Skip to main content

Advertisement

Log in

Segmentation of the Cerebellar Peduncles Using a Random Forest Classifier and a Multi-object Geometric Deformable Model: Application to Spinocerebellar Ataxia Type 6

  • Original Article
  • Published:
Neuroinformatics Aims and scope Submit manuscript

Abstract

The cerebellar peduncles, comprising the superior cerebellar peduncles (SCPs), the middle cerebellar peduncle (MCP), and the inferior cerebellar peduncles (ICPs), are white matter tracts that connect the cerebellum to other parts of the central nervous system. Methods for automatic segmentation and quantification of the cerebellar peduncles are needed for objectively and efficiently studying their structure and function. Diffusion tensor imaging (DTI) provides key information to support this goal, but it remains challenging because the tensors change dramatically in the decussation of the SCPs (dSCP), the region where the SCPs cross. This paper presents an automatic method for segmenting the cerebellar peduncles, including the dSCP. The method uses volumetric segmentation concepts based on extracted DTI features. The dSCP and noncrossing portions of the peduncles are modeled as separate objects, and are initially classified using a random forest classifier together with the DTI features. To obtain geometrically correct results, a multi-object geometric deformable model is used to refine the random forest classification. The method was evaluated using a leave-one-out cross-validation on five control subjects and four patients with spinocerebellar ataxia type 6 (SCA6). It was then used to evaluate group differences in the peduncles in a population of 32 controls and 11 SCA6 patients. In the SCA6 group, we have observed significant decreases in the volumes of the dSCP and the ICPs and significant increases in the mean diffusivity in the noncrossing SCPs, the MCP, and the ICPs. These results are consistent with a degeneration of the cerebellar peduncles in SCA6 patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Asman, A.J., & Landman, B.A. (2012). Formulating spatially varying performance in the statistical fusion framework. IEEE Transactions on Medical Imaging, 31(6), 1326–1336.

    Article  PubMed Central  PubMed  Google Scholar 

  • Avants, B.B., Epstein, C.L., Grossman, M., & Gee, J.C. (2008). Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Medical Image Analysis, 12(1), 26–41.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Awate, S.P., Hui, Z., & Gee, J.C. (2007). A fuzzy, nonparametric segmentation framework for DTI and MRI analysis: with applications to DTI-tract extraction. IEEE Transactions on Medical Imaging, 26(11), 1525–1536.

    Article  PubMed  Google Scholar 

  • Bazin, P.L., Ye, C., Bogovic, J.A., Shiee, N., Reich, D.S., Prince, J.L., & Pham, D.L. (2011). Direct segmentation of the major white matter tracts in diffusion tensor images. NeuroImage, 58(2), 458–468. doi:10.1016/j.neuroimage.2011.06.020.

    Article  PubMed Central  PubMed  Google Scholar 

  • Behrens, T.E.J., Berg, H.J., Jbabdi, S., Rushworth, M.F.S., & Woolrich, M.W. (2007). Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? NeuroImage, 34(1), 144–155.

    Article  CAS  PubMed  Google Scholar 

  • Bogovic, J.A., Prince, J.L., & Bazin, P.L. (2013). A multiple object geometric deformable model for image segmentation. Computer Vision and Image Understanding, 117(2), 145–157. doi:10.1016/j.cviu.2012.10.006.

    PubMed Central  PubMed  Google Scholar 

  • Breiman, L. (2001). Random forests. Machine Learning, 45(1), 5–32.

    Article  Google Scholar 

  • Breiman, L., Friedman, J., Stone C.J., & Olshen, R.A. (1984). Classification and regression trees. Boca Raton: CRC Press.

  • Buijink, A. W., Caan, M. W., Contarino, M. F., Schuurman, P. R., van den Munckhof, P., de Bie, R. M., Olabarriaga S. D., Speelman, J. D., & van Rootselaar A. F. (2014). Structural changes in cerebellar outflow tracts after thalamotomy in essential tremor. Parkinsonism & Related Disorders, 20(5), 554–557. doi:10.1016/j.parkreldis.2014.02.020.

  • Caselles, V., Kimmel, R., & Sapiro, G. (1997). Geodesic active contours. International Journal of Computer Vision, 22(1), 61–79.

    Article  Google Scholar 

  • Cavallari, M., Moscufo, N., Skudlarski, P., Meier, D., Panzer, V.P., Pearlson, G.D., White, W.B., Wolfson, L., & Guttmann, C.R. (2013). Mobility impairment is associated with reduced microstructural integrity of the inferior and superior cerebellar peduncles in elderly with no clinical signs of cerebellar dysfunction. NeuroImage: Clinical, 2(0), 332–340.

    Article  Google Scholar 

  • Clemm von Hohenberg, C., Schocke, M., Wigand, M., Nachbauer, W., Guttmann, C., Kubicki, M., Shenton, M., Boesch, S., & Egger, K. (2013). Radial diffusivity in the cerebellar peduncles correlates with clinical severity in Friedreich ataxia. Neurological Sciences, 34(8), 1459–1462. doi:10.1007/s10072-013-1402-0.

    Article  PubMed  Google Scholar 

  • Dice, L.R. (1945). Measures of the amount of ecologic association between species. Ecology, 26(3), 297–302.

    Article  Google Scholar 

  • Fan, X., Thompson, M., Bogovic, J.A., Bazin, P.L., & Prince, J.L. (2010). A novel contrast for DTI visualization for thalamus delineation. In Proceedings of SPIE medical imaging (Vol. 7625).

  • Friston, K.J., Holmes, A.P., Worsley, K.J., Poline, J.P., Frith, C.D., & Frackowiak, R.S. (1994). Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping, 2(4), 189–210.

    Article  Google Scholar 

  • Hagmann, P., Kurant, M., Gigandet, X., Thiran, P., Wedeen, V.J., Meuli, R., & Thiran, J.P. (2007). Mapping human whole-brain structural networks with diffusion MRI. PloS One, 2(7), e597.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hall, M., Frank, E., Holmes, G., Pfahringer, B., Reutemann, P., & Witten, I.H. (2009). The WEKA data mining software: an update. ACM SIGKDD Explorations Newsletter, 11(1), 10–18.

    Article  Google Scholar 

  • Hanaie, R., Mohri, I., Kagitani-Shimono, K., Tachibana, M., Azuma, J. , Matsuzaki, J., Watanabe, Y., Fujita, N., & Taniike, M. (2013). Altered microstructural connectivity of the superior cerebellar peduncle is related to motor dysfunction in children with autistic spectrum disorders. The Cerebellum, 12(5), 645–656. doi:10.1007/s12311-013-0475-x.

    Article  PubMed  Google Scholar 

  • Hao, X., Zygmunt, K., Whitaker, R.T., & Fletcher, P.T. (2014). Improved segmentation of white matter tracts with adaptive riemannian metrics. Medical Image Analysis, 18(1), 161– 175.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hess, C.P., Mukherjee, P., Han, E.T., Xu, D., & Vigneron, D.B. (2006). Q-ball reconstruction of multimodal fiber orientations using the spherical harmonic basis. Magnetic Resonance in Medicine, 56(1), 104–117. doi:10.1002/mrm.20931.

    Article  PubMed  Google Scholar 

  • Hüttlova, J., Kikinis, Z., Kerkovsky, M., Bouix, S., Vu, M.A., Makris, N., Shenton, M., & Kasparek, T. (2014). Abnormalities in myelination of the superior cerebellar peduncle in patients with schizophrenia and deficits in movement sequencing. The Cerebellum, 1–10. doi:10.1007/s12311-014-0550-y.

  • Knutsson, H. (1985). Producing a continuous and distance preserving 5-D vector representation of 3-D orientation. In IEEE computer society workshop on computer architecture for pattern analysis and image database management (pp. 175–182). doi:10.1109/ISBI.2010.5490203.

  • Landman, B. A., Farrell, J. A. D., Patel, N. L., Mori, S., & Prince, J. L. (2007). DTI fiber tracking: the importance of adjusting DTI gradient tables for motion correction. CATNAP—a tool to simplify and accelerate DTI analysis. In Proc. org human brain mapping 13th annual meeting.

  • Landman, B. A., Bogovic, J. A., Wan, H., ElShahaby, F. E. Z., Bazin, P. L., & Prince, J. L. (2012). Resolution of crossing fibers with constrained compressed sensing using diffusion tensor MRI. NeuroImage, 59(3), 2175–2186.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lawes, I.N.C., Barrick, T.R., Murugam, V., Spierings, N., Evans, D.R., Song, M., & Clark, C.A. (2008). Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. NeuroImage, 39(1), 62–79.

    Article  PubMed  Google Scholar 

  • Le Bihan, D., Mangin, J.F., Poupon, C., Clark, C.A., Pappata, S., Molko, N., & Chabriat, H. (2001). Diffusion tensor imaging: concepts and applications. Journal of Magnetic Resonance Imaging, 13(4), 534–546.

    Article  CAS  PubMed  Google Scholar 

  • Lenglet, C., Rousson, M., & Deriche, R. (2006). DTI segmentation by statistical surface evolution. IEEE Transactions on Medical Imaging, 25(6), 685–700.

    Article  PubMed  Google Scholar 

  • Lucas, B.C., Bogovic, J.A., Carass, A., Bazin, P.L., Prince, J.L., Pham, D.L., & Landman, B.A. (2010). The Java image science toolkit (JIST) for rapid prototyping and publishing of neuroimaging software. Neuroinformatics, 8(1), 5–17.

    Article  PubMed Central  PubMed  Google Scholar 

  • Maddah, M., Mewes, A.U.J., Haker, S., Grimson, W.E.L., & Warfield, S.K. (2005). Automated atlas-based clustering of white matter fiber tracts from DTMRI. In Medical image computing and computer-assisted intervention–MICCAI 2005 (Vol. 3749, pp. 188–195).

  • Maddah, M., Grimson, W.E.L., Warfield, S.K., & Wells, W.M. (2008). A unified framework for clustering and quantitative analysis of white matter fiber tracts. Medical Image Analysis, 12(2), 191–202. doi:10.1016/j.media.2007.10.003.

    Article  PubMed Central  PubMed  Google Scholar 

  • Malcolm, J.G., Michailovich, O., Bouix, S., Westin, C.F., Shenton, M.E., & Rathi, Y. (2010). A filtered approach to neural tractography using the Watson directional function. Medical Image Analysis, 14(1), 58–69.

    Article  PubMed Central  PubMed  Google Scholar 

  • Michailovich, O., Rathi, Y., & Dolui, S. (2011). Spatially regularized compressed sensing for high angular resolution diffusion imaging. IEEE Transactions on Medical Imaging, 30(5), 1100– 1115.

    Article  PubMed Central  PubMed  Google Scholar 

  • Mori, S., Wakana, S., van Zijl, P.C.M., & Nagae-Poetscher, L.M. (2005). MRI Atlas of human white matter, 1st edn. Amsterdam: Elsevier Science.

    Google Scholar 

  • Murata, Y., Kawakami, H., Yamaguchi, S., Nishimura, M., Kohriyama, T., Ishizaki, F., Matsuyama, Z., Mimori, Y., & Nakamura, S. (1998). Characteristic magnetic resonance imaging findings in spinocerebellar ataxia 6. Archives of Neurology, 55(10), 1348.

    Article  CAS  PubMed  Google Scholar 

  • Nicoletti, G., Fera, F., Condino, F., Auteri, W., Gallo, O., Pugliese, P., Arabia, G., Morgante, L., Barone, P., Zappia, M., & Quattrone, A. (2006). MR imaging of middle cerebellar peduncle width: differentiation of multiple system atrophy from Parkinson disease. Radiology, 239(3), 825–830.

    Article  PubMed  Google Scholar 

  • Nolte, J. (2002). The human brain: an introduction to its functional anatomy. St. Louis: Mosby.

    Google Scholar 

  • O’Donnell, L.J., & Westin, C.F. (2007). Automatic tractography segmentation using a high-dimensional white matter atlas. IEEE Transactions on Medical Imaging, 26(11), 1562–1575.

    Article  PubMed  Google Scholar 

  • O’Donnell, L. J., Kubicki, M., Shenton, M. E., Dreusicke, M. H., Grimson, W. E. L., & Westin, C. F. (2006). A method for clustering white matter fiber tracts. American Journal of Neuroradiology, 27(5), 1032–1036. http://www.ajnr.org/content/27/5/1032.full.pdf+html.

  • Oishi, K., Mori, S., Donohue, P. K., Ernst, T., Anderson, L., Buchthal, S., Faria, A., Jiang, H., Li, X., Miller, M. I., van Zijl, P. C., & Chang, L. (2011). Multi-contrast human neonatal brain atlas: application to normal neonate development analysis. NeuroImage, 56(1), 8–20.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ojemann, J.G., Partridge, S.C., Poliakov, A.V., Niazi, T.N., Shaw, D.W., Ishak, G.E., Lee, A., Browd, S.R., Geyer, J., & Ellenbogen, R.G. (2013). Diffusion tensor imaging of the superior cerebellar peduncle identifies patients with posterior fossa syndrome. Child’s Nervous System, 29(11), 2071–2077. doi:10.1007/s00381-013-2205-6.

    Article  PubMed  Google Scholar 

  • Peled, S., Friman, O., Jolesz, F., & Westin, C.F. (2006). Geometrically constrained two-tensor model for crossing tracts in DWI. Magnetic Resonance Imaging, 24(9), 1263–1270.

    Article  PubMed Central  PubMed  Google Scholar 

  • Perrini, P., Tiezzi, G., Castagna, M., & Vannozzi, R. (2012). Three-dimensional microsurgical anatomy of cerebellar peduncles. Neurosurgical Review, 1–11.

  • Qazi, A.A., Radmanesh, A., O’Donnell, L., Kindlmann, G., Peled, S., Whalen, S., Westin, C.F., & Golby, A.J. (2009). Resolving crossings in the corticospinal tract by two-tensor streamline tractography: method and clinical assessment using fMRI. NeuroImage, 47, 98–106.

    Article  Google Scholar 

  • Ramirez-Manzanares, A., Rivera, M., Vemuri, B.C., Carney, P., & Mareci, T. (2007). Diffusion basis functions decomposition for estimating white matter intravoxel fiber geometry. IEEE Transactions on Medical Imaging, 26(8), 1091–1102.

    Article  PubMed  Google Scholar 

  • Sinke, R.J., Ippel, E.F., Diepstraten, C.M., Beemer, F.A., Wokke, J.H., van Hilten, B.J., Knoers, N. V., van Amstel, H.K.P., & Kremer, H. (2001). Clinical and molecular correlations in spinocerebellar ataxia type 6: a study of 24 Dutch families. Archives of Neurology, 58(11), 1839.

    Article  CAS  PubMed  Google Scholar 

  • Sivaswamy, L., Kumar, A., Rajan, D., Behen, M., Muzik, O., Chugani, D., & Chugani, H. (2010). A diffusion tensor imaging study of the cerebellar pathways in children with autism spectrum disorder. Journal of Child Neurology, 25(10), 1223–1231.

    Article  PubMed  Google Scholar 

  • Suarez, R.O., Commowick, O., Prabhu, S.P., & Warfield, S.K. (2012). Automated delineation of white matter fiber tracts with a multiple region-of-interest approach. NeuroImage, 59(4), 3690–3700. doi:10.1016/j.neuroimage.2011.11.043.

    Article  PubMed Central  PubMed  Google Scholar 

  • Tournier, J.D., Calamante, F., & Connelly, A. (2007). Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. NeuroImage, 35(4), 1459–1472.

    Article  PubMed  Google Scholar 

  • Tuch, D. S. (2004). Q-ball imaging. Magnetic Resonance in Medicine, 52(6), 1358–1372. 10.1002/mrm.20279.

    Article  PubMed  Google Scholar 

  • Tuch, D.S., Reese, T.G., Wiegell, M.R., Makris, N., Belliveau, J.W., & Wedeen, V.J. (2002). High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magnetic Resonance in Medicine, 48(4), 577–582. doi:10.1002/mrm.10268.

    Article  PubMed  Google Scholar 

  • Wang, Z., & Vemuri, B.C. (2005). DTI segmentation using an information theoretic tensor dissimilarity measure. IEEE Transactions on Medical Imaging, 24(10), 1267–1277.

    Article  PubMed  Google Scholar 

  • Wang, F., Sun, Z., Du, X., Wang, X., Cong, Z., Zhang, H., Zhang, D., & Hong, N. (2003). A diffusion tensor imaging study of middle and superior cerebellar peduncle in male patients with schizophrenia. Neuroscience Letters, 348(3), 135–138.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Grimson, W.E.L., & Westin, C.F. (2011). Tractography segmentation using a hierarchical dirichlet processes mixture model. NeuroImage, 54(1), 290–302.

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang, S., Fan, G.G., Xu, K., & Wang, C. (2014). Altered microstructural connectivity of the superior and middle cerebellar peduncles are related to motor dysfunction in children with diffuse periventricular leucomalacia born preterm: a DTI tractography study. European Journal of Radiology, 83(6), 997–1004. doi:10.1016/j.ejrad.2014.03.010.

    Article  PubMed  Google Scholar 

  • Warfield, S.K., Zou, K.H., & Wells, W.M. (2004). Simultaneous truth and performance level estimation (STAPLE): an algorithm for the validation of image segmentation. IEEE Transactions on Medical Imaging, 23(7), 903–921.

    Article  PubMed Central  PubMed  Google Scholar 

  • Wedeen, V.J., Hagmann, P., Tseng, W.Y.I., Reese, T.G., & Weisskoff, R.M. (2005). Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magnetic Resonance in Medicine, 54(6), 1377–1386. doi:10.1002/mrm.20642.

    Article  PubMed  Google Scholar 

  • Westin, C.F., Peled, S., Gudbjartsson, H., Kikinis, R., & Jolesz, F.A. (1997). Geometrical diffusion measures for MRI from tensor basis analysis. In Proceedings of ISMRM (Vol. 97, pp. 1742).

  • Xu, C., Yezzi, A., & Prince, J.L. (2000). On the relationship between parametric and geometric active contours. In IEEE conference record of the thirty-fourth asilomar conference on signals, systems and computers, 2000 (Vol. 1, pp. 483–489).

  • Ye, C., Bazin, P.L., Bogovic, J.A., Ying, S.H., & Prince, J.L. (2012). Labeling of the cerebellar peduncles using a supervised Gaussian classifier with volumetric tract segmentation. In Proceedings of SPIE medical imaging (Vol. 8314, p. 143).

  • Ye, C., Bogovic, J.A., Ying, S.H., & Prince, J.L. (2013). Segmentation of the complete superior cerebellar peduncles using a multi-object geometric deformable model. In 2013 IEEE 10th International Symposium on Biomedical Imaging (ISBI) (pp. 49–52).

  • Ying, S.H., Landman, B.A., Chowdhury, S., Sinofsky, A.H., Gambini, A., Mori, S., Zee, D.S., & Prince, J.L. (2009). Orthogonal diffusion-weighted MRI measures distinguish region-specific degeneration in cerebellar ataxia subtypes. Journal of Neurology, 256(11), 1939–1942.

    Article  PubMed Central  PubMed  Google Scholar 

  • Yushkevich, P.A., Zhang, H., Simon, T.J., & Gee, J.C. (2008). Structure-specific statistical mapping of white matter tracts. NeuroImage, 41(2), 448–461.

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang, H., Avants, B.B., Yushkevich, P.A., Woo, J.H., Wang, S., McCluskey, L.F., Elman, L.B., Melhem, E.R., & Gee, J.C. (2007). High-dimensional spatial normalization of diffusion tensor images improves the detection of white matter differences: an example study using amyotrophic lateral sclerosis. IEEE Transactions on Medical Imaging, 26(11), 1585–1597.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, S., Correia, S., & Laidlaw, D.H. (2008). Identifying white-matter fiber bundles in DTI data using an automated proximity-based fiber-clustering method. IEEE Transactions on Visualization and Computer Graphics, 14(5), 1044–1053. doi:10.1109/TVCG.2008.52.

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhou, Q., Michailovich, O., & Rathi, Y. (2014). Resolving complex fibre architecture by means of sparse spherical deconvolution in the presence of isotropic diffusion. In SPIE medical imaging, international society for optics and photonics (pp. 903,425–903,425).

Download references

Acknowledgments

This work is supported by NIH/NINDS 5R01NS056307-08 and the China Scholarship Council.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chuyang Ye.

Additional information

The method is available on the Neuroimaging Informatics Tools and Resources Clearinghouse (NITRC) website (http://www.nitrc.org/). The instructions and other details are at http://www.iacl.ece.jhu.edu/Chuyang/CPSeg.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ye, C., Yang, Z., Ying, S.H. et al. Segmentation of the Cerebellar Peduncles Using a Random Forest Classifier and a Multi-object Geometric Deformable Model: Application to Spinocerebellar Ataxia Type 6. Neuroinform 13, 367–381 (2015). https://doi.org/10.1007/s12021-015-9264-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12021-015-9264-7

Keywords

Navigation