Label-free optical imaging in developmental biology [Invited].

Application of optical imaging in developmental biology marks an exciting frontier in biomedical optics. Optical resolution and imaging depth allow for investigation of growing embryos at subcellular, cellular, and whole organism levels, while the complexity and variety of embryonic processes set multiple challenges stimulating the development of various live dynamic embryonic imaging approaches. Among other optical methods, label-free optical techniques attract an increasing interest as they allow investigation of developmental mechanisms without application of exogenous markers or fluorescent reporters. There has been a boost in development of label-free optical imaging techniques for studying embryonic development in animal models over the last decade, which revealed new information about early development and created new areas for investigation. Here, we review the recent progress in label-free optical embryonic imaging, discuss specific applications, and comment on future developments at the interface of photonics, engineering, and developmental biology.

[1]  Jie Tian,et al.  In-vivo Optical Tomography of Small Scattering Specimens: time-lapse 3D imaging of the head eversion process in Drosophila melanogaster , 2014, Scientific Reports.

[2]  Delong Zhang,et al.  Label-free imaging of lipid-droplet intracellular motion in early Drosophila embryos using femtosecond-stimulated Raman loss microscopy. , 2012, Biophysical journal.

[3]  Wihan Kim,et al.  In vivo molecular contrast OCT imaging of methylene blue. , 2015, Optics letters.

[4]  Michael W. Jenkins,et al.  4D embryonic cardiography using gated optical coherence tomography. , 2006, Optics express.

[5]  Jan Laufer,et al.  In vivo photoacoustic imaging of mouse embryos. , 2012, Journal of biomedical optics.

[6]  Saurabh Sinha,et al.  Intravital imaging by simultaneous label-free autofluorescence-multiharmonic microscopy , 2018, Nature Communications.

[7]  Victor X D Yang,et al.  High speed, wide velocity dynamic range Doppler optical coherence tomography (Part II): Imaging in vivo cardiac dynamics of Xenopus laevis. , 2003, Optics express.

[8]  Paola Borri,et al.  Quantitative imaging of lipids in live mouse oocytes and early embryos using CARS microscopy , 2016, Development.

[9]  Rafael Yuste,et al.  Fluorescence microscopy today , 2005, Nature Methods.

[10]  Michael W. Jenkins,et al.  Ultrahigh-speed optical coherence tomography imaging and visualization of the embryonic avian heart using a buffered Fourier Domain Mode Locked laser. , 2007, Optics express.

[11]  Adrian Mariampillai,et al.  Doppler optical cardiogram gated 2D color flow imaging at 1000 fps and 4D in vivo visualization of embryonic heart at 45 fps on a swept source OCT system. , 2007, Optics express.

[12]  J. Izatt,et al.  High resolution imaging of in vivo cardiac dynamics using color Doppler optical coherence tomography. , 1997, Optics express.

[13]  Andrew M. Rollins,et al.  Capturing structure and function in an embryonic heart with biophotonic tools , 2014, Front. Physiol..

[14]  Yuta Suzuki,et al.  Motionless volumetric photoacoustic microscopy with spatially invariant resolution , 2017, Nature Communications.

[15]  Kirill V. Larin,et al.  4D Reconstruction of the Beating Embryonic Heart From Two Orthogonal Sets of Parallel Optical Coherence Tomography Slice-Sequences , 2013, IEEE Transactions on Medical Imaging.

[16]  Lei Xi,et al.  Label-free photoacoustic imaging of the cardio-cerebrovascular development in the embryonic zebrafish. , 2017, Biomedical optics express.

[17]  Kirill V. Larin,et al.  Sequential Turning Acquisition and Reconstruction (STAR) method for four-dimensional imaging of cyclically moving structures , 2012, Biomedical optics express.

[18]  D. Sampson,et al.  Optical coherence elastography - OCT at work in tissue biomechanics [Invited]. , 2017, Biomedical optics express.

[19]  Sevan Goenezen,et al.  Blood flow dynamics reflect degree of outflow tract banding in Hamburger–Hamilton stage 18 chicken embryos , 2014, Journal of The Royal Society Interface.

[20]  Joseph A. Izatt,et al.  Optical Coherence Tomography: A New High-Resolution Imaging Technology to Study Cardiac Development in Chick Embryos , 2002, Circulation.

[21]  Sandra Rugonyi,et al.  4-D Computational Modeling of Cardiac Outflow Tract Hemodynamics over Looping Developmental Stages in Chicken Embryos , 2019, Journal of cardiovascular development and disease.

[22]  Vladislav V. Yakovlev,et al.  Seeing cells in a new light: a renaissance of Brillouin spectroscopy , 2016 .

[23]  M. Jenkins,et al.  In vivo gated 4D imaging of the embryonic heart using optical coherence tomography. , 2007, Journal of biomedical optics.

[24]  William J. Polacheck,et al.  Noncontact three-dimensional mapping of intracellular hydro-mechanical properties by Brillouin microscopy , 2015, Nature Methods.

[25]  Adrian Bradu,et al.  Closed loop tracked Doppler optical coherence tomography based heart monitor for the Drosophila melanogaster larvae , 2016, Journal of biophotonics.

[26]  Christopher P. Toseland,et al.  Fluorescent labeling and modification of proteins , 2013, Journal of chemical biology.

[27]  James Sharpe,et al.  Optical projection tomography as a new tool for studying embryo anatomy , 2003, Journal of anatomy.

[28]  Ulrich Pohl,et al.  Label-Free Determination of Hemodynamic Parameters in the Microcirculaton with Third Harmonic Generation Microscopy , 2014, PloS one.

[29]  Yoonsung Lee,et al.  Label‐free optical projection tomography for quantitative three‐dimensional anatomy of mouse embryo , 2019, Journal of biophotonics.

[30]  Benjamin J Vakoc,et al.  Multimodality optical imaging of embryonic heart microstructure. , 2007, Journal of biomedical optics.

[31]  A. Fercher,et al.  Optical coherence tomography - principles and applications , 2003 .

[32]  K. Anderson,et al.  The transformation of the model organism: a decade of developmental genetics , 2003, Nature Genetics.

[33]  Sandra Rugonyi,et al.  Biomechanics of early cardiac development , 2012, Biomechanics and modeling in mechanobiology.

[34]  Kirill V Larin,et al.  Four‐dimensional live imaging of hemodynamics in mammalian embryonic heart with Doppler optical coherence tomography , 2016, Journal of biophotonics.

[35]  George Filippidis,et al.  Cell tracking in live Caenorhabditis elegans embryos via third harmonic generation imaging microscopy measurements. , 2011, Journal of biomedical optics.

[36]  William A Mohler,et al.  Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues. , 2002, Biophysical journal.

[37]  Satoshi Tsukamoto,et al.  Synthesis and maintenance of lipid droplets are essential for mouse preimplantation embryonic development , 2019, Development.

[38]  N. Greene,et al.  Genetics and development of neural tube defects , 2010, The Journal of pathology.

[39]  Narendran Sudheendran,et al.  Optical coherence tomography for live phenotypic analysis of embryonic ocular structures in mouse models. , 2012, Journal of biomedical optics.

[40]  James Sharpe,et al.  Cell tracing reveals a dorsoventral lineage restriction plane in the mouse limb bud mesenchyme , 2007, Development.

[41]  M. Fordham,et al.  An evaluation of confocal versus conventional imaging of biological structures by fluorescence light microscopy , 1987, The Journal of cell biology.

[42]  F. Légaré,et al.  Probing microtubules polarity in mitotic spindles in situ using Interferometric Second Harmonic Generation Microscopy , 2017, Scientific Reports.

[43]  Kotaro Oka,et al.  Raman Spectroscopic Imaging of the Whole Ciona intestinalis Embryo during Development , 2013, PloS one.

[44]  Jörg Männer,et al.  How does the tubular embryonic heart work? Looking for the physical mechanism generating unidirectional blood flow in the valveless embryonic heart tube , 2010, Developmental dynamics : an official publication of the American Association of Anatomists.

[45]  Manmohan Singh,et al.  Rotational imaging optical coherence tomography for full-body mouse embryonic imaging , 2016, Journal of biomedical optics.

[46]  David L Wilson,et al.  High temporal resolution OCT using image-based retrospective gating. , 2009, Optics express.

[47]  Chi-Kuang Sun,et al.  Higher harmonic generation microscopy of in vitro cultured mammal oocytes and embryos. , 2008, Optics express.

[48]  Steve D. M. Brown,et al.  High-throughput discovery of novel developmental phenotypes , 2017 .

[49]  Ruikang K. Wang,et al.  Optical coherence tomography based angiography [Invited]. , 2017, Biomedical optics express.

[50]  Kirill V Larin,et al.  Live four-dimensional optical coherence tomography reveals embryonic cardiac phenotype in mouse mutant. , 2015, Journal of biomedical optics.

[51]  Shi Gu,et al.  Increased regurgitant flow causes endocardial cushion defects in an avian embryonic model of congenital heart disease , 2017, Congenital heart disease.

[52]  Ruikang K. Wang,et al.  Assessment of strain and strain rate in embryonic chick heart in vivo using tissue Doppler optical coherence tomography , 2011, Physics in medicine and biology.

[53]  Peng Li,et al.  Optical coherence tomography provides an ability to assess mechanical property of cardiac wall of developing outflow tract in embryonic heart in vivo , 2012, Journal of biomedical optics.

[54]  J. Fujimoto,et al.  Optical Coherence Tomography , 1991 .

[55]  Jan Laufer,et al.  Photoacoustic imaging using genetically encoded reporters: a review , 2017, Journal of biomedical optics.

[56]  Tao Xu,et al.  Segmentation of Drosophila heart in optical coherence microscopy images using convolutional neural networks , 2018, Journal of biophotonics.

[57]  Ruikang K. Wang,et al.  Quantifying blood flow and wall shear stresses in the outflow tract of chick embryonic hearts. , 2011, Computers & structures.

[58]  Pilhan Kim,et al.  In vivo measurement of age-related stiffening in the crystalline lens by Brillouin optical microscopy. , 2011, Biophysical journal.

[59]  Venkat Keshav Chivukula,et al.  Blood flow through the embryonic heart outflow tract during cardiac looping in HH13–HH18 chicken embryos , 2015, Journal of The Royal Society Interface.

[60]  Ana Rolo,et al.  Neural tube closure: cellular, molecular and biomechanical mechanisms , 2017, Development.

[61]  Shang Wang,et al.  Optical coherence tomography guided microinjections in live mouse embryos: high-resolution targeted manipulation for mouse embryonic research , 2015, Journal of biomedical optics.

[62]  Kirill V. Larin,et al.  Increasing the field-of-view of dynamic cardiac OCT via post-acquisition mosaicing without affecting frame-rate or spatial resolution , 2011, Biomedical optics express.

[63]  Kirill V Larin,et al.  Live imaging of rat embryos with Doppler swept-source optical coherence tomography. , 2009, Journal of biomedical optics.

[64]  Ruikang K. Wang,et al.  Biomechanics of the Chick Embryonic Heart Outflow Tract at HH18 Using 4D Optical Coherence Tomography Imaging and Computational Modeling , 2012, PloS one.

[65]  Thomas Lecuit,et al.  Lighting up developmental mechanisms: how fluorescence imaging heralded a new era , 2010, Development.

[66]  Daniele Fioretto,et al.  Brillouin Light Scattering: Applications in Biomedical Sciences , 2019, Chemical reviews.

[67]  Gabriel Popescu,et al.  Measurement of red blood cell mechanics during morphological changes , 2010, Proceedings of the National Academy of Sciences.

[68]  Andrew M. Rollins,et al.  4D shear stress maps of the developing heart using Doppler optical coherence tomography , 2012, Biomedical optics express.

[69]  Kirill V. Larin,et al.  Speckle variance OCT imaging of the vasculature in live mammalian embryos , 2011 .

[70]  R. Sturmey,et al.  Role of fatty acids in energy provision during oocyte maturation and early embryo development. , 2009, Reproduction in domestic animals = Zuchthygiene.

[71]  Ganga Karunamuni,et al.  Embryonic aortic arch hemodynamics are a functional biomarker for ethanol-induced congenital heart defects [Invited]. , 2017, Biomedical optics express.

[72]  Junjie Yao,et al.  Multi-scale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe , 2015, Nature Methods.

[73]  Philipp J. Keller,et al.  Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy , 2012, Nature Methods.

[74]  Ruikang K. Wang,et al.  Efficient postacquisition synchronization of 4-D nongated cardiac images obtained from optical coherence tomography: application to 4-D reconstruction of the chick embryonic heart. , 2009, Journal of biomedical optics.

[75]  James Sharpe,et al.  Quantification of gene expression patterns to reveal the origins of abnormal morphogenesis , 2018, bioRxiv.

[76]  Joseph Izatt,et al.  Quantitative Measurement of Blood Flow Dynamics in Embryonic Vasculature Using Spectral Doppler Velocimetry , 2009, Anatomical record.

[77]  Vasilis Ntziachristos,et al.  Multispectral photoacoustic imaging of fluorochromes in small animals. , 2007, Optics letters.

[78]  Stephen A. Boppart,et al.  Imaging developing neural morphology using optical coherence tomography , 1996, Journal of Neuroscience Methods.

[79]  Irina V Larina,et al.  Staging mouse preimplantation development in vivo using optical coherence microscopy , 2019, Journal of biophotonics.

[80]  Gabriel Popescu,et al.  Label-Free Characterization of Emerging Human Neuronal Networks , 2014, Scientific Reports.

[81]  Jorge Ripoll,et al.  Microscopic Optical Projection Tomography In Vivo , 2011, PloS one.

[82]  V. Magidson,et al.  Circumventing photodamage in live-cell microscopy. , 2013, Methods in cell biology.

[83]  R. Baldock,et al.  3D modelling, gene expression mapping and post-mapping image analysis in the developing human brain , 2005, Brain Research Bulletin.

[84]  Chen Wu,et al.  Evaluating the effects of maternal alcohol consumption on murine fetal brain vasculature using optical coherence tomography , 2018, Journal of biophotonics.

[85]  Leopold Schmetterer,et al.  Doppler Optical Coherence Tomography , 2014, Progress in Retinal and Eye Research.

[86]  Da-Kang Yao,et al.  Label-free photoacoustic microscopy of peripheral nerves , 2014, Journal of biomedical optics.

[87]  Lihong V. Wang,et al.  Photoacoustic Tomography: In Vivo Imaging from Organelles to Organs , 2012, Science.

[88]  Dennis E. Discher,et al.  Heart-Specific Stiffening in Early Embryos Parallels Matrix and Myosin Expression to Optimize Beating , 2013, Current Biology.

[89]  M. Dickinson,et al.  Hemodynamic measurements from individual blood cells in early mammalian embryos with Doppler swept source OCT. , 2009, Optics letters.

[90]  Michael Liebling,et al.  Rapid three‐dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[91]  Lihong V. Wang,et al.  Photoacoustic tomography: principles and advances. , 2016, Electromagnetic waves.

[92]  Heung-Il Suk,et al.  Deep Learning in Medical Image Analysis. , 2017, Annual review of biomedical engineering.

[93]  Wesley R. Legant,et al.  Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution , 2014, Science.

[94]  Robert H. Anderson,et al.  DEVELOPMENT OF THE HEART: (1) FORMATION OF THE CARDIAC CHAMBERS AND ARTERIAL TRUNKS , 2003, Heart.

[95]  Nanguang Chen,et al.  A method to study the hemodynamics of chicken embryo's aortic arches using optical coherence tomography , 2017, Journal of biophotonics.

[96]  Simon Arridge,et al.  Accelerated Optical Projection Tomography Applied to In Vivo Imaging of Zebrafish , 2015, PloS one.

[97]  Kirill V Larin,et al.  Optical Coherence Tomography for live imaging of mammalian development. , 2011, Current opinion in genetics & development.

[98]  Qifa Zhou,et al.  Optimal ultraviolet wavelength for in vivo photoacoustic imaging of cell nuclei. , 2012, Journal of biomedical optics.

[99]  Giuliano Scarcelli,et al.  Tissue biomechanics during cranial neural tube closure measured by Brillouin microscopy and optical coherence tomography , 2018, Birth defects research.

[100]  Ruikang K. Wang,et al.  In vivo assessment of wall strain in embryonic chick heart by spectral domain optical coherence tomography. , 2015, Applied optics.

[101]  Hang Yu,et al.  Real-time volumetric microscopy of in-vivo dynamics and large-scale samples with SCAPE 2.0 , 2019, Nature Methods.

[102]  David Mayerich,et al.  Comparison and combination of rotational imaging optical coherence tomography and selective plane illumination microscopy for embryonic study. , 2017, Biomedical optics express.

[103]  J. Izatt,et al.  In vivo spectral domain optical coherence tomography volumetric imaging and spectral Doppler velocimetry of early stage embryonic chicken heart development. , 2008, Journal of the Optical Society of America. A, Optics, image science, and vision.

[104]  Alexander Jesacher,et al.  Long-term imaging of mouse embryos using adaptive harmonic generation microscopy. , 2011, Journal of biomedical optics.

[105]  Lihong V. Wang,et al.  A practical guide to photoacoustic tomography in the life sciences , 2016, Nature Methods.

[106]  Kirill V. Larin,et al.  Direct four-dimensional structural and functional imaging of cardiovascular dynamics in mouse embryos with 1.5 MHz optical coherence tomography. , 2015, Optics letters.

[107]  Quing Zhu,et al.  In vivo photoacoustic tomography of mouse cerebral edema induced by cold injury. , 2011, Journal of biomedical optics.

[108]  Srinivas C. Turaga,et al.  In Toto Imaging and Reconstruction of Post-Implantation Mouse Development at the Single-Cell Level , 2018, Cell.

[109]  J. Fujimoto,et al.  Noninvasive assessment of the developing Xenopus cardiovascular system using optical coherence tomography. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[110]  Alexander Jesacher,et al.  Adaptive harmonic generation microscopy of mammalian embryos. , 2009, Optics letters.

[111]  James Sharpe,et al.  Spleen versus pancreas: strict control of organ interrelationship revealed by analyses of Bapx1-/- mice. , 2006, Genes & development.

[112]  E. Manders,et al.  Controlled light-exposure microscopy reduces photobleaching and phototoxicity in fluorescence live-cell imaging , 2007, Nature Biotechnology.

[113]  Xiaoming Dou,et al.  Raman imaging diagnosis of the early stage differentiation of mouse embryonic stem cell (mESC). , 2020, Spectrochimica acta. Part A, Molecular and biomolecular spectroscopy.

[114]  S. Yun,et al.  Brillouin optical microscopy for corneal biomechanics. , 2012, Investigative ophthalmology & visual science.

[115]  V Lombardi,et al.  Probing myosin structural conformation in vivo by second-harmonic generation microscopy , 2010, Proceedings of the National Academy of Sciences.

[116]  Elena Perevedentseva,et al.  Raman spectroscopy on live mouse early embryo while it continues to develop into blastocyst in vitro , 2019, Scientific Reports.

[117]  Leslie M Loew,et al.  Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms , 2003, Nature Biotechnology.

[118]  Jörg Männer,et al.  High‐resolution in vivo imaging of the cross‐sectional deformations of contracting embryonic heart loops using optical coherence tomography , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[119]  Ji-Xin Cheng,et al.  Coherent Anti-Stokes Raman Scattering Microscopy , 2007, 2008 Conference on Lasers and Electro-Optics and 2008 Conference on Quantum Electronics and Laser Science.

[120]  James Sharpe,et al.  In vitro whole-organ imaging: 4D quantification of growing mouse limb buds , 2008, Nature Methods.

[121]  Airong Li,et al.  Optogenetic pacing in Drosophila melanogaster , 2015, Science Advances.

[122]  Junjie Yao,et al.  Single-impulse Panoramic Photoacoustic Computed Tomography of Small-animal Whole-body Dynamics at High Spatiotemporal Resolution , 2017, Nature Biomedical Engineering.

[123]  Igor R Efimov,et al.  Optical Coherence Tomography as a Tool for Measuring Morphogenetic Deformation of the Looping Heart , 2007, Anatomical record.

[124]  Srirang Manohar,et al.  Photoacoustics: a historical review , 2016 .

[125]  Sergey Plotnikov,et al.  Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure , 2012, Nature Protocols.

[126]  Kirill V Larin,et al.  Dynamic imaging and quantitative analysis of cranial neural tube closure in the mouse embryo using optical coherence tomography. , 2017, Biomedical optics express.

[127]  Eugene W. Myers,et al.  Adaptive light-sheet microscopy for long-term, high-resolution imaging in living organisms , 2016, Nature Biotechnology.

[128]  Christian Depeursinge,et al.  Quantitative phase imaging in biomedicine , 2018, Nature Photonics.

[129]  Anna I Hickerson,et al.  The Embryonic Vertebrate Heart Tube Is a Dynamic Suction Pump , 2006, Science.

[130]  Krzysztof Krawiec,et al.  Optical coherence microscopy as a novel, non-invasive method for the 4D live imaging of early mammalian embryos , 2017, Scientific Reports.

[131]  Giuliano Scarcelli,et al.  Evaluating biomechanical properties of murine embryos using Brillouin microscopy and optical coherence tomography. , 2017, Journal of biomedical optics.

[132]  Marie M. Lockhart,et al.  Extracellular matrix and heart development. , 2011, Birth defects research. Part A, Clinical and molecular teratology.

[133]  Yongyang Huang,et al.  Optical Coherence Tomography for Brain Imaging and Developmental Biology , 2016, IEEE Journal of Selected Topics in Quantum Electronics.

[134]  Jean-François Colas,et al.  Live optical projection tomography , 2009, Organogenesis.

[135]  Chen Wu,et al.  Applicability, usability, and limitations of murine embryonic imaging with optical coherence tomography and optical projection tomography. , 2016, Biomedical optics express.

[136]  Bodo Heimann,et al.  Rotationally acquired four-dimensional optical coherence tomography of embryonic chick hearts using retrospective gating on the common central A-scan. , 2011, Journal of biomedical optics.

[137]  Lihong V. Wang,et al.  Photoacoustic imaging in biomedicine , 2006 .

[138]  David L Wilson,et al.  Measuring hemodynamics in the developing heart tube with four-dimensional gated Doppler optical coherence tomography. , 2010, Journal of biomedical optics.

[139]  Xianxu Zeng,et al.  A Circadian Clock Gene, Cry, Affects Heart Morphogenesis and Function in Drosophila as Revealed by Optical Coherence Microscopy , 2015, PloS one.

[140]  Jürgen Czarske,et al.  Mechanical Mapping of Spinal Cord Growth and Repair in Living Zebrafish Larvae by Brillouin Imaging , 2018, Biophysical journal.

[141]  Jiayi Ding,et al.  Raman spectrum: A potential biomarker for embryo assessment during in vitro fertilization , 2017, Experimental and therapeutic medicine.

[142]  Raksha Raghunathan,et al.  Assessing the acute effects of prenatal synthetic cannabinoid exposure on murine fetal brain vasculature using optical coherence tomography , 2019, Journal of biophotonics.

[143]  Sevan Goenezen,et al.  Alterations in pulse wave propagation reflect the degree of outflow tract banding in HH18 chicken embryos. , 2013, American journal of physiology. Heart and circulatory physiology.

[144]  Wolfram Bunk,et al.  Label-free live-cell imaging with confocal Raman microscopy. , 2012, Biophysical journal.

[145]  S. Yun,et al.  Confocal Brillouin microscopy for three-dimensional mechanical imaging. , 2007, Nature photonics.

[146]  Shang Wang,et al.  Speckle variance optical coherence tomography of blood flow in the beating mouse embryonic heart , 2017, Journal of biophotonics.

[147]  J. Bolker,et al.  Model systems in developmental biology , 1995, BioEssays : news and reviews in molecular, cellular and developmental biology.

[148]  Michael J. Moore,et al.  Simultaneous ultra-high frequency photoacoustic microscopy and photoacoustic radiometry of zebrafish larvae in vivo , 2018, Photoacoustics.

[149]  Hidetoshi Sato,et al.  Non-destructive monitoring of mouse embryo development and its qualitative evaluation at the molecular level using Raman spectroscopy , 2017, Scientific Reports.

[150]  V. Srinivasan,et al.  Optical coherence microscopy for deep tissue imaging of the cerebral cortex with intrinsic contrast , 2012, Optics express.

[151]  J. Hecksher-Sørensen,et al.  Optical Projection Tomography as a Tool for 3D Microscopy and Gene Expression Studies , 2002, Science.

[152]  Raksha Raghunathan,et al.  Optical coherence tomography for embryonic imaging: a review , 2016, Journal of biomedical optics.

[153]  Richard Baldock,et al.  3 dimensional modelling of early human brain development using optical projection tomography , 2004, BMC Neuroscience.

[154]  Lucile Houyel,et al.  Standardised imaging pipeline for phenotyping mouse laterality defects and associated heart malformations, at multiple scales and multiple stages , 2019, Disease Models & Mechanisms.

[155]  Gurneet S. Sangha,et al.  In vivo photoacoustic lipid imaging in mice using the second near-infrared window. , 2017, Biomedical optics express.

[156]  Renato Zenobi,et al.  Modern Raman imaging: vibrational spectroscopy on the micrometer and nanometer scales. , 2013, Annual review of analytical chemistry.

[157]  Shi Gu,et al.  Optical coherence tomography captures rapid hemodynamic responses to acute hypoxia in the cardiovascular system of early embryos , 2012, Developmental dynamics : an official publication of the American Association of Anatomists.

[158]  Qifa Zhou,et al.  Label-free imaging of zebrafish larvae in vivo by photoacoustic microscopy , 2012, Biomedical optics express.

[159]  Irina V. Larina,et al.  Second harmonic generation microscopy of early embryonic mouse hearts. , 2019, Biomedical optics express.

[160]  Shang Wang,et al.  Optical coherence elastography for tissue characterization: a review , 2015, Journal of biophotonics.

[161]  Changhuei Yang,et al.  Molecular Contrast Optical Coherence Tomography: A Review¶ , 2005, Photochemistry and photobiology.

[162]  Kirill V. Larin,et al.  Optical coherence tomography for high-resolution imaging of mouse development in utero. , 2011, Journal of biomedical optics.

[163]  Vasilis Ntziachristos,et al.  Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo , 2009 .

[164]  Chii-Wann Lin,et al.  Label-free imaging of Drosophila larva by multiphoton autofluorescence and second harmonic generation microscopy. , 2008, Journal of biomedical optics.

[165]  Pu Wang,et al.  Mapping lipid and collagen by multispectral photoacoustic imaging of chemical bond vibration , 2012, Journal of biomedical optics.

[166]  John White,et al.  Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability , 1999, Nature Biotechnology.

[167]  A. Talari,et al.  Raman Spectroscopy of Biological Tissues , 2007 .

[168]  Andrew M. Rollins,et al.  Phenotyping transgenic embryonic murine hearts using optical coherence tomography , 2007 .

[169]  Gert-Jan Bakker,et al.  Third harmonic generation microscopy of cells and tissue organization , 2016, Journal of Cell Science.

[170]  Stephen M Griffey,et al.  A lacZ reporter gene expression atlas for 313 adult KOMP mutant mouse lines , 2015, Genome research.

[171]  Junjie Yao,et al.  Photoacoustic tomography: fundamentals, advances and prospects. , 2011, Contrast media & molecular imaging.

[172]  Carolyn L Bayer,et al.  Ultrasound-guided spectral photoacoustic imaging of hemoglobin oxygenation during development. , 2017, Biomedical optics express.

[173]  Narendran Sudheendran,et al.  Comparative assessments of the effects of alcohol exposure on fetal brain development using optical coherence tomography and ultrasound imaging , 2013, Journal of biomedical optics.

[174]  M. Mir,et al.  Simultaneous optical measurements of cell motility and growth , 2011, Biomedical optics express.

[175]  P. Bourgine,et al.  Cell Lineage Reconstruction of Early Zebrafish Embryos Using Label-Free Nonlinear Microscopy , 2010, Science.

[176]  Masashi Tachikawa,et al.  Golgi apparatus self-organizes into the characteristic shape via postmitotic reassembly dynamics , 2017, Proceedings of the National Academy of Sciences.

[177]  Ruikang K. Wang,et al.  Extracting cardiac shapes and motion of the chick embryo heart outflow tract from four-dimensional optical coherence tomography images , 2012, Journal of biomedical optics.

[178]  Alexander Jesacher,et al.  Characterisation of the dynamic behaviour of lipid droplets in the early mouse embryo using adaptive harmonic generation microscopy , 2010, BMC Cell Biology.

[179]  Edward Z. Zhang,et al.  Dual modality optical coherence and whole-body photoacoustic tomography imaging of chick embryos in multiple development stages. , 2014, Biomedical optics express.

[180]  R. Mark Henkelman,et al.  4D atlas of the mouse embryo for precise morphological staging , 2015, Development.

[181]  V. Ntziachristos,et al.  Unleashing Optics and Optoacoustics for Developmental Biology. , 2015, Trends in biotechnology.

[182]  Alex Cable,et al.  Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography. , 2008, Journal of biomedical optics.

[183]  Bifeng Liu,et al.  Optical molecular imaging for systems biology: from molecule to organism , 2006, Analytical and bioanalytical chemistry.

[184]  Donald E Ingber,et al.  Mechanical control of tissue and organ development , 2010, Development.