Cell Reports (Dec 2023)
Development of white matter fiber covariance networks supports executive function in youth
- Joëlle Bagautdinova,
- Josiane Bourque,
- Valerie J. Sydnor,
- Matthew Cieslak,
- Aaron F. Alexander-Bloch,
- Maxwell A. Bertolero,
- Philip A. Cook,
- Raquel E. Gur,
- Ruben C. Gur,
- Fengling Hu,
- Bart Larsen,
- Tyler M. Moore,
- Hamsanandini Radhakrishnan,
- David R. Roalf,
- Russel T. Shinohara,
- Tinashe M. Tapera,
- Chenying Zhao,
- Aristeidis Sotiras,
- Christos Davatzikos,
- Theodore D. Satterthwaite
Affiliations
- Joëlle Bagautdinova
- Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA
- Josiane Bourque
- Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA
- Valerie J. Sydnor
- Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA
- Matthew Cieslak
- Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA
- Aaron F. Alexander-Bloch
- Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA
- Maxwell A. Bertolero
- Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA
- Philip A. Cook
- Department of Radiology, University of Pennsylvania, Philadelphia, PA 19104, USA
- Raquel E. Gur
- Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Radiology, University of Pennsylvania, Philadelphia, PA 19104, USA
- Ruben C. Gur
- Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Radiology, University of Pennsylvania, Philadelphia, PA 19104, USA
- Fengling Hu
- Department of Biostatistics, Epidemiology, and Informatics, University of Pennsylvania, Philadelphia, PA 19104, USA; Center for Biomedical Image Computing and Analytics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Penn Statistics in Imaging and Visualization Center, Department of Biostatistics, Epidemiology, and Informatics, University of Pennsylvania, Philadelphia, PA 19104, USA
- Bart Larsen
- Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA
- Tyler M. Moore
- Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA
- Hamsanandini Radhakrishnan
- Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA
- David R. Roalf
- Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA
- Russel T. Shinohara
- Department of Biostatistics, Epidemiology, and Informatics, University of Pennsylvania, Philadelphia, PA 19104, USA; Center for Biomedical Image Computing and Analytics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Penn Statistics in Imaging and Visualization Center, Department of Biostatistics, Epidemiology, and Informatics, University of Pennsylvania, Philadelphia, PA 19104, USA
- Tinashe M. Tapera
- Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA
- Chenying Zhao
- Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Bioengineering, School of Engineering and Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA
- Aristeidis Sotiras
- Department of Radiology and Institute for Informatics, Mallinckrodt Institute of Radiology, Washington University School of Medicine, St. Louis, MO 63130, USA
- Christos Davatzikos
- Department of Radiology, University of Pennsylvania, Philadelphia, PA 19104, USA; Center for Biomedical Image Computing and Analytics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
- Theodore D. Satterthwaite
- Penn Lifespan Informatics and Neuroimaging Center (PennLINC), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Lifespan Brain Institute (LiBI) of Penn Medicine and Children’s Hospital of Philadelphia (CHOP), University of Pennsylvania, Philadelphia, PA 19104, USA; Center for Biomedical Image Computing and Analytics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Corresponding author
- Journal volume & issue
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Vol. 42,
no. 12
p. 113487
Abstract
Summary: During adolescence, the brain undergoes extensive changes in white matter structure that support cognition. Data-driven approaches applied to cortical surface properties have led the field to understand brain development as a spatially and temporally coordinated mechanism that follows hierarchically organized gradients of change. Although white matter development also appears asynchronous, previous studies have relied largely on anatomical tract-based atlases, precluding a direct assessment of how white matter structure is spatially and temporally coordinated. Harnessing advances in diffusion modeling and machine learning, we identified 14 data-driven patterns of covarying white matter structure in a large sample of youth. Fiber covariance networks aligned with known major tracts, while also capturing distinct patterns of spatial covariance across distributed white matter locations. Most networks showed age-related increases in fiber network properties, which were also related to developmental changes in executive function. This study delineates data-driven patterns of white matter development that support cognition.