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Fast macro-scale transmission imaging of microvascular networks using KESMDavid Mayerich, Jaerock Kwon, Chul Sung, Louise Abbott, John Keyser, and Yoonsuck Choe »View Author Affiliations
David Mayerich,1
Jaerock Kwon,2
Chul Sung,4
Louise Abbott,3
John Keyser,4
and Yoonsuck Choe4,*
1Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign, Urbana IL, 61801, USA 2Department of Electrical and Computer Engineering, Kettering University, Flint, MI, 48504, USA 3Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, TX 77843, USA 4Department of Computer Science and Engineering, Texas A&M University, College Station, TX 77843, USA *Corresponding author: choe@cs.tamu.edu |
Biomedical Optics Express, Vol. 2, Issue 10, pp. 2888-2896 (2011)
http://dx.doi.org/10.1364/BOE.2.002888
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Abstract
Accurate microvascular morphometric information has significant implications in several fields, including the quantification of angiogenesis in cancer research, understanding the immune response for neural prosthetics, and predicting the nature of blood flow as it relates to stroke. We report imaging of the whole mouse brain microvascular system at resolutions sufficient to perform accurate morphometry. Imaging was performed using Knife-Edge Scanning Microscopy (KESM) and is the first example of this technique that can be directly applied to clinical research. We are able to achieve ≈ 0.7μm resolution laterally with 1μm depth resolution using serial sectioning. No alignment was necessary and contrast was sufficient to allow segmentation and measurement of vessels.
© 2011 OSA
OCIS Codes
(110.0180) Imaging systems : Microscopy
(170.1020) Medical optics and biotechnology : Ablation of tissue
(170.3880) Medical optics and biotechnology : Medical and biological imaging
(170.2945) Medical optics and biotechnology : Illumination design
ToC Category:
Microscopy
History
Original Manuscript: July 19, 2011
Revised Manuscript: August 29, 2011
Manuscript Accepted: September 19, 2011
Published: September 29, 2011
Citation
David Mayerich, Jaerock Kwon, Chul Sung, Louise Abbott, John Keyser, and Yoonsuck Choe, "Fast macro-scale transmission imaging of microvascular networks using KESM," Biomed. Opt. Express 2, 2888-2896 (2011)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-2-10-2888
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References
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- C. Sung, J. R. Chung, D. Mayerich, J. Kwon, D. Miller, T. Huffman, J. Keyser, L. Abbott, and Y. Choe, “Knife-edge scanning microscope brain atlas: A submicrometer-resolution web-based mouse brain atlas,” in “2011 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2011). Program No. 328.05. Online.
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- Y. Choe, D. Han, P. Huang, J. Keyser, J. Kwon, D. Mayerich, and L. Abbott, “Complete submicrometer scans of mouse brain microstructure: Neurons and vasculatures,” in “2009 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2009). Program No. 389.10. Online.
- C. Sung, J. R. Chung, D. Mayerich, J. Kwon, D. Miller, T. Huffman, J. Keyser, L. Abbott, and Y. Choe, “Knife-edge scanning microscope brain atlas: A submicrometer-resolution web-based mouse brain atlas,” in “2011 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2011). Program No. 328.05. Online.
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- A. R. Pries, A. J. M. Cornelissen, A. A. Sloot, M. Hinkeldey, M. R. Dreher, M. Hpfner, M. W. Dewhirst, and T. W. Secomb, “Structural adaptation and heterogeneity of normal and tumor microvascular networks,” PLoS Computational Biology5, e1000394 (2009). [CrossRef] [PubMed]
- E. M. Renkin, S. D. Gray, and L. R. Dodd, “Filling of microcirculation in skeletal muscles during timed india ink perfusion,” American Journal of Physiology - Heart and Circulatory Physiology241, H174 –H186 (1981).
- A. R. Pries, A. J. M. Cornelissen, A. A. Sloot, M. Hinkeldey, M. R. Dreher, M. Hpfner, M. W. Dewhirst, and T. W. Secomb, “Structural adaptation and heterogeneity of normal and tumor microvascular networks,” PLoS Computational Biology5, e1000394 (2009). [CrossRef] [PubMed]
- F. Cassot, F. Lauwers, S. Lorthois, P. Puwanarajah, V. Cances-Lauwers, and H. Duvernoy, “Branching patterns for arterioles and venules of the human cerebral cortex,” Brain Research1313, 62–78 (2010). [CrossRef]
- F. Lauwers, F. Cassot, V. Lauwers-Cances, P. Puwanarajah, and H. Duvernoy, “Morphometry of the human cerebral cortex microcirculation: General characteristics and space-related profiles,” NeuroImage39, 936–948 (2008). [CrossRef]
- F. Cassot, F. Lauwers, C. Fouard, S. Prohaska, and V. Lauwers-Cances, “A novel Three-Dimensional Computer-Assisted method for a quantitative study of microvascular networks of the human cerebral cortex,” Microcirculation13, 1–18 (2006). [CrossRef] [PubMed]
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- A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science330, 1404 –1408 (2010). [CrossRef] [PubMed]
- E. M. Renkin, S. D. Gray, and L. R. Dodd, “Filling of microcirculation in skeletal muscles during timed india ink perfusion,” American Journal of Physiology - Heart and Circulatory Physiology241, H174 –H186 (1981).
- B. R. Shepherd, H. Y. Chen, C. M. Smith, G. Gruionu, S. K. Williams, and J. B. Hoying, “Rapid perfusion and network remodeling in a microvascular construct after implantation,” Arteriosclerosis, Thrombosis, Vascular Biology24, 898 –904 (2004). [CrossRef]
- Y. Choe, D. Han, P. Huang, J. Keyser, J. Kwon, D. Mayerich, and L. Abbott, “Complete submicrometer scans of mouse brain microstructure: Neurons and vasculatures,” in “2009 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2009). Program No. 389.10. Online.
- X. He, E. Kischell, M. Rioult, and T. J. Holmes, “Three-Dimensional thinning algorithm that peels the outmost layer with application to neuron tracing,” Journal of Computer-Assisted Microscopy10, 123–135 (1998). [CrossRef]
- S. Heinzer, T. Krucker, M. Stampanoni, R. Abela, E. P. Meyer, A. Schuler, P. Schneider, and R. Muller, “Hierarchical microimaging for multiscale analysis of large vascular networks,” NeuroImage32, 626–636 (2006). [CrossRef] [PubMed]
- A. R. Pries, A. J. M. Cornelissen, A. A. Sloot, M. Hinkeldey, M. R. Dreher, M. Hpfner, M. W. Dewhirst, and T. W. Secomb, “Structural adaptation and heterogeneity of normal and tumor microvascular networks,” PLoS Computational Biology5, e1000394 (2009). [CrossRef] [PubMed]
- S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine63, 1637–1647 (2010). [CrossRef] [PubMed]
- X. He, E. Kischell, M. Rioult, and T. J. Holmes, “Three-Dimensional thinning algorithm that peels the outmost layer with application to neuron tracing,” Journal of Computer-Assisted Microscopy10, 123–135 (1998). [CrossRef]
- B. R. Shepherd, H. Y. Chen, C. M. Smith, G. Gruionu, S. K. Williams, and J. B. Hoying, “Rapid perfusion and network remodeling in a microvascular construct after implantation,” Arteriosclerosis, Thrombosis, Vascular Biology24, 898 –904 (2004). [CrossRef]
- A. R. Pries, A. J. M. Cornelissen, A. A. Sloot, M. Hinkeldey, M. R. Dreher, M. Hpfner, M. W. Dewhirst, and T. W. Secomb, “Structural adaptation and heterogeneity of normal and tumor microvascular networks,” PLoS Computational Biology5, e1000394 (2009). [CrossRef] [PubMed]
- Y. Choe, D. Han, P. Huang, J. Keyser, J. Kwon, D. Mayerich, and L. Abbott, “Complete submicrometer scans of mouse brain microstructure: Neurons and vasculatures,” in “2009 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2009). Program No. 389.10. Online.
- C. Sung, J. R. Chung, D. Mayerich, J. Kwon, D. Miller, T. Huffman, J. Keyser, L. Abbott, and Y. Choe, “Knife-edge scanning microscope brain atlas: A submicrometer-resolution web-based mouse brain atlas,” in “2011 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2011). Program No. 328.05. Online.
- P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron39, 27–41 (2003). [CrossRef] [PubMed]
- S. Akita, N. Tamai, A. Myoui, M. Nishikawa, T. Kaito, K. Takaoka, and H. Yoshikawa, “Capillary vessel network integration by inserting a vascular pedicle enhances bone formation in Tissue-Engineered bone using interconnected porous hydroxyapatite ceramics,” Tissue Engineering10, 789–795 (2004). [CrossRef] [PubMed]
- T. C. Lee, R. L. Kashyap, and C. N. Chu, “Building skeleton models via 3-D medial surface/axis thinning algorithms,” Graphical Models and Image Processing56, 462–478 (1994). [CrossRef]
- C. Sung, J. R. Chung, D. Mayerich, J. Kwon, D. Miller, T. Huffman, J. Keyser, L. Abbott, and Y. Choe, “Knife-edge scanning microscope brain atlas: A submicrometer-resolution web-based mouse brain atlas,” in “2011 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2011). Program No. 328.05. Online.
- D. Mayerich, B. H. McCormick, and J. Keyser, “Noise and artifact removal in Knife-Edge scanning microscopy,” Proceedings of the 4th IEEE International Symposium on Biomedical Imaging: From Nano to Macro pp. 556–559 (2007). [CrossRef]
- D. Mayerich, J. Kwon, Y. Choe, L. Abbott, and J. Keyser, “Constructing high resolution microvascular models,” in “Third Workshop on Microscopic Image Analysis with Applications in Biology,” (2008).
- Y. Choe, D. Han, P. Huang, J. Keyser, J. Kwon, D. Mayerich, and L. Abbott, “Complete submicrometer scans of mouse brain microstructure: Neurons and vasculatures,” in “2009 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2009). Program No. 389.10. Online.
- X. He, E. Kischell, M. Rioult, and T. J. Holmes, “Three-Dimensional thinning algorithm that peels the outmost layer with application to neuron tracing,” Journal of Computer-Assisted Microscopy10, 123–135 (1998). [CrossRef]
- P. Blinder, A. Y. Shih, C. Rafie, and D. Kleinfeld, “Topological basis for the robust distribution of blood to rodent neocortex,” Proceedings of the National Academy of Sciences107, 12670 –12675 (2010). [CrossRef]
- P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron39, 27–41 (2003). [CrossRef] [PubMed]
- S. Heinzer, T. Krucker, M. Stampanoni, R. Abela, E. P. Meyer, A. Schuler, P. Schneider, and R. Muller, “Hierarchical microimaging for multiscale analysis of large vascular networks,” NeuroImage32, 626–636 (2006). [CrossRef] [PubMed]
- T. Krucker, A. Lang, and E. P. Meyer, “New polyurethane-based material for vascular corrosion casting with improved physical and imaging characteristics,” Microscopy research and technique69, 138–147 (2006). [CrossRef] [PubMed]
- Y. Choe, D. Han, P. Huang, J. Keyser, J. Kwon, D. Mayerich, and L. Abbott, “Complete submicrometer scans of mouse brain microstructure: Neurons and vasculatures,” in “2009 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2009). Program No. 389.10. Online.
- D. Mayerich, J. Kwon, Y. Choe, L. Abbott, and J. Keyser, “Constructing high resolution microvascular models,” in “Third Workshop on Microscopic Image Analysis with Applications in Biology,” (2008).
- C. Sung, J. R. Chung, D. Mayerich, J. Kwon, D. Miller, T. Huffman, J. Keyser, L. Abbott, and Y. Choe, “Knife-edge scanning microscope brain atlas: A submicrometer-resolution web-based mouse brain atlas,” in “2011 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2011). Program No. 328.05. Online.
- T. Krucker, A. Lang, and E. P. Meyer, “New polyurethane-based material for vascular corrosion casting with improved physical and imaging characteristics,” Microscopy research and technique69, 138–147 (2006). [CrossRef] [PubMed]
- F. Cassot, F. Lauwers, S. Lorthois, P. Puwanarajah, V. Cances-Lauwers, and H. Duvernoy, “Branching patterns for arterioles and venules of the human cerebral cortex,” Brain Research1313, 62–78 (2010). [CrossRef]
- F. Lauwers, F. Cassot, V. Lauwers-Cances, P. Puwanarajah, and H. Duvernoy, “Morphometry of the human cerebral cortex microcirculation: General characteristics and space-related profiles,” NeuroImage39, 936–948 (2008). [CrossRef]
- F. Cassot, F. Lauwers, C. Fouard, S. Prohaska, and V. Lauwers-Cances, “A novel Three-Dimensional Computer-Assisted method for a quantitative study of microvascular networks of the human cerebral cortex,” Microcirculation13, 1–18 (2006). [CrossRef] [PubMed]
- F. Lauwers, F. Cassot, V. Lauwers-Cances, P. Puwanarajah, and H. Duvernoy, “Morphometry of the human cerebral cortex microcirculation: General characteristics and space-related profiles,” NeuroImage39, 936–948 (2008). [CrossRef]
- F. Cassot, F. Lauwers, C. Fouard, S. Prohaska, and V. Lauwers-Cances, “A novel Three-Dimensional Computer-Assisted method for a quantitative study of microvascular networks of the human cerebral cortex,” Microcirculation13, 1–18 (2006). [CrossRef] [PubMed]
- T. C. Lee, R. L. Kashyap, and C. N. Chu, “Building skeleton models via 3-D medial surface/axis thinning algorithms,” Graphical Models and Image Processing56, 462–478 (1994). [CrossRef]
- P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron39, 27–41 (2003). [CrossRef] [PubMed]
- A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science330, 1404 –1408 (2010). [CrossRef] [PubMed]
- A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science330, 1404 –1408 (2010). [CrossRef] [PubMed]
- F. Cassot, F. Lauwers, S. Lorthois, P. Puwanarajah, V. Cances-Lauwers, and H. Duvernoy, “Branching patterns for arterioles and venules of the human cerebral cortex,” Brain Research1313, 62–78 (2010). [CrossRef]
- A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science330, 1404 –1408 (2010). [CrossRef] [PubMed]
- D. Mayerich, L. C. Abbott, and B. H. McCormick, “Knife-Edge scanning microscopy for imaging and reconstruction of Three-Dimensional anatomical structures of the mouse brain,” Journal of Microscopy231, 134–143 (2008). [CrossRef] [PubMed]
- C. Sung, J. R. Chung, D. Mayerich, J. Kwon, D. Miller, T. Huffman, J. Keyser, L. Abbott, and Y. Choe, “Knife-edge scanning microscope brain atlas: A submicrometer-resolution web-based mouse brain atlas,” in “2011 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2011). Program No. 328.05. Online.
- D. Mayerich, B. H. McCormick, and J. Keyser, “Noise and artifact removal in Knife-Edge scanning microscopy,” Proceedings of the 4th IEEE International Symposium on Biomedical Imaging: From Nano to Macro pp. 556–559 (2007). [CrossRef]
- D. Mayerich, J. Kwon, Y. Choe, L. Abbott, and J. Keyser, “Constructing high resolution microvascular models,” in “Third Workshop on Microscopic Image Analysis with Applications in Biology,” (2008).
- Y. Choe, D. Han, P. Huang, J. Keyser, J. Kwon, D. Mayerich, and L. Abbott, “Complete submicrometer scans of mouse brain microstructure: Neurons and vasculatures,” in “2009 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2009). Program No. 389.10. Online.
- D. Mayerich, L. C. Abbott, and B. H. McCormick, “Knife-Edge scanning microscopy for imaging and reconstruction of Three-Dimensional anatomical structures of the mouse brain,” Journal of Microscopy231, 134–143 (2008). [CrossRef] [PubMed]
- D. Mayerich, B. H. McCormick, and J. Keyser, “Noise and artifact removal in Knife-Edge scanning microscopy,” Proceedings of the 4th IEEE International Symposium on Biomedical Imaging: From Nano to Macro pp. 556–559 (2007). [CrossRef]
- T. Krucker, A. Lang, and E. P. Meyer, “New polyurethane-based material for vascular corrosion casting with improved physical and imaging characteristics,” Microscopy research and technique69, 138–147 (2006). [CrossRef] [PubMed]
- S. Heinzer, T. Krucker, M. Stampanoni, R. Abela, E. P. Meyer, A. Schuler, P. Schneider, and R. Muller, “Hierarchical microimaging for multiscale analysis of large vascular networks,” NeuroImage32, 626–636 (2006). [CrossRef] [PubMed]
- K. D. Micheva and S. J. Smith, “Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits,” Neuron55, 25–36 (2007). [CrossRef] [PubMed]
- C. Sung, J. R. Chung, D. Mayerich, J. Kwon, D. Miller, T. Huffman, J. Keyser, L. Abbott, and Y. Choe, “Knife-edge scanning microscope brain atlas: A submicrometer-resolution web-based mouse brain atlas,” in “2011 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2011). Program No. 328.05. Online.
- A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron52, 205–220 (2006). [CrossRef] [PubMed]
- S. Heinzer, T. Krucker, M. Stampanoni, R. Abela, E. P. Meyer, A. Schuler, P. Schneider, and R. Muller, “Hierarchical microimaging for multiscale analysis of large vascular networks,” NeuroImage32, 626–636 (2006). [CrossRef] [PubMed]
- S. Akita, N. Tamai, A. Myoui, M. Nishikawa, T. Kaito, K. Takaoka, and H. Yoshikawa, “Capillary vessel network integration by inserting a vascular pedicle enhances bone formation in Tissue-Engineered bone using interconnected porous hydroxyapatite ceramics,” Tissue Engineering10, 789–795 (2004). [CrossRef] [PubMed]
- S. Akita, N. Tamai, A. Myoui, M. Nishikawa, T. Kaito, K. Takaoka, and H. Yoshikawa, “Capillary vessel network integration by inserting a vascular pedicle enhances bone formation in Tissue-Engineered bone using interconnected porous hydroxyapatite ceramics,” Tissue Engineering10, 789–795 (2004). [CrossRef] [PubMed]
- S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine63, 1637–1647 (2010). [CrossRef] [PubMed]
- S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine63, 1637–1647 (2010). [CrossRef] [PubMed]
- A. R. Pries, A. J. M. Cornelissen, A. A. Sloot, M. Hinkeldey, M. R. Dreher, M. Hpfner, M. W. Dewhirst, and T. W. Secomb, “Structural adaptation and heterogeneity of normal and tumor microvascular networks,” PLoS Computational Biology5, e1000394 (2009). [CrossRef] [PubMed]
- F. Cassot, F. Lauwers, C. Fouard, S. Prohaska, and V. Lauwers-Cances, “A novel Three-Dimensional Computer-Assisted method for a quantitative study of microvascular networks of the human cerebral cortex,” Microcirculation13, 1–18 (2006). [CrossRef] [PubMed]
- F. Cassot, F. Lauwers, S. Lorthois, P. Puwanarajah, V. Cances-Lauwers, and H. Duvernoy, “Branching patterns for arterioles and venules of the human cerebral cortex,” Brain Research1313, 62–78 (2010). [CrossRef]
- F. Lauwers, F. Cassot, V. Lauwers-Cances, P. Puwanarajah, and H. Duvernoy, “Morphometry of the human cerebral cortex microcirculation: General characteristics and space-related profiles,” NeuroImage39, 936–948 (2008). [CrossRef]
- P. Blinder, A. Y. Shih, C. Rafie, and D. Kleinfeld, “Topological basis for the robust distribution of blood to rodent neocortex,” Proceedings of the National Academy of Sciences107, 12670 –12675 (2010). [CrossRef]
- E. M. Renkin, S. D. Gray, and L. R. Dodd, “Filling of microcirculation in skeletal muscles during timed india ink perfusion,” American Journal of Physiology - Heart and Circulatory Physiology241, H174 –H186 (1981).
- X. He, E. Kischell, M. Rioult, and T. J. Holmes, “Three-Dimensional thinning algorithm that peels the outmost layer with application to neuron tracing,” Journal of Computer-Assisted Microscopy10, 123–135 (1998). [CrossRef]
- S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine63, 1637–1647 (2010). [CrossRef] [PubMed]
- S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine63, 1637–1647 (2010). [CrossRef] [PubMed]
- P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron39, 27–41 (2003). [CrossRef] [PubMed]
- S. Heinzer, T. Krucker, M. Stampanoni, R. Abela, E. P. Meyer, A. Schuler, P. Schneider, and R. Muller, “Hierarchical microimaging for multiscale analysis of large vascular networks,” NeuroImage32, 626–636 (2006). [CrossRef] [PubMed]
- S. Heinzer, T. Krucker, M. Stampanoni, R. Abela, E. P. Meyer, A. Schuler, P. Schneider, and R. Muller, “Hierarchical microimaging for multiscale analysis of large vascular networks,” NeuroImage32, 626–636 (2006). [CrossRef] [PubMed]
- A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron52, 205–220 (2006). [CrossRef] [PubMed]
- A. R. Pries, A. J. M. Cornelissen, A. A. Sloot, M. Hinkeldey, M. R. Dreher, M. Hpfner, M. W. Dewhirst, and T. W. Secomb, “Structural adaptation and heterogeneity of normal and tumor microvascular networks,” PLoS Computational Biology5, e1000394 (2009). [CrossRef] [PubMed]
- J. A. Sethian, Level Set Methods and Fast Marching Methods: Evolving Interfaces in Computational Geometry, Fluid Mechanics, Computer Vision, and Materials Science (Cambridge University Press, 1999).
- B. R. Shepherd, H. Y. Chen, C. M. Smith, G. Gruionu, S. K. Williams, and J. B. Hoying, “Rapid perfusion and network remodeling in a microvascular construct after implantation,” Arteriosclerosis, Thrombosis, Vascular Biology24, 898 –904 (2004). [CrossRef]
- P. Blinder, A. Y. Shih, C. Rafie, and D. Kleinfeld, “Topological basis for the robust distribution of blood to rodent neocortex,” Proceedings of the National Academy of Sciences107, 12670 –12675 (2010). [CrossRef]
- A. R. Pries, A. J. M. Cornelissen, A. A. Sloot, M. Hinkeldey, M. R. Dreher, M. Hpfner, M. W. Dewhirst, and T. W. Secomb, “Structural adaptation and heterogeneity of normal and tumor microvascular networks,” PLoS Computational Biology5, e1000394 (2009). [CrossRef] [PubMed]
- B. R. Shepherd, H. Y. Chen, C. M. Smith, G. Gruionu, S. K. Williams, and J. B. Hoying, “Rapid perfusion and network remodeling in a microvascular construct after implantation,” Arteriosclerosis, Thrombosis, Vascular Biology24, 898 –904 (2004). [CrossRef]
- K. D. Micheva and S. J. Smith, “Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits,” Neuron55, 25–36 (2007). [CrossRef] [PubMed]
- L. C. Abbott and C. Sotelo, “Ultrastructural analysis of catecholaminergic innervation in weaver and normal mouse cerebellar cortices,” The Journal of Comparative Neurology426, 316–329 (2000). [CrossRef] [PubMed]
- P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron39, 27–41 (2003). [CrossRef] [PubMed]
- S. Heinzer, T. Krucker, M. Stampanoni, R. Abela, E. P. Meyer, A. Schuler, P. Schneider, and R. Muller, “Hierarchical microimaging for multiscale analysis of large vascular networks,” NeuroImage32, 626–636 (2006). [CrossRef] [PubMed]
- C. Sung, J. R. Chung, D. Mayerich, J. Kwon, D. Miller, T. Huffman, J. Keyser, L. Abbott, and Y. Choe, “Knife-edge scanning microscope brain atlas: A submicrometer-resolution web-based mouse brain atlas,” in “2011 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2011). Program No. 328.05. Online.
- S. Akita, N. Tamai, A. Myoui, M. Nishikawa, T. Kaito, K. Takaoka, and H. Yoshikawa, “Capillary vessel network integration by inserting a vascular pedicle enhances bone formation in Tissue-Engineered bone using interconnected porous hydroxyapatite ceramics,” Tissue Engineering10, 789–795 (2004). [CrossRef] [PubMed]
- S. Akita, N. Tamai, A. Myoui, M. Nishikawa, T. Kaito, K. Takaoka, and H. Yoshikawa, “Capillary vessel network integration by inserting a vascular pedicle enhances bone formation in Tissue-Engineered bone using interconnected porous hydroxyapatite ceramics,” Tissue Engineering10, 789–795 (2004). [CrossRef] [PubMed]
- P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron39, 27–41 (2003). [CrossRef] [PubMed]
- P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron39, 27–41 (2003). [CrossRef] [PubMed]
- P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron39, 27–41 (2003). [CrossRef] [PubMed]
- S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine63, 1637–1647 (2010). [CrossRef] [PubMed]
- S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine63, 1637–1647 (2010). [CrossRef] [PubMed]
- A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science330, 1404 –1408 (2010). [CrossRef] [PubMed]
- A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron52, 205–220 (2006). [CrossRef] [PubMed]
- M. Wiercigroch and E. Budak, “Sources of nonlinearities, chatter generation and suppression in metal cutting,” Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences359, 663–693 (2001). [CrossRef]
- B. R. Shepherd, H. Y. Chen, C. M. Smith, G. Gruionu, S. K. Williams, and J. B. Hoying, “Rapid perfusion and network remodeling in a microvascular construct after implantation,” Arteriosclerosis, Thrombosis, Vascular Biology24, 898 –904 (2004). [CrossRef]
- A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science330, 1404 –1408 (2010). [CrossRef] [PubMed]
- P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron39, 27–41 (2003). [CrossRef] [PubMed]
- A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science330, 1404 –1408 (2010). [CrossRef] [PubMed]
- S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine63, 1637–1647 (2010). [CrossRef] [PubMed]
- T. S. Yoo, Insight into Images: Principles and Practice for Segmentation, Registration, and Image Analysis (A K Peters/CRC Press, 2004), 1st ed. [CrossRef]
- S. Akita, N. Tamai, A. Myoui, M. Nishikawa, T. Kaito, K. Takaoka, and H. Yoshikawa, “Capillary vessel network integration by inserting a vascular pedicle enhances bone formation in Tissue-Engineered bone using interconnected porous hydroxyapatite ceramics,” Tissue Engineering10, 789–795 (2004). [CrossRef] [PubMed]
- A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science330, 1404 –1408 (2010). [CrossRef] [PubMed]
- A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science330, 1404 –1408 (2010). [CrossRef] [PubMed]
American Journal of Physiology - Heart and Circulatory Physiology
- E. M. Renkin, S. D. Gray, and L. R. Dodd, “Filling of microcirculation in skeletal muscles during timed india ink perfusion,” American Journal of Physiology - Heart and Circulatory Physiology241, H174 –H186 (1981).
Arteriosclerosis, Thrombosis, Vascular Biology
- B. R. Shepherd, H. Y. Chen, C. M. Smith, G. Gruionu, S. K. Williams, and J. B. Hoying, “Rapid perfusion and network remodeling in a microvascular construct after implantation,” Arteriosclerosis, Thrombosis, Vascular Biology24, 898 –904 (2004). [CrossRef]
Brain Research
- F. Cassot, F. Lauwers, S. Lorthois, P. Puwanarajah, V. Cances-Lauwers, and H. Duvernoy, “Branching patterns for arterioles and venules of the human cerebral cortex,” Brain Research1313, 62–78 (2010). [CrossRef]
Graphical Models and Image Processing
- T. C. Lee, R. L. Kashyap, and C. N. Chu, “Building skeleton models via 3-D medial surface/axis thinning algorithms,” Graphical Models and Image Processing56, 462–478 (1994). [CrossRef]
Journal of Computer-Assisted Microscopy
- X. He, E. Kischell, M. Rioult, and T. J. Holmes, “Three-Dimensional thinning algorithm that peels the outmost layer with application to neuron tracing,” Journal of Computer-Assisted Microscopy10, 123–135 (1998). [CrossRef]
Journal of Microscopy
- D. Mayerich, L. C. Abbott, and B. H. McCormick, “Knife-Edge scanning microscopy for imaging and reconstruction of Three-Dimensional anatomical structures of the mouse brain,” Journal of Microscopy231, 134–143 (2008). [CrossRef] [PubMed]
Magnetic Resonance in Medicine
- S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine63, 1637–1647 (2010). [CrossRef] [PubMed]
Microcirculation
- F. Cassot, F. Lauwers, C. Fouard, S. Prohaska, and V. Lauwers-Cances, “A novel Three-Dimensional Computer-Assisted method for a quantitative study of microvascular networks of the human cerebral cortex,” Microcirculation13, 1–18 (2006). [CrossRef] [PubMed]
Microscopy research and technique
- T. Krucker, A. Lang, and E. P. Meyer, “New polyurethane-based material for vascular corrosion casting with improved physical and imaging characteristics,” Microscopy research and technique69, 138–147 (2006). [CrossRef] [PubMed]
NeuroImage
- S. Heinzer, T. Krucker, M. Stampanoni, R. Abela, E. P. Meyer, A. Schuler, P. Schneider, and R. Muller, “Hierarchical microimaging for multiscale analysis of large vascular networks,” NeuroImage32, 626–636 (2006). [CrossRef] [PubMed]
- F. Lauwers, F. Cassot, V. Lauwers-Cances, P. Puwanarajah, and H. Duvernoy, “Morphometry of the human cerebral cortex microcirculation: General characteristics and space-related profiles,” NeuroImage39, 936–948 (2008). [CrossRef]
Neuron
- P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron39, 27–41 (2003). [CrossRef] [PubMed]
- A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron52, 205–220 (2006). [CrossRef] [PubMed]
- K. D. Micheva and S. J. Smith, “Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits,” Neuron55, 25–36 (2007). [CrossRef] [PubMed]
Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences
- M. Wiercigroch and E. Budak, “Sources of nonlinearities, chatter generation and suppression in metal cutting,” Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences359, 663–693 (2001). [CrossRef]
PLoS Computational Biology
- A. R. Pries, A. J. M. Cornelissen, A. A. Sloot, M. Hinkeldey, M. R. Dreher, M. Hpfner, M. W. Dewhirst, and T. W. Secomb, “Structural adaptation and heterogeneity of normal and tumor microvascular networks,” PLoS Computational Biology5, e1000394 (2009). [CrossRef] [PubMed]
Proceedings of the National Academy of Sciences
- P. Blinder, A. Y. Shih, C. Rafie, and D. Kleinfeld, “Topological basis for the robust distribution of blood to rodent neocortex,” Proceedings of the National Academy of Sciences107, 12670 –12675 (2010). [CrossRef]
Science
- A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science330, 1404 –1408 (2010). [CrossRef] [PubMed]
The Journal of Comparative Neurology
- L. C. Abbott and C. Sotelo, “Ultrastructural analysis of catecholaminergic innervation in weaver and normal mouse cerebellar cortices,” The Journal of Comparative Neurology426, 316–329 (2000). [CrossRef] [PubMed]
Tissue Engineering
- S. Akita, N. Tamai, A. Myoui, M. Nishikawa, T. Kaito, K. Takaoka, and H. Yoshikawa, “Capillary vessel network integration by inserting a vascular pedicle enhances bone formation in Tissue-Engineered bone using interconnected porous hydroxyapatite ceramics,” Tissue Engineering10, 789–795 (2004). [CrossRef] [PubMed]
Other
- Y. Choe, D. Han, P. Huang, J. Keyser, J. Kwon, D. Mayerich, and L. Abbott, “Complete submicrometer scans of mouse brain microstructure: Neurons and vasculatures,” in “2009 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2009). Program No. 389.10. Online.
- D. Mayerich, J. Kwon, Y. Choe, L. Abbott, and J. Keyser, “Constructing high resolution microvascular models,” in “Third Workshop on Microscopic Image Analysis with Applications in Biology,” (2008).
- D. Mayerich, B. H. McCormick, and J. Keyser, “Noise and artifact removal in Knife-Edge scanning microscopy,” Proceedings of the 4th IEEE International Symposium on Biomedical Imaging: From Nano to Macro pp. 556–559 (2007). [CrossRef]
- T. S. Yoo, Insight into Images: Principles and Practice for Segmentation, Registration, and Image Analysis (A K Peters/CRC Press, 2004), 1st ed. [CrossRef]
- J. A. Sethian, Level Set Methods and Fast Marching Methods: Evolving Interfaces in Computational Geometry, Fluid Mechanics, Computer Vision, and Materials Science (Cambridge University Press, 1999).
- C. Sung, J. R. Chung, D. Mayerich, J. Kwon, D. Miller, T. Huffman, J. Keyser, L. Abbott, and Y. Choe, “Knife-edge scanning microscope brain atlas: A submicrometer-resolution web-based mouse brain atlas,” in “2011 Neuroscience Meeting Planner,” (Chicago, IL: Society for Neuroscience, 2011). Program No. 328.05. Online.
2010, Ungersma, Magnetic Resonance in Medicine
- S. E. Ungersma, G. Pacheco, C. Ho, S. F. Yee, J. Ross, N. van Bruggen, F. V. Peale, S. Ross, and R. A. Carano, “Vessel imaging with viable tumor analysis for quantification of tumor angiogenesis,” Magnetic Resonance in Medicine63, 1637–1647 (2010). [CrossRef] [PubMed]
- P. Blinder, A. Y. Shih, C. Rafie, and D. Kleinfeld, “Topological basis for the robust distribution of blood to rodent neocortex,” Proceedings of the National Academy of Sciences107, 12670 –12675 (2010). [CrossRef]
- F. Cassot, F. Lauwers, S. Lorthois, P. Puwanarajah, V. Cances-Lauwers, and H. Duvernoy, “Branching patterns for arterioles and venules of the human cerebral cortex,” Brain Research1313, 62–78 (2010). [CrossRef]
- A. Li, H. Gong, B. Zhang, Q. Wang, C. Yan, J. Wu, Q. Liu, S. Zeng, and Q. Luo, “Micro-Optical sectioning tomography to obtain a High-Resolution atlas of the mouse brain,” Science330, 1404 –1408 (2010). [CrossRef] [PubMed]
- A. R. Pries, A. J. M. Cornelissen, A. A. Sloot, M. Hinkeldey, M. R. Dreher, M. Hpfner, M. W. Dewhirst, and T. W. Secomb, “Structural adaptation and heterogeneity of normal and tumor microvascular networks,” PLoS Computational Biology5, e1000394 (2009). [CrossRef] [PubMed]
- F. Lauwers, F. Cassot, V. Lauwers-Cances, P. Puwanarajah, and H. Duvernoy, “Morphometry of the human cerebral cortex microcirculation: General characteristics and space-related profiles,” NeuroImage39, 936–948 (2008). [CrossRef]
- D. Mayerich, L. C. Abbott, and B. H. McCormick, “Knife-Edge scanning microscopy for imaging and reconstruction of Three-Dimensional anatomical structures of the mouse brain,” Journal of Microscopy231, 134–143 (2008). [CrossRef] [PubMed]
- K. D. Micheva and S. J. Smith, “Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits,” Neuron55, 25–36 (2007). [CrossRef] [PubMed]
- F. Cassot, F. Lauwers, C. Fouard, S. Prohaska, and V. Lauwers-Cances, “A novel Three-Dimensional Computer-Assisted method for a quantitative study of microvascular networks of the human cerebral cortex,” Microcirculation13, 1–18 (2006). [CrossRef] [PubMed]
- S. Heinzer, T. Krucker, M. Stampanoni, R. Abela, E. P. Meyer, A. Schuler, P. Schneider, and R. Muller, “Hierarchical microimaging for multiscale analysis of large vascular networks,” NeuroImage32, 626–636 (2006). [CrossRef] [PubMed]
- T. Krucker, A. Lang, and E. P. Meyer, “New polyurethane-based material for vascular corrosion casting with improved physical and imaging characteristics,” Microscopy research and technique69, 138–147 (2006). [CrossRef] [PubMed]
- A. B. Schwartz, X. T. Cui, D. J. Weber, and D. W. Moran, “Brain-Controlled interfaces: Movement restoration with neural prosthetics,” Neuron52, 205–220 (2006). [CrossRef] [PubMed]
- B. R. Shepherd, H. Y. Chen, C. M. Smith, G. Gruionu, S. K. Williams, and J. B. Hoying, “Rapid perfusion and network remodeling in a microvascular construct after implantation,” Arteriosclerosis, Thrombosis, Vascular Biology24, 898 –904 (2004). [CrossRef]
- S. Akita, N. Tamai, A. Myoui, M. Nishikawa, T. Kaito, K. Takaoka, and H. Yoshikawa, “Capillary vessel network integration by inserting a vascular pedicle enhances bone formation in Tissue-Engineered bone using interconnected porous hydroxyapatite ceramics,” Tissue Engineering10, 789–795 (2004). [CrossRef] [PubMed]
- P. S. Tsai, B. Friedman, A. Ifarraguerri, B. D. Thompson, V. Lev-Ram, C. B. Schaer, Q. Xiong, R. Y. Tsien, J. A. Squier, and D. Kleinfeld, “All-Optical histology using ultrashort laser pulses,” Neuron39, 27–41 (2003). [CrossRef] [PubMed]
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