Knife-edge scanning microscopy for connectomics research

In this paper, we will review a novel microscopy modality called Knife-Edge Scanning Microscopy (KESM) that we have developed over the past twelve years (since 1999) and discuss its relevance to connectomics and neural networks research. The operational principle of KESM is to simultaneously section and image small animal brains embedded in hard polymer resin so that a near-isotropic, sub-micrometer voxel size of 0.6 µm × 0.7 µm × 1.0 µm can be achieved over ∼1 cm3 volume of tissue which is enough to hold an entire mouse brain. At this resolution, morphological details such as dendrites, dendritic spines, and axons are visible (for sparse stains like Golgi). KESM has been successfully used to scan whole mouse brains stained in Golgi (neuronal morphology), Nissl (somata), and India ink (vasculature), providing unprecedented insights into the system-level architectural layout of microstructures within the mouse brain. In this paper, we will present whole-brain-scale data sets from KESM and discuss challenges and opportunities posed to connectomics and neural networks research by such detailed yet system-level data.

[1]  Joao Antonio Pereira,et al.  Linked: The new science of networks , 2002 .

[2]  P. Danielsson,et al.  Three-dimensional microscopy using a confocal laser scanning microscope. , 1985, Optics letters.

[3]  Yoonsuck Choe,et al.  Acquisition and mining of the whole mouse brain microstructure , 2009 .

[4]  Yoonsuck Choe,et al.  Cell tracking and segmentation in electron microscopy images using graph cuts , 2009, 2009 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[5]  R. Angus Silver,et al.  neuroConstruct: A Tool for Modeling Networks of Neurons in 3D Space , 2007, Neuron.

[6]  Bartlett W. Mel,et al.  Information Processing in Dendritic Trees , 1994, Neural Computation.

[7]  Daniel Chern-Yeow Eng,et al.  Stereo Pseudo 3D Rendering for Web-based Display of Scientific Volumetric Data , 2008, VG/PBG@SIGGRAPH.

[8]  Yoonsuck Choe,et al.  Automated lateral sectioning for Knife-Edge Scanning Microscopy , 2008, 2008 5th IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[9]  J. Keyser,et al.  Constructing High-Resolution Microvascular Models , 2008 .

[10]  Jeffrey L. Krichmar,et al.  Computer generation and quantitative morphometric analysis of virtual neurons , 2001, Anatomy and Embryology.

[11]  Allan R. Jones,et al.  Genome-wide atlas of gene expression in the adult mouse brain , 2007, Nature.

[12]  Derek K. Jones,et al.  Diffusion‐tensor MRI: theory, experimental design and data analysis – a technical review , 2002 .

[13]  Yoonsuck Choe,et al.  3D volume extraction of densely packed cells in EM data stack by forward and backward graph cuts , 2009, 2009 IEEE Symposium on Computational Intelligence for Multimedia Signal and Vision Processing.

[14]  D Mayerich,et al.  Knife‐edge scanning microscopy for imaging and reconstruction of three‐dimensional anatomical structures of the mouse brain , 2008, Journal of microscopy.

[15]  G. Shepherd.  The Synaptic Organization of the Brain , 1979 .

[16]  Andreas Thiel,et al.  Complex dynamics is abolished in delayed recurrent systems with distributed feedback times , 2003, Complex..

[17]  Olaf Sporns,et al.  Graph Theory Methods for the Analysis of Neural Connectivity Patterns , 2003 .

[18]  Olaf Sporns,et al.  Connectivity and complexity: the relationship between neuroanatomy and brain dynamics , 2000, Neural Networks.

[19]  Dong Hyeop Han,et al.  Rapid 3D tracing of the mouse brain neurovasculature with local maximum intensity projection and moving windows , 2009 .

[20]  ヌツィアシュリストス バシリス,et al.  The imaging system and method for imaging an object , 2012 .

[21]  W. Denk,et al.  Two-photon laser scanning fluorescence microscopy. , 1990, Science.

[22]  S. Subramaniam,et al.  Site-specific 3D imaging of cells and tissues with a dual beam microscope. , 2006, Journal of structural biology.

[23]  Yoonsuck Choe,et al.  A local maximum intensity projection tracing of vasculature in Knife-Edge Scanning Microscope volume data , 2009, 2009 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[24]  Yoonsuck Choe,et al.  Charting out the octopus connectome at submicron resolution using the knife-edge scanning microscope , 2010, BMC Neuroscience.

[25]  Henry Markram,et al.  Deriving physical connectivity from neuronal morphology , 2003, Biological Cybernetics.

[26]  Cem Yuksel,et al.  Visualization of Fibrous and Thread-like Data , 2006, IEEE Transactions on Visualization and Computer Graphics.

[27]  Yoonsuck Choe,et al.  Evolution of recollection and prediction in neural networks , 2009, 2009 International Joint Conference on Neural Networks.

[28]  Kunal K. Ghosh,et al.  Advances in light microscopy for neuroscience. , 2009, Annual review of neuroscience.

[29]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

[30]  Rainer Goebel,et al.  High-resolution diffusion tensor imaging and tractography of the human optic chiasm at 9.4 T , 2008, NeuroImage.

[31]  D. Long.  Networks of the Brain , 2011 .

[32]  James M. Bower,et al.  The Book of GENESIS , 1994, Springer New York.

[33]  Randal A. Koene,et al.  NETMORPH: A Framework for the Stochastic Generation of Large Scale Neuronal Networks With Realistic Neuron Morphologies , 2009, Neuroinformatics.

[34]  Daniel Chern-Yeow Eng,et al.  Autonomous Learning of the Semantics of Internal Sensory States Based on Motor Exploration , 2007, Int. J. Humanoid Robotics.

[35]  J C Fiala,et al.  Reconstruct: a free editor for serial section microscopy , 2005, Journal of microscopy.

[36]  D. Kleinfeld,et al.  All-Optical Histology Using Ultrashort Laser Pulses , 2003, Neuron.

[37]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[38]  Judea Pearl,et al.  Reasoning with Cause and Effect , 1999, IJCAI.

[39]  Yoonsuck Choe,et al.  Facilitating neural dynamics for delay compensation: A road to predictive neural dynamics? , 2009, Neural Networks.

[40]  Khalid A. Al-Kofahi,et al.  Rapid automated three-dimensional tracing of neurons from confocal image stacks , 2002, IEEE Transactions on Information Technology in Biomedicine.

[41]  Carol M. Petito.  The Synaptic Organization of the Brain, 4th Ed , 1998 .

[42]  Yoonsuck Choe,et al.  Knife-Edge Scanning Microscopy: High-throughput Imaging and Analysis of Massive Volumes of Biological Microstructures , 2008 .

[43]  H. Markram,et al.  Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex. , 2004, Cerebral cortex.

[44]  Yoonsuck Choe,et al.  Fast cell detection in high-throughput imagery using GPU-accelerated machine learning , 2011, 2011 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[45]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

[46]  J. Pawley,et al.  Handbook of Biological Confocal Microscopy , 1990, Springer US.

[47]  Gabriel Wittum,et al.  NeuGen: A tool for the generation of realistic morphology of cortical neurons and neural networks in 3D , 2006, Neurocomputing.

[48]  John Keyser,et al.  Visualization of Cellular and Microvascular Relationships , 2008, IEEE Transactions on Visualization and Computer Graphics.

[49]  Adam C Puche,et al.  Blood Vessels Form a Scaffold for Neuroblast Migration in the Adult Olfactory Bulb , 2007, The Journal of Neuroscience.

[50]  Stephen J. Smith,et al.  Array Tomography: A New Tool for Imaging the Molecular Architecture and Ultrastructure of Neural Circuits , 2007, Neuron.

[51]  Bruno A. Olshausen,et al.  Book Review , 2003, Journal of Cognitive Neuroscience.

[52]  William M. Wells,et al.  Validation of Image Segmentation and Expert Quality with an Expectation-Maximization Algorithm , 2002, MICCAI.

[53]  Yoonsuck Choe,et al.  Fast and accurate retinal vasculature tracing and kernel-Isomap-based feature selection , 2009, 2009 International Joint Conference on Neural Networks.

[54]  Yoonsuck Choe,et al.  Construction of anatomically correct models of mouse brain networks , 2004, Neurocomputing.

[55]  E M Glaser,et al.  Neuron imaging with Neurolucida--a PC-based system for image combining microscopy. , 1990, Computerized medical imaging and graphics : the official journal of the Computerized Medical Imaging Society.

[56]  H. Markram.  The Blue Brain Project , 2006, Nature Reviews Neuroscience.

[57]  Bartlett W. Mel,et al.  Computational subunits in thin dendrites of pyramidal cells , 2004, Nature Neuroscience.

[58]  Thomas K. Berger,et al.  Evaluating automated parameter constraining procedures of neuron models by experimental and surrogate data , 2008, Biological Cybernetics.

[59]  Joseph F. Murray,et al.  Supervised Learning of Image Restoration with Convolutional Networks , 2007, 2007 IEEE 11th International Conference on Computer Vision.

[60]  S. Shen-Orr,et al.  Network motifs: simple building blocks of complex networks. , 2002, Science.

[61]  W. Denk,et al.  Serial Block-Face Scanning Electron Microscopy to Reconstruct Three-Dimensional Tissue Nanostructure , 2004, PLoS biology.

[62]  Olaf Sporns,et al.  Classes of network connectivity and dynamics , 2001, Complex..

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

[64]  Hong Shen,et al.  Rapid automated tracing and feature extraction from retinal fundus images using direct exploratory algorithms , 1999, IEEE Transactions on Information Technology in Biomedicine.

[65]  V. Wedeen,et al.  Diffusion MRI of Complex Neural Architecture , 2003, Neuron.

[66]  G. Edelman,et al.  Large-scale model of mammalian thalamocortical systems , 2008, Proceedings of the National Academy of Sciences.