Development of an Interpretable Deep Learning System for the Identification of Patients with Alzheimer’s Disease

  • Chapter
  • First Online:
Advancement of Science and Technology in Sustainable Manufacturing and Process Engineering

Abstract

Deep learning using convolutional neural networks has shown great promise in analyzing neuroimaging data. Identification of Alzheimer’s disease patients from healthy individuals using structural magnetic resonance data is one of the clinical problems that has been widely explored by employing convolutional neural networks and producing very high classification accuracies. However, in most studies, the results were not supported by explainability tools.

In this study, an interpretable convolutional neural network model derived from pre-trained VGG-16 is proposed to classify Alzheimer’s disease patients versus healthy subjects using MRI data obtained from an Open Access Series of Imaging Studies (OASIS) dataset. The model was trained and validated based on a five-fold cross-validation loop and produced a classification accuracy of 71.62% on the validation set. Moreover, we incorporated four CNN visualization techniques that highlight important brain regions used by the model to identify AD patients: saliency map, gradient class activation map**, occlusion map**, and heatmap generated by Shapley additive explanation (SHAP) method. The potential of these explainability tools in identifying biased models that produce inflated erroneous results is also investigated, and the resulting heatmaps were able to indicate a bias in the model’s training procedure.

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

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
EUR 29.95
Price includes VAT (France)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 160.49
Price includes VAT (France)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
EUR 210.99
Price includes VAT (France)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Selkoe, D.J., Lansbury, P.J.: Alzheimer’s disease is the most common neurodegenerative disorder. In: Basic Neurochemistry: Molecular, Cellular and Medical Aspects, vol. 6, pp. 101–102. Lippincott-Raven, Philadelphia (1999)

    Google Scholar 

  2. Kelley, B.J., Petersen, R.C.: Alzheimer’s disease and mild cognitive impairment. Neurol. Clin. 25(3), 577–609 (2007)

    Article  Google Scholar 

  3. Small, G.W., Rabins, P.V., Barry, P.P., Buckholtz, N.S., DeKosky, S.T., Ferris, S.H., Finkel, S.I., Gwyther, L.P., Khachaturian, Z.S., Lebowitz, B.D., McRae, T.D.: Diagnosis and treatment of Alzheimer disease and related disorders: consensus statement of the American Association for Geriatric Psychiatry, the Alzheimer’s Association, and the American Geriatrics Society. JAMA. 278(16), 1363–1371 (1997)

    Article  Google Scholar 

  4. LeCun, Y., Bengio, Y., Hinton, G.: Deep learning. Nature. 521(7553), 436–444 (2015)

    Article  Google Scholar 

  5. Liu, M., Li, F., Yan, H., Wang, K., Ma, Y., Shen, L., Xu, M., Alzheimer’s Disease Neuroimaging Initiative: A multi-model deep convolutional neural network for automatic hippocampus segmentation and classification in Alzheimer’s disease. NeuroImage. 208, 116459 (2020)

    Article  Google Scholar 

  6. Oh, K., Chung, Y.C., Kim, K.W., Kim, W.S., Oh, I.S.: Classification and visualization of Alzheimer’s disease using volumetric convolutional neural network and transfer learning. Sci. Rep. 9(1), 1–16 (2019)

    Article  Google Scholar 

  7. Qiu, S.: Development and validation of an interpretable deep learning framework for Alzheimer’s disease classification. Brain. 143(6), 1920–1933 (2020)

    Article  Google Scholar 

  8. Wen, J., Thibeau-Sutre, E., Diaz-Melo, M., Samper-González, J., Routier, A., Bottani, S., Dormont, D., Durrleman, S., Burgos, N., Colliot, O., Alzheimer’s Disease Neuroimaging Initiative: Convolutional neural networks for classification of Alzheimer’s disease: overview and reproducible evaluation. Med. Image Anal. 63, 101694 (2020)

    Article  Google Scholar 

  9. Feng, W., Halm-Lutterodt, N.V., Tang, H., Mecum, A., Mesregah, M.K., Ma, Y., Li, H., Zhang, F., Wu, Z., Yao, E., Guo, X.: Automated MRI-based deep learning model for detection of Alzheimer’s disease process. Int. J. Neural Syst. 30(06), 2050032 (2020)

    Article  Google Scholar 

  10. Yagis, E., De Herrera, A.G.S., Citi, L.: Generalization performance of deep learning models in neurodegenerative disease classification. In: 2019 IEEE International Conference on Bioinformatics and Biomedicine (BIBM), (pp. 1692–1698). IEEE (2019)

    Google Scholar 

  11. Yagis, E., Atnafu, S.W., de Herrera García Seco, A., Marzi, C., Scheda, R., Giannelli, M., Tessa, C., Citi, L., Diciotti, S.: Effect of data leakage in brain MRI classification using 2D convolutional neural networks. Sci. Rep. 11(1), 22544 (2021)

    Article  Google Scholar 

  12. Reference

    Google Scholar 

  13. Puente-Castro, A., Fernandez-Blanco, E., Pazos, A., Munteanu, C.R.: Automatic assessment of Alzheimer’s disease diagnosis based on deep learning techniques. Comput. Biol. Med. 120, 103764 (2020)

    Article  Google Scholar 

  14. Saratxaga, C.L., Moya, I., Picón, A., Acosta, M., Moreno-Fernandez-de-Leceta, A., Garrote, E., Bereciartua-Perez, A.: MRI deep learning-based solution for Alzheimer’s disease prediction. J. Pers. Med. 11(9), 902 (2021)

    Article  Google Scholar 

  15. Mehmood, A., Maqsood, M., Bashir, M., Shuyuan, Y.: A deep Siamese convolution neural network for multi-class classification of Alzheimer disease. Brain Sci. 10(2), 84 (2020)

    Article  Google Scholar 

  16. Massalimova, A., Varol, H.A.: Input agnostic deep learning for Alzheimer’s disease classification using multimodal MRI images. In: 2021 43rd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC), (pp. 2875–2878). (2021)

    Google Scholar 

  17. Linardatos, P., Papastefanopoulos, V., Kotsiantis, S.: Explainable ai: a review of machine learning interpretability methods. Entropy. 23(1), 18 (2020)

    Article  Google Scholar 

  18. Lipton, Z.C.: The mythos of model interpretability: in machine learning, the concept of interpretability is both important and slippery. Queue. 16(3), 31–57 (2018)

    Article  Google Scholar 

  19. Gao, J., Chen, M., Li, Y., Gao, Y., Li, Y., Cai, S., Wang, J.: Multisite autism spectrum disorder classification using convolutional neural network classifier and individual morphological brain networks. Front. Neurosci. 14, 629630 (2021)

    Article  Google Scholar 

  20. Jimeno, M.M., Ravi, K.S., **, Z., Oyekunle, D., Ogbole, G., Geethanath, S.: ArtifactID: identifying artifacts in low-field MRI of the brain using deep learning. Magn. Reson. Imaging. 89, 42–48 (2021)

    Article  Google Scholar 

  21. Zhang, Y., Hong, D., McClement, D., Oladosu, O., Pridham, G., Slaney, G.: Grad-CAM helps interpret the deep learning models trained to classify multiple sclerosis types using clinical brain magnetic resonance imaging. J. Neurosci. Methods. 353, 109098 (2021)

    Article  Google Scholar 

  22. Tang, Z., Chuang, K.V., DeCarli, C., **, L.W., Beckett, L., Keiser, M.J., Dugger, B.N.: Interpretable classification of Alzheimer’s disease pathologies with a convolutional neural network pipeline. Nat. Commun. 10(1), 2173 (2019)

    Article  Google Scholar 

  23. Lu, P., Hu, L., Zhang, N., Liang, H., Tian, T., Lu, L.: A two-stage model for predicting mild cognitive impairment to Alzheimer’s disease conversion. Front. Aging Neurosci. 14, 826622 (2022)

    Article  Google Scholar 

  24. Iizuka, T., Fukasawa, M., Kameyama, M.: Deep-learning-based imaging-classification identified cingulate island sign in dementia with Lewy bodies. Sci. Rep. 9(1), 8944 (2019)

    Article  Google Scholar 

  25. Sánchez Fernández, I., Yang, E., Calvachi, P., Amengual-Gual, M., Wu, J.Y., Krueger, D., Northrup, H., Bebin, M.E., Sahin, M., Yu, K.H., Peters, J.M.: Deep learning in rare disease. Detection of tubers in tuberous sclerosis complex. PLoS One. 15(4), e0232376 (2020)

    Article  Google Scholar 

  26. Marcus, D.S., Wang, T.H., Parker, J., Csernansky, J.G., Morris, J.C., Buckner, R.L.: Open Access Series of Imaging Studies (OASIS): cross-sectional MRI data in young, middle aged, nondemented, and demented older adults. J. Cogn. Neurosci. 19(9), 1498–1507 (2007)

    Article  Google Scholar 

  27. Hon, M., Khan, N.M.: Towards Alzheimer’s disease classification through transfer learning. In: 2017 IEEE International Conference on Bioinformatics and Biomedicine (BIBM), (pp. 1166–1169). (2017)

    Google Scholar 

  28. Morris, J.C.: The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology. 43(11), 2412–2414 (1993)

    Article  Google Scholar 

  29. Han, X., Kwitt, R., Aylward, S., Bakas, S., Menze, B., Asturias, A., Vespa, P., Van Horn, J., Niethammer, M.: Brain extraction from normal and pathological images: a joint PCA/image-reconstruction approach. NeuroImage. 176, 431–445 (2018)

    Article  Google Scholar 

  30. Alzubaidi, L., Zhang, J., Humaidi, A.J., Al-Dujaili, A., Duan, Y., Al-Shamma, O., Santamaría, J., Fadhel, M.A., Al-Amidie, M., Farhan, L.: Review of deep learning: concepts, CNN architectures, challenges, applications, future directions. J Big Data. 8, 1–74 (2021)

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Atnafu, S.W., Diciotti, S. (2024). Development of an Interpretable Deep Learning System for the Identification of Patients with Alzheimer’s Disease. In: Mequanint, K., Tsegaw, A.A., Sendekie, Z.B., Kebede, B., Yetbarek Gedilu, E. (eds) Advancement of Science and Technology in Sustainable Manufacturing and Process Engineering. Green Energy and Technology. Springer, Cham. https://doi.org/10.1007/978-3-031-41173-1_2

Download citation

  • DOI: https://doi.org/10.1007/978-3-031-41173-1_2

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-031-41172-4

  • Online ISBN: 978-3-031-41173-1

  • eBook Packages: EnergyEnergy (R0)

Publish with us

Policies and ethics

Navigation