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A Deep Generative Model of Neonatal Cortical Surface Development

Part of the Lecture Notes in Computer Science book series (LNCS,volume 13413)

Abstract

The neonatal cortical surface is known to be affected by preterm birth, and the subsequent changes to cortical organisation have been associated with poorer neurodevelopmental outcomes. Deep Generative models have the potential to lead to clinically interpretable models of disease, but developing these on the cortical surface is challenging since established techniques for learning convolutional filters are inappropriate on non-flat topologies. To close this gap, we implement a surface-based CycleGAN using mixture model CNNs (MoNet) to translate sphericalised neonatal cortical surface features (curvature and T1w/T2w cortical myelin) between different stages of cortical maturity. Results show our method is able to reliably predict changes in individual patterns of cortical organisation at later stages of gestation, validated by comparison to longitudinal data; and translate appearance between preterm and term gestation (>37 weeks gestation), validated through comparison with a trained term/preterm classifier. Simulated differences in cortical maturation are consistent with observations in the literature.

Keywords

  • Geometric deep learning
  • Cortical surfaces
  • Neurodevelopment

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References

  1. Armanious, K., Gatidis, S., Nikolaou, K., Yang, B., Kustner, T.: Retrospective correction of rigid and non-rigid MR motion artifacts using GANs. In: 2019 IEEE 16th International Symposium on Biomedical Imaging (ISBI 2019), pp. 1550–1554. IEEE (2019)

    Google Scholar 

  2. Bass, C., da Silva, M., Sudre, C., Tudosiu, P.D., Smith, S., Robinson, E.: ICAM: interpretable classification via disentangled representations and feature attribution mapping. arXiv preprint arXiv:2006.08287 (2020)

  3. Bass, C., et al.: ICAM-REG: interpretable classification and regression with feature attribution for mapping neurological phenotypes in individual scans. arXiv preprint arXiv:2103.02561 (2021)

  4. Benson, S., Beets-Tan, R.: GAN-based anomaly detection in multi-modal MRI images. bioRxiv (2020)

    Google Scholar 

  5. Boardman, J.P., Counsell, S.J.: Invited review: factors associated with atypical brain development in preterm infants: insights from magnetic resonance imaging. Neuropathol. Appl. Neurobiol. 46(5), 413–421 (2020)

    CrossRef  Google Scholar 

  6. Bozek, J., et al.: Construction of a neonatal cortical surface atlas using multimodal surface matching in the developing human connectome project. Neuroimage 179, 11–29 (2018)

    CrossRef  Google Scholar 

  7. Bronstein, M.M., Bruna, J., LeCun, Y., Szlam, A., Vandergheynst, P.: Geometric deep learning: going beyond Euclidean data. IEEE Sig. Process. Mag. 34(4), 18–42 (2017). https://doi.org/10.1109/MSP.2017.2693418

    CrossRef  Google Scholar 

  8. Cirillo, M.D., Abramian, D., Eklund, A.: Vox2Vox: 3D-GAN for brain tumour segmentation. In: Crimi, A., Bakas, S. (eds.) BrainLes 2020. LNCS, vol. 12658, pp. 274–284. Springer, Cham (2021). https://doi.org/10.1007/978-3-030-72084-1_25

    CrossRef  Google Scholar 

  9. Costa, P., et al.: End-to-end adversarial retinal image synthesis. IEEE Trans. Med. Imaging 37(3), 781–791 (2017)

    CrossRef  Google Scholar 

  10. Dahan, S., Williams, L.Z.J., Rueckert, D., Robinson, E.C.: Improving phenotype prediction using long-range spatio-temporal dynamics of functional connectivity (2021)

    Google Scholar 

  11. Do, H., Helbert, D., Bourdon, P., Naudin, M., Guillevin, C., Guillevin, R.: MRI super-resolution using 3D cycle-consistent generative adversarial network. In: 2021 Sixth International Conference on Advances in Biomedical Engineering (ICABME), pp. 85–88. IEEE (2021)

    Google Scholar 

  12. Fawaz, A., et al.: Benchmarking geometric deep learning for cortical segmentation and neurodevelopmental phenotype prediction. bioRxiv (2021). https://doi.org/10.1101/2021.12.01.470730, https://www.biorxiv.org/content/early/2021/12/02/2021.12.01.470730

  13. Gadermayr, M., et al.: Image-to-image translation for simplified MRI muscle segmentation. Front. Radiol. 1 (2021). https://doi.org/10.3389/fradi.2021.664444, https://www.frontiersin.org/article/10.3389/fradi.2021.664444

  14. Han, C., et al.: MadGAN: unsupervised medical anomaly detection GAN using multiple adjacent brain MRI slice reconstruction. BMC Bioinformatics 22(2), 1–20 (2021)

    Google Scholar 

  15. Hiasa, Y., et al.: Cross-modality image synthesis from unpaired data using CycleGAN. In: Gooya, A., Goksel, O., Oguz, I., Burgos, N. (eds.) SASHIMI 2018. LNCS, vol. 11037, pp. 31–41. Springer, Cham (2018). https://doi.org/10.1007/978-3-030-00536-8_4

    CrossRef  Google Scholar 

  16. Hughes, E.J., et al.: A dedicated neonatal brain imaging system. Magn. Reson. Med. 78(2), 794–804 (2017)

    CrossRef  Google Scholar 

  17. Jiang, M., et al.: Fa-GAN: fused attentive generative adversarial networks for MRI image super-resolution. Comput. Med. Imaging Graph. 92, 101969 (2021)

    CrossRef  Google Scholar 

  18. Kingma, D.P., Welling, M.: Auto-encoding variational Bayes. arXiv preprint arXiv:1312.6114 (2013)

  19. Kline, J.E., Illapani, V.S.P., He, L., Altaye, M., Logan, J.W., Parikh, N.A.: Early cortical maturation predicts neurodevelopment in very preterm infants. Arch. Dis. Child Fetal Neonatal. Ed. 105(5), 460–465 (2020)

    CrossRef  Google Scholar 

  20. Kuklisova-Murgasova, M., et al.: A dynamic 4D probabilistic atlas of the developing brain. Neuroimage 54(4), 2750–2763 (2011)

    CrossRef  Google Scholar 

  21. 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. Med. Image Anal. 16(8), 1550–1564 (2012)

    CrossRef  Google Scholar 

  22. Larsen, A.B.L., Sønderby, S.K., Larochelle, H., Winther, O.: Autoencoding beyond pixels using a learned similarity metric. In: International Conference on Machine Learning, pp. 1558–1566. PMLR (2016)

    Google Scholar 

  23. Latif, S., Asim, M., Usman, M., Qadir, J., Rana, R.: Automating motion correction in multishot MRI using generative adversarial networks. arXiv preprint arXiv:1811.09750 (2018)

  24. Lefèvre, J., et al.: Are developmental trajectories of cortical folding comparable between cross-sectional datasets of fetuses and preterm newborns? Cereb. Cortex 26(7), 3023–3035 (2015)

    CrossRef  Google Scholar 

  25. Li, M., Tang, H., Chan, M.D., Zhou, X., Qian, X.: DC-AL GAN: pseudoprogression and true tumor progression of glioblastoma multiform image classification based on DCGAN and AlexNet. Med. Phys. 47(3), 1139–1150 (2020)

    CrossRef  Google Scholar 

  26. Makropoulos, A., et al.: Regional growth and atlasing of the developing human brain. Neuroimage 125, 456–478 (2016)

    CrossRef  Google Scholar 

  27. Makropoulos, A., et al.: The developing human connectome project: a minimal processing pipeline for neonatal cortical surface reconstruction. Neuroimage 173, 88–112 (2018)

    CrossRef  Google Scholar 

  28. Monti, F., Boscaini, D., Masci, J., Rodola, E., Svoboda, J., Bronstein, M.M.: Geometric deep learning on graphs and manifolds using mixture model CNNs. In: Proceedings of the IEEE Conference on Computer Vision and Pattern Recognition (CVPR), July 2017

    Google Scholar 

  29. Morel, B., et al.: Automated brain MRI metrics in the Epirmex cohort of preterm newborns: Correlation with the neurodevelopmental outcome at 2 years. Diagn. Interv. Imaging 102(4), 225–232 (2021)

    CrossRef  Google Scholar 

  30. Ran, M., et al.: Denoising of 3D magnetic resonance images using a residual encoder-decoder Wasserstein generative adversarial network. Med. Image Anal. 55, 165–180 (2019)

    CrossRef  Google Scholar 

  31. Robinson, E.C., et al.: Multimodal surface matching with higher-order smoothness constraints. Neuroimage 167, 453–465 (2018)

    CrossRef  Google Scholar 

  32. Robinson, E.C., et al.: MSM: a new flexible framework for multimodal surface matching. Neuroimage 100, 414–426 (2014)

    CrossRef  Google Scholar 

  33. Schuh, A., et al.: A deformable model for the reconstruction of the neonatal cortex. In: 2017 IEEE 14th International Symposium on Biomedical Imaging (ISBI 2017), pp. 800–803. IEEE (2017)

    Google Scholar 

  34. Shimony, J.S., et al.: Comparison of cortical folding measures for evaluation of developing human brain. Neuroimage 125, 780–790 (2016)

    CrossRef  Google Scholar 

  35. Vosylius, V., et al.: Geometric deep learning for post-menstrual age prediction based on the neonatal white matter cortical surface. In: Sudre, C.H., et al. (eds.) UNSURE/GRAIL -2020. LNCS, vol. 12443, pp. 174–186. Springer, Cham (2020). https://doi.org/10.1007/978-3-030-60365-6_17

    CrossRef  Google Scholar 

  36. Welander, P., Karlsson, S., Eklund, A.: Generative adversarial networks for image-to-image translation on multi-contrast MR images-a comparison of CycleGAN and unit. arXiv preprint arXiv:1806.07777 (2018)

  37. Williams, L.Z., Fawaz, A., Glasser, M.F., Edwards, D., Robinson, E.C.: Geometric deep learning of the human connectome project multimodal cortical parcellation. bioRxiv (2021)

    Google Scholar 

  38. Xia, T., Chartsias, A., Wang, C., Tsaftaris, S.A., Initiative, A.D.N., et al.: Learning to synthesise the ageing brain without longitudinal data. Med. Image Anal. 73, 102169 (2021)

    CrossRef  Google Scholar 

  39. Yan, P., Xu, S., Rastinehad, A.R., Wood, B.J.: Adversarial image registration with application for MR and TRUS image fusion. In: Shi, Y., Suk, H.-I., Liu, M. (eds.) MLMI 2018. LNCS, vol. 11046, pp. 197–204. Springer, Cham (2018). https://doi.org/10.1007/978-3-030-00919-9_23

    CrossRef  Google Scholar 

  40. Yan, W., et al.: The domain shift problem of medical image segmentation and vendor-adaptation by Unet-GAN. In: Shen, D., et al. (eds.) MICCAI 2019. LNCS, vol. 11765, pp. 623–631. Springer, Cham (2019). https://doi.org/10.1007/978-3-030-32245-8_69

    CrossRef  Google Scholar 

  41. Yang, H., et al.: Unpaired brain MR-to-CT synthesis using a structure-constrained CycleGAN. In: Stoyanov, D., et al. (eds.) DLMIA/ML-CDS -2018. LNCS, vol. 11045, pp. 174–182. Springer, Cham (2018). https://doi.org/10.1007/978-3-030-00889-5_20

    CrossRef  Google Scholar 

  42. Yang, Q., et al.: Low-dose CT image denoising using a generative adversarial network with Wasserstein distance and perceptual loss. IEEE Trans. Med. Imaging 37(6), 1348–1357 (2018)

    CrossRef  Google Scholar 

  43. Yi, X., Walia, E., Babyn, P.: Generative adversarial network in medical imaging: a review. Med. Image Anal. 58, 101552 (2019)

    CrossRef  Google Scholar 

  44. You, C., et al.: Ct super-resolution GAN constrained by the identical, residual, and cycle learning ensemble (GAN-circle). IEEE Trans. Med. Imaging 39(1), 188–203 (2019)

    CrossRef  Google Scholar 

  45. Zenati, H., Foo, C.S., Lecouat, B., Manek, G., Chandrasekhar, V.R.: Efficient GAN-based anomaly detection. arXiv preprint arXiv:1802.06222 (2018)

  46. Zhao, F., et al.: Spherical U-net on cortical surfaces: methods and applications. CoRR abs/1904.00906 (2019). http://arxiv.org/abs/1904.00906

  47. Zhu, J.Y., Park, T., Isola, P., Efros, A.A.: Unpaired image-to-image translation using cycle-consistent adversarial networks. In: Proceedings of the IEEE International Conference on Computer Vision, pp. 2223–2232 (2017)

    Google Scholar 

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Correspondence to Abdulah Fawaz .

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Fawaz, A., Williams, L.Z.J., Edwards, A.D., Robinson, E.C. (2022). A Deep Generative Model of Neonatal Cortical Surface Development. In: Yang, G., Aviles-Rivero, A., Roberts, M., Schönlieb, CB. (eds) Medical Image Understanding and Analysis. MIUA 2022. Lecture Notes in Computer Science, vol 13413. Springer, Cham. https://doi.org/10.1007/978-3-031-12053-4_35

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  • DOI: https://doi.org/10.1007/978-3-031-12053-4_35

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