Abstract

Neural tube closure is a critical feature of central nervous system morphogenesis during embryonic development. Failure of this process leads to neural tube defects, one of the most common forms of human congenital defects. Although molecular and genetic studies in model organisms have provided insights into the genes and proteins that are required for normal neural tube development, complications associated with live imaging of neural tube closure in mammals limit efficient morphological analyses. Here, we report the use of optical coherence tomography (OCT) for dynamic imaging and quantitative assessment of cranial neural tube closure in live mouse embryos in culture. Through time-lapse imaging, we captured two neural tube closure mechanisms in different cranial regions, zipper-like closure of the hindbrain region and button-like closure of the midbrain region. We also used OCT imaging for phenotypic characterization of a neural tube defect in a mouse mutant. These results suggest that the described approach is a useful tool for live dynamic analysis of normal neural tube closure and neural tube defects in the mouse model.

© 2016 Optical Society of America

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2016 (5)

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

J. Men, Y. Huang, J. Solanki, X. Zeng, A. Alex, J. Jerwick, Z. Zhang, R. E. Tanzi, A. Li, and C. Zhou, “Optical Coherence Tomography for Brain Imaging and Developmental Biology,” IEEE J. Sel. Top. Quantum Electron. 22(4), 120–132 (2016).
[Crossref] [PubMed]

R. Raghunathan, M. Singh, M. E. Dickinson, and K. V. Larin, “Optical coherence tomography for embryonic imaging: a review,” J. Biomed. Opt. 21(5), 050902 (2016).
[Crossref] [PubMed]

S. Wang, D. S. Lakomy, M. D. Garcia, A. L. Lopez, K. V. Larin, and I. V. Larina, “Four-dimensional live imaging of hemodynamics in mammalian embryonic heart with Doppler optical coherence tomography,” J. Biophotonics 9(8), 837–847 (2016).
[Crossref] [PubMed]

P. Ma, S. Gu, G. H. Karunamuni, M. W. Jenkins, M. Watanabe, and A. M. Rollins, “Cardiac neural crest ablation results in early endocardial cushion and hemodynamic flow abnormalities,” Am. J. Physiol. Heart Circ. Physiol. 311(5), H1150–H1159 (2016).
[Crossref] [PubMed]

2015 (11)

A. L. Lopez, S. Wang, K. V. Larin, P. A. Overbeek, and I. V. Larina, “Live four-dimensional optical coherence tomography reveals embryonic cardiac phenotype in mouse mutant,” J. Biomed. Opt. 20(9), 090501 (2015).
[Crossref] [PubMed]

G. Karunamuni, S. Gu, Y. Q. Doughman, A. I. Noonan, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Using optical coherence tomography to rapidly phenotype and quantify congenital heart defects associated with prenatal alcohol exposure,” Dev. Dyn. 244(4), 607–618 (2015).
[Crossref] [PubMed]

A. Alex, A. Li, R. E. Tanzi, and C. Zhou, “Optogenetic pacing in Drosophila melanogaster,” Sci. Adv. 1(9), e1500639 (2015).
[Crossref] [PubMed]

P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
[PubMed]

S. H. Syed, A. J. Coughlin, M. D. Garcia, S. Wang, J. L. West, K. V. Larin, and I. V. Larina, “Optical coherence tomography guided microinjections in live mouse embryos: high-resolution targeted manipulation for mouse embryonic research,” J. Biomed. Opt. 20(5), 051020 (2015).
[Crossref] [PubMed]

S. Wang, J. C. Burton, R. R. Behringer, and I. V. Larina, “In vivo micro-scale tomography of ciliary behavior in the mammalian oviduct,” Sci. Rep. 5, 13216 (2015).
[Crossref] [PubMed]

M. Midgett, V. K. Chivukula, C. Dorn, S. Wallace, and S. Rugonyi, “Blood flow through the embryonic heart outflow tract during cardiac looping in HH13-HH18 chicken embryos,” J. R. Soc. Interface 12(111), 20150652 (2015).
[Crossref] [PubMed]

J. C. Burton, S. Wang, C. A. Stewart, R. R. Behringer, and I. V. Larina, “High-resolution three-dimensional in vivo imaging of mouse oviduct using optical coherence tomography,” Biomed. Opt. Express 6(7), 2713–2723 (2015).
[Crossref] [PubMed]

S. Wang, M. Singh, A. L. Lopez, C. Wu, R. Raghunathan, A. Schill, J. Li, K. V. Larin, and I. V. Larina, “Direct four-dimensional structural and functional imaging of cardiovascular dynamics in mouse embryos with 1.5 MHz optical coherence tomography,” Opt. Lett. 40(20), 4791–4794 (2015).
[Crossref] [PubMed]

A. Alex, A. Li, X. Zeng, R. E. Tate, M. L. McKee, D. E. Capen, Z. Zhang, R. E. Tanzi, and C. Zhou, “A Circadian Clock Gene, Cry, Affects Heart Morphogenesis and Function in Drosophila as Revealed by Optical Coherence Microscopy,” PLoS One 10(9), e0137236 (2015).
[Crossref] [PubMed]

S. G. McShane, M. A. Molè, D. Savery, N. D. E. Greene, P. P. L. Tam, and A. J. Copp, “Cellular basis of neuroepithelial bending during mouse spinal neural tube closure,” Dev. Biol. 404(2), 113–124 (2015).
[Crossref] [PubMed]

2014 (3)

G. H. Karunamuni, S. Gu, M. R. Ford, L. M. Peterson, P. Ma, Y. T. Wang, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Capturing structure and function in an embryonic heart with biophotonic tools,” Front. Physiol. 5, 351 (2014).
[Crossref] [PubMed]

W. Wieser, W. Draxinger, T. Klein, S. Karpf, T. Pfeiffer, and R. Huber, “High definition live 3D-OCT in vivo: design and evaluation of a 4D OCT engine with 1 GVoxel/s,” Biomed. Opt. Express 5(9), 2963–2977 (2014).
[Crossref] [PubMed]

M. Midgett, S. Goenezen, and S. Rugonyi, “Blood flow dynamics reflect degree of outflow tract banding in Hamburger-Hamilton stage 18 chicken embryos,” J. R. Soc. Interface 11(100), 20140643 (2014).
[Crossref] [PubMed]

2013 (4)

A. Li, O. O. Ahsen, J. J. Liu, C. Du, M. L. McKee, Y. Yang, W. Wasco, C. H. Newton-Cheh, C. J. O’Donnell, J. G. Fujimoto, C. Zhou, and R. E. Tanzi, “Silencing of the Drosophila ortholog of SOX5 in heart leads to cardiac dysfunction as detected by optical coherence tomography,” Hum. Mol. Genet. 22(18), 3798–3806 (2013).
[Crossref] [PubMed]

R. Massarwa and L. Niswander, “In toto live imaging of mouse morphogenesis and new insights into neural tube closure,” Development 140(1), 226–236 (2013).
[Crossref] [PubMed]

Y. Yamaguchi and M. Miura, “How to form and close the brain: insight into the mechanism of cranial neural tube closure in mammals,” Cell. Mol. Life Sci. 70(17), 3171–3186 (2013).
[Crossref] [PubMed]

A. Osterhues, N. S. Ali, and K. B. Michels, “The Role of Folic Acid Fortification in Neural Tube Defects: A Review,” Crit. Rev. Food Sci. Nutr. 53(11), 1180–1190 (2013).
[Crossref] [PubMed]

2012 (5)

M. Rădulescu, E. C. Ulmeanu, M. Nedelea, and A. Oncescu, “Prenatal ultrasound diagnosis of neural tube defects. Pictorial essay,” Med. Ultrason. 14(2), 147–153 (2012).
[PubMed]

A. Ashe, N. C. Butterfield, L. Town, A. D. Courtney, A. N. Cooper, C. Ferguson, R. Barry, F. Olsson, K. F. Liem, R. G. Parton, B. J. Wainwright, K. V. Anderson, E. Whitelaw, and C. Wicking, “Mutations in mouse Ift144 model the craniofacial, limb and rib defects in skeletal ciliopathies,” Hum. Mol. Genet. 21(8), 1808–1823 (2012).
[Crossref] [PubMed]

A. Liu, X. Yin, L. Shi, P. Li, K. L. Thornburg, R. Wang, and S. Rugonyi, “Biomechanics of the Chick Embryonic Heart Outflow Tract at HH18 Using 4D Optical Coherence Tomography Imaging and Computational Modeling,” PLoS One 7(7), e40869 (2012).
[Crossref] [PubMed]

I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Sequential Turning Acquisition and Reconstruction (STAR) method for four-dimensional imaging of cyclically moving structures,” Biomed. Opt. Express 3(3), 650–660 (2012).
[Crossref] [PubMed]

L. M. Peterson, M. W. Jenkins, S. Gu, L. Barwick, M. Watanabe, and A. M. Rollins, “4D shear stress maps of the developing heart using Doppler optical coherence tomography,” Biomed. Opt. Express 3(11), 3022–3032 (2012).
[Crossref] [PubMed]

2011 (4)

P. Li, X. Yin, L. Shi, A. Liu, S. Rugonyi, and R. Wang, “Measurement of strain and strain rate in embryonic chick heart in vivo using spectral domain optical coherence tomography,” IEEE Trans. Biomed. Eng. 58(8), 2333–2338 (2011).
[PubMed]

L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med. 17(8), 1010–1014 (2011).
[Crossref] [PubMed]

P. Hahn, J. Migacz, R. O’Connell, R. S. Maldonado, J. A. Izatt, and C. A. Toth, “The Use of Optical Coherence Tomography in Intraoperative Ophthalmic Imaging,” Ophthalmic Surg. Lasers Imaging 42(4Suppl), S85–S94 (2011).
[Crossref] [PubMed]

Y. Yamaguchi, N. Shinotsuka, K. Nonomura, K. Takemoto, K. Kuida, H. Yosida, and M. Miura, “Live imaging of apoptosis in a novel transgenic mouse highlights its role in neural tube closure,” J. Cell Biol. 195(6), 1047–1060 (2011).
[Crossref] [PubMed]

2010 (5)

C. Pyrgaki, P. Trainor, A. K. Hadjantonakis, and L. Niswander, “Dynamic imaging of mammalian neural tube closure,” Dev. Biol. 344(2), 941–947 (2010).
[Crossref] [PubMed]

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, 066022 (2010).

A. J. Copp and N. D. E. Greene, “Genetics and development of neural tube defects,” J. Pathol. 220(2), 217–230 (2010).
[PubMed]

C. Zhou, Y. Wang, A. D. Aguirre, T.-H. Tsai, D. W. Cohen, J. L. Connolly, and J. G. Fujimoto, “Ex vivo imaging of human thyroid pathology using integrated optical coherence tomography and optical coherence microscopy,” J. Biomed. Opt. 15(1), 016001 (2010).
[Crossref] [PubMed]

C. Zhou, D. W. Cohen, Y. Wang, H.-C. Lee, A. E. Mondelblatt, T.-H. Tsai, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Integrated Optical Coherence Tomography and Microscopy for Ex Vivo Multiscale Evaluation of Human Breast Tissues,” Cancer Res. 70(24), 10071–10079 (2010).
[Crossref] [PubMed]

2009 (4)

A. Liu, R. Wang, K. L. Thornburg, and S. Rugonyi, “Efficient postacquisition synchronization of 4-D nongated cardiac images obtained from optical coherence tomography: application to 4-D reconstruction of the chick embryonic heart,” J. Biomed. Opt. 14, 044020 (2009).

V. Massa, D. Savery, P. Ybot-Gonzalez, E. Ferraro, A. Rongvaux, F. Cecconi, R. Flavell, N. D. E. Greene, and A. J. Copp, “Apoptosis is not required for mammalian neural tube closure,” Proc. Natl. Acad. Sci. U.S.A. 106(20), 8233–8238 (2009).
[Crossref] [PubMed]

H. G. Bezerra, M. A. Costa, G. Guagliumi, A. M. Rollins, and D. I. Simon, “Intracoronary Optical Coherence Tomography: A Comprehensive Review Clinical and Research Applications,” JACC Cardiovasc. Interv. 2(11), 1035–1046 (2009).
[Crossref] [PubMed]

F. T. Nguyen, A. M. Zysk, E. J. Chaney, J. G. Kotynek, U. J. Oliphant, F. J. Bellafiore, K. M. Rowland, P. A. Johnson, and S. A. Boppart, “Intraoperative Evaluation of Breast Tumor Margins with Optical Coherence Tomography,” Cancer Res. 69(22), 8790–8796 (2009).
[Crossref] [PubMed]

2007 (2)

M. J. Harris and D. M. Juriloff, “Mouse mutants with neural tube closure defects and their role in understanding human neural tube defects,” Birth Defects Res. A Clin. Mol. Teratol. 79(3), 187–210 (2007).
[Crossref] [PubMed]

M. W. Jenkins, O. Q. Chughtai, A. N. Basavanhally, M. Watanabe, and A. M. Rollins, “In vivo gated 4D imaging of the embryonic heart using optical coherence tomography,” J. Biomed. Opt. 12(3), 030505 (2007).
[Crossref] [PubMed]

2006 (2)

W. Luo, D. L. Marks, T. S. Ralston, and S. A. Boppart, “Three-dimensional optical coherence tomography of the embryonic murine cardiovascular system,” J. Biomed. Opt. 11(2), 021014 (2006).
[Crossref] [PubMed]

J. M. Rhee, M. K. Pirity, C. S. Lackan, J. Z. Long, G. Kondoh, J. Takeda, and A. K. Hadjantonakis, “In vivo imaging and differential localization of lipid-modified GFP-variant fusions in embryonic stem cells and mice,” Genesis 44(4), 202–218 (2006).
[Crossref] [PubMed]

2003 (2)

S. A. Boppart, “Optical coherence tomography: technology and applications for neuroimaging,” Psychophysiology 40(4), 529–541 (2003).
[Crossref] [PubMed]

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]

2002 (2)

T. M. Yelbuz, M. A. Choma, L. Thrane, M. L. Kirby, and J. A. Izatt, “Optical coherence tomography: a new high-resolution imaging technology to study cardiac development in chick embryos,” Circulation 106(22), 2771–2774 (2002).
[Crossref] [PubMed]

E. A. V. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
[Crossref] [PubMed]

2001 (1)

J.-F. Colas and G. C. Schoenwolf, “Towards a cellular and molecular understanding of neurulation,” Dev. Dyn. 221(2), 117–145 (2001).
[Crossref] [PubMed]

2000 (1)

D. M. Juriloff and M. J. Harris, “Mouse models for neural tube closure defects,” Hum. Mol. Genet. 9(6), 993–1000 (2000).
[Crossref] [PubMed]

1999 (2)

L. D. Botto, C. A. Moore, M. J. Khoury, and J. D. Erickson, “Neural-Tube Defects,” N. Engl. J. Med. 341(20), 1509–1519 (1999).
[Crossref] [PubMed]

D. H. Turnbull, “In utero ultrasound backscatter microscopy of early stage mouse embryos,” Comput. Med. Imaging Graph. 23(1), 25–31 (1999).
[Crossref] [PubMed]

1997 (1)

S. A. Boppart, G. J. Tearney, B. E. Bouma, J. F. Southern, M. E. Brezinski, and J. G. Fujimoto, “Noninvasive assessment of the developing Xenopus cardiovascular system using optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 94(9), 4256–4261 (1997).
[Crossref] [PubMed]

1995 (1)

D. H. Turnbull, T. S. Bloomfield, H. S. Baldwin, F. S. Foster, and A. L. Joyner, “Ultrasound backscatter microscope analysis of early mouse embryonic brain development,” Proc. Natl. Acad. Sci. U.S.A. 92(6), 2239–2243 (1995).
[Crossref] [PubMed]

1994 (1)

G. Morriss-Kay, H. Wood, and W. H. Chen, “Normal neurulation in mammals,” Ciba Foundation symposium 181, 51–63 (1994).

1991 (3)

M. V. S. R. Group and MRC Vitamin Study Research Group, “Prevention of neural tube defects: Results of the Medical Research Council Vitamin Study,” Lancet 338(8760), 131–137 (1991).
[Crossref] [PubMed]

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

T. Gridley, P. Soriano, and R. Jaenisch, “Insertional versus targeted mutagenesis in mice,” New Biol. 3(11), 1025–1034 (1991).
[PubMed]

1990 (1)

G. C. Schoenwolf and J. L. Smith, “Mechanisms of neurulation: traditional viewpoint and recent advances,” Development 109(2), 243–270 (1990).
[PubMed]

1988 (1)

R. J. Lemire, “Neural tube defects,” JAMA 259(4), 558–562 (1988).
[Crossref] [PubMed]

1986 (1)

L. R. Campbell, D. H. Dayton, and G. S. Sohal, “Neural tube defects: A review of human and animal studies on the etiology of neural tube defects,” Teratology 34(2), 171–187 (1986).
[Crossref] [PubMed]

Aguirre, A. D.

C. Zhou, Y. Wang, A. D. Aguirre, T.-H. Tsai, D. W. Cohen, J. L. Connolly, and J. G. Fujimoto, “Ex vivo imaging of human thyroid pathology using integrated optical coherence tomography and optical coherence microscopy,” J. Biomed. Opt. 15(1), 016001 (2010).
[Crossref] [PubMed]

C. Zhou, D. W. Cohen, Y. Wang, H.-C. Lee, A. E. Mondelblatt, T.-H. Tsai, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Integrated Optical Coherence Tomography and Microscopy for Ex Vivo Multiscale Evaluation of Human Breast Tissues,” Cancer Res. 70(24), 10071–10079 (2010).
[Crossref] [PubMed]

Ahsen, O. O.

A. Li, O. O. Ahsen, J. J. Liu, C. Du, M. L. McKee, Y. Yang, W. Wasco, C. H. Newton-Cheh, C. J. O’Donnell, J. G. Fujimoto, C. Zhou, and R. E. Tanzi, “Silencing of the Drosophila ortholog of SOX5 in heart leads to cardiac dysfunction as detected by optical coherence tomography,” Hum. Mol. Genet. 22(18), 3798–3806 (2013).
[Crossref] [PubMed]

Alex, A.

J. Men, Y. Huang, J. Solanki, X. Zeng, A. Alex, J. Jerwick, Z. Zhang, R. E. Tanzi, A. Li, and C. Zhou, “Optical Coherence Tomography for Brain Imaging and Developmental Biology,” IEEE J. Sel. Top. Quantum Electron. 22(4), 120–132 (2016).
[Crossref] [PubMed]

A. Alex, A. Li, X. Zeng, R. E. Tate, M. L. McKee, D. E. Capen, Z. Zhang, R. E. Tanzi, and C. Zhou, “A Circadian Clock Gene, Cry, Affects Heart Morphogenesis and Function in Drosophila as Revealed by Optical Coherence Microscopy,” PLoS One 10(9), e0137236 (2015).
[Crossref] [PubMed]

A. Alex, A. Li, R. E. Tanzi, and C. Zhou, “Optogenetic pacing in Drosophila melanogaster,” Sci. Adv. 1(9), e1500639 (2015).
[Crossref] [PubMed]

Ali, N. S.

A. Osterhues, N. S. Ali, and K. B. Michels, “The Role of Folic Acid Fortification in Neural Tube Defects: A Review,” Crit. Rev. Food Sci. Nutr. 53(11), 1180–1190 (2013).
[Crossref] [PubMed]

Anderson, K. V.

A. Ashe, N. C. Butterfield, L. Town, A. D. Courtney, A. N. Cooper, C. Ferguson, R. Barry, F. Olsson, K. F. Liem, R. G. Parton, B. J. Wainwright, K. V. Anderson, E. Whitelaw, and C. Wicking, “Mutations in mouse Ift144 model the craniofacial, limb and rib defects in skeletal ciliopathies,” Hum. Mol. Genet. 21(8), 1808–1823 (2012).
[Crossref] [PubMed]

Ashe, A.

A. Ashe, N. C. Butterfield, L. Town, A. D. Courtney, A. N. Cooper, C. Ferguson, R. Barry, F. Olsson, K. F. Liem, R. G. Parton, B. J. Wainwright, K. V. Anderson, E. Whitelaw, and C. Wicking, “Mutations in mouse Ift144 model the craniofacial, limb and rib defects in skeletal ciliopathies,” Hum. Mol. Genet. 21(8), 1808–1823 (2012).
[Crossref] [PubMed]

Baldwin, H. S.

D. H. Turnbull, T. S. Bloomfield, H. S. Baldwin, F. S. Foster, and A. L. Joyner, “Ultrasound backscatter microscope analysis of early mouse embryonic brain development,” Proc. Natl. Acad. Sci. U.S.A. 92(6), 2239–2243 (1995).
[Crossref] [PubMed]

Baran, U.

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

Baron, M. H.

E. A. V. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
[Crossref] [PubMed]

Barry, R.

A. Ashe, N. C. Butterfield, L. Town, A. D. Courtney, A. N. Cooper, C. Ferguson, R. Barry, F. Olsson, K. F. Liem, R. G. Parton, B. J. Wainwright, K. V. Anderson, E. Whitelaw, and C. Wicking, “Mutations in mouse Ift144 model the craniofacial, limb and rib defects in skeletal ciliopathies,” Hum. Mol. Genet. 21(8), 1808–1823 (2012).
[Crossref] [PubMed]

Barwick, L.

Basavanhally, A. N.

M. W. Jenkins, O. Q. Chughtai, A. N. Basavanhally, M. Watanabe, and A. M. Rollins, “In vivo gated 4D imaging of the embryonic heart using optical coherence tomography,” J. Biomed. Opt. 12(3), 030505 (2007).
[Crossref] [PubMed]

Behringer, R. R.

Bellafiore, F. J.

F. T. Nguyen, A. M. Zysk, E. J. Chaney, J. G. Kotynek, U. J. Oliphant, F. J. Bellafiore, K. M. Rowland, P. A. Johnson, and S. A. Boppart, “Intraoperative Evaluation of Breast Tumor Margins with Optical Coherence Tomography,” Cancer Res. 69(22), 8790–8796 (2009).
[Crossref] [PubMed]

Bezerra, H. G.

H. G. Bezerra, M. A. Costa, G. Guagliumi, A. M. Rollins, and D. I. Simon, “Intracoronary Optical Coherence Tomography: A Comprehensive Review Clinical and Research Applications,” JACC Cardiovasc. Interv. 2(11), 1035–1046 (2009).
[Crossref] [PubMed]

Bloomfield, T. S.

D. H. Turnbull, T. S. Bloomfield, H. S. Baldwin, F. S. Foster, and A. L. Joyner, “Ultrasound backscatter microscope analysis of early mouse embryonic brain development,” Proc. Natl. Acad. Sci. U.S.A. 92(6), 2239–2243 (1995).
[Crossref] [PubMed]

Boppart, S. A.

F. T. Nguyen, A. M. Zysk, E. J. Chaney, J. G. Kotynek, U. J. Oliphant, F. J. Bellafiore, K. M. Rowland, P. A. Johnson, and S. A. Boppart, “Intraoperative Evaluation of Breast Tumor Margins with Optical Coherence Tomography,” Cancer Res. 69(22), 8790–8796 (2009).
[Crossref] [PubMed]

W. Luo, D. L. Marks, T. S. Ralston, and S. A. Boppart, “Three-dimensional optical coherence tomography of the embryonic murine cardiovascular system,” J. Biomed. Opt. 11(2), 021014 (2006).
[Crossref] [PubMed]

S. A. Boppart, “Optical coherence tomography: technology and applications for neuroimaging,” Psychophysiology 40(4), 529–541 (2003).
[Crossref] [PubMed]

S. A. Boppart, G. J. Tearney, B. E. Bouma, J. F. Southern, M. E. Brezinski, and J. G. Fujimoto, “Noninvasive assessment of the developing Xenopus cardiovascular system using optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 94(9), 4256–4261 (1997).
[Crossref] [PubMed]

Botto, L. D.

L. D. Botto, C. A. Moore, M. J. Khoury, and J. D. Erickson, “Neural-Tube Defects,” N. Engl. J. Med. 341(20), 1509–1519 (1999).
[Crossref] [PubMed]

Bouma, B. E.

L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med. 17(8), 1010–1014 (2011).
[Crossref] [PubMed]

S. A. Boppart, G. J. Tearney, B. E. Bouma, J. F. Southern, M. E. Brezinski, and J. G. Fujimoto, “Noninvasive assessment of the developing Xenopus cardiovascular system using optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 94(9), 4256–4261 (1997).
[Crossref] [PubMed]

Brezinski, M. E.

S. A. Boppart, G. J. Tearney, B. E. Bouma, J. F. Southern, M. E. Brezinski, and J. G. Fujimoto, “Noninvasive assessment of the developing Xenopus cardiovascular system using optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 94(9), 4256–4261 (1997).
[Crossref] [PubMed]

Burton, J. C.

Butterfield, N. C.

A. Ashe, N. C. Butterfield, L. Town, A. D. Courtney, A. N. Cooper, C. Ferguson, R. Barry, F. Olsson, K. F. Liem, R. G. Parton, B. J. Wainwright, K. V. Anderson, E. Whitelaw, and C. Wicking, “Mutations in mouse Ift144 model the craniofacial, limb and rib defects in skeletal ciliopathies,” Hum. Mol. Genet. 21(8), 1808–1823 (2012).
[Crossref] [PubMed]

Campbell, L. R.

L. R. Campbell, D. H. Dayton, and G. S. Sohal, “Neural tube defects: A review of human and animal studies on the etiology of neural tube defects,” Teratology 34(2), 171–187 (1986).
[Crossref] [PubMed]

Capen, D. E.

A. Alex, A. Li, X. Zeng, R. E. Tate, M. L. McKee, D. E. Capen, Z. Zhang, R. E. Tanzi, and C. Zhou, “A Circadian Clock Gene, Cry, Affects Heart Morphogenesis and Function in Drosophila as Revealed by Optical Coherence Microscopy,” PLoS One 10(9), e0137236 (2015).
[Crossref] [PubMed]

Cecconi, F.

V. Massa, D. Savery, P. Ybot-Gonzalez, E. Ferraro, A. Rongvaux, F. Cecconi, R. Flavell, N. D. E. Greene, and A. J. Copp, “Apoptosis is not required for mammalian neural tube closure,” Proc. Natl. Acad. Sci. U.S.A. 106(20), 8233–8238 (2009).
[Crossref] [PubMed]

Chaney, E. J.

F. T. Nguyen, A. M. Zysk, E. J. Chaney, J. G. Kotynek, U. J. Oliphant, F. J. Bellafiore, K. M. Rowland, P. A. Johnson, and S. A. Boppart, “Intraoperative Evaluation of Breast Tumor Margins with Optical Coherence Tomography,” Cancer Res. 69(22), 8790–8796 (2009).
[Crossref] [PubMed]

Chang, W.

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

Chen, W. H.

G. Morriss-Kay, H. Wood, and W. H. Chen, “Normal neurulation in mammals,” Ciba Foundation symposium 181, 51–63 (1994).

Chivukula, V. K.

M. Midgett, V. K. Chivukula, C. Dorn, S. Wallace, and S. Rugonyi, “Blood flow through the embryonic heart outflow tract during cardiac looping in HH13-HH18 chicken embryos,” J. R. Soc. Interface 12(111), 20150652 (2015).
[Crossref] [PubMed]

Choma, M. A.

T. M. Yelbuz, M. A. Choma, L. Thrane, M. L. Kirby, and J. A. Izatt, “Optical coherence tomography: a new high-resolution imaging technology to study cardiac development in chick embryos,” Circulation 106(22), 2771–2774 (2002).
[Crossref] [PubMed]

Chughtai, O. Q.

M. W. Jenkins, O. Q. Chughtai, A. N. Basavanhally, M. Watanabe, and A. M. Rollins, “In vivo gated 4D imaging of the embryonic heart using optical coherence tomography,” J. Biomed. Opt. 12(3), 030505 (2007).
[Crossref] [PubMed]

Cohen, D. W.

C. Zhou, Y. Wang, A. D. Aguirre, T.-H. Tsai, D. W. Cohen, J. L. Connolly, and J. G. Fujimoto, “Ex vivo imaging of human thyroid pathology using integrated optical coherence tomography and optical coherence microscopy,” J. Biomed. Opt. 15(1), 016001 (2010).
[Crossref] [PubMed]

C. Zhou, D. W. Cohen, Y. Wang, H.-C. Lee, A. E. Mondelblatt, T.-H. Tsai, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Integrated Optical Coherence Tomography and Microscopy for Ex Vivo Multiscale Evaluation of Human Breast Tissues,” Cancer Res. 70(24), 10071–10079 (2010).
[Crossref] [PubMed]

Colas, J.-F.

J.-F. Colas and G. C. Schoenwolf, “Towards a cellular and molecular understanding of neurulation,” Dev. Dyn. 221(2), 117–145 (2001).
[Crossref] [PubMed]

Connolly, J. L.

C. Zhou, Y. Wang, A. D. Aguirre, T.-H. Tsai, D. W. Cohen, J. L. Connolly, and J. G. Fujimoto, “Ex vivo imaging of human thyroid pathology using integrated optical coherence tomography and optical coherence microscopy,” J. Biomed. Opt. 15(1), 016001 (2010).
[Crossref] [PubMed]

C. Zhou, D. W. Cohen, Y. Wang, H.-C. Lee, A. E. Mondelblatt, T.-H. Tsai, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Integrated Optical Coherence Tomography and Microscopy for Ex Vivo Multiscale Evaluation of Human Breast Tissues,” Cancer Res. 70(24), 10071–10079 (2010).
[Crossref] [PubMed]

Cooper, A. N.

A. Ashe, N. C. Butterfield, L. Town, A. D. Courtney, A. N. Cooper, C. Ferguson, R. Barry, F. Olsson, K. F. Liem, R. G. Parton, B. J. Wainwright, K. V. Anderson, E. Whitelaw, and C. Wicking, “Mutations in mouse Ift144 model the craniofacial, limb and rib defects in skeletal ciliopathies,” Hum. Mol. Genet. 21(8), 1808–1823 (2012).
[Crossref] [PubMed]

Copp, A. J.

S. G. McShane, M. A. Molè, D. Savery, N. D. E. Greene, P. P. L. Tam, and A. J. Copp, “Cellular basis of neuroepithelial bending during mouse spinal neural tube closure,” Dev. Biol. 404(2), 113–124 (2015).
[Crossref] [PubMed]

A. J. Copp and N. D. E. Greene, “Genetics and development of neural tube defects,” J. Pathol. 220(2), 217–230 (2010).
[PubMed]

V. Massa, D. Savery, P. Ybot-Gonzalez, E. Ferraro, A. Rongvaux, F. Cecconi, R. Flavell, N. D. E. Greene, and A. J. Copp, “Apoptosis is not required for mammalian neural tube closure,” Proc. Natl. Acad. Sci. U.S.A. 106(20), 8233–8238 (2009).
[Crossref] [PubMed]

Costa, M. A.

H. G. Bezerra, M. A. Costa, G. Guagliumi, A. M. Rollins, and D. I. Simon, “Intracoronary Optical Coherence Tomography: A Comprehensive Review Clinical and Research Applications,” JACC Cardiovasc. Interv. 2(11), 1035–1046 (2009).
[Crossref] [PubMed]

Coughlin, A. J.

S. H. Syed, A. J. Coughlin, M. D. Garcia, S. Wang, J. L. West, K. V. Larin, and I. V. Larina, “Optical coherence tomography guided microinjections in live mouse embryos: high-resolution targeted manipulation for mouse embryonic research,” J. Biomed. Opt. 20(5), 051020 (2015).
[Crossref] [PubMed]

Courtney, A. D.

A. Ashe, N. C. Butterfield, L. Town, A. D. Courtney, A. N. Cooper, C. Ferguson, R. Barry, F. Olsson, K. F. Liem, R. G. Parton, B. J. Wainwright, K. V. Anderson, E. Whitelaw, and C. Wicking, “Mutations in mouse Ift144 model the craniofacial, limb and rib defects in skeletal ciliopathies,” Hum. Mol. Genet. 21(8), 1808–1823 (2012).
[Crossref] [PubMed]

Crotty, D.

E. A. V. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
[Crossref] [PubMed]

Dayton, D. H.

L. R. Campbell, D. H. Dayton, and G. S. Sohal, “Neural tube defects: A review of human and animal studies on the etiology of neural tube defects,” Teratology 34(2), 171–187 (1986).
[Crossref] [PubMed]

Dickinson, M. E.

R. Raghunathan, M. Singh, M. E. Dickinson, and K. V. Larin, “Optical coherence tomography for embryonic imaging: a review,” J. Biomed. Opt. 21(5), 050902 (2016).
[Crossref] [PubMed]

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E. A. V. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
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G. Karunamuni, S. Gu, Y. Q. Doughman, A. I. Noonan, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Using optical coherence tomography to rapidly phenotype and quantify congenital heart defects associated with prenatal alcohol exposure,” Dev. Dyn. 244(4), 607–618 (2015).
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Drexler, W.

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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L. D. Botto, C. A. Moore, M. J. Khoury, and J. D. Erickson, “Neural-Tube Defects,” N. Engl. J. Med. 341(20), 1509–1519 (1999).
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D. H. Turnbull, T. S. Bloomfield, H. S. Baldwin, F. S. Foster, and A. L. Joyner, “Ultrasound backscatter microscope analysis of early mouse embryonic brain development,” Proc. Natl. Acad. Sci. U.S.A. 92(6), 2239–2243 (1995).
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E. A. V. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
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A. Li, O. O. Ahsen, J. J. Liu, C. Du, M. L. McKee, Y. Yang, W. Wasco, C. H. Newton-Cheh, C. J. O’Donnell, J. G. Fujimoto, C. Zhou, and R. E. Tanzi, “Silencing of the Drosophila ortholog of SOX5 in heart leads to cardiac dysfunction as detected by optical coherence tomography,” Hum. Mol. Genet. 22(18), 3798–3806 (2013).
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C. Zhou, D. W. Cohen, Y. Wang, H.-C. Lee, A. E. Mondelblatt, T.-H. Tsai, A. D. Aguirre, J. G. Fujimoto, and J. L. Connolly, “Integrated Optical Coherence Tomography and Microscopy for Ex Vivo Multiscale Evaluation of Human Breast Tissues,” Cancer Res. 70(24), 10071–10079 (2010).
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P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
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S. Wang, D. S. Lakomy, M. D. Garcia, A. L. Lopez, K. V. Larin, and I. V. Larina, “Four-dimensional live imaging of hemodynamics in mammalian embryonic heart with Doppler optical coherence tomography,” J. Biophotonics 9(8), 837–847 (2016).
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S. H. Syed, A. J. Coughlin, M. D. Garcia, S. Wang, J. L. West, K. V. Larin, and I. V. Larina, “Optical coherence tomography guided microinjections in live mouse embryos: high-resolution targeted manipulation for mouse embryonic research,” J. Biomed. Opt. 20(5), 051020 (2015).
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M. Midgett, S. Goenezen, and S. Rugonyi, “Blood flow dynamics reflect degree of outflow tract banding in Hamburger-Hamilton stage 18 chicken embryos,” J. R. Soc. Interface 11(100), 20140643 (2014).
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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 et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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G. Karunamuni, S. Gu, Y. Q. Doughman, A. I. Noonan, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Using optical coherence tomography to rapidly phenotype and quantify congenital heart defects associated with prenatal alcohol exposure,” Dev. Dyn. 244(4), 607–618 (2015).
[Crossref] [PubMed]

G. H. Karunamuni, S. Gu, M. R. Ford, L. M. Peterson, P. Ma, Y. T. Wang, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Capturing structure and function in an embryonic heart with biophotonic tools,” Front. Physiol. 5, 351 (2014).
[Crossref] [PubMed]

L. M. Peterson, M. W. Jenkins, S. Gu, L. Barwick, M. Watanabe, and A. M. Rollins, “4D shear stress maps of the developing heart using Doppler optical coherence tomography,” Biomed. Opt. Express 3(11), 3022–3032 (2012).
[Crossref] [PubMed]

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, 066022 (2010).

Guagliumi, G.

H. G. Bezerra, M. A. Costa, G. Guagliumi, A. M. Rollins, and D. I. Simon, “Intracoronary Optical Coherence Tomography: A Comprehensive Review Clinical and Research Applications,” JACC Cardiovasc. Interv. 2(11), 1035–1046 (2009).
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M. J. Harris and D. M. Juriloff, “Mouse mutants with neural tube closure defects and their role in understanding human neural tube defects,” Birth Defects Res. A Clin. Mol. Teratol. 79(3), 187–210 (2007).
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D. M. Juriloff and M. J. Harris, “Mouse models for neural tube closure defects,” Hum. Mol. Genet. 9(6), 993–1000 (2000).
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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 et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Hitzenberger, C. K.

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]

Huang, D.

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 et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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Huang, Y.

J. Men, Y. Huang, J. Solanki, X. Zeng, A. Alex, J. Jerwick, Z. Zhang, R. E. Tanzi, A. Li, and C. Zhou, “Optical Coherence Tomography for Brain Imaging and Developmental Biology,” IEEE J. Sel. Top. Quantum Electron. 22(4), 120–132 (2016).
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Huber, R.

Izatt, J. A.

P. Hahn, J. Migacz, R. O’Connell, R. S. Maldonado, J. A. Izatt, and C. A. Toth, “The Use of Optical Coherence Tomography in Intraoperative Ophthalmic Imaging,” Ophthalmic Surg. Lasers Imaging 42(4Suppl), S85–S94 (2011).
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T. M. Yelbuz, M. A. Choma, L. Thrane, M. L. Kirby, and J. A. Izatt, “Optical coherence tomography: a new high-resolution imaging technology to study cardiac development in chick embryos,” Circulation 106(22), 2771–2774 (2002).
[Crossref] [PubMed]

Jaenisch, R.

T. Gridley, P. Soriano, and R. Jaenisch, “Insertional versus targeted mutagenesis in mice,” New Biol. 3(11), 1025–1034 (1991).
[PubMed]

Jenkins, M. W.

P. Ma, S. Gu, G. H. Karunamuni, M. W. Jenkins, M. Watanabe, and A. M. Rollins, “Cardiac neural crest ablation results in early endocardial cushion and hemodynamic flow abnormalities,” Am. J. Physiol. Heart Circ. Physiol. 311(5), H1150–H1159 (2016).
[Crossref] [PubMed]

G. Karunamuni, S. Gu, Y. Q. Doughman, A. I. Noonan, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Using optical coherence tomography to rapidly phenotype and quantify congenital heart defects associated with prenatal alcohol exposure,” Dev. Dyn. 244(4), 607–618 (2015).
[Crossref] [PubMed]

G. H. Karunamuni, S. Gu, M. R. Ford, L. M. Peterson, P. Ma, Y. T. Wang, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Capturing structure and function in an embryonic heart with biophotonic tools,” Front. Physiol. 5, 351 (2014).
[Crossref] [PubMed]

L. M. Peterson, M. W. Jenkins, S. Gu, L. Barwick, M. Watanabe, and A. M. Rollins, “4D shear stress maps of the developing heart using Doppler optical coherence tomography,” Biomed. Opt. Express 3(11), 3022–3032 (2012).
[Crossref] [PubMed]

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, 066022 (2010).

M. W. Jenkins, O. Q. Chughtai, A. N. Basavanhally, M. Watanabe, and A. M. Rollins, “In vivo gated 4D imaging of the embryonic heart using optical coherence tomography,” J. Biomed. Opt. 12(3), 030505 (2007).
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Jerwick, J.

J. Men, Y. Huang, J. Solanki, X. Zeng, A. Alex, J. Jerwick, Z. Zhang, R. E. Tanzi, A. Li, and C. Zhou, “Optical Coherence Tomography for Brain Imaging and Developmental Biology,” IEEE J. Sel. Top. Quantum Electron. 22(4), 120–132 (2016).
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Johnson, P. A.

F. T. Nguyen, A. M. Zysk, E. J. Chaney, J. G. Kotynek, U. J. Oliphant, F. J. Bellafiore, K. M. Rowland, P. A. Johnson, and S. A. Boppart, “Intraoperative Evaluation of Breast Tumor Margins with Optical Coherence Tomography,” Cancer Res. 69(22), 8790–8796 (2009).
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Jones, E. A. V.

E. A. V. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
[Crossref] [PubMed]

Joyner, A. L.

D. H. Turnbull, T. S. Bloomfield, H. S. Baldwin, F. S. Foster, and A. L. Joyner, “Ultrasound backscatter microscope analysis of early mouse embryonic brain development,” Proc. Natl. Acad. Sci. U.S.A. 92(6), 2239–2243 (1995).
[Crossref] [PubMed]

Juriloff, D. M.

M. J. Harris and D. M. Juriloff, “Mouse mutants with neural tube closure defects and their role in understanding human neural tube defects,” Birth Defects Res. A Clin. Mol. Teratol. 79(3), 187–210 (2007).
[Crossref] [PubMed]

D. M. Juriloff and M. J. Harris, “Mouse models for neural tube closure defects,” Hum. Mol. Genet. 9(6), 993–1000 (2000).
[Crossref] [PubMed]

Karpf, S.

Karunamuni, G.

G. Karunamuni, S. Gu, Y. Q. Doughman, A. I. Noonan, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Using optical coherence tomography to rapidly phenotype and quantify congenital heart defects associated with prenatal alcohol exposure,” Dev. Dyn. 244(4), 607–618 (2015).
[Crossref] [PubMed]

Karunamuni, G. H.

P. Ma, S. Gu, G. H. Karunamuni, M. W. Jenkins, M. Watanabe, and A. M. Rollins, “Cardiac neural crest ablation results in early endocardial cushion and hemodynamic flow abnormalities,” Am. J. Physiol. Heart Circ. Physiol. 311(5), H1150–H1159 (2016).
[Crossref] [PubMed]

G. H. Karunamuni, S. Gu, M. R. Ford, L. M. Peterson, P. Ma, Y. T. Wang, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Capturing structure and function in an embryonic heart with biophotonic tools,” Front. Physiol. 5, 351 (2014).
[Crossref] [PubMed]

Khoury, M. J.

L. D. Botto, C. A. Moore, M. J. Khoury, and J. D. Erickson, “Neural-Tube Defects,” N. Engl. J. Med. 341(20), 1509–1519 (1999).
[Crossref] [PubMed]

Kirby, M. L.

T. M. Yelbuz, M. A. Choma, L. Thrane, M. L. Kirby, and J. A. Izatt, “Optical coherence tomography: a new high-resolution imaging technology to study cardiac development in chick embryos,” Circulation 106(22), 2771–2774 (2002).
[Crossref] [PubMed]

Klein, T.

Kondoh, G.

J. M. Rhee, M. K. Pirity, C. S. Lackan, J. Z. Long, G. Kondoh, J. Takeda, and A. K. Hadjantonakis, “In vivo imaging and differential localization of lipid-modified GFP-variant fusions in embryonic stem cells and mice,” Genesis 44(4), 202–218 (2006).
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Kotynek, J. G.

F. T. Nguyen, A. M. Zysk, E. J. Chaney, J. G. Kotynek, U. J. Oliphant, F. J. Bellafiore, K. M. Rowland, P. A. Johnson, and S. A. Boppart, “Intraoperative Evaluation of Breast Tumor Margins with Optical Coherence Tomography,” Cancer Res. 69(22), 8790–8796 (2009).
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Kuida, K.

Y. Yamaguchi, N. Shinotsuka, K. Nonomura, K. Takemoto, K. Kuida, H. Yosida, and M. Miura, “Live imaging of apoptosis in a novel transgenic mouse highlights its role in neural tube closure,” J. Cell Biol. 195(6), 1047–1060 (2011).
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E. A. V. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
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Kulkarni, P. M.

P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
[PubMed]

Lackan, C. S.

J. M. Rhee, M. K. Pirity, C. S. Lackan, J. Z. Long, G. Kondoh, J. Takeda, and A. K. Hadjantonakis, “In vivo imaging and differential localization of lipid-modified GFP-variant fusions in embryonic stem cells and mice,” Genesis 44(4), 202–218 (2006).
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Lakomy, D. S.

S. Wang, D. S. Lakomy, M. D. Garcia, A. L. Lopez, K. V. Larin, and I. V. Larina, “Four-dimensional live imaging of hemodynamics in mammalian embryonic heart with Doppler optical coherence tomography,” J. Biophotonics 9(8), 837–847 (2016).
[Crossref] [PubMed]

Larin, K. V.

S. Wang, D. S. Lakomy, M. D. Garcia, A. L. Lopez, K. V. Larin, and I. V. Larina, “Four-dimensional live imaging of hemodynamics in mammalian embryonic heart with Doppler optical coherence tomography,” J. Biophotonics 9(8), 837–847 (2016).
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R. Raghunathan, M. Singh, M. E. Dickinson, and K. V. Larin, “Optical coherence tomography for embryonic imaging: a review,” J. Biomed. Opt. 21(5), 050902 (2016).
[Crossref] [PubMed]

A. L. Lopez, S. Wang, K. V. Larin, P. A. Overbeek, and I. V. Larina, “Live four-dimensional optical coherence tomography reveals embryonic cardiac phenotype in mouse mutant,” J. Biomed. Opt. 20(9), 090501 (2015).
[Crossref] [PubMed]

P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
[PubMed]

S. H. Syed, A. J. Coughlin, M. D. Garcia, S. Wang, J. L. West, K. V. Larin, and I. V. Larina, “Optical coherence tomography guided microinjections in live mouse embryos: high-resolution targeted manipulation for mouse embryonic research,” J. Biomed. Opt. 20(5), 051020 (2015).
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S. Wang, M. Singh, A. L. Lopez, C. Wu, R. Raghunathan, A. Schill, J. Li, K. V. Larin, and I. V. Larina, “Direct four-dimensional structural and functional imaging of cardiovascular dynamics in mouse embryos with 1.5 MHz optical coherence tomography,” Opt. Lett. 40(20), 4791–4794 (2015).
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I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Sequential Turning Acquisition and Reconstruction (STAR) method for four-dimensional imaging of cyclically moving structures,” Biomed. Opt. Express 3(3), 650–660 (2012).
[Crossref] [PubMed]

Larina, I. V.

S. Wang, D. S. Lakomy, M. D. Garcia, A. L. Lopez, K. V. Larin, and I. V. Larina, “Four-dimensional live imaging of hemodynamics in mammalian embryonic heart with Doppler optical coherence tomography,” J. Biophotonics 9(8), 837–847 (2016).
[Crossref] [PubMed]

P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
[PubMed]

A. L. Lopez, S. Wang, K. V. Larin, P. A. Overbeek, and I. V. Larina, “Live four-dimensional optical coherence tomography reveals embryonic cardiac phenotype in mouse mutant,” J. Biomed. Opt. 20(9), 090501 (2015).
[Crossref] [PubMed]

S. H. Syed, A. J. Coughlin, M. D. Garcia, S. Wang, J. L. West, K. V. Larin, and I. V. Larina, “Optical coherence tomography guided microinjections in live mouse embryos: high-resolution targeted manipulation for mouse embryonic research,” J. Biomed. Opt. 20(5), 051020 (2015).
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W. Luo, D. L. Marks, T. S. Ralston, and S. A. Boppart, “Three-dimensional optical coherence tomography of the embryonic murine cardiovascular system,” J. Biomed. Opt. 11(2), 021014 (2006).
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P. Hahn, J. Migacz, R. O’Connell, R. S. Maldonado, J. A. Izatt, and C. A. Toth, “The Use of Optical Coherence Tomography in Intraoperative Ophthalmic Imaging,” Ophthalmic Surg. Lasers Imaging 42(4Suppl), S85–S94 (2011).
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S. G. McShane, M. A. Molè, D. Savery, N. D. E. Greene, P. P. L. Tam, and A. J. Copp, “Cellular basis of neuroepithelial bending during mouse spinal neural tube closure,” Dev. Biol. 404(2), 113–124 (2015).
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M. Rădulescu, E. C. Ulmeanu, M. Nedelea, and A. Oncescu, “Prenatal ultrasound diagnosis of neural tube defects. Pictorial essay,” Med. Ultrason. 14(2), 147–153 (2012).
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R. Massarwa and L. Niswander, “In toto live imaging of mouse morphogenesis and new insights into neural tube closure,” Development 140(1), 226–236 (2013).
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P. Hahn, J. Migacz, R. O’Connell, R. S. Maldonado, J. A. Izatt, and C. A. Toth, “The Use of Optical Coherence Tomography in Intraoperative Ophthalmic Imaging,” Ophthalmic Surg. Lasers Imaging 42(4Suppl), S85–S94 (2011).
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A. Li, O. O. Ahsen, J. J. Liu, C. Du, M. L. McKee, Y. Yang, W. Wasco, C. H. Newton-Cheh, C. J. O’Donnell, J. G. Fujimoto, C. Zhou, and R. E. Tanzi, “Silencing of the Drosophila ortholog of SOX5 in heart leads to cardiac dysfunction as detected by optical coherence tomography,” Hum. Mol. Genet. 22(18), 3798–3806 (2013).
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M. Rădulescu, E. C. Ulmeanu, M. Nedelea, and A. Oncescu, “Prenatal ultrasound diagnosis of neural tube defects. Pictorial essay,” Med. Ultrason. 14(2), 147–153 (2012).
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A. Osterhues, N. S. Ali, and K. B. Michels, “The Role of Folic Acid Fortification in Neural Tube Defects: A Review,” Crit. Rev. Food Sci. Nutr. 53(11), 1180–1190 (2013).
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A. L. Lopez, S. Wang, K. V. Larin, P. A. Overbeek, and I. V. Larina, “Live four-dimensional optical coherence tomography reveals embryonic cardiac phenotype in mouse mutant,” J. Biomed. Opt. 20(9), 090501 (2015).
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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, 066022 (2010).

Peterson, L. M.

G. H. Karunamuni, S. Gu, M. R. Ford, L. M. Peterson, P. Ma, Y. T. Wang, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Capturing structure and function in an embryonic heart with biophotonic tools,” Front. Physiol. 5, 351 (2014).
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L. M. Peterson, M. W. Jenkins, S. Gu, L. Barwick, M. Watanabe, and A. M. Rollins, “4D shear stress maps of the developing heart using Doppler optical coherence tomography,” Biomed. Opt. Express 3(11), 3022–3032 (2012).
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Pfeiffer, T.

Pirity, M. K.

J. M. Rhee, M. K. Pirity, C. S. Lackan, J. Z. Long, G. Kondoh, J. Takeda, and A. K. Hadjantonakis, “In vivo imaging and differential localization of lipid-modified GFP-variant fusions in embryonic stem cells and mice,” Genesis 44(4), 202–218 (2006).
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Puliafito, C. A.

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 et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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Pyrgaki, C.

C. Pyrgaki, P. Trainor, A. K. Hadjantonakis, and L. Niswander, “Dynamic imaging of mammalian neural tube closure,” Dev. Biol. 344(2), 941–947 (2010).
[Crossref] [PubMed]

Radulescu, M.

M. Rădulescu, E. C. Ulmeanu, M. Nedelea, and A. Oncescu, “Prenatal ultrasound diagnosis of neural tube defects. Pictorial essay,” Med. Ultrason. 14(2), 147–153 (2012).
[PubMed]

Raghunathan, R.

Ralston, T. S.

W. Luo, D. L. Marks, T. S. Ralston, and S. A. Boppart, “Three-dimensional optical coherence tomography of the embryonic murine cardiovascular system,” J. Biomed. Opt. 11(2), 021014 (2006).
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P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
[PubMed]

Rhee, J. M.

J. M. Rhee, M. K. Pirity, C. S. Lackan, J. Z. Long, G. Kondoh, J. Takeda, and A. K. Hadjantonakis, “In vivo imaging and differential localization of lipid-modified GFP-variant fusions in embryonic stem cells and mice,” Genesis 44(4), 202–218 (2006).
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Rollins, A. M.

P. Ma, S. Gu, G. H. Karunamuni, M. W. Jenkins, M. Watanabe, and A. M. Rollins, “Cardiac neural crest ablation results in early endocardial cushion and hemodynamic flow abnormalities,” Am. J. Physiol. Heart Circ. Physiol. 311(5), H1150–H1159 (2016).
[Crossref] [PubMed]

G. Karunamuni, S. Gu, Y. Q. Doughman, A. I. Noonan, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Using optical coherence tomography to rapidly phenotype and quantify congenital heart defects associated with prenatal alcohol exposure,” Dev. Dyn. 244(4), 607–618 (2015).
[Crossref] [PubMed]

G. H. Karunamuni, S. Gu, M. R. Ford, L. M. Peterson, P. Ma, Y. T. Wang, A. M. Rollins, M. W. Jenkins, and M. Watanabe, “Capturing structure and function in an embryonic heart with biophotonic tools,” Front. Physiol. 5, 351 (2014).
[Crossref] [PubMed]

L. M. Peterson, M. W. Jenkins, S. Gu, L. Barwick, M. Watanabe, and A. M. Rollins, “4D shear stress maps of the developing heart using Doppler optical coherence tomography,” Biomed. Opt. Express 3(11), 3022–3032 (2012).
[Crossref] [PubMed]

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, 066022 (2010).

H. G. Bezerra, M. A. Costa, G. Guagliumi, A. M. Rollins, and D. I. Simon, “Intracoronary Optical Coherence Tomography: A Comprehensive Review Clinical and Research Applications,” JACC Cardiovasc. Interv. 2(11), 1035–1046 (2009).
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M. W. Jenkins, O. Q. Chughtai, A. N. Basavanhally, M. Watanabe, and A. M. Rollins, “In vivo gated 4D imaging of the embryonic heart using optical coherence tomography,” J. Biomed. Opt. 12(3), 030505 (2007).
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Rongvaux, A.

V. Massa, D. Savery, P. Ybot-Gonzalez, E. Ferraro, A. Rongvaux, F. Cecconi, R. Flavell, N. D. E. Greene, and A. J. Copp, “Apoptosis is not required for mammalian neural tube closure,” Proc. Natl. Acad. Sci. U.S.A. 106(20), 8233–8238 (2009).
[Crossref] [PubMed]

Rowland, K. M.

F. T. Nguyen, A. M. Zysk, E. J. Chaney, J. G. Kotynek, U. J. Oliphant, F. J. Bellafiore, K. M. Rowland, P. A. Johnson, and S. A. Boppart, “Intraoperative Evaluation of Breast Tumor Margins with Optical Coherence Tomography,” Cancer Res. 69(22), 8790–8796 (2009).
[Crossref] [PubMed]

Roysam, B.

P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
[PubMed]

Rugonyi, S.

M. Midgett, V. K. Chivukula, C. Dorn, S. Wallace, and S. Rugonyi, “Blood flow through the embryonic heart outflow tract during cardiac looping in HH13-HH18 chicken embryos,” J. R. Soc. Interface 12(111), 20150652 (2015).
[Crossref] [PubMed]

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Supplementary Material (3)

NameDescription
» Visualization 1: MOV (6689 KB)      Time-lapse 3D OCT imaging of the cranial neural tube closure in the mouse embryo for over 16 hours.
» Visualization 2: MOV (936 KB)      Zipper-like closure of neural tube at the hindbrain region of the mouse embryo.
» Visualization 3: MOV (1638 KB)      Button-like closure of neural tube at the midbrain region of the mouse embryo.

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Figures (5)

Fig. 1
Fig. 1

Live mouse embryo culture combined with OCT imaging for analysis of cranial neural tube closure. (A) Setup of the OCT sample arm inside a humidified incubator for static mouse embryo culture (Top); An enlarged side view of the culturing setup for the mouse embryo where a transparent Teflon film is placed on top of the medium to avoid evaporation (Bottom). (B) An example of 3D OCT embryonic imaging with a live mouse embryo at the stage of early E8.0 when the neural plates are formed yet not bent. The green line in the dorsal view indicates the position where the anterior view is taken. Scale bars correspond to 200 µm.

Fig. 2
Fig. 2

Time-lapse 3D OCT imaging of the cranial neural tube closure in the mouse embryo for over 16 hours. (A) A 3D image of the mouse embryo shows the three major parts of the cranial region, the forebrain, the midbrain and the hindbrain. (B) 3D images of the mouse embryo at the beginning and ending time points of the imaging session show the size increase and the yolk sac vascular remolding through development. The red arrows indicate the capillary plexus (left) and the remodeled blood vessels (right). (C) Representative frames from 3D OCT time-lapse demonstrate cranial neural tube closure while the embryo is turning (see Visualization 1). In the images of selected time points, the solid, dashed and dotted arrows point at forebrain, midbrain and hindbrain of the embryo, respectively, and the triangle points at a closure initiation site between the forebrain and midbrain. All scale bars correspond to 300 µm. The time stamps of images correspond to Visualization 1. The playback is 5000 times faster.

Fig. 3
Fig. 3

Zipper-like closure of neural tube at the hindbrain region of the mouse embryo. (A) Time-resolved 3D OCT images of the mouse embryo hindbrain region show a zipper-like neural tube closure (see Visualization 2). The red arrows point at the site where zipper-like closure occurs. The yellow lines between the head folds (0 min) represent the positions where distances are measured. (B) Distances between neural folds at different line positions plotted over time indicate the zipper-like process of neural tube closure at the hindbrain region. Scale bars correspond to 200 µm. The time stamps of images correspond to Visualization 2. The playback is 5000 times faster.

Fig. 4
Fig. 4

Button-like closure of neural tube at the midbrain region of the mouse embryo. (A) Time-resolved 3D OCT images of the mouse embryo midbrain region show a button-like neural tube closure (see Visualization 3). The red arrows point at the sites where button-like closure occurs. The yellow lines between the head folds (0 min) represent the positions where distances are measured. (B) Distances between neural folds at different line positions plotted over time indicate the button-like process of neural tube closure at the midbrain region. Scale bars correspond to 200 µm. The time stamps of images correspond to Visualization 3. The playback is 5000 times faster.

Fig. 5
Fig. 5

Phenotypic characterization of neural tube closure at the forebrain of the Wdr19 mutant mouse embryo. 3D OCT images of the forebrain region from the (A) control and (B) Wdr19 mouse embryos at E8.5 show a clear difference in the neural tube phenotype. The red arrows point at the forebrain region. The green lines in the ventral views indicate the locations where the anterior views are taken. The yellow lines in the anterior views show the positions of distance measurement. All scale bars correspond to 300 µm. (C) Quantification for the distance between neural folds at the forebrain region of the embryos show a larger distance (statistically significant) from the Wdr19 embryos in comparison with the control. The central thick lines represent the mean and the whiskers represent the standard deviation. The number of samples N = 10 for both groups. The p value is from a two-sample t test.

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