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
This is a preview of subscription content, access via your institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
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)
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)
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)
Benson, S., Beets-Tan, R.: GAN-based anomaly detection in multi-modal MRI images. bioRxiv (2020)
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)
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)
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
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
Costa, P., et al.: End-to-end adversarial retinal image synthesis. IEEE Trans. Med. Imaging 37(3), 781–791 (2017)
Dahan, S., Williams, L.Z.J., Rueckert, D., Robinson, E.C.: Improving phenotype prediction using long-range spatio-temporal dynamics of functional connectivity (2021)
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)
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
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
Han, C., et al.: MadGAN: unsupervised medical anomaly detection GAN using multiple adjacent brain MRI slice reconstruction. BMC Bioinformatics 22(2), 1–20 (2021)
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
Hughes, E.J., et al.: A dedicated neonatal brain imaging system. Magn. Reson. Med. 78(2), 794–804 (2017)
Jiang, M., et al.: Fa-GAN: fused attentive generative adversarial networks for MRI image super-resolution. Comput. Med. Imaging Graph. 92, 101969 (2021)
Kingma, D.P., Welling, M.: Auto-encoding variational Bayes. arXiv preprint arXiv:1312.6114 (2013)
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)
Kuklisova-Murgasova, M., et al.: A dynamic 4D probabilistic atlas of the developing brain. Neuroimage 54(4), 2750–2763 (2011)
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)
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)
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)
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)
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)
Makropoulos, A., et al.: Regional growth and atlasing of the developing human brain. Neuroimage 125, 456–478 (2016)
Makropoulos, A., et al.: The developing human connectome project: a minimal processing pipeline for neonatal cortical surface reconstruction. Neuroimage 173, 88–112 (2018)
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
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)
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)
Robinson, E.C., et al.: Multimodal surface matching with higher-order smoothness constraints. Neuroimage 167, 453–465 (2018)
Robinson, E.C., et al.: MSM: a new flexible framework for multimodal surface matching. Neuroimage 100, 414–426 (2014)
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)
Shimony, J.S., et al.: Comparison of cortical folding measures for evaluation of developing human brain. Neuroimage 125, 780–790 (2016)
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
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)
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)
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)
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
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
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
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)
Yi, X., Walia, E., Babyn, P.: Generative adversarial network in medical imaging: a review. Med. Image Anal. 58, 101552 (2019)
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)
Zenati, H., Foo, C.S., Lecouat, B., Manek, G., Chandrasekhar, V.R.: Efficient GAN-based anomaly detection. arXiv preprint arXiv:1802.06222 (2018)
Zhao, F., et al.: Spherical U-net on cortical surfaces: methods and applications. CoRR abs/1904.00906 (2019). http://arxiv.org/abs/1904.00906
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)
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this paper
Cite this paper
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
Download citation
DOI: https://doi.org/10.1007/978-3-031-12053-4_35
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-12052-7
Online ISBN: 978-3-031-12053-4
eBook Packages: Computer ScienceComputer Science (R0)