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Neurodevelopmental Patterns of Early Postnatal White Matter Maturation Represent Distinct Underlying Microstructure and Histology

52 Pages Posted: 26 Apr 2022 Publication Status: Accepted

See all articles by Arash Nazeri

Arash Nazeri

Washington University in St. Louis - Mallinckrodt Institute of Radiology

Željka Krsnik

University of Zagreb - School of Medicine

Ivica Kostovic

University of Zagreb - School of Medicine

Sung Min Ha

Washington University in St. Louis - Mallinckrodt Institute of Radiology

Janja Kopić

University of Zagreb - School of Medicine

Dimitrios Alexopoulos

University of Washington - Department of Neurology

Sydney Kaplan

University of Washington - Department of Neurology

Dominique Meyer

University of Washington - Department of Neurology

Joan Luby

Washington University in St. Louis - Department of Psychiatry

Barbara Warner

Washington University in St. Louis - Department of Pediatrics

Cynthia Rogers

Washington University in St. Louis - Department of Psychiatry

Deanna M. Barch Barch

Washington University in St. Louis

Joshua S. Shimony

Washington University in St. Louis - Mallinckrodt Institute of Radiology

Robert C. McKinstry

Washington University in St. Louis - Mallinckrodt Institute of Radiology

Jeffrey J. Neil

University of Washington - Department of Neurology

Chris Smyser

Washington University in St. Louis - Department of Neurology

Aristeidis Sotiras

Washington University School of Medicine - Mallinckrodt Institute of Radiology

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Abstract

During the early postnatal period, cerebral white matter undergoes rapid maturation through a complex series of interrelated cellular and histogenetic processes. Accurate quantification of these processes is important for improving understanding of early brain development, developmental abnormalities related to prematurity, and neurodevelopmental diseases. Past efforts have used magnetic resonance imaging (MRI) to track these developmental processes in vivo. However, most previous studies have relied on a single imaging modality data or have often been limited by small samples and analytics that do not evaluate complex multivariate imaging patterns. Here, we applied an advanced unsupervised multivariate pattern analysis technique, non-negative matrix factorization (NMF), to T2w/T1w signal ratio maps from a large cohort of newborns (Developing Human Connectome Project [dHCP], n=342), revealing patterns of coordinated white matter maturation. These patterns showed divergent age-related maturational trajectories and differential susceptibility to premature birth, which were replicated in an independent large sample of newborns (Early Life Adversity, Biological Embedding, and Risk for Developmental Precursors of Mental Disorders [eLABE], n=239). Furthermore, we showed that T2w/T1w signal variations in white matter maturational patterns are explained by differential contributions of white matter microstructure indices (i.e., free water content and neurite density index) derived from neurite orientation dispersion and density imaging (NODDI) modeling of diffusion-weighted MRI. Finally, we demonstrated how white matter maturation patterns relate to distinct histological features by comparing our findings with postmortem late fetal/early postnatal brain tissue staining. Together, these results delineate a novel MRI representation of white matter microstructural and histological reorganization during early postnatal development.

Keywords: Postnatal neurodevelopment, white matter, MRI, Diffusion-weighted MRI, MRI-histology correlation

Suggested Citation

Nazeri, Arash and Krsnik, Željka and Kostovic, Ivica and Ha, Sung Min and Kopić, Janja and Alexopoulos, Dimitrios and Kaplan, Sydney and Meyer, Dominique and Luby, Joan and Warner, Barbara and Rogers, Cynthia and Barch, Deanna and Shimony, Joshua S. and McKinstry, Robert C. and Neil, Jeffrey J. and Smyser, Chris and Sotiras, Aristeidis, Neurodevelopmental Patterns of Early Postnatal White Matter Maturation Represent Distinct Underlying Microstructure and Histology. Available at SSRN: https://ssrn.com/abstract=4094330 or http://dx.doi.org/10.2139/ssrn.4094330
This version of the paper has not been formally peer reviewed.

Arash Nazeri

Washington University in St. Louis - Mallinckrodt Institute of Radiology ( email )

Željka Krsnik

University of Zagreb - School of Medicine ( email )

Trg maršala Tita 14
Zagreb
Croatia

Ivica Kostovic

University of Zagreb - School of Medicine ( email )

Trg maršala Tita 14
Zagreb
Croatia

Sung Min Ha

Washington University in St. Louis - Mallinckrodt Institute of Radiology ( email )

Janja Kopić

University of Zagreb - School of Medicine ( email )

Trg maršala Tita 14
Zagreb
Croatia

Dimitrios Alexopoulos

University of Washington - Department of Neurology ( email )

WA
United States

Sydney Kaplan

University of Washington - Department of Neurology ( email )

WA
United States

Dominique Meyer

University of Washington - Department of Neurology ( email )

WA
United States

Joan Luby

Washington University in St. Louis - Department of Psychiatry ( email )

Barbara Warner

Washington University in St. Louis - Department of Pediatrics ( email )

Cynthia Rogers

Washington University in St. Louis - Department of Psychiatry ( email )

Deanna Barch

Washington University in St. Louis ( email )

1 Brookings Drive
St. Louis, MO 63130
United States
3149358729 (Phone)

Joshua S. Shimony

Washington University in St. Louis - Mallinckrodt Institute of Radiology ( email )

Robert C. McKinstry

Washington University in St. Louis - Mallinckrodt Institute of Radiology ( email )

Jeffrey J. Neil

University of Washington - Department of Neurology ( email )

WA
United States

Chris Smyser

Washington University in St. Louis - Department of Neurology ( email )

St. Louis, MO
United States

Aristeidis Sotiras (Contact Author)

Washington University School of Medicine - Mallinckrodt Institute of Radiology ( email )

St. Louis, MO
United States

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