Construction of a Deformable Spatiotemporal MRI Atlas of the Fetal Brain: Evaluation of Similarity Metrics and Deformation Models

  • Ali Gholipour
  • Catherine Limperopoulos
  • Sean Clancy
  • Cedric Clouchoux
  • Alireza Akhondi-Asl
  • Judy A. Estroff
  • Simon K. Warfield
Part of the Lecture Notes in Computer Science book series (LNCS, volume 8674)


The development and identification of best methods in fetal brain MRI analysis is crucial as we expect an outburst of studies on groupwise and longitudinal analysis of early brain development in the upcoming years. To address this critical need, in this paper, we have developed a mathematical framework for the construction of an unbiased deformable spatiotemporal atlas of the fetal brain MRI and compared it to alternative configurations in terms of similarity metrics and deformation models. Our contributions are twofold: first we suggest a novel approach to fetal brain spatiotemporal atlas construction that shows high capability in capturing anatomic variation between subjects; and second, within our atlas construction framework we evaluate and compare a set of plausible configurations for inter-subject fetal brain MRI registration and identify the most accurate approach that can potentially lead to most accurate results in population atlas construction, atlas-based segmentation, and group analysis. Our evaluation results indicate that symmetric diffeomorphic deformable registration with cross correlation similarity metric outperforms other configurations in this application and results in sharp unbiased atlases that can be used in fetal brain MRI analysis.


Mutual Information Image Registration Fetal Brain Deformation Model Similarity Metrics 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Studholme, C.: Mapping fetal brain development in utero using magnetic resonance imaging: The big bang of brain mapping. Annual Review of Biomedical Engineering 13, 345–368 (2011)CrossRefzbMATHGoogle Scholar
  2. 2.
    Gholipour, A., Estroff, J., Warfield, S.: Robust super-resolution volume reconstruction from slice acquisitions: application to fetal brain MRI. IEEE Transactions on Medical Imaging 29(10), 1739–1758 (2010)CrossRefGoogle Scholar
  3. 3.
    Kuklisova-Murgasova, M., Quaghebeur, G., Rutherford, M.A., Hajnal, J.V., Schnabel, J.A.: Reconstruction of fetal brain MRI with intensity matching and complete outlier removal. Medical Image Analysis 16(8), 1550–1564 (2012)CrossRefzbMATHGoogle Scholar
  4. 4.
    Habas, P.A., Kim, K., Rousseau, F., Glenn, O.A., Barkovich, A.J., Studholme, C.: Atlas-based segmentation of developing tissues in the human brain with quantitative validation in young fetuses. Human Brain Mapping 31(9), 1348–1358 (2010)CrossRefGoogle Scholar
  5. 5.
    Habas, P., Kim, K., Corbett-Detig, J., Rousseau, F., Glenn, O., Barkovich, A., Studholme, C.: A spatiotemporal atlas of MR intensity, tissue probability and shape of the fetal brain. Neuroimage 53(2), 460–470 (2010)CrossRefGoogle Scholar
  6. 6.
    Rajagopalan, V., Scott, J., Habas, P., Kim, K., Corbett-Detig, J., et al.: Local tissue growth patterns underlying normal fetal human brain gyrification quantified in utero. The Journal of Neuroscience 31(8), 2878–2887 (2011)CrossRefGoogle Scholar
  7. 7.
    Clouchoux, C., Kudelski, D., Gholipour, A., Warfield, S.K., Viseur, S., Bouyssi-Kobar, M., Mari, J.L., Evans, A.C., du Plessis, A.J., Limperopoulos, C.: Quantitative in vivo MRI measurement of cortical development in the fetus. Brain Structure and Function 217(1), 127–139 (2012)CrossRefGoogle Scholar
  8. 8.
    Gholipour, A., Akhondi-Asl, A., Estroff, J.A., Warfield, S.K.: Multi-atlas multi-shape segmentation of fetal brain MRI for volumetric and morphometric analysis of ventriculomegaly. NeuroImage 60(3), 1819–1831 (2012)CrossRefGoogle Scholar
  9. 9.
    Serag, A., Aljabar, P., Ball, G., Counsell, S.J., Boardman, J.P., Rutherford, M.A., Edwards, A.D., Hajnal, J.V., Rueckert, D.: Construction of a consistent high-definition spatio-temporal atlas of the developing brain using adaptive kernel regression. NeuroImage 59(3), 2255–2265 (2012)CrossRefGoogle Scholar
  10. 10.
    Kuklisova-Murgasova, M., Aljabar, P., et al.: A dynamic 4D probabilistic atlas of the developing brain. NeuroImage 54(4), 2750–2763 (2011)CrossRefGoogle Scholar
  11. 11.
    Avants, B., Gee, J.: Geodesic estimation for large deformation anatomical shape averaging and interpolation. NeuroImage 23, S139–S150 (2004)Google Scholar
  12. 12.
    Klein, A., Andersson, J., Ardekani, B.A., Ashburner, J., Avants, B., et al.: Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage 46(3), 786–802 (2009)CrossRefGoogle Scholar
  13. 13.
    Avants, B.B., Tustison, N.J., Song, G., Cook, P.A., Klein, A., Gee, J.C.: A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54(3), 2033–2044 (2011)CrossRefGoogle Scholar
  14. 14.
    Gholipour, A., Kehtarnavaz, N., Briggs, R., Devous, M., Gopinath, K.: Brain functional localization: a survey of image registration techniques. IEEE Transactions on Medical Imaging 26(4), 427–451 (2007)CrossRefGoogle Scholar
  15. 15.
    Avants, B., Epstein, C., Grossman, M., Gee, J.: Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain. Medical Image Analysis 12(1), 26 (2008)CrossRefGoogle Scholar
  16. 16.
    Joshi, S., Davis, B., Jomier, M., Gerig, G.: Unbiased diffeomorphic atlas construction for computational anatomy. NeuroImage 23, S151–S160 (2004)Google Scholar
  17. 17.
    Davis, B., Fletcher, P., Bullitt, E., Joshi, S.: Population shape regression from random design data. Int. Journal of Computer Vision 90(2), 255–266 (2010)CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Ali Gholipour
    • 1
  • Catherine Limperopoulos
    • 2
  • Sean Clancy
    • 1
  • Cedric Clouchoux
    • 2
  • Alireza Akhondi-Asl
    • 1
  • Judy A. Estroff
    • 1
  • Simon K. Warfield
    • 1
  1. 1.Department of RadiologyBoston Children’s Hospital, and Harvard Medical SchoolBostonUSA
  2. 2.Children’s National Medical CenterWashingtonUSA

Personalised recommendations