A three-dimensional image processing program for accurate, rapid, and semi-automated segmentation of neuronal somata with dense neurite outgrowth

Frontiers in Neuroanatomy

Volumn 9, Issue July, 2015, Pages

  Ross, James D ^a,b   Cullen, D Kacy ^c,d   Harris, James P ^c,d   LaPlaca, Michelle C ^a   DeWeerth, Stephen P ^a,b  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Confocal; Fluorescent microscopy; Image processing; Neural constructs; Segmentation

Indexed keywords

ALGORITHM; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL VIABILITY; COMPUTER INTERFACE; CONFOCAL LASER MICROSCOPY; FETUS; FLUORESCENCE MICROSCOPY; IMAGE ANALYSIS; IMAGE PROCESSING; MATHEMATICAL MODEL; MEASUREMENT ACCURACY; METHODOLOGY; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; RAT; STATISTICAL PARAMETERS; THREE DIMENSIONAL IMAGING;

EID: 84937910017     PISSN: 16625129     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2015.00087     Document Type: Article

References (34)

1. Adiga, P. S. U., and Chaudhuri, B. B. (2000). Region based techniques for segmentation of volumetric histo-pathological images. Comput. Methods Programs Biomed. 61, 23-47. doi: 10.1016/S0169-2607(99)00026-7
2. Adiga, P. S. U., and Chaudhuri, B. B. (2001). An efficient method based on watershed and rule-based merging for segmentation of 3-D histo-pathological images. Pattern Recognit. 34, 1449-1458. doi: 10.1016/S0031-3203(00)00076-5
3. Al-Kofahi, K. A., Can, A., Lasek, S., Szarowski, D. H., Dowell-Mesfin, N., Shain, W., et al. (2003). Median-based robust algorithms for tracing neurons from noisy confocal microscope images. IEEE Trans. Inf. Technol. Biomed. 7, 302-317. doi: 10.1109/TITB.2003.816564
4. Al-Kofahi, K. A., Lasek, S., Szarowski, D. H., Pace, C. J., Nagy, G., Turner, J. N., et al. (2002). Rapid automated three-dimensional tracing of neurons from confocal image stacks. IEEE Trans. Inf. Technol. Biomed. 6, 171-187. doi: 10.1109/TITB.2002.1006304
5. Belien, J. A. M., van Ginkel, H., Tekola, P., Ploeger, L. S., Poulin, N. M., and van Diest, P. J. (2002). Confocal DNA cytometry: a contour-based segmentation algorithm for automated three-dimensional image segmentation. Cytometry 49, 12-21. doi: 10.1002/cyto.10138
6. Bjornsson, C. S., Lin, G., Al-Kofahi, Y., Narayanaswamy, A., Smith, K. L., Shain, W., et al. (2008). Associative image analysis: a method for automated quantification of 3D multi-parameter images of brain tissue. J. Neurosci. Methods 170, 165-178. doi: 10.1016/j.jneumeth.2007.12.024
7. Chawla, M. K., Lin, G., Olson, K., Vazdarjanova, A., Burke, S. N., Mcnaughton, B. L., et al. (2004). 3D-catFISH: a system for automated quantitative three-dimensional compartmental analysis of temporal gene transcription activity imaged by fluorescence in situ hybridization. J. Neurosci. Methods 139, 13-24. doi: 10.1016/j.jneumeth.2004.04.017
8. Crespo, J., and Maoio, V. (1999). "Shape preservation in morphological filtering and segmentation," in Computer Graphics and Image Processing, 1999. Proceedings. XII Brazilian Symposium on (Campinas: IEEE), 247-256.
9. Cullen, D. K., and Laplaca, M. C. (2006). Neuronal response to high rate shear deformation depends on heterogeneity of the local strain field. J. Neurotrauma 23, 1304-1319. doi: 10.1089/neu.2006.23.1304
10. Cullen, D. K., Lessing, M. C., and Laplaca, M. C. (2007). Collagen-dependent neurite outgrowth and response to dynamic deformation in three-dimensional neuronal cultures. Ann. Biomed. Eng. 35, 835-846. doi: 10.1007/s10439-007-9292-z
11. Cullen, D. K., Wolf, J. A., Vernekar, V. N., Vukasinovic, J., and Laplaca, M. C. (2011). Neural tissue engineering and biohybridized microsystems for neurobiological investigation in vitro (part 1). Crit. Rev. Biomed. Eng. 39, 201-240. doi: 10.1615/CritRevBiomedEng.v39.i3.30
12. Gobel, W., Kampa, B. M., and Helmchen, F. (2007). Imaging cellular network dynamics in three dimensions using fast 3D laser scanning. Nat. Methods 4, 73-79. doi: 10.1038/nmeth989
13. Gonzalez, R. C., and Woods, R. E. (2002). Digital Image Processing, 2nd Edn. New Jersey, NJ: Prentice Hall.
14. Gutierrez-Ospina, G., Uribe-Querol, E., Sanchez, N., Geovannini, H., Padilla, P., and Hernandez-Echeagaray, E. (2004). Similar synapse density in layer IV columns of the primary somatosensory cortex of transgenic mice with different brain size: implications for mechanisms underlying the differential allocation of cortical space.Brain Behav. Evol. 64, 61-69. doi: 10.1159/000079116
15. Hopkins, A. M., Desimone, E., Chwalek, K., and Kaplan, D. L. (2015). 3D in vitro modeling of the central nervous system. Prog. Neurobiol. 125, 1-25. doi: 10.1016/j.pneurobio.2014.11.003
16. Irinopoulou, T., Vassy, J., Beil, M., Nicolopoulou, P., Encaoua, D., and Rigaut, J. P. (1997). Three-dimensional DNA image cytometry by confocal scanning laser microscopy in thick tissue blocks of prostatic lesions. Cytometry 27, 99-105.
17. Koh, I. Y. Y., Lindquist, W. B., Zito, K., Nimchinsky, E. A., and Svoboda, K. (2002). An image analysis algorithm for dendritic spines. Neural Comput. 14, 1283-1310. doi: 10.1162/089976602753712945
18. Kumar, J., and Shunmugam, M. S. (2006). Morphological operations on engineering surfaces using a 3D-structuring element of an appropriate size. Meas. Sci. Technol. 17, 2655-2664. doi: 10.1088/0957-0233/17/10/018
19. Latorre, A., Alonso-Nanclares, L., Muelas, S., Peòa, J.-M., and Defelipe, J. (2013). 3D segmentations of neuronal nuclei from confocal microscope image stacks. Front. Neuroanat. 7:49. doi: 10.3389/fnana.2013.00049
20. Lin, G., Adiga, U., Olson, K., Guzowski, J. F., Barnes, C. A., and Roysam, B. (2003). A hybrid 3D watershed algorithm incorporating gradient cues and object models for automatic segmentation of nuclei in confocal image stacks. Cytometry A 56, 23-36. doi: 10.1002/cyto.a.10079
21. Lin, G., Chawla, M. K., Olson, K., Guzowski, J. F., Barnes, C. A., and Roysam, B. (2005a). Hierarchical, model-based merging of multiple fragments for improved three-dimensional segmentation of nuclei. Cytometry A 63, 20-33. doi: 10.1002/cyto.a.20099
22. Lin, P. W., Wu, C. C., Chen, C. H., Ho, H. O., Chen, Y. C., and Sheu, M. T. (2005b). Characterization of cortical neuron outgrowth in two- and three-dimensional culture systems. J. Biomed. Mater. Res. B Appl. Biomater. 75B, 146-157. doi: 10.1002/jbm.b.30276
23. Luisi, J., Narayanaswamy, A., Galbreath, Z., and Roysam, B. (2011). The FARSIGHT trace editor: an open source tool for 3-D inspection and efficient pattern analysis aided editing of automated neuronal reconstructions. Neuroinformatics 9, 305-315. doi: 10.1007/s12021-011-9115-0
24. Meijering, E., Jacob, M., Sarria, J. C. F., Steiner, P., Hirling, H., and Unser, M. (2004). Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry Part A 58A, 167-176. doi: 10.1002/cyto.a.20022
25. Sarti, A., De Solorzano, C. O., Lockett, S., and Malladi, R. (2000). A geometric model for 3-D confocal image analysis. IEEE Trans. Biomed. Eng. 47, 1600-1609. doi: 10.1109/10.887941
26. Seeger, G., Gartner, U., and Arendt, T. (2005). Transgenic activation of Ras in neurons increases synapse formation in mouse neocortex. J. Neural. Transm. 112, 751-761. doi: 10.1007/s00702-004-0226-8
27. Solórzano, C. O., Rodriguez, E. G., Jones, A., Pinkel, D., Gray, J. W., Sudar, D., et al. (1999). Segmentation of confocal microscope images of cell nuclei in thick tissue sections. J. Microsc. 193, 212-226. doi: 10.1046/j.1365-2818.1999.00463.x
28. Stosiek, C., Garaschuk, O., Holthoff, K., and Konnerth, A. (2003). In vivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. U.S.A. 100, 7319-7324. doi: 10.1073/pnas.1232232100
29. Sullivan, M. R., Nimmerjahn, A., Sarkisov, D. V., Helmchen, F., and Wang, S. S. H. (2005). In vivo calcium imaging of circuit activity in cerebellar cortex. J. Neurophysiol. 94, 1636-1644. doi: 10.1152/jn.01013.2004
30. Tekola, P., Baak, J. P. A., van Ginkel, H., Belien, J. A. M., van Diest, P. J., Broeckaert, M. A., et al. (1996). Three-dimensional confocal laser scanning DNA ploidy cytometry in thick histological sections. J. Pathol. 180, 214-222.
31. Umesh Adiga, B. B. C. (2001). An efficient method based on watershed and rule-based merging for segmentation of 3-D histo-pathological images. Pattern Recognit. 34, 1449-1458. doi: 10.1016/S0031-3203(00)00076-5
32. Umesh Adiga, P. S., and Chaudhuri, B. B. (1999). Efficient cell segmentation tool for confocal microscopy tissue images and quantitative evaluation of FISH signals.Microsc. Res. Tech. 44, 49-68.
33. Yu, X. J., Dillon, G. P., and Bellamkonda, R. V. (1999). A laminin and nerve growth factor-laden three-dimensional scaffold for enhanced neurite extension. Tissue Eng. 5, 291-304. doi: 10.1089/ten.1999.5.291
34. Zhang, Y., Zhou, X. B., Degterev, A., Lipinski, M., Adjeroh, D., Yuan, J. Y., et al. (2007). A novel tracing algorithm for high throughput imaging - screening of neuron-based assays. J. Neurosci. Methods 160, 149-162. doi: 10.1016/j.jneumeth.2006.07.028