Automated neuron tracing using probability hypothesis density filtering

Motivation: The functionality of neurons and their role in neuronal networks is tightly connected to the cell morphology. A fundamental problem in many neurobiological studies aiming to unravel this connection is the digital reconstruction of neuronal cell morphology from microscopic image data. Many methods have been developed for this, but they are far from perfect, and better methods are needed. Results: Here we present a new method for tracing neuron centerlines needed for full reconstruction. The method uses a fundamentally different approach than previous methods by considering neuron tracing as a Bayesian multi‐object tracking problem. The problem is solved using probability hypothesis density filtering. Results of experiments on 2D and 3D fluorescence microscopy image datasets of real neurons indicate the proposed method performs comparably or even better than the state of the art. Availability and Implementation: Software implementing the proposed neuron tracing method was written in the Java programming language as a plugin for the ImageJ platform. Source code is freely available for non‐commercial use at https://bitbucket.org/miroslavradojevic/phd. Contact: meijering@imagescience.org Supplementary information: Supplementary data are available at Bioinformatics online.

[1]  Branko Ristic,et al.  Beyond the Kalman Filter: Particle Filters for Tracking Applications , 2004 .

[2]  Hanchuan Peng,et al.  A distance-field based automatic neuron tracing method , 2013, BMC Bioinformatics.

[3]  A. Doucet,et al.  Sequential Monte Carlo methods for multitarget filtering with random finite sets , 2005, IEEE Transactions on Aerospace and Electronic Systems.

[4]  G. Ascoli Computational Neuroanatomy , 2002, Humana Press.

[5]  Xiaobo Zhou,et al.  Automated neurite extraction using dynamic programming for high-throughput screening of neuron-based assays , 2007, NeuroImage.

[6]  Eugene W. Myers,et al.  Automatic 3D neuron tracing using all-path pruning , 2011, Bioinform..

[7]  Giorgio A. Ascoli,et al.  Digital Reconstructions of Neuronal Morphology: Three Decades of Research Trends , 2012, Front. Neurosci..

[8]  Michael D. Abràmoff,et al.  Image processing with ImageJ , 2004 .

[9]  Shih-Fu Chang,et al.  Automatic Reconstruction of Neural Morphologies with Multi-Scale Tracking , 2012, Front. Neural Circuits.

[10]  Badrinath Roysam,et al.  Improved detection of branching points in algorithms for automated neuron tracing from 3D confocal images , 2008, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[11]  Julio Chapeton,et al.  Active learning of neuron morphology for accurate automated tracing of neurites , 2014, Front. Neuroanat..

[12]  Ioannis A. Kakadiaris,et al.  Automatic Morphological Reconstruction of Neurons from Multiphoton and Confocal Microscopy Images Using 3D Tubular Models , 2015, Neuroinformatics.

[13]  G. Ascoli,et al.  NeuroMorpho.Org: A Central Resource for Neuronal Morphologies , 2007, The Journal of Neuroscience.

[14]  Scott T. Acton,et al.  Tubularity Flow Field—A Technique for Automatic Neuron Segmentation , 2015, IEEE Transactions on Image Processing.

[15]  Douglas B. Ehlenberger,et al.  New techniques for imaging, digitization and analysis of three-dimensional neural morphology on multiple scales , 2005, Neuroscience.

[16]  Simo Srkk,et al.  Bayesian Filtering and Smoothing , 2013 .

[17]  Pascal Fua,et al.  Automated Reconstruction of Dendritic and Axonal Trees by Global Optimization with Geometric Priors , 2011, Neuroinformatics.

[18]  Aaron D. Lanterman,et al.  Probability hypothesis density-based multitarget tracking with bistatic range and Doppler observations , 2005 .

[19]  Gongning Luo,et al.  Neuron anatomy structure reconstruction based on a sliding filter , 2015, BMC Bioinformatics.

[20]  Ashraf A. Kassim,et al.  Data-Driven Probability Hypothesis Density Filter for Visual Tracking , 2008, IEEE Transactions on Circuits and Systems for Video Technology.

[21]  Ronald P. S. Mahler,et al.  Statistical Multisource-Multitarget Information Fusion , 2007 .

[22]  Karel Svoboda,et al.  The Past, Present, and Future of Single Neuron Reconstruction , 2011, Neuroinformatics.

[23]  Giulio Iannello,et al.  Automated Neuron Tracing Methods: An Updated Account , 2016, Neuroinformatics.

[24]  Lawrence D. Stone,et al.  Bayesian Multiple Target Tracking , 1999 .

[25]  Hanchuan Peng,et al.  APP2: automatic tracing of 3D neuron morphology based on hierarchical pruning of a gray-weighted image distance-tree , 2013, Bioinform..

[26]  Guido Gerig,et al.  Three-dimensional multi-scale line filter for segmentation and visualization of curvilinear structures in medical images , 1998, Medical Image Anal..

[27]  Stephen T. C. Wong,et al.  Repulsive force based snake model to segment and track neuronal axons in 3D microscopy image stacks , 2006, NeuroImage.

[28]  Alfredo Rodriguez,et al.  Three-dimensional neuron tracing by voxel scooping , 2009, Journal of Neuroscience Methods.

[29]  Erik Meijering,et al.  Neuron tracing in perspective , 2010, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[30]  R Marsault,et al.  Overexpression of neuronal Sec1 enhances axonal branching in hippocampal neurons , 2002, Neuroscience.

[31]  Feng Lin,et al.  A Graph-Theoretical Approach for Tracing Filamentary Structures in Neuronal and Retinal Images , 2016, IEEE Transactions on Medical Imaging.

[32]  Ronald P. S. Mahler,et al.  Particle-systems implementation of the PHD multitarget-tracking filter , 2003, SPIE Defense + Commercial Sensing.

[33]  Stephen L. Senft,et al.  A Brief History of Neuronal Reconstruction , 2011, Neuroinformatics.

[34]  Hanchuan Peng,et al.  V3D enables real-time 3D visualization and quantitative analysis of large-scale biological image data sets , 2010, Nature Biotechnology.

[35]  Ju Lu,et al.  The DIADEM Data Sets: Representative Light Microscopy Images of Neuronal Morphology to Advance Automation of Digital Reconstructions , 2011, Neuroinformatics.

[36]  Emilio Maggio,et al.  Efficient Multitarget Visual Tracking Using Random Finite Sets , 2008, IEEE Transactions on Circuits and Systems for Video Technology.

[37]  Ba-Ngu Vo,et al.  Improved SMC implementation of the PHD filter , 2010, 2010 13th International Conference on Information Fusion.

[38]  Eugene W. Myers,et al.  Automated Reconstruction of Neuronal Morphology Based on Local Geometrical and Global Structural Models , 2011, Neuroinformatics.

[39]  Ronald R. Coifman,et al.  Quantitative Arbor Analytics: Unsupervised Harmonic Co-Clustering of Populations of Brain Cell Arbors Based on L-Measure , 2014, Neuroinformatics.

[40]  Thia Kirubarajan,et al.  Estimation with Applications to Tracking and Navigation: Theory, Algorithms and Software , 2001 .

[41]  J. Ainge,et al.  Ontogeny of neural circuits underlying spatial memory in the rat , 2012, Front. Neural Circuits.

[42]  Erik H. W. Meijering,et al.  Fuzzy-Logic Based Detection and Characterization of Junctions and Terminations in Fluorescence Microscopy Images of Neurons , 2015, Neuroinformatics.

[43]  Hang Zhou,et al.  NeuroGPS-Tree: automatic reconstruction of large-scale neuronal populations with dense neurites , 2015, Nature Methods.

[44]  Deniz Erdogmus,et al.  Principal Curves as Skeletons of Tubular Objects , 2011, Neuroinformatics.

[45]  Daniel E. Clark,et al.  Particle PHD filter multiple target tracking in sonar image , 2007, IEEE Transactions on Aerospace and Electronic Systems.

[46]  Daniel E. Clark,et al.  Marker-Less Stage Drift Correction in Super-Resolution Microscopy Using the Single-Cluster PHD Filter , 2016, IEEE Journal of Selected Topics in Signal Processing.

[47]  Pascal Fua,et al.  Automated reconstruction of tree structures using path classifiers and Mixed Integer Programming , 2012, 2012 IEEE Conference on Computer Vision and Pattern Recognition.

[48]  Yuan Liu,et al.  DIADEMchallenge.Org: A Compendium of Resources Fostering the Continuous Development of Automated Neuronal Reconstruction , 2011, Neuroinformatics.

[49]  Simon J. Godsill,et al.  On sequential Monte Carlo sampling methods for Bayesian filtering , 2000, Stat. Comput..

[50]  Chia-Ling Tsai,et al.  A Broadly Applicable 3-D Neuron Tracing Method Based on Open-Curve Snake , 2011, Neuroinformatics.

[51]  Vivek Mehta,et al.  Automated Tracing of Neurites from Light Microscopy Stacks of Images , 2011, Neuroinformatics.

[52]  Giorgio A. Ascoli,et al.  Automated reconstruction of neuronal morphology: An overview , 2011, Brain Research Reviews.

[53]  Yakov Bar-Shalom,et al.  Multitarget-Multisensor Tracking: Principles and Techniques , 1995 .

[54]  Sidong Liu,et al.  Rivulet: 3D Neuron Morphology Tracing with Iterative Back-Tracking , 2016, Neuroinformatics.

[55]  David A. Wilkinson,et al.  Simplified Multitarget Tracking Using the PHD Filter for Microscopic Video Data , 2012, IEEE Transactions on Circuits and Systems for Video Technology.

[56]  R. Mahler Multitarget Bayes filtering via first-order multitarget moments , 2003 .

[57]  Hang Zhang,et al.  Ubiquitous Log Odds: A Common Representation of Probability and Frequency Distortion in Perception, Action, and Cognition , 2012, Front. Neurosci..

[58]  Neil J. Gordon,et al.  A tutorial on particle filters for online nonlinear/non-Gaussian Bayesian tracking , 2002, IEEE Trans. Signal Process..

[59]  Yizong Cheng,et al.  Mean Shift, Mode Seeking, and Clustering , 1995, IEEE Trans. Pattern Anal. Mach. Intell..

[60]  Badrinath Roysam,et al.  3-D Image Pre-processing Algorithms for Improved Automated Tracing of Neuronal Arbors , 2011, Neuroinformatics.

[61]  Wei Tsang Ooi,et al.  Neurite Tracing With Object Process , 2016, IEEE Transactions on Medical Imaging.

[62]  E Meijering,et al.  Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images , 2004, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[63]  Ba-Ngu Vo,et al.  The Gaussian Mixture Probability Hypothesis Density Filter , 2006, IEEE Transactions on Signal Processing.

[64]  Ioannis A. Kakadiaris,et al.  Improved Automatic Centerline Tracing for Dendritic and Axonal Structures , 2015, Neuroinformatics.

[65]  Sean L. Hill,et al.  BigNeuron: Large-Scale 3D Neuron Reconstruction from Optical Microscopy Images , 2015, Neuron.

[66]  Scott T. Acton,et al.  Segmentation and Tracing of Single Neurons from 3D Confocal Microscope Images , 2013, IEEE Journal of Biomedical and Health Informatics.