TY - JOUR
T1 - Neurodevelopmental patterns of early postnatal white matter maturation represent distinct underlying microstructure and histology
AU - Nazeri, Arash
AU - Krsnik, Željka
AU - Kostović, Ivica
AU - Ha, Sung Min
AU - Kopić, Janja
AU - Alexopoulos, Dimitrios
AU - Kaplan, Sydney
AU - Meyer, Dominique
AU - Luby, Joan L.
AU - Warner, Barbara B.
AU - Rogers, Cynthia E.
AU - Barch, Deanna M.
AU - Shimony, Joshua S.
AU - McKinstry, Robert C.
AU - Neil, Jeffrey J.
AU - Smyser, Christopher D.
AU - Sotiras, Aristeidis
N1 - Funding Information:
A.N. was supported by Canon Medical Systems USA, Inc./Radiological Society of North America Research & Education (RSNA R&E) Foundation Research Resident Grant ( RR1953 ) and Foundation of the American Society of Neuroradiology (ASNR) Grant Program. A.S. was partially supported by the National Institutes of Health ( NIH ) award R01AG067103 . J.S.S. was supported by NIH award P50 HD103525 to the Intellectual and Developmental Disabilities Research Center at Washington University. Data were provided by the developing Human Connectome Project, KCL-Imperial-Oxford Consortium funded by the European Research Council under the European Union Seventh Framework Programme ( FP/2007-2013 )/ ERC grant agreement no. 319456 . We are grateful to the families who generously supported this trial. The eLABE study was supported by NIH award R01MH113883 . This research was partly funded by the Research Cooperability Program of the Croatian Science Foundation funded by the European Union from the European Social Fund under the Operational Programme Efficient Human Resources 2014-2020 PSZ-2019-02-4710 (Z.K.). Computations were performed using the facilities of the Washington University Center for High Performance Computing, which were partially funded by NIH grants 1S10RR022984-01A1 and 1S10OD018091-01 .
Funding Information:
A.N. was supported by Canon Medical Systems USA, Inc./Radiological Society of North America Research & Education (RSNA R&E) Foundation Research Resident Grant (RR1953) and Foundation of the American Society of Neuroradiology (ASNR) Grant Program. A.S. was partially supported by the National Institutes of Health (NIH) award R01AG067103. J.S.S. was supported by NIH award P50 HD103525 to the Intellectual and Developmental Disabilities Research Center at Washington University. Data were provided by the developing Human Connectome Project, KCL-Imperial-Oxford Consortium funded by the European Research Council under the European Union Seventh Framework Programme (FP/2007-2013)/ERC grant agreement no. 319456. We are grateful to the families who generously supported this trial. The eLABE study was supported by NIH award R01MH113883. This research was partly funded by the Research Cooperability Program of the Croatian Science Foundation funded by the European Union from the European Social Fund under the Operational Programme Efficient Human Resources 2014-2020 PSZ-2019-02-4710 (Z.K.). Computations were performed using the facilities of the Washington University Center for High Performance Computing, which were partially funded by NIH grants 1S10RR022984-01A1 and 1S10OD018091-01. Conceptualization, A.N. and A.S.; methodology, A.N. Z.K. I.K. S.M.H. D.M.B. C.D.S. and A.S.; investigation, A.N. Z.K. I.K. J.K. D.A. C.D.S. and A.S.; data curation, A.N. Z.K. D.A. S.K. and D.M.; formal analysis, A.N. and A.S.; writing—original draft, A.N. and A.S.; writing—review & editing, A.N. Z.K. I.K. S.M.H. J.K. D.A. S.K. D.M. J.L.L. B.B.W. C.E.R. D.M.B. J.S.S. R.C.M, J.J.N. C.D.S. and A.S.; visualization, A.N. and Z.K.; resources, Z.K. C.D.S. and A.S. A.S. holds equity in TheraPanacea and has received personal compensation for serving on the Alzheimer's Disease Research Program Scientific Review Committee of the BrightFocus Foundation. We support inclusive, diverse, and equitable conduct of research.
Publisher Copyright:
© 2022 Elsevier Inc.
PY - 2022/12/7
Y1 - 2022/12/7
N2 - Cerebral white matter undergoes a rapid and complex maturation during the early postnatal period. Prior magnetic resonance imaging (MRI) studies of early postnatal development have often been limited by small sample size, single-modality imaging, and univariate analytics. Here, we applied nonnegative matrix factorization, an unsupervised multivariate pattern analysis technique, to T2w/T1w signal ratio maps from the Developing Human Connectome Project (n = 342 newborns) revealing patterns of coordinated white matter maturation. These patterns showed divergent age-related maturational trajectories, which were replicated in another independent cohort (n = 239). Furthermore, we showed that T2w/T1w signal variations in these maturational patterns are explained by differential contributions of white matter microstructural indices derived from 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 concise and effective representation of early postnatal white matter reorganization.
AB - Cerebral white matter undergoes a rapid and complex maturation during the early postnatal period. Prior magnetic resonance imaging (MRI) studies of early postnatal development have often been limited by small sample size, single-modality imaging, and univariate analytics. Here, we applied nonnegative matrix factorization, an unsupervised multivariate pattern analysis technique, to T2w/T1w signal ratio maps from the Developing Human Connectome Project (n = 342 newborns) revealing patterns of coordinated white matter maturation. These patterns showed divergent age-related maturational trajectories, which were replicated in another independent cohort (n = 239). Furthermore, we showed that T2w/T1w signal variations in these maturational patterns are explained by differential contributions of white matter microstructural indices derived from 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 concise and effective representation of early postnatal white matter reorganization.
KW - MRI
KW - Neurodevelopment
KW - data-driven parcellation
KW - histology
KW - newborn
KW - subplate remnant
KW - tissue microstructure
KW - topography
KW - unsupervised machine learning
KW - white matter maturation
UR - http://www.scopus.com/inward/record.url?scp=85140994375&partnerID=8YFLogxK
U2 - 10.1016/j.neuron.2022.09.020
DO - 10.1016/j.neuron.2022.09.020
M3 - Article
C2 - 36243003
AN - SCOPUS:85140994375
SN - 0896-6273
VL - 110
SP - 4015-4030.e4
JO - Neuron
JF - Neuron
IS - 23
ER -