Automated Neuron Detection in High-Content Fluorescence Microscopy Images Using Machine Learning.
Fluorescence microscopy
High-content analysis
Machine learning
Neuron detection
Journal
Neuroinformatics
ISSN: 1559-0089
Titre abrégé: Neuroinformatics
Pays: United States
ID NLM: 101142069
Informations de publication
Date de publication:
04 2019
04 2019
Historique:
pubmed:
15
9
2018
medline:
23
8
2019
entrez:
15
9
2018
Statut:
ppublish
Résumé
The study of neuronal morphology in relation to function, and the development of effective medicines to positively impact this relationship in patients suffering from neurodegenerative diseases, increasingly involves image-based high-content screening and analysis. The first critical step toward fully automated high-content image analyses in such studies is to detect all neuronal cells and distinguish them from possible non-neuronal cells or artifacts in the images. Here we investigate the performance of well-established machine learning techniques for this purpose. These include support vector machines, random forests, k-nearest neighbors, and generalized linear model classifiers, operating on an extensive set of image features extracted using the compound hierarchy of algorithms representing morphology, and the scale-invariant feature transform. We present experiments on a dataset of rat hippocampal neurons from our own studies to find the most suitable classifier(s) and subset(s) of features in the common practical setting where there is very limited annotated data for training. The results indicate that a random forests classifier using the right feature subset ranks best for the considered task, although its performance is not statistically significantly better than some support vector machine based classification models.
Identifiants
pubmed: 30215167
doi: 10.1007/s12021-018-9399-4
pii: 10.1007/s12021-018-9399-4
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Pagination
253-269Subventions
Organisme : Ministerio de Economía y Competitividad (ES)
ID : MTM2014-54151-P
Pays : International
Organisme : Ministerio de Economía y Competitividad (ES)
ID : UNLC08-1E-002
Pays : International
Organisme : Ministerio de Economía y Competitividad
ID : UNLC13-13-3503
Pays : International
Organisme : Universidad de La Rioja
ID : FPI-UR-13
Pays : International
Organisme : European Regional Development Fund ()
ID : 612.001.018
Pays : International
Organisme : Ministerio de Economía y Competitividad (ES)
ID : FJCI-2015-26071
Pays : International
Références
Anderl, J.L., Redpath, S., Ball, A.J. (2009). A neuronal and astrocyte co-culture assay for high content analysis of neurotoxicity. Journal of Visualized Experiments, 5(27), 1173.
Antony, P.M.A., Trefois, C., Stojanovic, A., Baumuratov, A.S., Kozak, K. (2013). Light microscopy applications in systems biology: opportunities and challenges. Cell Communication and Signaling, 11(24), 1–19.
Arganda-Carreras, I., Kaynig, V., Rueden, C., Eliceiri, K.W., Schindelin, J., Cardona, A., Seung, H.S. (2017). Trainable Weka Segmentation: a machine learning tool for microscopy pixel classification. Bioinformatics, 33(15), 2424–2426.
doi: 10.1093/bioinformatics/btx180
pubmed: 28369169
Ascoli, G.A. (2015). Trees of the brain, roots of the mind. Cambridge: MIT Press.
doi: 10.7551/mitpress/10292.001.0001
Bianchini, M., & Scarselli, F. (2014). On the complexity of neural network classifiers: a comparison between shallow and deep architectures. IEEE Transactions on Neural Networks and Learning Systems, 25(8), 1553–1565.
doi: 10.1109/TNNLS.2013.2293637
pubmed: 25050951
Bischl, B., Mersmann, O., Trautmann, H., Weihs, C. (2012). Resampling methods for meta-model validation with recommendations for evolutionary computation. Evolutionary Computation, 20(2), 249–275.
doi: 10.1162/EVCO_a_00069
pubmed: 22339368
Bischl, B., Lang, M., Kotthoff, L., Schiffner, J., Richter, J., Jones, Z., Casalicchio, G. (2016). mlr: Machine Learning in R. https://CRAN.R-project.org/package=mlr .
Bishop, C.M. (2006). Pattern recognition and machine learning. New York: Springer.
Boser, B.E., Guyon, I.M., Vapnik, V.N. (1992). A training algorithm for optimal margin classifiers. In Proceedings of the 5th Annual ACM Workshop on Computational Learning Theory (pp. 144–152).
Bougen-Zhukov, N., Loh, S.Y., Lee, H.K., Loo, L.H. (2017). Large-scale image-based screening and profiling of cellular phenotypes. Cytometry Part A, 91(2), 115–125.
doi: 10.1002/cyto.a.22909
Branco, P., Torgo, L., Ribeiro, R.P. (2016). A survey of predictive modeling on imbalanced domains. ACM Computing Surveys, 49(2), 31:1–31:50.
doi: 10.1145/2907070
Bredenbeek, P.J., Frolov, I., Rice, C.M., Schlesinger, S. (1993). Sindbis virus expression vectors: packaging of RNA, replicons by using defective helper RNAs. Journal of Virology, 67(11), 6439–6446.
pubmed: 8411346
pmcid: 238079
Breiman, L. (2001). Random forests. Machine Learning, 45(1), 5–32.
doi: 10.1023/A:1010933404324
Burges, C.J.C. (1998). A tutorial on support vector machines for pattern recognition. Data Mining and Knowledge Discovery, 2(2), 121–167.
doi: 10.1023/A:1009715923555
Charoenkwan, P., Hwang, E., Cutler, R.W., Lee, H.C., Ko, L.W., Huang, H.L., Ho, S.Y. (2013). HCS-Neurons: identifying phenotypic changes in multi-neuron images upon drug treatments of high-content screening. BMC Bioinformatics, 14(S16), S12.
doi: 10.1186/1471-2105-14-S16-S12
pubmed: 24564437
pmcid: 3853092
Chawla, N.V., Bowyer, K.W., Hall, L.O., Kegelmeyer, W.P. (2002). SMOTE: Synthetic minority over-sampling technique. Journal of Artificial Intelligence Research, 16(1), 321–357.
doi: 10.1613/jair.953
Chawla, N.V., Japkowicz, N., Kotcz, A. (2004). Editorial: Special issue on learning from imbalanced data sets. ACM SIGKDD Explorations Newsletter, 6(1), 1–6.
doi: 10.1145/1007730.1007733
Cover, T., & Hart, P. (1967). Nearest neighbor pattern classification. IEEE Transactions on Information Theory, 13(1), 21–27.
doi: 10.1109/TIT.1967.1053964
Cristianini, N., & Shawe-Taylor, J. (2000). An introduction to support vector machines and other Kernel-Based learning methods. Cambridge: University Press.
doi: 10.1017/CBO9780511801389
Cuesto, G., Enriquez-Barreto, L., Caramés, C., Cantarero, M., Gasull, X., Sandi, C., Ferrús, A., Acebes, Á., Morales, M. (2011). Phosphoinositide-3-kinase activation controls synaptogenesis and spinogenesis in hippocampal neurons. Journal of Neuroscience, 31(8), 2721–2733.
doi: 10.1523/JNEUROSCI.4477-10.2011
pubmed: 21414895
Dalal, N., & Triggs, B. (2005). Histograms of oriented gradients for human detection. In Proceedings of the IEEE Computer Society Conference on Computer Vision and Pattern Recognition (pp. 886–893).
Daskalaki, S., Kopanas, I., Avouris, N. (2006). Evaluation of classifiers for an uneven class distribution problem. Applied Artificial Intelligence, 20(5), 381–417.
doi: 10.1080/08839510500313653
Dehmelt, L., Poplawski, G., Hwang, E., Halpain, S. (2011). NeuriteQuant: an open source toolkit for high content screens of neuronal morphogenesis. BMC Neuroscience, 12(100), 1–13.
Dragunow, M. (2008). High-content analysis in neuroscience. Nature Reviews Neuroscience, 9(10), 779–788.
doi: 10.1038/nrn2492
pubmed: 18784656
Ebrahimpour, M.K., Zare, M., Eftekhari, M., Aghamolaei, G. (2017). Occam’s razor in dimension reduction: using reduced row Echelon, form for finding linear independent features in high dimensional microarray datasets. Engineering Applications of Artificial Intelligence, 62, 214–221.
doi: 10.1016/j.engappai.2017.04.006
Enriquez-Barreto, L., Cuesto, G., Dominguez-Iturza, N., Gavilán, E., Ruano, D., Sandi, C., Fernández-Ruiz, A., Martín-Vázquez, G., Herreras, O., Morales, M. (2014). Learning improvement after PI3K, activation correlates with de novo formation of functional small spines. Frontiers in Molecular Neuroscience, 6, 54.
doi: 10.3389/fnmol.2013.00054
pubmed: 24427113
pmcid: 3877779
Enriquez-Barreto, L., & Morales, M. (2016). The PI3K, signaling pathway as a pharmacological target in autism related disorders and schizophrenia. Molecular and Cellular Therapies, 4, 2.
doi: 10.1186/s40591-016-0047-9
pubmed: 26877878
pmcid: 4751644
Fawcett, T. (2006). An introduction to ROC, analysis. Pattern Recognition Letters, 27(8), 861–874.
doi: 10.1016/j.patrec.2005.10.010
Fei-Fei, L., & Perona, P. (2005). A Bayesian hierarchical model for learning natural scene categories. In Proceedings of the IEEE Conference on Computer Vision and Pattern Recognition, (Vol. 2 pp. 524–531).
Fernandez-Lozano, C., Gestal, M., Munteanu, C.R., Dorado, J., Pazos, A. (2016). A methodology for the design of experiments in computational intelligence with multiple regression models. PeerJ, 4, e2721.
doi: 10.7717/peerj.2721
pubmed: 27920952
pmcid: 5136129
Finner, H. (1993). On a monotonicity problem in step-down multiple test procedures. Journal of the American Statistical Association, 88(423), 920–923.
doi: 10.1080/01621459.1993.10476358
Forman, G., & Scholz, M. (2010). Apples-to-apples in cross-validation studies: pitfalls in classifier performance measurement. ACM SIGKDD Explorations Newsletter, 12(1), 49–57.
doi: 10.1145/1882471.1882479
Friedman, M. (1940). A comparison of alternative tests of significance for the problem of m rankings. Annals of Mathematical Statistics, 11(1), 86–92.
doi: 10.1214/aoms/1177731944
Friedman, J., Hastie, T., Tibshirani, R. (2010). Regularization paths for generalized linear models via coordinate descent. Journal of Statistical Software, 33(1), 1–22.
doi: 10.18637/jss.v033.i01
pubmed: 20808728
pmcid: 2929880
Gabor, D. (1946). Theory of communication. Journal of the Institution of Electrical Engineers — Part III: Radio and Communication Engineering, 93(26), 429–457.
García, S., Fernández, A., Luengo, J., Herrera, F. (2010). Advanced nonparametric tests for multiple comparisons in the design of experiments in computational intelligence and data mining: experimental analysis of power. Information Sciences, 180(10), 2044–2064.
doi: 10.1016/j.ins.2009.12.010
García, V., Mollineda, R.A., Sȧnchez, J.S. (2014). A bias correction function for classification performance assessment in two-class imbalanced problems. Knowledge-Based Systems, 59, 66–74.
doi: 10.1016/j.knosys.2014.01.021
Ghosh, A., Kumar, H., Sastry, P.S. (2017). Robust loss functions under label noise for deep neural networks. In Proceedings of the AAAI Conference on Artificial Intelligence (pp. 1919–1925).
Goslin, K., Asumussen, H., Banker, G. (1998). Rat hippocampal neurons in low-density culture. In Culturing Nerve cells (pp. 339–370). Cambridge: The MIT Press.
Gosain, A., & Sardana, S. (2017). Handling class imbalance problem using oversampling techniques: a review, In Proceedings of the International Conference on Advances in Computing, Communications and Informatics (pp. 79–85).
Gradshteyn, I.S., & Ryzhik, I.M. (1994). Table of integrals, series and products. New York: Academic Press.
Greenspan, H., van Ginneken, B., Summers, R.M. (2016). Deep learning in medical imaging: overview and future promise of an exciting new technique. IEEE Transactions on Medical Imaging, 35(5), 1153–1159.
doi: 10.1109/TMI.2016.2553401
Gupta, P., Batra, S.S., Jayadeva. (2017). Sparse short-term time series forecasting models via minimum model complexity. Neurocomputing, 243, 1–11.
doi: 10.1016/j.neucom.2017.02.002
Hadjidementriou, E., Grossberg, M., Nayar, S. (2001). Spatial information in multiresolution histograms. In Proceedings of the IEEE Conference on Computer Vision and Pattern Recognition (pp. I.702–I.709).
Haixiang, G., Yijing, L., Shang, J., Mingyun, G., Yuanyue, H., Bing, G. (2017). Learning from class-imbalanced data: review of methods and applications. Expert Systems with Applications, 73, 220–239.
doi: 10.1016/j.eswa.2016.12.035
Haralick, R.M., Shanmugam, K., Dinstein, I. (1973). Textural features for image classification. IEEE Transactions on Systems, Man, and Cybernetics, 3(6), 610–621.
doi: 10.1109/TSMC.1973.4309314
He, H., & Garcia, E.A. (2009). Learning from imbalanced data. IEEE Transactions on Knowledge and Data Engineering, 21(9), 1263–1284.
doi: 10.1109/TKDE.2008.239
He, K., Zhang, X., Ren, S., Sun, J. (2016). Deep residual learning for image recognition. In Proceedings of the IEEE Conference on Computer Vision and Pattern Recognition (pp. 770–778).
Hechenbichler, K., & Schliep, K. (2004). Weighted k-nearest-neighbor techniques and ordinal classification. Sonderforschungsbereich, 386(399), 1–16.
Hong, X., Gao, J., Chen, S., Harris, C.J. (2013). Particle swarm optimisation assisted classification using elastic net prefiltering. Neurocomputing, 122, 210–220.
doi: 10.1016/j.neucom.2013.06.030
Horvath, P., Wild, T., Kutay, U., Csucs, G. (2011). Machine learning improves the precision and robustness of high-content screens: using nonlinear multiparametric methods to analyze screening results. Journal of Biomolecular Screening, 16(9), 1059–1067.
doi: 10.1177/1087057111414878
pubmed: 21807964
Iacca, G., Neri, F., Mininno, E., Ong, Y.S., Lim, M.H. (2012). Ockham’s razor in memetic computing: three stage optimal memetic exploration. Information Sciences, 188, 17–43.
doi: 10.1016/j.ins.2011.11.025
Jain, S., van Kesteren, R.E., Heutink, P. (2012). High content screening in neurodegenerative diseases. Journal of Visualized Experiments, 59, e3452.
Jiang, R.M., Crookes, D., Luo, N., Davidson, M.W. (2010). Live-cell tracking using SIFT, features in DIC microscopic videos. IEEE Transactions on Biomedical Engineering, 57(9), 2219–2228.
doi: 10.1109/TBME.2010.2045376
pubmed: 20483698
Kingma, D.P., & Ba, J. (2014). Adam: a method for stochastic optimization, Computing Research Repository arXiv: 1412.6980 .
Kraus, O.Z., & Frey, B.J. (2016). Computer vision for high content screening. Critical Reviews in Biochemistry and Molecular Biology, 51(2), 102–109.
doi: 10.3109/10409238.2015.1135868
pubmed: 26806341
Krawczyk, B. (2016). Learning from imbalanced data: open challenges and future directions. Progress in Artificial Intelligence, 5(4), 221–232.
doi: 10.1007/s13748-016-0094-0
Kuminski, E., George, J., Wallin, J., Shamir, L. (2014). Combining human and machine learning for morphological analysis of galaxy images. Publications of the Astronomical Society of the Pacific, 126(944), 959–967.
doi: 10.1086/678977
Lazebnik, S., Schmid, C., Ponce, J. (2006). Beyond bags of features: Spatial pyramid matching for recognizing natural scene categories. In Proceedings of the IEEE Conference on Computer Vision and Pattern Recognition, (Vol. 2 pp. 2169–2178).
LeCun, Y., Bengio, Y., Hinton, G. (2015). Deep learning. Nature, 521(7553), 436–444.
doi: 10.1038/nature14539
pubmed: 26017442
Lee, D.H., Lee, D.W., Han, B.S. (2016). Possibility study of scale invariant feature transform (SIFT), algorithm application to spine magnetic resonance imaging. PLOS ONE, 11(4), 1–9.
Li, J., Fong, S., Wong, R.K., Chu, V.W. (2018). Adaptive multi-objective swarm fusion for imbalanced data classification. Information Fusion, 39, 1–24.
doi: 10.1016/j.inffus.2017.03.007
Liaw, A., & Wiener, M. (2002). Classification and regression by randomForest. R News, 2(3), 18–22.
Litjens, G., Kooi, T., Bejnordi, B.E., Setio, A.A.A., Ciompi, F., Ghafoorian, M., van der Laak, J.A.W.M., van Ginneken, B., Sánchez, C.I. (2017). A survey on deep learning in medical image analysis. Medical Image Analysis, 42, 60–88.
doi: 10.1016/j.media.2017.07.005
pubmed: 28778026
Lowe, D.G. (2004). Distinctive image features from scale-invariant keypoints. International Journal of Computer Vision, 60(2), 91–110.
doi: 10.1023/B:VISI.0000029664.99615.94
MacQueen, J. (1967). Some methods for classification and analysis of multivariate observations. In Proceedings of the 5th Berkeley Symposium on Mathematical Statistics and Probability — Volume 1: Statistics (pp. 281–297). Berkeley: University of California Press.
Mata, G., Radojević, M., Smal, I., Morales, M., Meijering, E., Rubio, J. (2016). Automatic detection of neurons in high-content microscope images using machine learning approaches. In Proceedings of the IEEE International Symposium on Biomedical Imaging: From Nano to Macro (pp. 330–333).
MathWorks. (2016). Version 9.0.0.341360 (R2016a). Natick: MA.
Meijering, E. (2010). Neuron tracing in perspective. Cytometry Part A, 77(7), 693–704.
doi: 10.1002/cyto.a.20895
Meijering, E., Carpenter, A.E., Peng, H., Hamprecht, F.A., Olivo-Marin, J.C. (2016). Imagining the future of bioimage analysis. Nature Biotechnology, 34(12), 1250–1255.
doi: 10.1038/nbt.3722
pubmed: 27926723
Meyer, D., Dimitriadou, E., Hornik, K., Weingessel, A., Leisch, F. (2017). e1071: Misc Functions of the Department of Statistics, Probability Theory Group (Formerly: E1071), TU Wien. https://CRAN.R-project.org/package=e1071 .
Mualla, F., Scholl, S., Sommerfeldt, B., Maier, A., Hornegger, J. (2013). Automatic cell detection in bright-field microscope images using SIFT, random forests, and hierarchical clustering. IEEE Transactions on Medical Imaging, 32(12), 2274–2286.
doi: 10.1109/TMI.2013.2280380
pubmed: 24001988
Ni, D., Chui, Y.P., Qu, Y., Yang, X.S., Qin, J., Wong, T.T., Ho, S.S.H., Heng, P.A. (2009). Reconstruction of volumetric ultrasound panorama based on improved 3D, SIFT. Computerized Medical Imaging and Graphics, 33(7), 559–566.
doi: 10.1016/j.compmedimag.2009.05.006
pubmed: 19524403
Orlov, N., Shamir, L., Macura, T., Johnston, J., Eckley, D.M., Goldberg, I.G. (2008). WND-CHARM: Multi-purpose image classification using compound image transforms. Pattern Recognition Letters, 29(11), 1684–1693.
doi: 10.1016/j.patrec.2008.04.013
pubmed: 18958301
pmcid: 2573471
Otsu, N. (1979). A threshold selection method from gray-level histograms. IEEE Transactions on Systems, Man, and Cybernetics, 9(1), 62–66.
doi: 10.1109/TSMC.1979.4310076
van Pelt, J., van Ooyen, A., Uylings, H. (2001). The need for integrating neuronal morphology databases and computational environments in exploring neuronal structure and function. Anatomy and Embryology, 204(4), 255–265.
doi: 10.1007/s004290100197
pubmed: 11720232
Prewitt, J.M.S. (1970). Object enhancement and extraction. In Picture Processing and psychopictorics (pp. 75–149). New York: Academic Press.
R Core Team. (2016). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org/ .
Radio, N. (2012). Neurite outgrowth assessment using high content analysis methodology. Methods in Molecular Biology, 846, 247–260.
doi: 10.1007/978-1-61779-536-7_22
pubmed: 22367817
Ramón y Cajal, S. (2007). Histología del sistema nervioso del hombre y de los vertebrados. CSIC Madrid reprinted in.
Saeys, Y., Inza, I., Larrañaga, P. (2007). A review of feature selection techniques in bioinformatics. Bioinformatics, 23(19), 2507–2517.
doi: 10.1093/bioinformatics/btm344
pubmed: 17720704
Sáez, J.A., Luengo, J., Stefanowski, J., Herrera, F. (2015). SMOTE-IPF: Addressing the noisy and borderline examples problem in imbalanced classification by a re-sampling method with filtering. Information Sciences, 291, 184–203.
doi: 10.1016/j.ins.2014.08.051
Samworth, R.J. (2012). Optimal weighted nearest neighbour classifiers. The Annals of Statistics, 40(5), 2733–2763.
doi: 10.1214/12-AOS1049
Schliep, K., & Hechenbichler, K. (2016). kknn: Weighted k-Nearest Neighbors. https://CRAN.R-project.org/package=kknn .
Shaikhina, T., & Khovanova, N.A. (2017). Handling limited datasets with neural networks in medical applications: a small-data approach. Artificial Intelligence in Medicine, 75, 51–63.
doi: 10.1016/j.artmed.2016.12.003
pubmed: 28363456
Shamir, L., Orlov, N., Eckley, D.M., Macura, T., Johnston, J., Goldberg, I.G. (2008). Wndchrm – an open source utility for biological image analysis. Source Code for Biology and Medicine, 3(1), 1–13.
doi: 10.1186/1751-0473-3-13
Shamir, L., Delaney, J.D., Orlov, N., Eckley, D.M., Goldberg, I.G. (2010). Pattern recognition software and techniques for biological image analysis. PLOS Computational Biology, 6(11), e1000974.
doi: 10.1371/journal.pcbi.1000974
pubmed: 21124870
pmcid: 2991255
Shamir, L. (2012a). Automatic detection of peculiar galaxies in large datasets of galaxy images. Journal of Computational Science, 3(3), 181–189.
doi: 10.1016/j.jocs.2012.03.004
Shamir, L., & Tarakhovsky, J.A. (2012b). Computer analysis of art. Journal on Computing and Cultural Heritage, 5(2), 7.
doi: 10.1145/2307723.2307726
Shapiro, S.S., & Wilk, M.B. (1965). An analysis of variance test for normality (complete samples). Biometrika, 52(3-4), 591– 611.
doi: 10.1093/biomet/52.3-4.591
Shen, D., Wu, G., Suk, H.I. (2017). Deep learning in medical image analysis. Annual Review of Biomedical Engineering, 19, 221– 248.
doi: 10.1146/annurev-bioeng-071516-044442
pubmed: 28301734
pmcid: 5479722
Simon, R. (2007). Resampling strategies for model assessment and selection. In Fundamentals of Data Mining in Genomics and Proteomics (pp. 173–186). Boston: Springer.
Simonyan, K., & Zisserman, A. (2014). Very deep convolutional networks for large-scale image recognition. Computing Research Repository arXiv: 1409.1556 .
Singh, S., Carpenter, A.E., Genovesio, A. (2014). Increasing the content of high-content screening: an overview. Journal of Biomolecular Screening, 19(5), 640–650.
doi: 10.1177/1087057114528537
pubmed: 24710339
pmcid: 4230961
Smafield, T., Pasupuleti, V., Sharma, K., Huganir, R.L., Ye, B., Zhou, J. (2015). Automatic dendritic length quantification for high throughput screening of mature neurons. Neuroinformatics, 13(4), 443–458.
doi: 10.1007/s12021-015-9267-4
pubmed: 25854493
pmcid: 4600005
Sommer, C., & Gerlich, D.W. (2013). Machine learning in cell biology – teaching computers to recognize phenotypes. Journal of Cell Science, 126(24), 5529–5539.
doi: 10.1242/jcs.123604
pubmed: 24259662
Squire, L.R. (1992). Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychological Review, 99(2), 195–231.
doi: 10.1037/0033-295X.99.2.195
Strobl, C., Hothorn, T., Zeileis, A. (2009). A new, conditional variable importance measure for random forests available in the party package. The R Journal, 1(2), 14–17.
doi: 10.32614/RJ-2009-013
Tajbakhsh, N., Shin, J.Y., Gurudu, S.R., Hurst, R.T., Kendall, C.B., Gotway, M.B., Liang, J. (2016). Convolutional neural networks for medical image analysis: full training or fine tuning?. IEEE Transactions on Medical Imaging, 35(5), 1299–1312.
doi: 10.1109/TMI.2016.2535302
pubmed: 26978662
Tamura, H., Mori, S., Yamawaki, T. (1978). Textural features corresponding to visual perception. IEEE Transactions on Systems Man, and Cybernetics, 8(6), 460–473.
doi: 10.1109/TSMC.1978.4309999
Tibshirani, R. (1996). Regression shrinkage and selection via the lasso. Journal of the Royal Statistical Society: Series B (Statistical Methodology), 58(1), 267–288.
Uhlmann, V., Singh, S., Carpenter, A.E. (2016). CP-CHARM: segmentation-free image classification made accessible. BMC Bioinformatics, 17(1), 51.
doi: 10.1186/s12859-016-0895-y
pubmed: 26817459
pmcid: 4729047
Vallotton, P., Lagerstrom, R., Sun, C., Buckley, M., Wang, D., Silva, M.D., Tan, S.S., Gunnersen, J.M. (2007). Automated analysis of neurite branching in cultured cortical neurons using HCA-Vision. Cytometry Part A, 71(10), 889–895.
doi: 10.1002/cyto.a.20462
Vapnik, V.N. (1998). Statistical learning theory. New York: Wiley.
Vapnik, V.N. (1999). The nature of statistical learning theory. New York: Springer-Verlag.
Vedaldi, A., & Fulkerson, B. (2008). VLFeat: An Open and Portable Library of Computer Vision Algorithms. http://www.vlfeat.org/ .
Vert, J.P., Tsuda, K., Schölkopf, B. (2004). A primer on kernel methods. In Kernel Methods in Computational Biology (pp. 35–70). Cambridge: MIT Press.
Wickham, H. (2009). Ggplot2: Elegant Graphics for Data Analysis. New York: Springer.
doi: 10.1007/978-0-387-98141-3
Wu, C., Schulte, J., Sepp, K.J., Littleton, J.T., Hong, P. (2010). Automatic robust neurite detection and morphological analysis of neuronal cell cultures in high-content screening. Neuroinformatics, 8(2), 83–100.
doi: 10.1007/s12021-010-9067-9
pubmed: 20405243
pmcid: 3022421
Xia, X., & Wong, S.T.C. (2012). Concise review: a high-content screening approach to stem cell research and drug discovery. Stem Cells, 30(9), 1800–1807.
doi: 10.1002/stem.1168
pubmed: 22821636
Yang, J., Yu, K., Gong, Y., Huang, T. (2009). Linear spatial pyramid matching using sparse coding for image classification. In Proceedings of the IEEE Conference on Computer Vision and Pattern Recognition (pp. 1794–1801).
Yu, D., Yang, F., Yang, C., Leng, C., Cao, J., Wang, Y., Tian, J. (2016). Fast rotation-free feature-based image registration using improved N-SIFT, and GMM-based parallel optimization. IEEE Transactions on Biomedical Engineering, 63(8), 1653–1664.
doi: 10.1109/TBME.2015.2465855
pubmed: 26259212
Zhang, Y., Zhou, X., Degterev, A., Lipinski, M., Adjeroh, D., Yuan, J., Wong, S.T.C. (2007). A novel tracing algorithm for high throughput imaging: screening of neuron-based assays. Journal of Neuroscience Methods, 160(1), 149–162.
doi: 10.1016/j.jneumeth.2006.07.028
pubmed: 16987551
Zhang, R., Zhou, W., Li, Y., Yu, S., Xie, Y. (2013). Nonrigid registration of lung CT images based on tissue features. Computational and Mathematical Methods in Medicine, 2013, 834192.
pubmed: 24324526
pmcid: 3845410