Deep multimodal saliency parcellation of cerebellar pathways: Linking microstructure and individual function through explainable multitask learning.

Journal: Human brain mapping
PMID:

Abstract

Parcellation of human cerebellar pathways is essential for advancing our understanding of the human brain. Existing diffusion magnetic resonance imaging tractography parcellation methods have been successful in defining major cerebellar fibre tracts, while relying solely on fibre tract structure. However, each fibre tract may relay information related to multiple cognitive and motor functions of the cerebellum. Hence, it may be beneficial for parcellation to consider the potential importance of the fibre tracts for individual motor and cognitive functional performance measures. In this work, we propose a multimodal data-driven method for cerebellar pathway parcellation, which incorporates both measures of microstructure and connectivity, and measures of individual functional performance. Our method involves first training a multitask deep network to predict various cognitive and motor measures from a set of fibre tract structural features. The importance of each structural feature for predicting each functional measure is then computed, resulting in a set of structure-function saliency values that are clustered to parcellate cerebellar pathways. We refer to our method as Deep Multimodal Saliency Parcellation (DeepMSP), as it computes the saliency of structural measures for predicting cognitive and motor functional performance, with these saliencies being applied to the task of parcellation. Applying DeepMSP to a large-scale dataset from the Human Connectome Project Young Adult study (n = 1065), we found that it was feasible to identify multiple cerebellar pathway parcels with unique structure-function saliency patterns that were stable across training folds. We thoroughly experimented with all stages of the DeepMSP pipeline, including network selection, structure-function saliency representation, clustering algorithm, and cluster count. We found that a 1D convolutional neural network architecture and a transformer network architecture both performed comparably for the multitask prediction of endurance, strength, reading decoding, and vocabulary comprehension, with both architectures outperforming a fully connected network architecture. Quantitative experiments demonstrated that a proposed low-dimensional saliency representation with an explicit measure of motor versus cognitive category bias achieved the best parcellation results, while a parcel count of four was most successful according to standard cluster quality metrics. Our results suggested that motor and cognitive saliencies are distributed across the cerebellar white matter pathways. Inspection of the final k = 4 parcellation revealed that the highest-saliency parcel was most salient for the prediction of both motor and cognitive performance scores and included parts of the middle and superior cerebellar peduncles. Our proposed saliency-based parcellation framework, DeepMSP, enables multimodal, data-driven tractography parcellation. Through utilising both structural features and functional performance measures, this parcellation strategy may have the potential to enhance the study of structure-function relationships of the cerebellar pathways.

Authors

  • Ari Tchetchenian
    Biomedical Image Computing Group, School of Computer Science and Engineering, University of New South Wales (UNSW), Sydney, New South Wales, Australia.
  • Leo Zekelman
    Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA.
  • Yuqian Chen
  • Jarrett Rushmore
    Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, USA.
  • Fan Zhang
    Department of Anesthesiology, Bishan Hospital of Chongqing Medical University, Chongqing, China.
  • Edward H Yeterian
    Department of Psychology, Colby College, Waterville, Maine, USA.
  • Nikos Makris
    Harvard Medical School, Boston MA, USA.
  • Yogesh Rathi
    Brigham and Women's Hospital, Harvard Medical School, Boston, USA.
  • Erik Meijering
    Biomedical Imaging Group Rotterdam, Departments of Medical Informatics and Radiology, Erasmus University Medical Center, Rotterdam, the Netherlands.
  • Yang Song
    Biomedical and Multimedia Information Technology (BMIT) Research Group, School of IT, University of Sydney, NSW 2006, Australia. Electronic address: yson1723@uni.sydney.edu.au.
  • Lauren J O'Donnell
    Brigham and Women's Hospital, Harvard Medical School, Boston, USA.