Maturation and interhemispheric asymmetry in neurite density and orientation dispersion in early childhood
Dennis Dimond,
Stella Heo,
Amanda Ip,
Christiane S. Rohr,
Ryann Tansey,
Kirk Graff,
Thijs Dhollander,
Robert E. Smith,
Catherine Lebel,
Deborah Dewey,
Alan Connelly,
Signe Bray
Affiliations
Dennis Dimond
Department of Neuroscience, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada; Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada; Child and Adolescent Imaging Research Program, University of Calgary, Calgary, AB, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada; Corresponding author: Alberta Children's Hospital, 28 Oki Drive NW, Calgary, Alberta, T3B 6A8, Canada.
Stella Heo
Department of Neuroscience, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
Amanda Ip
Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada; Child and Adolescent Imaging Research Program, University of Calgary, Calgary, AB, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada; Owerko Centre, University of Calgary, Calgary, AB, Canada; Mathison Centre for Mental Health Research and Education, University of Calgary, Calgary, AB, Canada; Department of Radiology, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
Christiane S. Rohr
Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada; Child and Adolescent Imaging Research Program, University of Calgary, Calgary, AB, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada; Mathison Centre for Mental Health Research and Education, University of Calgary, Calgary, AB, Canada; Department of Radiology, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
Ryann Tansey
Department of Neuroscience, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada; Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada; Child and Adolescent Imaging Research Program, University of Calgary, Calgary, AB, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada
Kirk Graff
Department of Neuroscience, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada; Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada; Child and Adolescent Imaging Research Program, University of Calgary, Calgary, AB, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada
Thijs Dhollander
Developmental Imaging, Murdoch Children's Research Institute, Melbourne, VIC, Australia
Robert E. Smith
The Florey Institute of Neuroscience and Mental Health, Melbourne, VIC, Australia; The Florey Department of Neuroscience and Mental Health, The University of Melbourne, Melbourne, VIC, Australia
Catherine Lebel
Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada; Child and Adolescent Imaging Research Program, University of Calgary, Calgary, AB, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada; Owerko Centre, University of Calgary, Calgary, AB, Canada; Mathison Centre for Mental Health Research and Education, University of Calgary, Calgary, AB, Canada
Deborah Dewey
Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada; Owerko Centre, University of Calgary, Calgary, AB, Canada; Department of Paediatrics, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada; Department of Community Health Sciences, University of Calgary, Calgary, AB, Canada
Alan Connelly
The Florey Institute of Neuroscience and Mental Health, Melbourne, VIC, Australia; The Florey Department of Neuroscience and Mental Health, The University of Melbourne, Melbourne, VIC, Australia
Signe Bray
Alberta Children's Hospital Research Institute, University of Calgary, Calgary, AB, Canada; Child and Adolescent Imaging Research Program, University of Calgary, Calgary, AB, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada; Owerko Centre, University of Calgary, Calgary, AB, Canada; Mathison Centre for Mental Health Research and Education, University of Calgary, Calgary, AB, Canada; Department of Radiology, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada
Background: The brain's white matter undergoes profound changes during early childhood, which are believed to underlie the rapid development of cognitive and behavioral skills during this period. Neurite density, and complexity of axonal projections, have been shown to change across the life span, though changes during early childhood are poorly characterized. Here, we utilize neurite orientation dispersion and density imaging (NODDI) to investigate maturational changes in tract-wise neurite density index (NDI) and orientation dispersion index (ODI) during early childhood. Additionally, we assess hemispheric asymmetry of tract-wise NDI and ODI values, and longitudinal changes. Methods: Two sets of diffusion weighted images with different diffusion-weighting were collected from 125 typically developing children scanned at baseline (N = 125; age range = 4.14–7.29; F/M = 73/52), 6-month (N = 8; F/M = 8/0), and 12-month (N = 52; F/M = 39/13) timepoints. NODDI and template-based tractography using constrained spherical deconvolution were utilized to calculate NDI and ODI values for major white matter tracts. Mixed-effects models controlling for sex, handedness, and in-scanner head motion were utilized to assess developmental changes in tract-wise NDI and ODI. Additional mixed-effects models were used to assess interhemispheric differences in tract-wise NDI and ODI values and hemispheric asymmetries in tract-wise development. Results: Maturational increases in NDI were seen in all major white matter tracts, though we did not observe the expected tract-wise pattern of maturational rates (e.g. fast commissural/projection and slow frontal/temporal tract change). ODI did not change significantly with age in any tract. We observed greater NDI and ODI values in the right as compared to the left hemisphere for most tracts, but no hemispheric asymmetry for rate of change with age. Conclusions: These findings suggest that neurite density, but not orientation dispersion, increases with age during early childhood. In relation to NDI growth trends reported in infancy and late-childhood, our results suggest that early childhood may be a transitional period for neurite density maturation wherein commissural/projection fibers are approaching maturity, maturation in long range association fibers is increasing, and changes in limbic/frontal fibers remain modest. Rightward asymmetry in NDI and ODI values, but no asymmetry in developmental changes, suggests that rightward asymmetry of neurite density and orientation dispersion is established prior to age 4.
