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Coordinated brain development: exploring the synchrony between changes in grey and white matter during childhood maturation

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Abstract

Brain development during childhood and early adolescence is characterized by global changes in brain architecture. Neuroimaging studies have revealed overall decreases in cortical thickness (CT) and increases in fractional anisotropy (FA). Furthermore, previous studies have shown that certain cortical regions display coordinated growth during development. However, there is significant heterogeneity in the timing and speed of these developmental transformations, and it is still unclear whether white and grey matter changes are co-localized. In this multimodal neuroimaging study, we investigated the relationship between grey and white matter developmental changes and asynchronous maturation within brain regions in 249 normally developing children between the ages 7–14. We used structural magnetic resonance imaging (MRI) and diffusion tensor imaging (DTI) to analyze CT and FA, respectively, as well as their covariance across development. Consistent with previous studies, we observed overall cortical thinning with age, which was accompanied by increased FA. We then compared the coordinated development of grey and white matter as indexed by covariance measures. Covariance between grey matter regions and the microstructure of white matter tracts connecting those regions were highly similar, suggesting that coordinated changes in the cortex were mirrored by coordinated changes in their respective tracts. Examining within-brain divergent trajectories, we found significant structural decoupling (decreased covariance) between several brain regions and tracts in the 9- to 11-year-old group, particularly involving the forceps minor and the regions that it connects to. We argue that this decoupling could reflect a developmental pattern within the prefrontal region in 9- and 11-year-old children, possibly related to the significant changes in cognitive control observed at this age.

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Acknowledgments

The opinions, hypotheses, conclusions, and recommendations of this study are the responsibilities of the authors and are not necessarily representative of the opinions of the funding agencies. The authors are grateful to the CAPES Foundation for the fellowship (Moura, L.M. 17930/12-0), the Sao Paulo Research Foundation–FAPESP (Sato, J.R. grant nos. 2013/ 10498-6 and 2013/00506-1 and Jackowski, A.P. grant no. 2013/08531-5), and CNPq, Brazil for funding this research. This study is from the National Institutes of Science and Technology for Developmental Psychiatry of Children and Adolescents (INPD) and is supported by CNPq (573974/2008-0) and FAPESP (2008/ 57896-8).

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Authors and Affiliations

  1. Department of Psychiatry, Federal University of Sao Paulo, Rua Borges Lagoa, 570 1°Andar, CEP, São Paulo, 04039-032, Brazil

    L. M. Moura, A. Zugman, P. M. Pan, A. Gadelha, M. A. G. Del Aquilla, J. de Jesus Mari, R. A. Bressan & A. P. Jackowski

  2. Interdisciplinary Lab of Clinical Neurosciences (LiNC), Federal University of Sao Paulo (UNIFESP), Sao Paulo, Brazil

    L. M. Moura, A. Zugman, P. M. Pan, A. Gadelha, M. A. G. Del Aquilla, R. A. Bressan & A. P. Jackowski

  3. Institute of Psychiatry, Psychology and Neurosciences, King’s College London, London, UK

    L. M. Moura, N. A. Crossley, A. Zugman & P. McGuire

  4. Biological and Medical Engineering Institute and Department of Psychiatry, P. Catholic University of Chile, Santiago, Chile

    N. A. Crossley

  5. National Institute of Developmental Psychiatry for Children and Adolescents, National Counsel of Technological and Scientific Development (CNPq), São Paulo, Brazil

    F. A. Picon, M. Anés & L. A. Rohde

  6. Department of Psychiatry, Federal University of Rio Grande do Sul, Rio Grande do Sul, Brazil

    L. A. Rohde

  7. Department of Psychiatry, Sao Paulo Medical School, University of Sao Paulo, Sao Paulo, Brazil

    E. C. Miguel

  8. Radiology Department, Sao Paulo Medical School, University of Sao Paulo, Sao Paulo, Brazil

    E. Amaro Jr.

  9. Center of Mathematics, Computation and Cognition, Universidade Federal do ABC, Santo Andre, Brazil

    J. R. Sato

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  1. L. M. Moura
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Correspondence to L. M. Moura.

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The ethics committee at the University of Sao Paulo (Sao Paulo, Brazil) approved the study procedures (IORG0004884, 1138/08) and have therefore been performed in accordance with ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Written informed consent was obtained from all parents, and all children provided verbal (or if possible, written) assent.

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Moura, L.M., Crossley, N.A., Zugman, A. et al. Coordinated brain development: exploring the synchrony between changes in grey and white matter during childhood maturation. Brain Imaging and Behavior 11, 808–817 (2017). https://doi.org/10.1007/s11682-016-9555-0

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