A fuzzy-registration approach to track cell divisions in time-lapse fluorescence microscopy

Background Particle-tracking in 3D is an indispensable computational tool to extract critical information on dynamical processes from raw time-lapse imaging. This is particularly true with in vivo time-lapse fluorescence imaging in cell and developmental biology, where complex dynamics are observed at high temporal resolution. Common tracking algorithms used with time-lapse data in fluorescence microscopy typically assume a continuous signal where background, recognisable keypoints and independently moving objects of interest are permanently visible. Under these conditions, simple registration and identity management algorithms can track the objects of interest over time. In contrast, here we consider the case of transient signals and objects whose movements are constrained within a tissue, where standard algorithms fail to provide robust tracking. Results To optimize 3D tracking in these conditions, we propose the merging of registration and tracking tasks into a fuzzy registration algorithm to solve the identity management problem. We describe the design and application of such an algorithm, illustrated in the domain of plant biology, and make it available as an open-source software implementation. The algorithm is tested on mitotic events in 4D data-sets obtained with light-sheet fluorescence microscopy on growing Arabidopsis thaliana roots expressing CYCB::GFP. We validate the method by comparing the algorithm performance against both surrogate data and manual tracking. Conclusion This method fills a gap in existing tracking techniques, following mitotic events in challenging data-sets using transient fluorescent markers in unregistered images.

[1]  Tony P. Pridmore,et al.  Tissue-level segmentation and tracking of cells in growing plant roots , 2012, Machine Vision and Applications.

[2]  J. Tiihonen,et al.  Amygdala-orbitofrontal structural and functional connectivity in females with anxiety disorders, with and without a history of conduct disorder , 2018, Scientific Reports.

[3]  H. Schnabel,et al.  Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification. , 1997, Developmental biology.

[4]  M. Garcia-Parajo,et al.  A review of progress in single particle tracking: from methods to biophysical insights , 2015, Reports on progress in physics. Physical Society.

[5]  Mark Weiser,et al.  Source Code , 1987, Computer.

[6]  Andreas Karrenbauer,et al.  A novel method for automatic single molecule tracking of blinking molecules at low intensities. , 2013, Physical chemistry chemical physics : PCCP.

[7]  A. Roy-Chowdhury,et al.  Automated tracking of stem cell lineages of Arabidopsis shoot apex using local graph matching. , 2010, The Plant journal : for cell and molecular biology.

[8]  R. Waterston,et al.  Automated cell lineage tracing in Caenorhabditis elegans. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[9]  James J. Little,et al.  A Boosted Particle Filter: Multitarget Detection and Tracking , 2004, ECCV.

[10]  Nathalie Harder,et al.  An Objective Comparison of Cell Tracking Algorithms , 2017, Nature Methods.

[11]  Eric Mjolsness,et al.  Tracking Cell Signals in Fluorescent Images , 2005, 2005 IEEE Computer Society Conference on Computer Vision and Pattern Recognition (CVPR'05) - Workshops.

[12]  Philipp J. Keller,et al.  Reconstruction of Zebrafish Early Embryonic Development by Scanned Light Sheet Microscopy , 2008, Science.

[13]  M. Labouesse [Caenorhabditis elegans]. , 2003, Medecine sciences : M/S.

[14]  William J. Godinez,et al.  Objective comparison of particle tracking methods , 2014, Nature Methods.

[15]  G. Sena,et al.  Externally imposed electric field enhances plant root tip regeneration , 2016, Regeneration.

[16]  I. Johnstone,et al.  Ideal spatial adaptation by wavelet shrinkage , 1994 .

[17]  Emmanuelle Gouillart,et al.  scikit-image: image processing in Python , 2014, PeerJ.

[18]  I. Smal,et al.  Tracking in cell and developmental biology. , 2009, Seminars in cell & developmental biology.

[19]  A. Campilho,et al.  Time-lapse analysis of stem-cell divisions in the Arabidopsis thaliana root meristem. , 2006, The Plant journal : for cell and molecular biology.

[20]  E. Meyerowitz,et al.  Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana , 2004, Development.

[21]  Charles E. Melvin,et al.  Multi-sample Arabidopsis Growth and Imaging Chamber (MAGIC) for long term imaging in the ZEISS Lightsheet Z.1. , 2016, Developmental biology.

[22]  Donald Reid An algorithm for tracking multiple targets , 1978 .

[23]  Ingemar J. Cox,et al.  An Efficient Implementation of Reid's Multiple Hypothesis Tracking Algorithm and Its Evaluation for the Purpose of Visual Tracking , 1996, IEEE Trans. Pattern Anal. Mach. Intell..

[24]  Baba C. Vemuri,et al.  Robust Point Set Registration Using Gaussian Mixture Models , 2011, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[25]  Karl Rohr,et al.  Tracking Multiple Particles in Fluorescence Time-Lapse Microscopy Images via Probabilistic Data Association , 2015, IEEE Transactions on Medical Imaging.

[26]  Mei Chen,et al.  Mitosis Detection in Phase Contrast Microscopy Image Sequences of Stem Cell Populations: A Critical Review , 2017, IEEE Transactions on Big Data.

[27]  Wolfram Burgard,et al.  Tracking multiple moving targets with a mobile robot using particle filters and statistical data association , 2001, Proceedings 2001 ICRA. IEEE International Conference on Robotics and Automation (Cat. No.01CH37164).

[28]  Ramin Rahni,et al.  Week-long imaging of cell divisions in the Arabidopsis root meristem , 2018, Plant Methods.

[29]  J. Friml,et al.  Live tracking of moving samples in confocal microscopy for vertically grown roots , 2017, eLife.

[30]  Serge Beucher,et al.  Watershed, Hierarchical Segmentation and Waterfall Algorithm , 1994, ISMM.

[31]  Yuanyuan Ma,et al.  Recent advances in optical microscopic methods for single-particle tracking in biological samples , 2019, Analytical and Bioanalytical Chemistry.

[32]  Chen Geng,et al.  Accurate and Robust Non-rigid Point Set Registration using Student’s-t Mixture Model with Prior Probability Modeling , 2018, Scientific Reports.

[33]  Andrew W. Fitzgibbon,et al.  Robust Registration of 2D and 3D Point Sets , 2003, BMVC.

[34]  Takeo Kanade,et al.  Cell image analysis: Algorithms, system and applications , 2011, 2011 IEEE Workshop on Applications of Computer Vision (WACV).

[35]  Paul J. Besl,et al.  A Method for Registration of 3-D Shapes , 1992, IEEE Trans. Pattern Anal. Mach. Intell..

[36]  G. Sena,et al.  Light Sheet Fluorescence Microscopy Optimized for Long-Term Imaging of Arabidopsis Root Development. , 2018, Methods in molecular biology.

[37]  B. S. Manjunath,et al.  Simultaneous cell tracking and image alignment in 3D CLSM imagery of growing Arabidopsis thaliana sepals , 2013, 2013 IEEE 10th International Symposium on Biomedical Imaging.

[38]  Kenneth D. Birnbaum,et al.  Quantitation of Cellular Dynamics in Growing Arabidopsis Roots with Light Sheet Microscopy , 2011, PloS one.