3D particle tracking,” Meas. Sci. Technol. 17(7), 1680–1692 (2006).
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Grammer, T. C.

M. K. Khokha, C. Chung, E. L. Bustamante, L. W. Gaw, K. A. Trott, J. Yeh, N. Lim, J. C. Lin, N. Taverner, E. Amaya, N. Papalopulu, J. C. Smith, A. M. Zorn, R. M. Harland, and T. C. Grammer, “Techniques and probes for the study of Xenopus tropicalis development,” Dev. Dyn. 225(4), 499–510 (2002).
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Gregori, G.

Gregory, K.

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

Gu, S.

M. W. Jenkins, L. Peterson, S. Gu, M. Gargesha, D. L. Wilson, M. Watanabe, and A. M. Rollins, “Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography,” J. Biomed. Opt. 15(6), 066022 (2010).
[CrossRef] [PubMed]

Guirao, B.

B. Guirao, A. Meunier, S. Mortaud, A. Aguilar, J. M. Corsi, L. Strehl, Y. Hirota, A. Desoeuvre, C. Boutin, Y. G. Han, Z. Mirzadeh, H. Cremer, M. Montcouquiol, K. Sawamoto, and N. Spassky, “Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia,” Nat. Cell Biol. 12(4), 341–350 (2010).
[CrossRef] [PubMed]

B. Guirao and J. F. Joanny, “Spontaneous creation of macroscopic flow and metachronal waves in an array of cilia,” Biophys. J. 92(6), 1900–1917 (2007).
[CrossRef] [PubMed]

Hammer, D. X.

Han, Y. G.

B. Guirao, A. Meunier, S. Mortaud, A. Aguilar, J. M. Corsi, L. Strehl, Y. Hirota, A. Desoeuvre, C. Boutin, Y. G. Han, Z. Mirzadeh, H. Cremer, M. Montcouquiol, K. Sawamoto, and N. Spassky, “Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia,” Nat. Cell Biol. 12(4), 341–350 (2010).
[CrossRef] [PubMed]

Harland, R. M.

M. K. Khokha, C. Chung, E. L. Bustamante, L. W. Gaw, K. A. Trott, J. Yeh, N. Lim, J. C. Lin, N. Taverner, E. Amaya, N. Papalopulu, J. C. Smith, A. M. Zorn, R. M. Harland, and T. C. Grammer, “Techniques and probes for the study of Xenopus tropicalis development,” Dev. Dyn. 225(4), 499–510 (2002).
[CrossRef] [PubMed]

Haycraft, C. J.

A. G. Kramer-Zucker, F. Olale, C. J. Haycraft, B. K. Yoder, A. F. Schier, and I. A. Drummond, “Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer’s vesicle is required for normal organogenesis,” Development 132(8), 1907–1921 (2005).
[CrossRef] [PubMed]

Hee, M. R.

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

Hill, K. L.

J. R. Colantonio, J. Vermot, D. Wu, A. D. Langenbacher, S. Fraser, J. N. Chen, and K. L. Hill, “The dynein regulatory complex is required for ciliary motility and otolith biogenesis in the inner ear,” Nature 457(7226), 205–209 (2009).
[CrossRef] [PubMed]

Hirokawa, N.

Y. Okada, S. Takeda, Y. Tanaka, J. C. I. Belmonte, and N. Hirokawa, “Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination,” Cell 121(4), 633–644 (2005).
[CrossRef] [PubMed]

Hirota, Y.

B. Guirao, A. Meunier, S. Mortaud, A. Aguilar, J. M. Corsi, L. Strehl, Y. Hirota, A. Desoeuvre, C. Boutin, Y. G. Han, Z. Mirzadeh, H. Cremer, M. Montcouquiol, K. Sawamoto, and N. Spassky, “Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia,” Nat. Cell Biol. 12(4), 341–350 (2010).
[CrossRef] [PubMed]

Hitzenberger, C. K.

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(6919), 172–177 (2003).
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C. J. Pedersen, D. Huang, M. A. Shure, and A. M. Rollins, “Measurement of absolute flow velocity vector using dual-angle, delay-encoded Doppler optical coherence tomography,” Opt. Lett. 32(5), 506–508 (2007).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Huber, R.

Huck, W. T. S.

A. D. Stroock, M. Weck, D. T. Chiu, W. T. S. Huck, P. J. A. Kenis, R. F. Ismagilov, and G. M. Whitesides, “Patterning electro-osmotic flow with patterned surface charge,” Phys. Rev. Lett. 84(15), 3314–3317 (2000).
[CrossRef] [PubMed]

Huisman, F.

B. Mitchell, J. L. Stubbs, F. Huisman, P. Taborek, C. Yu, and C. Kintner, “The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin,” Curr. Biol. 19(11), 924–929 (2009).
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Iftimia, N. V.

Ikegami, K.

K. Ikegami, S. Sato, K. Nakamura, L. E. Ostrowski, and M. Setou, “Tubulin polyglutamylation is essential for airway ciliary function through the regulation of beating asymmetry,” Proc. Natl. Acad. Sci. U.S.A. 107(23), 10490–10495 (2010).
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Ismagilov, R. F.

A. D. Stroock, M. Weck, D. T. Chiu, W. T. S. Huck, P. J. A. Kenis, R. F. Ismagilov, and G. M. Whitesides, “Patterning electro-osmotic flow with patterned surface charge,” Phys. Rev. Lett. 84(15), 3314–3317 (2000).
[CrossRef] [PubMed]

Izatt, J.

A. Davis, J. Izatt, and F. Rothenberg, “Quantitative measurement of blood flow dynamics in embryonic vasculature using spectral Doppler velocimetry,” Anat. Rec. (Hoboken) 292(3), 311–319 (2009).
[CrossRef] [PubMed]

Izatt, J. A.

M. A. Choma, A. K. Ellerbee, S. Yazdanfar, and J. A. Izatt, “Doppler flow imaging of cytoplasmic streaming using spectral domain phase microscopy,” J. Biomed. Opt. 11(2), 024014 (2006).
[CrossRef] [PubMed]

J. A. Izatt, M. D. Kulkarni, H. W. Wang, K. Kobayashi, and M. V. Sivak, “Optical coherence tomography and microscopy in gastrointestinal tissues,” IEEE J. Sel. Top. Quantum Electron. 2(4), 1017–1028 (1996).
[CrossRef]

Jacobs, R.

B. Mitchell, R. Jacobs, J. Li, S. Chien, and C. Kintner, “A positive feedback mechanism governs the polarity and motion of motile cilia,” Nature 447(7140), 97–101 (2007).
[CrossRef] [PubMed]

Jenkins, M. W.

M. W. Jenkins, L. Peterson, S. Gu, M. Gargesha, D. L. Wilson, M. Watanabe, and A. M. Rollins, “Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography,” J. Biomed. Opt. 15(6), 066022 (2010).
[CrossRef] [PubMed]

Jiao, S.

Joanny, J. F.

B. Guirao and J. F. Joanny, “Spontaneous creation of macroscopic flow and metachronal waves in an array of cilia,” Biophys. J. 92(6), 1900–1917 (2007).
[CrossRef] [PubMed]

Jung, W.

Jung, W. G.

Y. C. Ahn, W. G. Jung, and Z. P. Chen, “Optical sectioning for microfluidics: secondary flow and mixing in a meandering microchannel,” Lab Chip 8(1), 125–133 (2008).
[CrossRef] [PubMed]

Kenis, P. J. A.

A. D. Stroock, M. Weck, D. T. Chiu, W. T. S. Huck, P. J. A. Kenis, R. F. Ismagilov, and G. M. Whitesides, “Patterning electro-osmotic flow with patterned surface charge,” Phys. Rev. Lett. 84(15), 3314–3317 (2000).
[CrossRef] [PubMed]

Khokha, M. K.

M. K. Khokha, C. Chung, E. L. Bustamante, L. W. Gaw, K. A. Trott, J. Yeh, N. Lim, J. C. Lin, N. Taverner, E. Amaya, N. Papalopulu, J. C. Smith, A. M. Zorn, R. M. Harland, and T. C. Grammer, “Techniques and probes for the study of Xenopus tropicalis development,” Dev. Dyn. 225(4), 499–510 (2002).
[CrossRef] [PubMed]

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S. J. Lee and S. Kim, “Advanced particle-based velocimetry techniques for microscale flows,” Microfluidics Nanofluidics 6(5), 577–588 (2009).
[CrossRef]

Kintner, C.

B. Mitchell, J. L. Stubbs, F. Huisman, P. Taborek, C. Yu, and C. Kintner, “The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin,” Curr. Biol. 19(11), 924–929 (2009).
[CrossRef] [PubMed]

B. Mitchell, R. Jacobs, J. Li, S. Chien, and C. Kintner, “A positive feedback mechanism governs the polarity and motion of motile cilia,” Nature 447(7140), 97–101 (2007).
[CrossRef] [PubMed]

Klein, T.

Kobayashi, K.

J. A. Izatt, M. D. Kulkarni, H. W. Wang, K. Kobayashi, and M. V. Sivak, “Optical coherence tomography and microscopy in gastrointestinal tissues,” IEEE J. Sel. Top. Quantum Electron. 2(4), 1017–1028 (1996).
[CrossRef]

Kolbitsch, C.

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(6919), 172–177 (2003).
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Supplementary Material (2)

» Media 1: MOV (9519 KB)     
» Media 2: MOV (994 KB)     

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Figures (9)

Fig. 1
Fig. 1

Left: Idealized cilia-driven flow seeded with tracer particles (black dots). Velocity vectors v(x,y,z) are open-tipped arrows. The ability of OCT to perform depth-resolved imaging along its depth of focus (DOF) enables visualization of flow generated by a ciliated surface that is largely orthogonal to the optical axis. Right: Scanning electron micrograph of a ciliated Xenopus tropicalis epithelial cell. Each multicilated cell is surrounded by several non-ciliated cells. The scale bar is 5 μm.

Fig. 2
Fig. 2

Photomicrograph of stage 36 X. tropicalis embryo in a well for OCT imaging.

Fig. 3
Fig. 3

Top: Particle and embryo coordinate system. Bottom: Overview of image processing for OCT-based particle tracking velocimetry. tan−1 is the four-quadrant arctangent function.

Fig. 4
Fig. 4

OCT imaging of X. tropicalis epithelial cilia-driven flow. (a) B-scan of embryo in microparticle-seeded physiologic solution. Original image stack filtered with a 2x2x2 (x,z,t) pixel filter. (b) Background-subtracted B-mode image. The inset in (b) is the minimum projection image across all B-scans over the 5.7 s acquisition. (c) OCT pathline imaging generated by taking the maximum projection over all background-subtracted images over the 5.7 s acquisition. (d) Color-encoding of time pathline imaging. b, body; e, eye; h, head; m, microsphere; t, tail; w, water-air interface. A, anterior; P, posterior. Scale image to have square pixels. Media 1 shows the OCT movie, background-subtracted movie, and related cumulative maximum projection (i.e. cumulative particle pathline) movies.

Fig. 7
Fig. 7

OCT-based particle tracking velocimetry of non-recirculatory cilia-driven fluid flow. Note that the same embryo was imaged in Figs. 6 and 7 and only the image well water volume differs between the two image acquisition sessions. (a) shows the particle pathline image and (b) shows the two-dimensional, two-component flow velocity field. The vector arrows at the air/water interface in (b) are artifactual b, body; e, eye; h, head; ps, polystyrene microsphere; t, tail; w, air/water interface. A, anterior; P, posterior.

Fig. 5
Fig. 5

Recirculating flow patterns. Each panel is a cumulative maximum projection image (i.e. cumulative particle pathline) through the timestamp on each image. Media 2 is the movie from which these still images were taken.

Fig. 6
Fig. 6

OCT-based particle tracking velocimetry of recirculatory/vortical cilia-driven fluid flow. Note that the same embryo was imaged in Figs. 6 and 7 and only the image well water volume differs between the two image acquisition sessions. (a) shows the particle pathline image. (b) shows the two-dimensional, two-component (i.e. v = vx i + vz k) flow velocity field superimposed on the particle pathline image. The arrow direction encodes vector direction, while the arrow color encodes vector magnitude. The recirculatory/vortical whorl noted with a blue arrow in (a) has a faster fluid flow closer to the body than further away. Near the surface of the embryo, the flow is largely anterior-to-posterior (i.e. head-to-tail), while “return” flow current is in a posterior-to-anterior direction. b, body; e, eye; h, head; ps, polystyrene microsphere; t, tail; w, air/water interface. A, anterior; P, posterior.

Fig. 8
Fig. 8

Particle residence time in B-scan field of view. The embryo has the same position and orientation as in Fig. 6. The grayscale intensity of the streaks encodes the duration in the field of view. The red rectangle marks the particle that was used for the upper plots in Fig. 9, blue marks the particle used for the lower plots in Fig. 9.

Fig. 9
Fig. 9

Plots demonstrating convergence of estimated particle displacement as a function of measurements used in the estimation. The plots on the left side display mean displacement along the x-axis, the right plots mean displacement along the z-axis. The upper two plots are extracted from the pathline in the red rectangle in Fig. 8, the lower two plots are extracted from the pathline in the blue rectangle.

Equations (6)

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

I ( x , z , m Δ t ) = n = 1 N P S F ( x , z ) δ ( x x n ( m Δ t ) , z z n ( m Δ t ) ) .
x c , n = i j R O I n i P i j I i j i j R O I n P i j I i j ; z c , n = i j R O I n j P i j I i j i j R O I n P i j I i j .
Δ x n ( m Δ t ) = x n ( ( m + 1 ) Δ t ) x n ( m Δ t ) ; v x , n ( m Δ t ) = Δ x n ( m Δ t ) Δ t .
| v n ( m Δ t ) | = Δ x n 2 + Δ y n 2 + Δ z n 2 Δ t ; θ n ( m Δ t ) = tan 1 ( Δ z n Δ x n ) .
v s l i p = 2 9 r 2 ( ρ p ρ w ) η a p ,
s r m s = ( 4 D Δ t ) 1 / 2 ,

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