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White Matter Bundle Reconstruction From Single‐Shell Diffusion Magnetic Resonance Imaging: Test–Retest Reliability and Predictive Capability Across Orientation Distribution Function Reconstruction Methods

Human Brain Mapping, vol. 46, pp. e70429

Abstract

Deriving white matter (WM) bundles in vivo has thus far mainly been applied in research settings, leveraging high angular resolution, multi-shell diffusion MRI (dMRI) acquisitions that enable modern reconstruction methods. However, these advanced acquisitions are both time-consuming and costly to acquire. The ability to reconstruct WM bundles in the massive amounts of existing single-shelled, lower angular resolution data from legacy research studies and healthcare systems would offer much broader clinical applications and population-level generalizability. While legacy scans may offer a valuable, large-scale complement to contemporary research datasets, the reliability of white matter bundles derived from these scans remains unclear. Here, we leverage a large research dataset where each 64-direction dMRI scan was acquired as two independent 32-direction runs per subject. To investigate how a state-of-the-art bundle-specific reconstruction method generalizes to this data, we evaluated the test-retest reliability of WM bundles reconstructed from the two 32-direction scans across three orientation distribution function (ODF) reconstruction methods: generalized q-sampling imaging (GQI), constrained spherical deconvolution (CSD), and single-shell three-tissue CSD (SS3T). We found that the majority of WM bundles could be reliably extracted from dMRI scans that were acquired using the 32-direction, single-shell acquisition scheme. The mean Dice coefficient of reconstructed WM bundles was consistently higher within subject than between subject for all WM bundles and ODF reconstruction methods, illustrating preservation of person-specific anatomy. Further, when using features of the bundles to predict complex reasoning assessed using a computerized cognitive battery, we observed stable prediction accuracies (r: 0.15-0.36) across the test-retest data. Among the three ODF reconstruction methods, SS3T had a good balance between sensitivity and specificity when comparing the reconstructed bundles to atlas bundles, a high intra-class correlation of extracted features, more plausible bundles, and strong predictive performance. More broadly, these results demonstrate that bundle-specific reconstruction can achieve robust performance even on lower angular resolution, single-shell dMRI, with particular advantages for ODF methods optimized for single-shell data. This highlights the considerable potential for dMRI collected in healthcare settings and legacy research datasets to accelerate and expand the scope of WM research.

Authors 19

  1. Forschungszentrum Jülich · RWTH Aachen University

    Affiliation as printed

    Department of Psychiatry, Psychotherapy and Psychosomatics, Faculty of Medicine RWTH Aachen University Aachen Germany

    Institute of Neuroscience and Medicine, Brain and Behaviour (INM‐7) Research Center Jülich Jülich Germany

  2. Children's Hospital of Philadelphia · University of Pennsylvania Health System · University of Pennsylvania

    Affiliation as printed

    Department of Psychiatry University of Pennsylvania Philadelphia Pennsylvania USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania Philadelphia Pennsylvania USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania Philadelphia Pennsylvania USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania, Philadelphia, Pennsylvania, USA

  3. Children's Hospital of Philadelphia · University of Pennsylvania Health System · University of Pennsylvania

    Affiliation as printed

    Department of Child and Adolescent Psychiatry and Behavioral Science The Children's Hospital of Philadelphia Philadelphia Pennsylvania USA

    Department of Psychiatry University of Pennsylvania Philadelphia Pennsylvania USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania Philadelphia Pennsylvania USA

    Department of Child and Adolescent Psychiatry and Behavioral Science, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania, Philadelphia, Pennsylvania, USA

  4. Children's Hospital of Philadelphia · University of Pennsylvania Health System · University of Pennsylvania

    Affiliation as printed

    Department of Psychiatry University of Pennsylvania Philadelphia Pennsylvania USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania Philadelphia Pennsylvania USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania Philadelphia Pennsylvania USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania, Philadelphia, Pennsylvania, USA

  5. University of Pennsylvania

    Affiliation as printed

    Department of Psychiatry University of Pennsylvania Philadelphia Pennsylvania USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania Philadelphia Pennsylvania USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania, Philadelphia, Pennsylvania, USA

  6. Children's Hospital of Philadelphia · University of Pennsylvania Health System · University of Pennsylvania

    Affiliation as printed

    Department of Psychiatry University of Pennsylvania Philadelphia Pennsylvania USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania Philadelphia Pennsylvania USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania, Philadelphia, Pennsylvania, USA

  7. Children's Hospital of Philadelphia · University of Pennsylvania Health System · University of Pennsylvania

    Affiliation as printed

    Department of Psychiatry University of Pennsylvania Philadelphia Pennsylvania USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania Philadelphia Pennsylvania USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania, Philadelphia, Pennsylvania, USA

  8. Children's Hospital of Philadelphia · University of Pennsylvania Health System · University of Pennsylvania

    Affiliation as printed

    Department of Psychiatry University of Pennsylvania Philadelphia Pennsylvania USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania Philadelphia Pennsylvania USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania Philadelphia Pennsylvania USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania, Philadelphia, Pennsylvania, USA

  9. Semma Therapeutics (United States) · University of Pennsylvania

    Affiliation as printed

    Department of Psychiatry, Brain Behavior Laboratory, Perelman School of Medicine University of Pennsylvania Philadelphia Pennsylvania USA

    Sama Therapeutics Cambridge Massachusetts USA

    Department of Psychiatry, Brain Behavior Laboratory, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Sama Therapeutics, Cambridge, Massachusetts, USA

  10. Forschungszentrum Jülich · Düsseldorf University Hospital · Heinrich Heine University Düsseldorf

    Affiliation as printed

    Institute of Neuroscience and Medicine, Brain and Behaviour (INM‐7) Research Center Jülich Jülich Germany

    Institute of Systems Neuroscience, Medical Faculty and University Hospital Düsseldorf Heinrich Heine University Düsseldorf Düsseldorf Germany

  11. RWTH Aachen University

    Affiliation as printed

    Section for Translational Neurodegeneration, Department of Neurology RWTH Aachen University Aachen Germany

    Section for Translational Neurodegeneration, Department of Neurology, RWTH Aachen University, Aachen, Germany

  12. Children's Hospital of Philadelphia · University of Pennsylvania Health System · University of Pennsylvania

    Affiliation as printed

    Department of Psychiatry University of Pennsylvania Philadelphia Pennsylvania USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania Philadelphia Pennsylvania USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania, Philadelphia, Pennsylvania, USA

  13. University of Pennsylvania

    Affiliation as printed

    Center for AI and Data Science for Integrated Diagnostics (AI2D), University of Pennsylvania Philadelphia Pennsylvania USA

    Penn Statistics in Imaging and Visualization Endeavor (PennSIVE), Perelman School of Medicine, University of Pennsylvania Philadelphia Pennsylvania USA

    Center for AI and Data Science for Integrated Diagnostics (AI2D), University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Penn Statistics in Imaging and Visualization Endeavor (PennSIVE), Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA

  14. Children's Hospital of Philadelphia · University of Pennsylvania

    Affiliation as printed

    Department of Radiology Perelman School of Medicine at the University of Pennsylvania Philadelphia Pennsylvania USA

    Division of Neuroradiology Children's Hospital of Philadelphia Philadelphia Pennsylvania USA

    Department of Radiology, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Division of Neuroradiology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA

  15. University of Pittsburgh · University of Pittsburgh Medical Center

    Affiliation as printed

    Department of Psychiatry University of Pittsburgh Medical Center, University of Pittsburgh Pittsburgh Pennsylvania USA

    Department of Psychiatry, University of Pittsburgh Medical Center, University of Pittsburgh, Pittsburgh, Pennsylvania, USA

  16. Children's Hospital of Philadelphia · University of Pennsylvania

    Affiliation as printed

    Department of Radiology Perelman School of Medicine at the University of Pennsylvania Philadelphia Pennsylvania USA

    Division of Neuroradiology Children's Hospital of Philadelphia Philadelphia Pennsylvania USA

    Department of Radiology, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Division of Neuroradiology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA

  17. Forschungszentrum Jülich · Düsseldorf University Hospital · Heinrich Heine University Düsseldorf

    Affiliation as printed

    Institute of Neuroscience and Medicine, Brain and Behaviour (INM‐7) Research Center Jülich Jülich Germany

    Institute of Systems Neuroscience, Medical Faculty and University Hospital Düsseldorf Heinrich Heine University Düsseldorf Düsseldorf Germany

  18. Children's Hospital of Philadelphia · University of Pennsylvania Health System · University of Pennsylvania

    Affiliation as printed

    Department of Psychiatry University of Pennsylvania Philadelphia Pennsylvania USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania Philadelphia Pennsylvania USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania Philadelphia Pennsylvania USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania, Philadelphia, Pennsylvania, USA

  19. Children's Hospital of Philadelphia · University of Pennsylvania Health System · University of Pennsylvania

    Affiliation as printed

    Department of Psychiatry University of Pennsylvania Philadelphia Pennsylvania USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania Philadelphia Pennsylvania USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania Philadelphia Pennsylvania USA

    Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Lifespan Brain Institute (LiBI) of Penn Medicine and CHOP, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    The Penn Lifespan Informatics and Neuroimaging Center (PennLINC), University of Pennsylvania, Philadelphia, Pennsylvania, USA

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References 94